1 running head: tetraspanin genes in arabidopsis … · 103 in primary root growth and lateral root...

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Running head: TETRASPANIN genes in Arabidopsis development 1

Author for correspondence: 2

Mieke Van Lijsebettens 3

Department of Plant Systems Biology 4

VIB-Ghent University 5

Technologiepark 927 6

B-9052 Gent (Belgium) 7

Tel.: +32 9 3313970; Fax: +32 9 3313809 8

E-mail: [email protected] 9

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Journal research area: Genes, Development and Evolution: Associate Editors Jiming Jiang 11

(Madison) and Hong Ma (Shanghai and University Park) 12

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Plant Physiology Preview. Published on September 28, 2015, as DOI:10.1104/pp.15.01310

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Functional Analysis of Arabidopsis TETRASPANIN Gene Family in Plant Growth and 14

Development1[OPEN] 15

Feng Wang, Antonella Muto, Jan Van de Velde, Pia Neyt, Kristiina Himanen2, Klaas 16

Vandepoele, and Mieke Van Lijsebettens* 17

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Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (F.W, A.M., J.V.d.V., P.N., 19

K.H., K.V., M.V.L.); Department of Plant Biotechnology and Bioinformatics, Ghent University, 20

B-9052 Ghent, Belgium (F.W, A.M., J.V.d.V., P.N., K.H., K.V., M.V.L.); and Department of 21

Biology, Ecology and Earth Sciences, University of Calabria, 87036 Arcavacata of Rende, Italy 22

(A.M.) 23

ORCID KV 0000-0003-4790-2725, JVDV 0000-0001-7742-1266, MVL 0000-0002-7632-1463. 24

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One-sentence summary: TETRASPANIN gene expression patterns and mutational analysis 26

inferred function in plant growth and development, which was furthered by cis regulatory 27

elements and a TF-TET regulatory network 28

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1 This work was supported by the China Scholarship Council (CSC) (predoctoral fellowship to 30

F.W.), and by the Ministero dell' Istruzione, dell'Università e della Ricerca (MIUR) 31

(predoctoral fellowship to A.M.). KV acknowledges the Multidisciplinary Research 32

Partnership “Bioinformatics: from nucleotides to networks” Project (no 01MR0310W) of 33

Ghent University. J.VdV. is indebted to the Agency for Innovation by Science and Technology 34

(IWT) in Flanders for a predoctoral fellowship. 35 2 Present address: Department of Agricultural Sciences, University of Helsinki, 000014 Helsinki, 36

Finland 37 * Address correspondence to [email protected]. 38

The author responsible for distribution of materials integral to the findings presented in this 39

article in accordance with the policy described in the Instructions for Authors 40

(www.plantphysiol.org) is: Mieke Van Lijsebettens ([email protected]). 41 [OPEN] Articles can be viewed without a subscription. 42

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Abstract 44

TETRASPANIN (TET) genes encode conserved integral membrane proteins that are known in 45

animals to function in cellular communication during gamete fusion, immunity reaction and 46

pathogen recognition. In plants, functional information is limited to one of the 17 members of the 47

Arabidopsis TET gene family and to expression data in reproductive stages. Here, the promoter 48

activity of all 17 Arabidopsis TET genes was investigated by pAtTET::NLS-GFP/GUS reporter 49

lines throughout the life cycle, which predicted functional divergence in the paralogous genes per 50

clade. However, partial overlap was observed for many TET genes across the clades, correlating 51

with few phenotypes in single mutants and therefore requiring double mutant combinations for 52

functional investigation. Mutational analysis showed a role for TET13 in primary root growth and 53

lateral root development, and redundant roles for TET5 and TET6 in leaf and root growth through 54

negative regulation of cell proliferation. Strikingly, a number of TET genes were expressed in 55

embryonic and seedling progenitor cells and remained expressed until the differentiation state in 56

the mature plant, suggesting a dynamic function over developmental stages. cis-regulatory 57

elements together with transcription factor binding data provided molecular insight into the site, 58

conditions and perturbations that affect TET gene expression, and positioned the TET genes in 59

different molecular pathways; the data represent a hypothesis-generating resource for further 60

functional analyses. 61

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Key words: Arabidopsis; tetraspanin; gene duplication; lateral root development; vascular tissue; 63

promoter elements; transcription factor regulatory network 64

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During embryogenesis in plants, the fertilized egg cell develops gradually by consecutive, but 67

partially overlapping, processes, such as cell division, patterning and growth, into the 68

rudimentary body plan of the mature embryo. Early pattern formation in the embryo generates the 69

body plan polarity with apical and basal stem cell progenitor domains and the different concentric 70

progenitor tissue layers, in which cells interpret their position, acquire cell fate and differentiate 71

into specific morphologies and functions after germination. Then, the apical meristems are 72

activated to generate the primary root and the above-ground vegetative structures (Murray et al., 73

2012; Perilli et al., 2012). In the seedling, patterning processes occur in the epidermis to generate 74

specialized cells such as trichomes and stomata, in the shoot apical meristem (SAM) upon leaf 75

initiation and in the primary root pericycle upon lateral root initiation. Developmental programs 76

such as germination, photomorphogenesis and floral transition occur in response to 77

environmental stimuli, such as light, circadian clock and temperature, and hormonal stimuli that 78

require cellular communication and signaling. Membrane proteins, located at the plasma 79

membrane, are the most upstream components in signaling perception and transduction during 80

cellular communication. It is estimated that 20 to 30% of all genes in most genomes encode 81

integral proteins (Krogh et al., 2001), which are transmembrane proteins. 82

Tetraspanins are a distinct class of conserved integral proteins with four transmembrane 83

domains, a small extracellular loop and a large, cystein-rich extracellular loop, which is important 84

for interacting with each other and other proteins to form tetraspanin-enriched microdomains that 85

participate in cell-to-cell communication processes during cell morphogenesis, motility and 86

fusion (Yáñez-Mó et al., 2009). Tetraspanins comprise large gene families in multicellular 87

organisms; 33 in human, and 36 in Drosophila melanogaster (Huang et al., 2005). Mutations in 88

animal tetraspanins result in severe defects, such as incurable blindness and impaired fertility 89

(Kaji et al., 2002; Goldberg, 2006). In plants, phylogenetic studies identified 17 tetraspanin genes 90

in the Arabidopsis genome, most of which are duplicated (Cnops et al., 2006; Wang et al., 2012; 91

Boavida et al., 2013). Mutants of the Arabidopsis TETRASPANIN1/TORNADO2/EKEKO 92

(TET1/TRN2) show defects in leaf lamina symmetry and venation pattern, root epidermal 93

patterning (Cnops et al., 2000; Cnops et al., 2006), peripheral zone identity of the SAM (Chiu et 94

al., 2007) and megasporogenesis (Lieber et al., 2011). A number of Arabidopsis tetraspanins are 95

expressed in reproductive tissues and at fertilization, and are localized at the plasma membrane of 96

protoplasts (Boavida et al., 2013). However, a systematic analysis of all members of the plant 97



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TET gene family in embryonic and vegetative development and upon hormonal and 98

environmental stimuli is lacking. 99

Here, the 17 members of the Arabidopsis TET gene family were analyzed for their cellular 100

expression during embryonic and vegetative development by pAtTET1-17::NLS-GFP/GUS 101

reporter lines, which was instrumental for further mutational analyses. Indeed, a role for TET13 102

in primary root growth and lateral root development, and redundant roles for TET5 and TET6 in 103

leaf and root growth were identified, as was suggested by the site of their expression. 104

Complementary experimental and computational regulatory datasets were integrated to identify 105

putative cis-regulatory elements in the TET promoters. A transcription factor (TF)-TET gene 106

regulatory network was delineated and regulatory interactions were confirmed by perturbation 107

expression data. 108

RESULTS 109

Expression of TET Genes in Specific Tissues, Domains and Cells throughout the Plant’s Life 110

Cycle 111

The promoter activities of the 17 TET gene family members were analyzed by pAtTET::NLS-112

GFP/GUS lines throughout the life cycle in order to reveal their site and timing of activity and 113

help in designing further mutational analyses. Per TET gene, at least three independent T2 114

pAtTET::NLS-GFP/GUS lines, with a single-locus insertion, were analyzed by X-Gluc 115

histochemical staining in embryo, root, leaf and flower organs. None of the TET genes was 116

expressed in all organs and only a few had similar expression patterns (Fig. 1). Moreover, within 117

a specific organ, TET gene expression was not constitutive but restricted to specific domains, 118

tissues or cell types. 119

Nine TET genes, i.e. TET1, TET3, TET4, TET5, TET8, TET10, TET13, TET14 and TET15, 120

were expressed in the early globular and heart stage embryo, in which patterning takes place (Fig. 121

2). TET3 was expressed in the SAM progenitor domain of all embryo stages, TET13 in the 122

hypophysis and TET15 in the basal part of the embryo, including the hypophysis, suggesting that 123

TET3, TET13 and TET15 might participate in apical-basal patterning. TET1 was asymmetrically 124

expressed in vascular tissue precursor cells of the heart stage embryo. TET5 expression was 125

restricted to vascular tissue progenitor cells in the centre of the globular, heart and torpedo stage 126

embryo, a pattern similar to that of TMO5 (TARGET OF MONOPTEROS5), which is necessary 127



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for the periclinal cell division and vascular tissue initiation (De Rybel et al., 2013). TET4 and 128

TET10 were expressed in the central part of the embryo, including the vascular bundle progenitor 129

region; TET14 expression was restricted to the vascular progenitor strand in the cotyledons, 130

suggesting TET1, TET4, TET5, TET10 and TET14 might participate in radial patterning. TET8 131

was expressed in the apical domain of the heart stage embryo and in the tip regions of the 132

cotyledons of the torpedo and mature stage embryo (Fig. 2). After germination, expression 133

remained at the apical domains and vascular tissues, i.e. TET3 in the SAM-organizing center 134

(Supplemental Fig. S1A), TET1 and TET15 in the lateral root cap (Fig. 2), TET13 in the quiescent 135

centre (QC) of the primary root (Fig. 2), TET1, TET5, TET10 in the vascular bundle of the 136

primary root and rosette leaves (Fig. 2; Fig. 5, A and B; Supplemental Fig. S1C), and TET14 in 137

the vascular tissue of rosette leaves (Supplemental Fig. S1N). 138

Remarkably, TET2 was specifically expressed after germination in the stomatal guard cell 139

lineage during early leaf development. TET2 expression was not detected in the meristemoid 140

mother cell (MMC) that originates from a protodermal cell, but it was in the small triangle-141

shaped daughter cell (called meristemoid) generated after the first asymmetric division (Fig. 3A), 142

and not in the large daughter cell (called stomatal lineage ground cell, SLGC). TET2 expression 143

remained in the guard mother cell (GMC, Fig. 3D) after the first and subsequent asymmetric 144

divisions (Fig. 3, B and C) and in mature guard cells (Fig. 3E). 145

TET gene expression in progenitor tissues, domains and cells remained in stem cells of shoot 146

or root apical meristems or in their derived differentiated tissues or cell types in the seedling, 147

suggesting their function is required at different developmental stages. The variation in spatial 148

and temporal expression patterns of the 17 TET genes suggests a range of functions in the plant’s 149

life cycle. 150

Divergent TET Expression Patterns within Clades, but Overlapping amongst Clades 151

The TET gene family consists of different clades with duplicated or triplicated members 152

(Cnops et al., 2006; Wang et al., 2012; Boavida et al., 2013), showing diverging expression 153

profiles (Fig. 1, 2, 3). Indeed, the duplicated genes TET1 and TET2 had strikingly divergent gene 154

expression patterns. The TET1 asymmetric gene expression pattern was found in vascular tissue 155

precursor cells in the embryo, in the columella cells and vascular tissues of the primary root (Fig. 156

2), in the vascular tissues of cotyledons and rosette leaves, and in the stigma and transmitting 157

tissue of the female gametophyte (Supplemental Fig. S1, C, J and N; Supplemental Fig. S2, A and 158



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B), which correlated with tet1 mutant phenotypes observed in root and leaf (Cnops et al., 2000; 159

Cnops et al., 2006), in SAM (Chiu et al., 2007), in embryo (Lieber et al., 2011), and in fertility, 160

and which was strikingly different from TET2 expression specifically in the stomatal cell lineage 161

(Fig. 3). The duplicated genes TET3 and TET4 also had divergent expression patterns. TET3 was 162

expressed in the SAM precursor cells during embryogenesis (Fig. 2), and in the SAM-organizing 163

center of the seedling (Supplemental Fig. S1A). The TET3-GFP protein moved toward and along 164

the plasma membrane and localized itself at the plasmodesmata (Supplemental Fig. S1B; 165

Supplemental Movie S1), which confirmed previous purification from the Arabidopsis 166

Plasmodesmal Proteome (Fernandez-Calvino et al., 2011). In the primary root, TET3 was 167

expressed in the cortex, endodermis and pericycle at the differentiation zone (Fig. 2). TET4 was 168

expressed in vascular tissue progenitor cells during embryonic development, in the QC and 169

vascular tissue of the primary root (Fig. 2), in stomatal guard cells of cotyledons and anthers, and 170

in the basal region of the flower (Supplemental Fig. S1E; Supplemental Fig. S2A). Similarly, the 171

triplicated genes TET7, TET8 and TET9 had distinct expression patterns. TET7 expression was 172

restricted to the pollen (Supplemental Fig. S2C). TET8 was expressed in the apical domain of the 173

embryo, starting from the heart stage (Fig. 2), in the differentiation zone of the primary root 174

(Fig. 2), in stipules and hydathodes of rosette leaves (Supplemental Fig. S1, F and G). TET9 was 175

expressed in the vascular tissues of the primary root (Fig. 2), cotyledons and rosette leaves, in the 176

SAM, and in trichomes and surrounding pavement cells (Supplemental Fig. S1, J-L). TET11 was 177

only expressed in the pollen (Supplemental Fig. S2C), its duplicated gene, TET12, was expressed 178

in the primary root and stipules (Fig 2; Supplemental Fig. S1M), suggesting a thoroughly 179

diverged function. The triplicated genes TET13, TET14 and TET15 diverged in expression 180

patterns. TET13 was expressed in the embryonal hypophysis, in the QC, stem cells and columella 181

cells of the primary root and the LRP (Fig. 2; Fig. 4, A, E-N). TET14 expression was restricted to 182

vascular precursor cells of heart stage embryos and in the cotyledonary vascular tissues of the 183

mature embryo (Fig. 2). TET15 was expressed in the basal domain of the heart stage embryo, in 184

the LR cap and columella cells (Fig. 2), in the pollen tubes and stomatal guard cells of sepals 185

(Supplemental Fig. S2, B and C). TET16 was only expressed in the basal region of the flower and 186

pollen (Supplemental Fig. S2C), no TET17 gene expression was detected in any of the organs, 187

which was consistent with the absence of gene expression in transcriptome data of 188

Genevestigator or the eFP browser throughout development. Nevertheless, triple nuclear-189



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localized pAtTET17-GFP protein was detected in mature pollen (Boavida et al., 2013). 190

However, overlapping expression patterns were observed in TET genes of different clades in 191

pollen (TET1, TET2, TET3, TET4, TET7, TET8, TET9, TET10, TET11, TET13, TET14, TET15 192

and TET16) (Supplemental Fig. S1C) and in vascular tissues of the embryo and/or the seedling 193

(TET1, TET3, TET4, TET5, TET6, TET8, TET9, TET10, TET12 and TET14) (Fig. 2; 194

Supplemental Fig. S1), suggesting redundancy in function which might complicate functional 195

analysis by mutational approach. T-DNA insertion lines in TET genes were characterized as 196

knock-out or knock-down alleles by qRT-PCR and phenotyping in the respective mutants was 197

done with particular attention to organs in which the respective TET gene was expressed. 198

Strikingly, only in the TET13 knock-out line, tet13-1, a clear phenotype was observed in the 199

primary and lateral root development, which correlated with its site of expression (Supplemental 200

Table S1). Although the single mutant analysis was not exhaustive for putative phenotypes, the 201

identification of a phenotype for only one TET gene argued for functional redundancy amongst 202

the other TET genes and showed the need for double, triple mutant combinations. 203

TET13 Function in Primary Root Growth and Lateral Root Development 204

TET13 expression and mutant phenotypes were studied in more detail during primary and 205

lateral root development. Arabidopsis root identity is specified early during embryogenesis. The 206

cells at the basal region of the globular embryo will give rise to the hypocotyl, primary root and 207

root stem cells. The lens-shaped cells at this region are the progenitors of the QC, which is crucial 208

for maintaining root stem cells identity (van den Berg et al., 1997). In wild-type plants, the stem 209

cells surrounding the QC are maintained in the undifferentiated state. In the primary root, TET13 210

was predominately detected in the QC, most of the stem cells (cortex/endodermis initials, 211

pericycle initials, vascular tissue initials and columella initials, but not epidermis initials), the 212

first two columella cell layers and the two middle cells in the root cap (Fig. 4A). TET13 promoter 213

activity was equally present at the two QC cells of 35 seedlings, indicating that TET13 was not 214

cell cycle-regulated. The function of TET13 in primary root and LR development was studied in 215

the T-DNA insertion line tet13-1 (SALK_011012C), in which the T-DNA is located at the first 216

exon, resulting in a gene knock-out (Boavida et al., 2013). In addition, complementation of root 217

phenotypes was studied in the C1 and C5 complementation lines of tet13-1 containing one and 218

two, T-DNA loci with p35S::TET13, respectively. The primary root length was significantly 219

reduced in tet13-1 (Fig. 4, B and C), partially restored to wild type in the C1 line, and fully 220



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restored and even larger than wild type in the C5 line (Fig. 4C). The primary root length is 221

determined by several parameters such as meristem, elongation zone and differentiation zone 222

size, and cell length at these zones. The meristem size, defined as the number of cells from the 223

QC to the first elongated cell in the cortex cell file (Casamitjana-Martínez et al., 2003) was 224

significantly reduced in tet13-1 (27 ± sd 3 cells) as compared to the wild type (34 ± 4 cells) (Fig. 225

4D, Supplemental Fig. S3A). Below the QC, there are one or two layers of undifferentiated 226

columella initials that generate the differentiated columella cells containing starch that stains 227

purple by Lugol solution. One of the functions of the QC is to keep the surrounding initials in an 228

undifferentiated state because defective QC function results in a differentiated cell layer below 229

the QC instead of the columella initial cell layer (van den Berg et al., 1997, Sarkar et al., 2007). 230

Exogenous auxin (1-naphthaleneacetic acid, NAA) or auxin transport inhibitor (N-1-231

naphthylphthalamic acid, NPA) promoted the differentiation of columella initial cells in wild-type 232

seedlings, but not in mutants in auxin biosynthesis or transport (Ding and Friml, 2010). In tet13-1 233

mutants, one or two columella initial cell layers were measured in primary roots, which is 234

comparable with the wild type, and no precocious differentiation of the columella initials was 235

observed (Supplemental Fig. S3, B and C), hence, columella initial cell identity was maintained 236

in the tet13-1 mutant under normal conditions and after NAA and NPA treatment (Supplemental 237

Fig. S3, D-F). The architecture of the QC and initials was normal in the tet13-1 mutant, as 238

visualized by confocal microscopy with propidium iodide staining (Supplemental Fig. S3G), 239

indicating no function of TET13 in cytokinesis. tet13-1 seedlings were equally insensitive as 240

wild-type seedlings to hydroxyurea, a replication-blocking agent, because no dead cells were 241

observed after propidium iodide staining (Supplemental Fig. S3, H and I). 242

Auxin oscillation in the pericycle of the primary root basal meristem (De Smet et al., 2007) 243

determines the LR founder cell fate, and their anticlinal asymmetric division results in a single-244

layered primordium composed of small daughter cells flanked by two large daughter cells, termed 245

stage I. During LR development, TET13 was active at the two neighboring pericycle cells before 246

the asymmetric division (Fig. 4E). At stage I, the expression was stronger in the two newly 247

generated, small daughter cells (Fig. 4F). From stage II to VII (Fig. 4G-L), anticlinal and 248

periclinal divisions form a dome-shaped primordium with two to seven cell layers. At stage II, 249

TET13 was expressed equally strong in the tip cells at the outer layer (OL), as well as in the 250

middle two cells at the inner layer (IL) (Fig. 4G). From stage III on, TET13 expression was 251



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always stronger in the tip cells at the OL (Fig. 4, H-M) and comparable to that of the pDR5::GUS 252

reporter gene (Benková et al., 2003). At stage VIII, upon LR emergence, TET13 was expressed in 253

the QC and columella (Fig. 4N). 254

Lateral root initiation stages and LR emergence were analyzed in tet13-1 mutants: the number 255

of stage-I LRPs was severely reduced (Fig. 4O), which correlated with early TET13 expression in 256

the pericycle founder cells before the first asymmetric division (Fig. 4E); stage-IV, -V and -VI 257

LRP densities were significantly increased, whereas the number of stage-II, -III and -VII LRP 258

was slightly increased in tet13-1 (Fig. 4O); the emerged LR (EMLR) density was significantly 259

reduced (Fig. 4, O and P). Because the LRP and EMLR densities, defined as the number of LRP 260

and EMLRs per centimeter primary root, were significantly increased and reduced, respectively 261

(Fig. 4O), TET13 has a potential role in restricting LR initiation and promoting LR emergence. 262

The EMLR density in the complementation lines C1 and C5 was restored to wild type (Fig. 4P). 263

In an assay for synchronous LR initiation (Himanen et al., 2002), seedlings were first incubated 264

on medium containing the auxin transport inhibitor NPA, then transferred to NAA medium, after 265

which synchronous LR initiation was monitored. The TET13 promoter activity was induced after 266

2 h of NAA induction at the xylem pole of the pericycle, which coincides with the onset of LRI 267

(Fig. 4Q); after 3 h of NAA induction, two clear blue lines marked the pericycle (Fig. 4Q), which 268

was similar to the pDR5::GUS reporter gene expression pattern (Fig. 4R), indicating that TET13 269

expression is auxin inducible and specific for pericycle cells. In the tet13-1 mutant, the 270

pDR5::GUS reporter gene was not or very weakly expressed at the basal meristem in eight out of 271

thirteen tested seedlings (Fig. 4S), whereas in all eleven wild-type seedlings it was expressed 272

(Fig. 4T), indicating that auxin accumulation in the pericycle founder cells is affected. Hence, the 273

tet13-1 mutant allele and the complementation lines showed that TET13 has a function in the 274

primary root affecting apical meristem size and root length and in lateral root initiation and 275

emergence, which is consistent with its expression sites in the root. 276

TET5 and TET6 Have Redundant Functions in Root and Leaf Growth 277

TET5 and TET6 were the only duplicated genes with similar expression patterns, i.e. in the 278

vascular tissue of all organs, except for embryos, in which only TET5 was expressed (Fig. 1). At 279

the globular stage, TET5 expression was restricted to the vascular tissue progenitor cells (Fig. 1). 280

After germination, both TET5 and TET6 were expressed in the pericycle, the vascular tissues of 281

the primary root starting from the transition zone, the hypocotyl, cotyledons and rosette leaves 282



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(Fig. 5, A and B). Transverse sections of the primary root showed that, at the meristem-elongation 283

transition zone, TET5 and TET6 were expressed in the phloem, a few procambial cells 284

surrounding the phloem and the phloem-pole pericycle, but not in the protoxylem (Fig. 5A, lower 285

panels). At the differentiation zone, they were expressed in the pericycle and all vascular tissues 286

except for the protoxylem (Fig. 5A, upper panels). In the siliques, they were expressed in the 287

funiculus that has a function in guiding the pollen tube to reach the micropyle during fertilization 288

(Supplemental Fig. S2B). The redundant expression patterns suggest redundant functions, which 289

was confirmed by single and double mutant analyses. Several tet5 and tet6 mutant alleles were 290

analysed for their TET5 and TET6 gene expression: tet5-1 (GABI-Kat: 290A02; insert in 291

promoter), is a TET5 knock-down, tet5-2 (SALK_148216, first exon, knock-out; Boavida et al., 292

2013), tet5-3 (SALK_020009C, insert in second exon) is a TET5 knock-out, tet6-1 293

(SALK_005482C, insert in promoter), TET6 upregulated and tet6-2 (SALK_139305, insert in 294

promoter) is a TET6 knock-down (Fig. 5C). No morphological alterations or patterning defects 295

were observed in the roots, leaves or inflorescences of the single mutants tet5-1, tet5-2, tet5-3 and 296

tet6-2. However, morphological analysis of three different double mutant combinations, i.e. tet6-297

2tet5-1 (Supplemental Fig. S4), tet5-2tet6-2 (Supplemental Fig. S4) and tet5-3tet6-2 (Fig. 5E-I), 298

revealed synergistic phenotypes, such as an enlarged leaf size in seedlings at all stages of rosette 299

development (Fig. 5F) due to a significantly increased total number of cells per leaf (23,238 ± 300

2967 in tet5-3tet6-2 compared with 15,495 ± 1635 in tet5-3 and 15,197 ± 2887 in tet6-2, Fig. 301

5G), increased fresh weight in 21-d-old seedlings (Fig. 5H), longer primary roots in a root growth 302

kinetic study (Fig. 5I), confirming redundant functions of TET5 and TET6 in restricting cell 303

proliferation during root and leaf growth. 304

TET Promoter Cis-Regulatory Elements to Predict Responses to Environmental and 305

Developmental Stimuli 306

Cis-regulatory elements (or shortly motifs) were identified in the TET promoter regions using 307

an integrative bioinformatics approach (see Materials and Methods) in order to further study and 308

explain the divergence, overlap and redundancy in TET gene expression. Cis-regulatory elements 309

also provided information about environmental and developmental stimuli that might influence 310

TET gene expression, which could be used for further functional analysis. Apart from mapping 311

known cis-regulatory elements to the 2-kb promoters of the different TET genes, also co-312

regulatory genes, evolutionary sequence conservation and information about open chromatin 313



13

regions (DNaseI-hypersensitive (DH) sites) were integrated to identify cis-regulatory elements 314

and TFs putatively regulating TET genes. Recently, we have shown that combining 315

complementary regulatory data sources has a positive impact on reducing the high number of 316

false positives associated with simple mapping of cis-regulatory elements and strongly increases 317

the likelihood that retained regulatory interactions are biologically functional (Vandepoele et al., 318

2009; Van de Velde et al., 2014). To identify TET cis-regulatory elements shared with co-319

regulated genes, for each TET gene, Genevestigator was first used to identify a set of tissue and 320

perturbation experiments in which the gene was strongly responsive (see Materials and Methods). 321

Next, co-regulated genes were identified under these conditions and enrichment analysis was 322

performed to identify cis-regulatory elements significantly shared between each TET gene and its 323

co-regulated genes, considering the motifs obtained by simple motif mapping, simple motif 324

mappings filtered for DH sites or filtered for evolutionary conservation (indicated with Analysis 325

type ‘motif’, ‘DH’ and ‘CM’ in Supplemental Table S2, respectively). In total, 128 cis-regulatory 326

elements were identified in the TET promoters and their respective co-regulated genes, yielding 327

regulatory information about thirteen TET genes (no result for TET11, TET13, TET16 and 328

TET17). More than half of the regulatory elements (71/128) were identified through the 329

enrichment analysis using the motif mapping files filtered for DH sites or evolutionary 330

conservation, indicating they are functionally related to accessible TF binding sites in open 331

chromatin regions or to regulatory elements that have been conserved during hundreds of 332

millions of years of evolution (Supplemental Table S2). 333

A heat map was generated with TET differential gene expression upon a selection of 334

perturbations in Genevestigator (Supplemental Fig. S5A), and used to verify the cis-regulatory 335

elements in TET promoters identified in Supplemental Table S2. Cis-regulatory elements 336

identified from TET1, TET2, TET3, TET4, TET5, TET6, TET8, TET9, TET16 correlated with their 337

expression patterns or inducible conditions. TET1 up-regulation by high light correlates with the 338

enrichment in the light-regulated gene binding sites, and induction upon brassinolide treatment 339

with a GATA PROMOTER MOTIF (Supplemental Table S2) that can be recognized by GATA 340

family TFs, some of which mediate the cross-talk between brassinosteroid and light signaling 341

pathways (Luo et al., 2010). TET2 promoter elements are mainly related to stress response, 342

including cold, dehydration, and drought response (Supplemental Table S2), and fit with the up-343

regulation of TET2 in response to abscisic acid (ABA), cold and drought (Supplemental Fig. 344



14

S4A), which can induce stomatal closure. TET2 function in the mature stomatal guard cell might 345

relate to stomatal closure caused by stress conditions. TET3 up-regulation by ABA, cold, drought 346

and in the CBF3 overexpression background (Supplemental Fig. S4A) correlates with cold and 347

drought responsive elements and the CBFHB element that is the binding site of CBF3 (CRT/DRE 348

binding factor 3) (Supplemental Table S2), a TF involved in cold response. The TET3 expression 349

pattern in the SAM and the cold response element at the promoter region suggest a function in 350

cold sensing at the SAM or upon floral transition. TET4 is also up-regulated by ABA, cold, 351

drought and in the CBF3 overexpression background (Supplemental Fig. S4A) and correlates 352

with ABA response elements and elements in seed-specific promoters (Supplemental Table S2) 353

(Ezcurra et al., 2000; Chandrasekharan et al., 2003). TET5 and TET6, both expressed in the 354

vascular tissue, contain distinct sugar response promoter elements that suggest a role in sugar 355

sensing and growth (Supplemental Table S2). TET8 and TET9 promoter regions contain defense 356

and pathogen response elements (Supplemental Table S2), which correlate with high up-357

regulation by pathogen and elicitors (Supplemental Fig. S4A); in addition, there are three 358

endosperm-specific elements which fit with TET8 expression in the endosperm (Supplemental 359

Table S2; Supplemental Fig. S1H). One of them is the MYB98 binding site, MYB98 expression is 360

observed in the synergid cells (Kasahara et al., 2005). Presumably TET8 is expressed in the 361

synergid cells as well (Supplemental Fig. S1I). TET16 is 63 times up-regulated during pollen tube 362

growth (Supplemental Fig. S4) and it is expressed specifically in pollen (Supplemental Fig. S2C), 363

suggesting a function in this process. 364

In conclusion, the cis-regulatory element analysis confirmed the divergence in reporter 365

expression of duplicated TET genes. The presence of the same regulatory elements in TET genes 366

of different clades, such as the root-specific element in TET4 and TET10, and the vascular tissue-367

specific element in TET4, TET8, TET9 and TET12 (Supplemental Table S2), supported the 368

redundancy of the reporter expression of TET genes over the different clades. 369

TF-TET Gene Regulatory Network to Predict Function in Molecular Pathways 370

In order to obtain a better understanding of the transcriptional regulation of TETs and their 371

position in molecular pathways, a TF-TET gene regulatory network was built by combining 372

different regulatory datasets. Apart from conserved TF binding sites, also chromatin 373

immunoprecipitation (ChIP) TF binding data and TF expression perturbation information was 374

integrated to generate a TF-TET gene regulatory network (data types denoted as ‘conserved 375



15

motif’, ‘ChIP’ and ‘DE’ in Figure 6, respectively). Although these datasets cover different 376

aspects of gene regulation, it is important to note that the obtained gene regulatory network only 377

offers a partial view on TET regulation, as for many Arabidopsis TFs, no binding site information 378

or experimental data are available. 379

The conservation of cis-regulatory elements has been used to delineate gene regulatory 380

networks in different species (Aerts, 2012) and a recent study in Arabidopsis used a phylogenetic 381

footprinting approach to delineate conserved gene regulatory networks based on known binding 382

sites for 157 TFs (Van de Velde et al., 2014). TF ChIP-Seq and ChIP-chip have been used to 383

identify target genes of different plant regulators, including TFs involved in flowering, circadian 384

rhythm and light signaling, cell cycle and hormone signaling (Mejia-Guerra et al., 2012). To 385

integrate experimental ChIP TF binding information, the network of Heyndrickx and co-workers 386

was used (Heyndrickx et al., 2014), in which 27 publicly available TF-ChIP data sets have been 387

reprocessed through an analysis pipeline consisting of quality control, platform-specific signal 388

processing, and peak calling to generate TF-TET gene interactions. Next to the physical binding 389

of a TF in the vicinity of a TET gene, which can serve as a proxy for TET gene regulation, 390

information about the regulation of a TET gene by a specific TF was also taken into account. 391

Therefore, we screened differentially expressed (DE) genes that were obtained through transcript 392

profiling after perturbation (knock-out or overexpression) of the normal activity of a TF from 15 393

publicly available studies. DE genes from five studies, in which regulatory information about 394

TET genes was reported, were retained, complementing the ChIP binding data for AGL15, BES1, 395

LFY and FUS3 (see Materials and Methods). Most of the TETs were regulated by multiple TFs, 396

i.e. TET3, TET4, TET8, TET9 and TET14. Some duplicated TETs shared common TFs, i.e. TET3 397

and TET4, TET5 and TET6, TET8 and TET9 (Fig. 6). 398

To further validate regulatory interactions in the network, such as those inferred through ChIP 399

and conserved TF binding sites, expression perturbation data from Genevestigator was obtained 400

for nine TFs (AGL15, AP1, PI, EIN3, LFY, PIF4, PIF5, TOC1 and SR1) and TFs-TETs 401

interactions were confirmed by significant differential expression after TF perturbation (Table 1). 402

The TFs in the regulatory networks were related to light response (PIF4, PIF5), circadian clock 403

(TOC1), floral organ identity (AP1, AP2, AP3, SEP3, PI), flowering initiation (AGL15, LFY) 404

and defence response (EIN3, MYB4, SR1) and identify the respective TET genes as novel 405

components of specific developmental or physiological pathways. 406



16

DISCUSSION 407

Arabidopsis TET genes are expressed in different organs/tissues and cell types during 408

embryonic and vegetative development. Intriguingly, the onset of expression coincided with the 409

onset of patterning and cell specification at globular or heart stage embryos (TET1, TET3, TET4, 410

TET5, TET8, TET10, TET13, TET14 and TET15) and in seedlings at the initiation of the stomatal 411

cell lineage (TET2), or at the asymmetric division in the primary root pericycle upon lateral root 412

initiation (TET13), which suggests a role for these TET genes in cell specification. Plant cells are 413

surrounded by a rigid, but dynamic, cell wall, which prevents them from migration during 414

specification, hence, they acquire their fate by positional information from neighboring cells. The 415

cellular communication involves diffusible or actively transported molecules, such as peptides, 416

small RNAs, transcription factors or phytohormones, that upon recognition by competent cells 417

trigger signaling cascades that result in the initiation or repression of specific developmental 418

programs (Sparks et al., 2013). Remarkably, nine TETRASPANINs (TET1, TET3, TET4, TET5, 419

TET8, TET10, TET13, TET14 and TET15) are expressed in embryonic progenitor tissue and three 420

early in cell lineage of the seedling until differentiation (TET2, TET9 and TET13). The expression 421

in the progenitor cells of a cell lineage suggests they might be required in progenitor cell identity 422

establishment or maintenance, or in lateral inhibition of neighboring cells. Their expression later 423

in the differentiated cells of the same cell lineage, suggests a function in the physiology or 424

biochemistry of the mature cells, which might be related or not to its early function. In animals, 425

the same tetraspanin can be expressed in a cell lineage and is required for the expression of the 426

partner protein, whereas the partner protein is expressed more stage-specifically (Shoham et al., 427

2003). Hence, the expression of certain TET genes in plants, very early in a cell lineage until 428

differentiated state, might indicate dynamic interactions in time with partner proteins that are 429

components of different molecular pathways. 430

Most of the duplicated TET genes have diverged expression patterns during the plant’s life 431

cycle, as was demonstrated in the pTET-reporter lines and coincided with different regulatory 432

elements in their promoters (Supplemental Table S2). Even though the duplicated TET5 and 433

TET6 genes showed redundant expression in vascular tissue, different regulatory elements related 434

to sugar sensing were identified in their promoters (Supplemental Table S2). Largely overlapping 435

expression patterns were observed in TET genes over the clades in embryos, primary roots, 436

rosette leaves and pollen, and might refer to the conservation of ancestral TET gene functions in 437



17

specific tissues or cells. Indeed, similar regulatory elements were identified in TET promoters 438

belonging to different clades such as ABA-responsive, root-specific and light-related motifs, 439

which add to putative overlap in function (Supplemental Table S2). So, here, it might be more 440

logical to suggest these paralogous TET genes evolved in their promoter, through sub-441

functionalization (Moore and Purugganan, 2005). 442

These overlaps might explain the mild or undetectable phenotypes in single mutants in our 443

mutational analysis (Supplemental Table S1), and demonstrates the need for making double or 444

triple mutant combinations over the clades to detect phenotypes. Such a strategy was rewarding 445

in animals, resulting in strong phenotypes in mice and Drosophila melanogaster (Fradkin et al., 446

2002; Rubinstein et al., 2006). 447

TET5 and TET6 duplicated genes have the same promoter activity pattern in post-embryonic 448

vascular tissues and in cells surrounding procambial cells and the phloem, suggesting a putative 449

redundant function in vascular bundle activity, such as in nutrient or photoassimilates transport, 450

rather than in patterning, because no venation patterning defect was observed in the double 451

tet5tet6 mutant. Combining the single tet5 and tet6 mutants resulted in a significantly enhanced 452

growth by cell proliferation in root and shoot, suggesting that TET5 and TET6 restrict growth 453

through a sugar-sensing mechanism because such cis-regulatory elements were identified in their 454

promoters (Supplemental Table S2). Indeed, sucrose promotes cell proliferation by activating cell 455

cycle (Riou-Khamlichi et al., 2000). Arabidopsis tetraspanins can form homo- and heterodimers 456

when expressed in yeast (Boavida et al., 2013). The redundant function of TET5 and TET6 457

suggests that for proper activity, heterodimers might need to be formed or interaction with a 458

common protein is required, which needs further testing. 459

TET13 expression in the pericycle founder cells and the gradual spatial pattern in the LRP 460

resembles auxin accumulation and gradients that regulate LR development (Benková et al., 461

2003). TET13 shows overlapping expression in the pericycle with TET3, TET4, TET5, TET6, 462

TET8, TET9, TET10 and TET12, that might explain the mild phenotype in LR development in 463

tet13-1. Significant reduction of stage-I LRP density in tet13-1 indicates that LR initiation is 464

affected and TET13 is required to promote LR initiation. It nicely correlated with TET13-specific 465

expression in the two pericycle founder cells before the asymmetric divisions that precede LR 466

initiation and with its early inducible expression in the xylem-pole pericycle at the root basal 467

meristem upon NAA treatment (Himanen et al., 2002). Significant increase of stage-II to -VII 468



18

LRP densities but reduced EMLR density indicate that the emergence of the LR is also affected 469

in tet13-1, a process that is highly regulated by the transcellular auxin-dependent signaling 470

pathway that results in cell wall remodeling in the adjacent endodermal, cortical and epidermal 471

cells overlaying the primordium (Swarup et al., 2008). Thus, TET13 regulates two different 472

aspects of LR development, restricting LR initiation and promoting LR emergence. 473

Meta-analysis of gene responses to certain perturbations gives a general idea about the gene 474

function in biological processes. However, these responses, as measured through differential 475

expression, could be due to the indirect or secondary regulation. The regulatory elements residing 476

in the promoter regions are primarily responsible for the gene response to the perturbations, 477

because they are the binding sites for the TFs that regulate gene expression. The identification of 478

upstream TFs that bind to these regulatory elements together with other regulatory data sets 479

complemented the inference of TET gene functions and allowed to position TET genes in specific 480

regulatory networks describing flowering time, circadian clock and defense response. Integration 481

of the different expression and regulatory analyses presented in this work suggests function for 482

TET3 in flowering response under low temperature. Indeed, TET3 is expressed in the SAM-483

organizing center progenitor cells in embryos that remain in the seedling. Cold and dehydration 484

response elements are enriched in the TET3 promoter that correlate with up-regulation of TET3 485

gene expression by ABA, cold and drought treatment. The PRR5, AGL15, and PIF4 TFs that 486

regulate TET3 (Fig. 6) have a function in flowering response (Adamczyk et al., 2007; Nakamichi 487

et al., 2007; Kumar et al., 2012), and in the TF genetic perturbation backgrounds, AGL15 and 488

LFY expression levels are negatively correlated with TET3 (Table 1). Thus, the meta-analysis is 489

hypothesis-generating and will be helpful for experimental design in further functional analyses. 490

Our analyses suggest a function for TET8 in defense response. The TET8 gene is up-regulated 491

upon pathogen treatment, which correlated with enrichment of defense response cis-regulatory 492

elements in its promoter. The SR1/CAMTA3, MYB4 and EIN3 TFs that putatively regulate 493

TET8 (Fig. 6) are involved in defense response; SR1 suppresses defense response (Nie et al., 494

2012), MYB4 is a transcriptional repressor that is induced by elicitor FLG22 (Schenke et al., 495

2011), and EIN3 activates downstream immune-responsive genes in an ethylene-dependent way, 496

such as FLS2, which has EIN3 binding sites at the promoter region (Boutrot et al., 2010). TET8 is 497

up-regulated in the loss-of-function sr1 allele and down-regulated in the ein3-1eil1-1 double 498

mutant, indicating that TET8 expression is antagonistically regulated by SR1 and EIN3 in the 499



19

immune signaling pathway. TET8 gene expression was significantly induced by the FLG22 and 500

EF-Tu elicitors that mimicked pathogen infection (Supplemental Fig. S4B), which confirmed the 501

perturbation heat map, the cis-regulatory elements in the promoter region and the TF-TET8 gene 502

regulatory network. 503

In conclusion, combining in planta expression and mutational analyses with meta-analyses on 504

perturbation responses, cis-regulatory element identification, and the construction of a TF-TET 505

regulatory network provided an exciting novel and integrated approach, revealing already the 506

function of a few plant tetraspanins and enabling the functional prediction of many more TET 507

genes in future work. 508

MATERIALS AND METHODS 509

Plant Materials and Growth Conditions 510

The mutant lines tet5-1 (GABI-Kat: 290A02), tet5-2 (SALK_148216), tet5-3 511

(SALK_020009C), tet6-1 (SALK_005482C), tet6-2 (SALK_139305) and tet13-1 512

(SALK_011012C) were obtained from Arabidopsis GABI-Kat (http://www.gabi-kat.de/) and the 513

European Arabidopsis Stock Centre (http://www.arabidopsis.org/), respectively. The presence of 514

the T-DNA was confirmed by PCR with a T-DNA-specific and gene-specific primers 515

(Supplemental Table S3). 516

Seeds were germinated on Murashige and Skoog medium supplemented with 1% (w/v) 517

sucrose, 0.8% (w/v) agarose, pH 5.7. Seeds were surface sterilized and stratified at 4°C for two 518

nights and moved to the growth chamber. For pAtTET::NLS-GFP/GUS lines, 6-day-old seedlings 519

grown vertically at 21°C under 24-h light conditions (75~100 µmol m-2 s-1) were used for SAM 520

and root analysis; 14-day-old seedlings corresponding to the growth stage 1.04 (Boyes et al., 521

2001) and grown horizontally at 21°C under 16-h light/ 8-h dark conditions were used for 522

cotyledon, emerging leaf 1, 2, 3 and 4 primordia analysis; 6-w-old plants grown in the soil at 523

21°C under 16-h light/ 8-h dark conditions were used for analysis of inflorescences, different 524

stages of flowers, siliques and embryos. 525

Promoter and Open Reading Frame Cloning, Construction of Expression Vectors and Plant 526

Transformation 527

Promoter sequences, defined as intergenic regions with sizes ranging between 396 and 3400 528



20

bp, and open reading frame sequences were amplified from the Arabidopsis thaliana genome 529

with primers listed in Supplemental Table S2 and cloned into the entry vectors using BP clonase 530

(Invitrogen) to generate the entry clone. 531

For complementation of tet13-1, full-length genomic DNA of AtTET13 was amplified with 532

primers listed in Supplemental Table S3 and cloned into the entry vectors using BP clonase 533

(Invitrogen) to generate the entry clone. The expression clones were constructed by LR clonase 534

(Invitrogen) with the entry clone and the destination vectors pMK7S*NFm14GW (pAtTET1-535

17::NLS-GFP/GUS), pK7FWG2 (p35S::TET3:GFP) and pB2GW7 (p35S::TET13) (Karimi et al., 536

2007). The plasmids were transferred into Agrobacterium tumefaciens pMP90 cells. All 537

constructs were transferred into Arabidopsis ecotype Columbia-0 (Col-0) or tet13-1 by floral dip 538

transformation. 25 mg transgenic seeds of the T1 generation was used for high-density plating on 539

50 mg/L kanamycin (pAtTET1-17::NLS-GFP/GUS and p35S::TET3:GFP) or 7.5 mg/L DL-540

phosphinothricin (Duchefa) (complementation of tet13-1 with p35S::TET13). The resistant 541

seedlings were transferred into soil for T2 generation seed harvest. 542

For pAtTET1-17::NLS-GFP/GUS reporter lines, the number of T-DNA loci was analyzed in 7 543

to 35 T2 populations per construct after germination on kanamycin, three lines per construct with 544

a single-locus insertion were analyzed by X-Gluc histochemical staining to score the promoter 545

activity during development. For the complementation analysis of tet13-1, T2 seedlings of lines 546

C1 and C5 containing one and two T-DNA loci with p35S::TET13, respectively, were genotyped 547

for the presence of the p35S::TET13 T-DNA using bar primers (Supplemental Table S3), and 548

used for primary root growth and emerged lateral root density measurements. 549

Histochemical, Histological and Phenotypic Analyses and Statistical Tests 550

The 5-bromo-4-chloro-3-indolyl-β-D-glucuronide (X-Gluc) assay was performed as described 551

previously (Coussens et al., 2012). Ovules were cleared overnight in an 8: 2: 1 (g: mL: mL) 552

mixture of chloral hydrate: distilled water: glycerol and mounted on the microscope slides with 553

the same solution (Grini et al., 2002). For the LRP staging and a better visualization of the TET13 554

expression pattern in the LRP, the samples were treated as described previously with some 555

modifications (Malamy and Benfey, 1997). Both fresh and stained samples were fixed in 70% 556

ethanol overnight and transferred into 4% HCl, 20% methanol and incubated at 62°C for 40 min 557

in 7% NaOH and 60% ethanol at room temperature for 15 minutes. The samples were then 558

rehydrated for 10 min in either 60%, 40%, 20% or 10% ethanol at room temperature. Finally, the 559



21

samples were infiltrated in 25% glycerol and 5% ethanol for 10 min and mounted with 50% 560

glycerol. The root meristem size was determined as the number of cells in the cortex cell file 561

from the QC to the first elongated cell (Casamitjana-Martínez et al., 2003). The samples were 562

mounted with 50% lactic acid and observed immediately. For the hydroxyurea, NAA and NPA 563

treatment, 5-d-old seedlings were transferred onto the MS medium supplemented for 24 h with 564

1 mM hydroxyurea, 1 µM NAA or 1 µM NPA, respectively. Seedlings treated with hydroxyurea 565

were counterstained with propidium iodide (PI) and observed with a confocal microscope. 566

Seedlings treated with NAA or NPA were also treated for 1 min with Lugol solution to stain the 567

starch granules, mounted with chloral hydrate and checked immediately with microscope. 568

For the epidermal cell imaging, leaves were fixed in 100% ethanol overnight and mounted with 569

90% lactic acid. The leaf area was measured with the ImageJ software (http://rsbweb.nih.gov/ij/). 570

The epidermal cells on the abaxial side were drawn with a DMLB microscope equipped with a 571

drawing tube and differential interference contrast objectives. The total number of cells per leaf 572

was determined as described previously (De Veylder et al., 2001). 573

All samples were imaged with a binocular Leica microscope or an Olympus DIC-BX51 574

microscope. The confocal images were taken with an Olympus Fluo View FV1000 microscope or 575

Zeiss LSM5 Exiter confocal. The fluorescence was detected after a 488 nm (GFP), 543 nm (PI) 576

or 514 nm (FM4-64) excitation and an emission of 495-520 nm for GFP, 590-620 nm for PI and 577

600-700 nm for FM4-64. Transverse section was done according to De Smet et al. (2004). 578

Means between samples were compared by a two-tailed Student’s t-test, an f-test was assessed 579

for the equality between population variances. 580

Elicitor Treatment 581

EF-Tu and FLG22 were synthesized and purchased from GenScript 582

(http://www.genscript.com). Col-0 plant samples were grown on MS medium for 16 days and 583

transferred into liquid MS medium supplemented with EF-Tu or FLG22 at the final concentration 584

of 1 µM for 2 h on an orbital shaker. 585

Quantitative Real-Time PCR Analysis 586

Total RNA was prepared with the RNeasy kit (QIAGEN). One µg RNA was used as template 587

to synthesize cDNA with the iScript cDNA synthesis Kit (Bio-Rad). The expression level was 588

analyzed on a LightCycler 480 apparatus (Roche) with SYBR Green and all reactions were 589



22

performed in three technical replicates. Expression levels were normalized to reference genes 590

PP2A and UBC. 591

Cis-Regulatory Element Analysis 592

Known TF binding sites and DNA motifs were mapped on the 2-kb upstream sequence for all 593

genes and for all included species using DNA-pattern allowing no mismatches (Thomas-Chollier 594

et al., 2008). 692 cis-regulatory elements were obtained from AGRIS (Davuluri et al., 2003), 595

PLACE (Higo et al., 1999) and Athamap (Steffens et al., 2004). In addition, 44 positional count 596

matrices were obtained from Athamap and for 15 TFs, positional count matrices were obtained 597

from ChIP-Seq data (Heyndrickx et al., 2014). Positional count matrices were mapped genome-598

wide using MatrixScan using a p-value cut-off <1e-05 (Thomas-Chollier et al., 2008). In order to 599

reduce the high false-positive rates associated with interfering regulatory interactions based on 600

simple motif mapping, two types of filtering were used. A first approach to enrich for functional 601

interactions consisted of filtering motif matches using cross-species sequence conservation or 602

open chromatin regions. Therefore, motif matches were filtered using conserved non-coding 603

sequences (Van de Velde et al., 2014) and DNaseI hypersensitive (DH) sites. The DH sites were 604

downloaded from the NCBI SRA database (accession ID SRP009678) (Zhang et al., 2012). A 605

second approach started from tightly co-regulated genes to identify co-regulatory motifs or TF 606

binding sites. For each TET gene, motif mapping information was combined with a set of co-607

regulated genes from Genevestigator. In the “perturbations tool”, the perturbations under which 608

TET genes were two times up-regulated (p-value < 0.05) were selected to create new sample sets. 609

Then, in the “co-expression tool”, the top 200 positively correlated genes under the categories 610

“anatomy” and “perturbations” were selected. The overlapping genes were defined as “co-611

regulated” genes. Only motifs present in the upstream or downstream TET sequence and showing 612

significant enrichment in the co-regulation cluster were retained. Motif enrichment was 613

determined using the hypergeometric distribution using false discovery rate correction. Only 614

significantly (p-value < 0.05) enriched motifs were retained. 615

Gene Regulatory Network Inference 616

The gene regulatory networks based on conserved non-coding sequences from Van de Velde et 617

al. (2014) and on TF-ChIP data from Heyndrickx et al. (2014) were filtered for TET target genes. 618

For TFs with ChIP data, DE genes after TF perturbation were also included for AT5G13790 619



23

(AGL15) (Zheng et al., 2009), AT1G19350 (BES1) (Yu et al., 2011), AT5G61850 (LFY) (Schmid 620

et al., 2003) and AT3G26790 (FUS3) (Yamamoto et al., 2010; Lumba et al., 2012). For other TFs, 621

DE genes after TF perturbation were obtained through Genevestigator. 622

GO Enrichment 623

GO enrichment was performed using the hypergeometric distribution with Bonferroni 624

correction. 625

Supplemental Data 626

The following supplemental materials are available. 627

Supplemental Figure S1. TET expression in seedlings, seeds and TET3 protein localization. 628

Supplemental Figure S2. TET expression in flower organs. 629

Supplemental Figure S3. tet13-1 primary root morphology. 630

Supplemental Figure S4. tet5 and tet6 single and double mutant phenotypes in other alleles 631

Supplemental Figure S5. Heat map of TET response to different perturbations and TET8 632

expression levels after elicitors treatment. 633

Supplemental Table S1. tet mutants collected in this study. 634

Supplemental Table S2. TET cis-regulatory element information. 635

Supplemental Table S3. Primers used in the study. 636

Supplemental Movie S1. TET3-GFP movement on the plasma membrane. 637

ACKNOWLEDGMENTS 638

The authors would like to thank Annick Bleys for help in preparing the manuscript, Matyas 639

Fendrych for help in confocal imaging, Carina Braeckman for plant transformation. 640

641

AUTHOR CONTRIBUTIONS 642

FW designed, performed and interpreted experiments, wrote the manuscript; AM, PN performed 643

experiments, JVdV and KVDP designed, performed and interpreted the bioinformatic analyses, 644

wrote the manuscript; KH designed and interpreted experiments; MVL designed the project and 645

experimental approach, coordinated the work, wrote the manuscript. 646

647

648



24

FIGURE LEGENDS 649

650

Figure 1. Schematic overview of TET expression patterns in different organs. Duplicated gene 651

pairs are indicated with square brackets (The length of the square brackets does not represent the 652

evolutionary distance). E: embryo; R: root; m: primary root meristem and root tip; d: primary 653

root differentiation zone; lrp: lateral root primordia; C: cotyledon; L: rosette leaf; F: flower; se: 654

sepal; pe: petal; st: stamen; ca: carpel. 655

656

Figure 2. TET expression patterns during embryogenesis and in the primary root meristem after 657

germination. Transgenic plants shown are: pAtTET1::NLS-GFP/GUS, pAtTET3::NLS-GFP/GUS, 658

pAtTET4::NLS-GFP/GUS, pAtTET5::NLS-GFP/GUS, pAtTET8::NLS-GFP/GUS, 659

pAtTET10::NLS-GFP/GUS, pAtTET13::NLS-GFP/GUS, pAtTET14::NLS-GFP/GUS, and 660

pAtTET15::NLS-GFP/GUS. Columns represent consecutive developmental stages: globular, 661

heart, torpedo and mature. Dotted lines delineate the outlines of the young embryos. Arrows in 662

TET1, TET3 and TET14 panels indicate gene expression sites. Scale bars represent 0.01 mm 663

(globular, heart and torpedo stages), 0.1 mm (mature embryo and root meristem). 664

665

Figure 3. Diagram of Arabidopsis stomatal development (left) and the respective TET2 666

expression patterns at the abaxial epidermis of 6-d-old cotyledons of the pAtTET2::NLS-667

GFP/GUS line (right). A, TET2 expression in the meristemoid after entry division. B and C, 668

TET2 expression in the meristemoid after one or two additional asymmetric divisions. The arrow 669

indicates the meristemoid. D and E, TET2 expression in the GMC and the mature guard cells, 670

respectively. Cells in different colors are: MMC, gray; meristemoid, blue; SLGC, white; GMC, 671

red; guard cell, green; pavement cell, light green. Scale bars represent 0.01 mm. 672

673

Figure 4. TET13 expression in the primary root and LRP, tet13-1 root phenotypes and 674

complementation. Transgenic plants shown are: pAtTET13::NLS-GFP/GUS (A, E-N and Q), 675

tet13-1 (B, C, D, O, P)C1 and C5 (tet13-1 containing one, respectively two T-DNA loci with 676

p35S::TET13) (C, P), pDR5::GUS (R and T) and tet13-1xpDR5::GUS (S). A, TET13 expression 677

in the primary root tip. B, tet13-1 scheme, 12-d-old seedlings of Col-0 and tet13-1 growing 678

vertically under 24-h light condition. C, Primary root growth kinetics. Means are presented ± sd 679



25

(n=22-33). Asterisks mark significant differences: *p < 0.05, **p < 0.01 and ***p < 0.001. D, 680

Root meristem size (defined as the number of RM cells) of 6-d-old seedlings. Means are 681

presented ± sd (n=28-39). E-N, Detailed expression analysis of TET13 at different stages during 682

LR development. Corresponding developmental stages I-VII and EMLR are indicated in the top 683

right corner. IL and OL: inner and outer layers, respectively; ep: epidermis; c: cortex; en: 684

endodermis; p: pericycle. Arrowheads indicate the division planes. Inset in I shows the top view 685

of stage IV. O, Staging of LRP and EMLR densities. Means are presented ± sd (n=20). P, EMLR 686

densities. Means are presented ± sd (n=22-33). ns, not significant. Asterisks mark significant 687

differences: *p < 0.05, **p < 0.01 and ***p < 0.001. Q and R, NAA-induced TET13 (Q) and 688

pDR5::GUS (R) expression. The seedlings were grown on 10 µM NPA medium for 72 h after 689

germination and then transferred to 10 µM NAA medium for 0 h, 2 h and 3 h. S and T, 690

DR5::GUS expression patterns at the root basal meristem in 7-d-old tet13-1xpDR5::GUS (S) and 691

wild-type (T) seedlings. Q-T, black arrowheads indicate sites of inducible expression. Scale bars 692

represent 0.01 mm (E-N), 0.1 mm (S and T), 0.5 mm (Q and R). 693

694

Figure 5. TET5 and TET6 expression, and tet5-3, tet6-2 and tet5-3tet6-2 mutant phenotypes. 695

Transgenic plants shown are: pAtTET5::NLS-GFP/GUS, pAtTET6::NLS-GFP/GUS, tet5-3, tet6-2 696

and tet5-3tet6-2. A, TET5 and TET6 expression in the vascular tissue of the meristem-elongation 697

transition zone (between dotted lines) and the differentiation zone (upper) of the primary root. 698

Transverse sections show the transition zone and differentiation zone, as indicated by the dashed 699

lines. ep: epidermis; c: cortex; e: endodermis; p: pericycle. Arrowheads and arrows indicate 700

phloem-pole, pericycle and protoxylem, respectively. B, TET5 and TET6 expression in the rosette 701

leaves. C, TET5 and TET6 schemes with T-DNA insertions. Bold, thin and breaking lines indicate 702

exons, introns and promoter, respectively. D, Relative TET5 (right) and TET6 (left) transcript 703

level in 7-d-old seedlings measured by qRT-PCR. Means are presented ± sd (n=3). E, Rosette and 704

leaf series of 21-d-old seedlings. From left to right are leaf 1 to leaf 8, incisions were made to 705

make the leaves fully expanded when necessary. F, Quantification of rosette leaf size in E. Means 706

are presented ± sd (n=8-10). G, Total number of cells per leaf. Leaf 1 and/or 2 were used. Means 707

are presented ± sd (n=3). H, Fresh weight of 21-d-old seedlings. Only rosette leaves were used 708

for the experiment. I, Primary root growth kinetics (root length). Means are presented ± sd (n=31-709

39). Asterisks in all graphs mark significant differences: *p < 0.05, **p < 0.01 and ***p < 0.001. 710



26

Scale bars represent 0.01 mm (A, transverse section), 0.1 mm (A, longitudinal section), and 1 mm 711

(B). 712

713

Figure 6. TF-TET gene regulatory network. Nodes and arrows depict genes and regulatory 714

interactions, yellow and gray rounded rectangles are TFs and TETs, respectively. The arrows do 715

not represent any positive or negative regulation between the TFs and TETs. Regulation identified 716

by ChIP-Seq and conserved binding motif are shown with doubled lines and solid lines, 717

respectively. Differentially expressed regulation is shown with dashed lines. AGL15: 718

AGAMOUS-LIKE 15, AP1: APETALA1, AP2: APETALA2, AP3: APETALA3, ATAF2: 719

ARABIDOPSIS NAC DOMAIN CONTAINING PROTEIN 81, BES1: BRI1-EMS-720

SUPPRESSOR 1, EIN3: ETHYLENE-INSENSITIVE 3, ERF115: ETHYLENE RESPONSE 721

FACTOR 115, FHY3: FAR-RED ELONGATED HYPOCOTYLS 3, GL3: GLABRA3, LFY: 722

LEAFY, MYB4: MYB DOMAIN PROTEIN 4, PI: PISTILLATA, PIF4: PHYTOCHROME 723

INTERACTING FACTOR 4, PIF5: PHYTOCHROME INTERACTING FACTOR 5, PRR5: 724

PSEUDO-RESPONSE REGULATOR 5, SEP3: SEPALLATA3, SR1/CAMTA3: SIGNAL 725

RESPONSIVE 1/CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3, TOC1: 726

TIMING OF CAB EXPRESSION 1. 727

728



27

TABLE 729

Table 1. TETs transcript changes upon TF perturbation. Genevestigator microarray studies on 730

genotypes perturbed for the TFs identified in Figure 5 were analyzed for differential TET 731

transcript levels at p-value < 0.05. In double mutant and amiRNA backgrounds, only the TFs of 732

interest were listed. Fold-change was calculated from Log(2)-ratio, DE, differentially expressed. 733

"-" and "+" represent down-regulation and up-regulation, respectively. *, data were obtained from 734

the same studies in Figure 6. 735

Genotype DE TF fold-change DE TF p-value DE TET fold-change

DE TET p-value

agl15-4agl18-1/Col* AGL15 -3.77 <0.001

TET3 +1.35 0.03 TET4 +1.66 <0.001 TET5 +1.17 0.207 TET6 +1.33 0.039 TET8 +1.80 0.019 TET9 +2.17 <0.001 TET11 +1.18 0.107

35S::amiR-mads-2(MIR319a)_strong/Col-0

AP1 -5.24 <0.001 TET4 -1.18 0.051 TET14 -1.04 0.71

PI -1.95 0.004 TET3 -1.77 0.054 TET4 -1.18 0.051 TET14 -1.04 0.71

ein3-1eil1-1/coi1-2 EIN3 -9.53 0.003 TET8 -1.40 0.049 35S:LFY-GR/Ler LFY +36.58 <0.001 TET3 -1.19 0.002 lfy-12/Col-0* (shoot apex, rosette is 50% of final size) LFY -3.33 0.007 TET3 +1.63 0.006

lfy-12/Col-0* (inflorescence, first flower open) LFY -1.82 0.006 TET3 +1.80 0.018

pif4-101pif5-3/Col-0 PIF4, PIF5 -1.04, -70.1 0.746, <0.001

TET3 -1.28 0.008 TET14 +1.24 0.064

Alc::TOC1/Col-0 TOC1 +8.59 <0.001 TET8 -1.17 0.013 camta3-2/Col-0 SR1 -5.61 0.003 TET8 +1.88 0.027

736

737



28

LITERATURE CITED 738

Adamczyk BJ, Lehti-Shiu MD, Fernandez DE (2007) The MADS domain factors AGL15 and 739

AGL18 act redundantly as repressors of the floral transition in Arabidopsis. Plant J 50: 740

1007-1019 741

Aerts S (2012) Computational strategies for the genome-wide identification of cis-regulatory 742

elements and transcriptional targets. Curr Top Dev Biol 98: 121-145 743

Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) 744

Local, efflux-dependent auxin gradients as a common module for plant organ formation. 745

Cell 115: 591-602 746

Boavida LC, Qin P, Broz M, Becker JD, McCormick S (2013) Arabidopsis tetraspanins are 747

confined to discrete expression domains and cell types in reproductive tissues and form 748

homo- and hetero-dimers when expressed in yeast. Plant Physiol 163: 696-712 749

Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP (2010) Direct 750

transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-751

dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA 107: 14502-752

14507 753

Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) 754

Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput 755

functional genomics in plants. Plant Cell 13: 1499-1510 756

Casamitjana-Martínez E, Hofhuis HF, Xu J, Liu C-M, Heidstra R, Scheres B (2003) Root-757

specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway 758

in the control of Arabidopsis root meristem maintenance. Curr Biol 13: 1435-1441 759

Chandrasekharan MB, Bishop KJ, Hall TC (2003) Module-specific regulation of the β-760

phaseolin promoter during embryogenesis. Plant J 33: 853-866 761

Chiu W-H, Chandler J, Cnops G, Van Lijsebettens M, Werr W (2007) Mutations in the 762

TORNADO2 gene affect cellular decisions in the peripheral zone of the shoot apical 763

meristem of Arabidopsis thaliana. Plant Mol Biol 63: 731-744 764

Cnops G, Neyt P, Raes J, Petrarulo M, Nelissen H, Malenica N, Luschnig C, Tietz O, 765

Ditengou F, Palme K, et al (2006) The TORNADO1 and TORNADO2 genes function in 766

several patterning processes during early leaf development in Arabidopsis thaliana. Plant 767



29

Cell 18: 852-866 768

Cnops G, Wang X, Linstead P, Van Montagu M, Van Lijsebettens M, Dolan L (2000) 769

TORNADO1 and TORNADO2 are required for the specification of radial and 770

circumferential pattern in the Arabidopsis root. Development 127: 3385-3394 771

Coussens G, Aesaert S, Verelst W, Demeulenaere M, De Buck S, Njuguna E, Inzé D, Van 772

Lijsebettens M (2012) Brachypodium distachyon promoters as efficient building blocks 773

for transgenic research in maize. J Exp Bot 63: 4263-4273 774

Davuluri RV, Sun H, Palaniswamy SK, Matthews N, Molina C, Kurtz M, Grotewold E 775

(2003) AGRIS: Arabidopsis Gene Regulatory Information Server, an information resource 776

of Arabidopsis cis-regulatory elements and transcription factors. BMC Bioinformatics 4: 777

25 778

De Rybel B, Möller B, Yoshida S, Grabowicz I, de Reuille PB, Boeren S, Smith RS, Borst 779

JW, Weijers D (2013) A bHLH complex controls embryonic vascular tissue 780

establishment and indeterminate growth in Arabidopsis. Dev Cell 24: 426-437 781

De Smet I, Chaerle P, Vanneste S, De Rycke R, Inzé D, BeeckMan T (2004) An easy and 782

versatile embedding method for transverse sections. J Microsc 213: 76-80 783

De Smet I, Tetsumura T, De Rybel B, Frei dit Frey N, Laplaze L, Casimiro I, Swarup R, 784

Naudts M, Vanneste S, Audenaert D, et al (2007) Auxin-dependent regulation of lateral 785

root positioning in the basal meristem of Arabidopsis. Development 134: 681-690 786

De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren 787

E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase 788

inhibitors of Arabidopsis. Plant Cell 13: 1653-1668 789

Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc 790

Natl Acad Sci USA 107: 12046-12051 791

Ezcurra I, Wycliffe P, Nehlin L, Ellerström M, Rask L (2000) Transactivation of the Brassica 792

napus napin promoter by ABI3 requires interaction of the conserved B2 and B3 domains 793

of ABI3 with different cis-elements: B2 mediates activation through an ABRE, whereas 794

B3 interacts with an RY/G-box. Plant J 24: 57-66 795

Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, 796

Maule A (2011) Arabidopsis plasmodesmal proteome. PLoS ONE 6: e18880 797

Fradkin LG, Kamphorst JT, DiAntonio A, Goodman CS, Noordermeer JN (2002) 798



30

Genomewide analysis of the Drosophila tetraspanins reveals a subset with similar 799

function in the formation of the embryonic synapse. Proc Natl Acad Sci USA 99: 13663-800

13668 801

Goldberg AFX (2006) Role of peripherin/rds in vertebrate photoreceptor architecture and 802

inherited retinal degenerations. Int Rev Cytol 253: 131-175 803

Grini PE, Jürgens G, Hülskamp M (2002) Embryo and endosperm development is disrupted in 804

the female gametophytic capulet mutants of Arabidopsis. Genetics 162: 1911-1925 805

Heyndrickx KS, Van de Velde J, Wang C, Weigel D, Vandepoele K (2014) A functional and 806

evolutionary perspective on transcription factor binding in Arabidopsis thaliana. Plant 807

Cell 26: 3894-3910 808

Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements 809

(PLACE) database: 1999. Nucleic Acids Res 27: 297-300 810

Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T (2002) 811

Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14: 812

2339-2351 813

Huang S, Yuan S, Dong M, Su J, Yu C, Shen Y, Xie X, Yu Y, Yu X, Chen S, et al (2005) The 814

phylogenetic analysis of tetraspanins projects the evolution of cell-cell interactions from 815

unicellular to multicellular organisms. Genomics 86: 674-684 816

Kaji K, Oda S, Miyazaki S, Kudo A (2002) Infertility of CD9-deficient mouse eggs is reversed 817

by mouse CD9, human CD9, or mouse CD81; polyadenylated mRNA injection developed 818

for molecular analysis of sperm-egg fusion. Dev Biol 247: 327-334 819

Karimi M, Bleys A, Vanderhaeghen R, Hilson P (2007) Building blocks for plant gene 820

assembly. Plant Physiol 145: 1183-1191 821

Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN (2005) MYB98 822

is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant 823

Cell 17: 2981-2992 824

Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane 825

protein topology with a hidden Markov model: application to complete genomes. J Mol 826

Biol 305: 567-580 827

Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, Wigge PA (2012) 828

Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484: 829



31

242-245 830

Lieber D, Lora J, Schrempp S, Lenhard M, Laux T (2011) Arabidopsis WIH1 and WIH2 831

genes act in the transition from somatic to reproductive cell fate. Curr Biol 21: 1009-1017 832

Lumba S, Tsuchiya Y, Delmas F, Hezky J, Provart NJ, Shi Lu Q, McCourt P, Gazzarrini S 833

(2012) The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions 834

by negatively modulating ethylene-regulated gene expression in Arabidopsis. BMC Biol 835

10: 8 836

Luo X-M, Lin W-H, Zhu S, Zhu J-Y, Sun Y, Fan X-Y, Cheng M, Hao Y, Oh E, Tian M, et al 837

(2010) Integration of light- and brassinosteroid-signaling pathways by a GATA 838

transcription factor in Arabidopsis. Dev Cell 19: 872-883 839

Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of 840

Arabidopsis thaliana. Development 124: 33-44 841

Mejia-Guerra MK, Pomeranz M, Morohashi K, Grotewold E (2012) From plant gene 842

regulatory grids to network dynamics. Biochim Biophys Acta - Gene Regul Mech 1819: 843

454-465 844

Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr 845

Opin Plant Biol 8: 122-128 846

Murray JAH, Jones A, Godin C, Traas J (2012) Systems analysis of shoot apical meristem 847

growth and development: integrating hormonal and mechanical signaling. Plant Cell 24: 848

3907-3919 849

Nakamichi N, Kita M, Niinuma K, Ito S, Yamashino T, Mizoguchi T, Mizuno T (2007) 850

Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 and PRR5 851

coordinately and positively regulate flowering time through the canonical CONSTANS-852

dependent photoperiodic pathway. Plant Cell Physiol 48: 822-832 853

Nie H, Zhao C, Wu G, Wu Y, Chen Y, Tang D (2012) SR1, a calmodulin-binding transcription 854

factor, modulates plant defense and ethylene-induced senescence by directly regulating 855

NDR1 and EIN3. Plant Physiol 158: 1847-1859 856

Perilli S, Di Mambro R, Sabatini S (2012) Growth and development of the root apical 857

meristem. Curr Opin Plant Biol 15: 17–23 858

Riou-Khamlichi C, Menges M, Healy JMS, Murray JAH (2000) Sugar control of the plant 859

cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell 860



32

Biol 20: 4513-4521 861

Rubinstein E, Ziyyat A, Prenant M, Wrobel E, Wolf J-P, Levy S, Le Naour F, Boucheix C 862

(2006) Reduced fertility of female mice lacking CD81. Dev Biol 290: 351-358 863

Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, 864

Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana 865

shoot and root stem cell organizers. Nature 446: 811-814 866

Schenke D, Böttcher C, Scheel D (2011) Crosstalk between abiotic ultraviolet-B stress and 867

biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of 868

pathogen defence compound production. Plant, Cell and Environment 34: 1849-1864 869

Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) 870

Dissection of floral induction pathways using global expression analysis. Development 871

130: 6001-6012 872

Shoham T, Rajapaksa R, Boucheix C, Rubinstein E, Poe JC, Tedder TF, Levy S (2003) The 873

tetraspanin CD81 regulates the expression of CD19 during B cell development in a 874

postendoplasmic reticulum compartment. J Immunol 171: 4062-4072 875

Sparks E, Wachsman G, Benfey PN (2013) Spatiotemporal signalling in plant development. Nat 876

Rev Genet 14: 631-644 877

Steffens NO, Galuschka C, Schindler M, Bülow L, Hehl R (2004) AthaMap: an online 878

resource for in silico transcription factor binding sites in the Arabidopsis thaliana 879

genome. Nucleic Acids Res 32: D368-D372 880

Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet 881

I, Vanneste S, et al (2008) The auxin influx carrier LAX3 promotes lateral root 882

emergence. Nat Cell Biol 10: 946-954 883

Thomas-Chollier M, Sand O, Turatsinze J-V, Janky R, Defrance M, Vervisch E, Brohée S, 884

van Helden J (2008) RSAT: regulatory sequence analysis tools. Nucleic Acids Res 36: 885

W119-W127 886

Van de Velde J, Heyndrickx KS, Vandepoele K (2014) Inference of transcriptional networks in 887

Arabidopsis through conserved noncoding sequence analysis. Plant Cell 26: 2729-2745 888

van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control 889

of cell differentiation in the Arabidopsis root meristem. Nature 390: 287-289 890

Vandepoele K, Quimbaya M, Casneuf T, De Veylder L, Van de Peer Y (2009) Unraveling 891



33

transcriptional control in Arabidopsis using cis-regulatory elements and coexpression 892

networks. Plant Physiol 150: 535-546 893

Wang F, Vandepoele K, Van Lijsebettens M (2012) Tetraspanin genes in plants. Plant Sci 190: 894

9-15 895

Yamamoto A, Kagaya Y, Usui H, Hobo T, Takeda S, Hattori T (2010) Diverse roles and 896

mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 897

revealed by microarray analysis. Plant Cell Physiol 51: 2031-2046 898

Yáñez-Mó M, Barreiro O, Gordon-Alonso M, Sala-Valdés M, Sánchez-Madrid F (2009) 899

Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends 900

Cell Biol 19: 434-446 901

Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, et al 902

(2011) A brassinosteroid transcriptional network revealed by genome-wide identification 903

of BESI target genes in Arabidopsis thaliana. Plant J 65: 634-646 904

Zhang W, Zhang T, Wu Y, Jiang J (2012) Genome-wide identification of regulatory DNA 905

elements and protein-binding footprints using signatures of open chromatin in 906

Arabidopsis. Plant Cell 24: 2719-2731 907

Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of 908

the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21: 2563-2577 909

910



1

Figure 1. Schematic overview of TET expression patterns in different organs. Duplicated

gene pairs are indicated with square brackets (The length of the square brackets does not

represent the evolutionary distance). E: embryo; R: root; m: primary root meristem and root

tip; d: primary root differentiation zone; lrp: lateral root primordia; C: cotyledon; L: rosette

leaf; F: flower; se: sepal; pe: petal; st: stamen; ca: carpel.



1

Figure 2. TET expression patterns during embryogenesis and in the primary root meristem

after germination. Transgenic plants shown are: pAtTET1::NLS-GFP/GUS, pAtTET3::NLS-

GFP/GUS, pAtTET4::NLS-GFP/GUS, pAtTET5::NLS-GFP/GUS, pAtTET8::NLS-GFP/GUS,



2

pAtTET10::NLS-GFP/GUS, pAtTET13::NLS-GFP/GUS, pAtTET14::NLS-GFP/GUS, and

pAtTET15::NLS-GFP/GUS. Columns represent consecutive developmental stages: globular,

heart, torpedo and mature. Dotted lines delineate the outlines of the young embryos. Arrows

in TET1, TET3 and TET14 panels indicate gene expression sites. Scale bars represent

0.01 mm (globular, heart and torpedo stages), 0.1 mm (mature embryo and root meristem).



1

Figure 3. Diagram of Arabidopsis stomatal development (left) and the respective TET2

expression patterns at the abaxial epidermis of 6-d-old cotyledons of the pAtTET2::NLS-



2

GFP/GUS line (right). A, TET2 expression in the meristemoid after entry division. B and C,

TET2 expression in the meristemoid after one or two additional asymmetric divisions. The

arrow indicates the meristemoid. D and E, TET2 expression in the GMC and the mature guard

cells, respectively. Cells in different colors are: MMC, gray; meristemoid, blue; SLGC, white;

GMC, red; guard cell, green; pavement cell, light green. Scale bars represent 0.01 mm.



1



2

Figure 4. TET13 expression in the primary root and LRP, tet13-1 root phenotypes and

complementation. Transgenic plants shown are: pAtTET13::NLS-GFP/GUS (A, E-N and Q),

tet13-1 (B, C, D, O, P)C1 and C5 (tet13-1 containing one, respectively two T-DNA loci with

p35S::TET13) (C, P), pDR5::GUS (R and T) and tet13-1xpDR5::GUS (S). A, TET13

expression in the primary root tip. B, tet13-1 scheme, 12-d-old seedlings of Col-0 and tet13-1

growing vertically under 24-h light condition. C, Primary root growth kinetics. Means are

presented ± sd (n=22-33). Asterisks mark significant differences: *p < 0.05, **p < 0.01 and

***p < 0.001. D, Root meristem size (defined as the number of RM cells) of 6-d-old

seedlings. Means are presented ± sd (n=28-39). E-N, Detailed expression analysis of TET13 at

different stages during LR development. Corresponding developmental stages I-VII and

EMLR are indicated in the top right corner. IL and OL: inner and outer layers, respectively;

ep: epidermis; c: cortex; en: endodermis; p: pericycle. Arrowheads indicate the division

planes. Inset in I shows the top view of stage IV. O, Staging of LRP and EMLR densities.

Means are presented ± sd (n=20). P, EMLR densities. Means are presented ± sd (n=22-33).

ns, not significant. Asterisks mark significant differences: *p < 0.05, **p < 0.01 and ***p <

0.001. Q and R, NAA-induced TET13 (Q) and pDR5::GUS (R) expression. The seedlings

were grown on 10 µM NPA medium for 72 h after germination and then transferred to 10 µM

NAA medium for 0 h, 2 h and 3 h. S and T, DR5::GUS expression patterns at the root basal

meristem in 7-d-old tet13-1xpDR5::GUS (S) and wild-type (T) seedlings. Q-T, black

arrowheads indicate sites of inducible expression. Scale bars represent 0.01 mm (E-N),

0.1 mm (S and T), 0.5 mm (Q and R).



1

Figure 5. TET5 and TET6 expression, and tet5-3, tet6-2 and tet5-3tet6-2 mutant phenotypes.

Transgenic plants shown are: pAtTET5::NLS-GFP/GUS, pAtTET6::NLS-GFP/GUS, tet5-3,

tet6-2 and tet5-3tet6-2. A, TET5 and TET6 expression in the vascular tissue of the meristem-

elongation transition zone (between dotted lines) and the differentiation zone (upper) of the

primary root. Transverse sections show the transition zone and differentiation zone, as

indicated by the dashed lines. ep: epidermis; c: cortex; e: endodermis; p: pericycle.

Arrowheads and arrows indicate phloem-pole, pericycle and protoxylem, respectively. B,

TET5 and TET6 expression in the rosette leaves. C, TET5 and TET6 schemes with T-DNA

insertions. Bold, thin and breaking lines indicate exons, introns and promoter, respectively. D,

Relative TET5 (right) and TET6 (left) transcript level in 7-d-old seedlings measured by qRT-

PCR. Means are presented ± sd (n=3). E, Rosette and leaf series of 21-d-old seedlings. From

left to right are leaf 1 to leaf 8, incisions were made to make the leaves fully expanded when



2

necessary. F, Quantification of rosette leaf size in E. Means are presented ± sd (n=8-10). G,

Total number of cells per leaf. Leaf 1 and/or 2 were used. Means are presented ± sd (n=3). H,

Fresh weight of 21-d-old seedlings. Only rosette leaves were used for the experiment. I,

Primary root growth kinetics (root length). Means are presented ± sd (n=31-39). Asterisks in

all graphs mark significant differences: *p < 0.05, **p < 0.01 and ***p < 0.001. Scale bars

represent 0.01 mm (A, transverse section), 0.1 mm (A, longitudinal section), and 1 mm (B).



1

Figure 6. TF-TET gene regulatory network. Nodes and arrows depict genes and regulatory

interactions, yellow and gray rounded rectangles are TFs and TETs, respectively. The arrows

do not represent any positive or negative regulation between the TFs and TETs. Regulation

identified by ChIP-Seq and conserved binding motif are shown with doubled lines and solid

lines, respectively. Differentially expressed regulation is shown with dashed lines. AGL15:

AGAMOUS-LIKE 15, AP1: APETALA1, AP2: APETALA2, AP3: APETALA3, ATAF2:

ARABIDOPSIS NAC DOMAIN CONTAINING PROTEIN 81, BES1: BRI1-EMS-

SUPPRESSOR 1, EIN3: ETHYLENE-INSENSITIVE 3, ERF115: ETHYLENE RESPONSE

FACTOR 115, FHY3: FAR-RED ELONGATED HYPOCOTYLS 3, GL3: GLABRA3, LFY:

LEAFY, MYB4: MYB DOMAIN PROTEIN 4, PI: PISTILLATA, PIF4: PHYTOCHROME

INTERACTING FACTOR 4, PIF5: PHYTOCHROME INTERACTING FACTOR 5, PRR5:



2

PSEUDO-RESPONSE REGULATOR 5, SEP3: SEPALLATA3, SR1/CAMTA3: SIGNAL

RESPONSIVE 1/CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3, TOC1:

TIMING OF CAB EXPRESSION 1.



3



Parsed CitationsAdamczyk BJ, Lehti-Shiu MD, Fernandez DE (2007) The MADS domain factors AGL15 and AGL18 act redundantly as repressors ofthe floral transition in Arabidopsis. Plant J 50: 1007-1019

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Aerts S (2012) Computational strategies for the genome-wide identification of cis-regulatory elements and transcriptional targets.Curr Top Dev Biol 98: 121-145


Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxingradients as a common module for plant organ formation. Cell 115: 591-602


Boavida LC, Qin P, Broz M, Becker JD, McCormick S (2013) Arabidopsis tetraspanins are confined to discrete expression domainsand cell types in reproductive tissues and form homo- and hetero-dimers when expressed in yeast. Plant Physiol 163: 696-712


Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP (2010) Direct transcriptional control of the Arabidopsisimmune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA 107: 14502-14507


Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis ofArabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510


Casamitjana-Martínez E, Hofhuis HF, Xu J, Liu C-M, Heidstra R, Scheres B (2003) Root-specific CLE19 overexpression and thesol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr Biol 13: 1435-1441


Chandrasekharan MB, Bishop KJ, Hall TC (2003) Module-specific regulation of the ?-phaseolin promoter during embryogenesis.Plant J 33: 853-866


Chiu W-H, Chandler J, Cnops G, Van Lijsebettens M, Werr W (2007) Mutations in the TORNADO2 gene affect cellular decisions inthe peripheral zone of the shoot apical meristem of Arabidopsis thaliana. Plant Mol Biol 63: 731-744


Cnops G, Neyt P, Raes J, Petrarulo M, Nelissen H, Malenica N, Luschnig C, Tietz O, Ditengou F, Palme K, et al (2006) TheTORNADO1 and TORNADO2 genes function in several patterning processes during early leaf development in Arabidopsisthaliana. Plant Cell 18: 852-866


Cnops G, Wang X, Linstead P, Van Montagu M, Van Lijsebettens M, Dolan L (2000) TORNADO1 and TORNADO2 are required forthe specification of radial and circumferential pattern in the Arabidopsis root. Development 127: 3385-3394


Coussens G, Aesaert S, Verelst W, Demeulenaere M, De Buck S, Njuguna E, Inzé D, Van Lijsebettens M (2012) Brachypodiumdistachyon promoters as efficient building blocks for transgenic research in maize. J Exp Bot 63: 4263-4273


Davuluri RV, Sun H, Palaniswamy SK, Matthews N, Molina C, Kurtz M, Grotewold E (2003) AGRIS: Arabidopsis Gene RegulatoryInformation Server, an information resource of Arabidopsis cis-regulatory elements and transcription factors. BMC Bioinformatics4: 25

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http://search.crossref.org/?page=1&rows=2&q=Benkov� E, Michniewicz M, Sauer M, Teichmann T, Seifertov� D, J�rgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28AGRIS%3A Arabidopsis Gene Regulatory Information Server%2C an information resource of Arabidopsis cis%2Dregulatory elements and transcription factors%2E%5BTitle%5D%29 AND Davuluri RV%2C Sun H%2C Palaniswamy SK%2C Matthews N%2C Molina C%2C Kurtz M%2C Grotewold E%5BAuthor%5D&dopt=abstract


CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

De Rybel B, Möller B, Yoshida S, Grabowicz I, de Reuille PB, Boeren S, Smith RS, Borst JW, Weijers D (2013) A bHLH complexcontrols embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev Cell 24: 426-437


De Smet I, Chaerle P, Vanneste S, De Rycke R, Inzé D, BeeckMan T (2004) An easy and versatile embedding method fortransverse sections. J Microsc 213: 76-80


De Smet I, Tetsumura T, De Rybel B, Frei dit Frey N, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, et al(2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134: 681-690


De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inzé D (2001)Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13: 1653-1668


Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci USA 107: 12046-12051Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Ezcurra I, Wycliffe P, Nehlin L, Ellerström M, Rask L (2000) Transactivation of the Brassica napus napin promoter by ABI3 requiresinteraction of the conserved B2 and B3 domains of ABI3 with different cis-elements: B2 mediates activation through an ABRE,whereas B3 interacts with an RY/G-box. Plant J 24: 57-66


Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, Maule A (2011) Arabidopsis plasmodesmalproteome. PLoS ONE 6: e18880


Fradkin LG, Kamphorst JT, DiAntonio A, Goodman CS, Noordermeer JN (2002) Genomewide analysis of the Drosophilatetraspanins reveals a subset with similar function in the formation of the embryonic synapse. Proc Natl Acad Sci USA 99: 13663-13668


Goldberg AFX (2006) Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations. Int RevCytol 253: 131-175


Grini PE, Jürgens G, Hülskamp M (2002) Embryo and endosperm development is disrupted in the female gametophytic capuletmutants of Arabidopsis. Genetics 162: 1911-1925


Heyndrickx KS, Van de Velde J, Wang C, Weigel D, Vandepoele K (2014) A functional and evolutionary perspective on transcriptionfactor binding in Arabidopsis thaliana. Plant Cell 26: 3894-3910


Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic AcidsRes 27: 297-300


Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation duringearly lateral root initiation. Plant Cell 14: 2339-2351

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Microsc%5BTitle%5D%29 AND 213%5BVolume%5D AND 76%5BPagination%5D AND De Smet I%2C Chaerle P%2C Vanneste S%2C De Rycke R%2C Inz� D%2C BeeckMan T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=De Smet I, Chaerle P, Vanneste S, De Rycke R, Inz� D, BeeckMan T (2004) An easy and versatile embedding method for transverse sections. J Microsc 213: 76-80


http://scholar.google.com/scholar?as_q=An easy and versatile embedding method for transverse sections&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=An easy and versatile embedding method for transverse sections&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=De&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Development%5BTitle%5D%29 AND 134%5BVolume%5D AND 681%5BPagination%5D AND De Smet I%2C Tetsumura T%2C De Rybel B%2C Frei dit Frey N%2C Laplaze L%2C Casimiro I%2C Swarup R%2C Naudts M%2C Vanneste S%2C Audenaert D%2C et al%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=De Smet I, Tetsumura T, De Rybel B, Frei dit Frey N, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, et al (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134: 681-690


http://scholar.google.com/scholar?as_q=Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=De&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 13%5BVolume%5D AND 1653%5BPagination%5D AND De Veylder L%2C Beeckman T%2C Beemster GT%2C Krols L%2C Terras F%2C Landrieu I%2C van der Schueren E%2C Maes S%2C Naudts M%2C Inz� D%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inz� D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13: 1653-1668


http://scholar.google.com/scholar?as_q=Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=De&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proc Natl Acad Sci USA%5BTitle%5D%29 AND 107%5BVolume%5D AND 12046%5BPagination%5D AND Ding Z%2C Friml J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci USA 107: 12046-12051

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ding&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Auxin regulates distal stem cell differentiation in Arabidopsis roots&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Auxin regulates distal stem cell differentiation in Arabidopsis roots&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ding&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 24%5BVolume%5D AND 57%5BPagination%5D AND Ezcurra I%2C Wycliffe P%2C Nehlin L%2C Ellerstr�m M%2C Rask L%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ezcurra I, Wycliffe P, Nehlin L, Ellerstr�m M, Rask L (2000) Transactivation of the Brassica napus napin promoter by ABI3 requires interaction of the conserved B2 and B3 domains of ABI3 with different cis-elements: B2 mediates activation through an ABRE, whereas B3 interacts with an RY/G-box. Plant J 24: 57-66

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ezcurra&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Transactivation of the Brassica napus napin promoter by ABI3 requires interaction of the conserved B2 and B3 domains of ABI3 with different cis-elements: B2 mediates activation through an ABRE, whereas B3 interacts with an RY/G-box&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Transactivation of the Brassica napus napin promoter by ABI3 requires interaction of the conserved B2 and B3 domains of ABI3 with different cis-elements: B2 mediates activation through an ABRE, whereas B3 interacts with an RY/G-box&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ezcurra&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Arabidopsis plasmodesmal proteome%2E%5BTitle%5D%29 AND Fernandez%2DCalvino L%2C Faulkner C%2C Walshaw J%2C Saalbach G%2C Bayer E%2C Benitez%2DAlfonso Y%2C Maule A%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, Maule A (2011) Arabidopsis plasmodesmal proteome. PLoS ONE 6: e18880

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fernandez-Calvino&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis plasmodesmal proteome.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis plasmodesmal proteome.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fernandez-Calvino&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proc Natl Acad Sci USA%5BTitle%5D%29 AND 99%5BVolume%5D AND 13663%5BPagination%5D AND Fradkin LG%2C Kamphorst JT%2C DiAntonio A%2C Goodman CS%2C Noordermeer JN%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fradkin LG, Kamphorst JT, DiAntonio A, Goodman CS, Noordermeer JN (2002) Genomewide analysis of the Drosophila tetraspanins reveals a subset with similar function in the formation of the embryonic synapse. Proc Natl Acad Sci USA 99: 13663-13668

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fradkin&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Genomewide analysis of the Drosophila tetraspanins reveals a subset with similar function in the formation of the embryonic synapse&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Genomewide analysis of the Drosophila tetraspanins reveals a subset with similar function in the formation of the embryonic synapse&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fradkin&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Int Rev Cytol%5BTitle%5D%29 AND 253%5BVolume%5D AND 131%5BPagination%5D AND Goldberg AFX%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Goldberg AFX (2006) Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations. Int Rev Cytol 253: 131-175

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Goldberg&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Goldberg&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Genetics%5BTitle%5D%29 AND 162%5BVolume%5D AND 1911%5BPagination%5D AND Grini PE%2C J�rgens G%2C H�lskamp M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Grini PE, J�rgens G, H�lskamp M (2002) Embryo and endosperm development is disrupted in the female gametophytic capulet mutants of Arabidopsis. Genetics 162: 1911-1925

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Grini&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Embryo and endosperm development is disrupted in the female gametophytic capulet mutants of Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Embryo and endosperm development is disrupted in the female gametophytic capulet mutants of Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Grini&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 26%5BVolume%5D AND 3894%5BPagination%5D AND Heyndrickx KS%2C Van de Velde J%2C Wang C%2C Weigel D%2C Vandepoele K%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Heyndrickx KS, Van de Velde J, Wang C, Weigel D, Vandepoele K (2014) A functional and evolutionary perspective on transcription factor binding in Arabidopsis thaliana. Plant Cell 26: 3894-3910

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Heyndrickx&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A functional and evolutionary perspective on transcription factor binding in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A functional and evolutionary perspective on transcription factor binding in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Heyndrickx&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nucleic Acids Res%5BTitle%5D%29 AND 27%5BVolume%5D AND 297%5BPagination%5D AND Higo K%2C Ugawa Y%2C Iwamoto M%2C Korenaga T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27: 297-300

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Higo&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plant cis-acting regulatory DNA elements (PLACE) database: 1999&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Plant cis-acting regulatory DNA elements (PLACE) database: 1999&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Higo&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 14%5BVolume%5D AND 2339%5BPagination%5D AND Himanen K%2C Boucheron E%2C Vanneste S%2C de Almeida Engler J%2C Inz� D%2C Beeckman T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inz� D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14: 2339-2351

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Himanen&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Auxin-mediated cell cycle activation during early lateral root initiation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Auxin-mediated cell cycle activation during early lateral root initiation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Himanen&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1


Huang S, Yuan S, Dong M, Su J, Yu C, Shen Y, Xie X, Yu Y, Yu X, Chen S, et al (2005) The phylogenetic analysis of tetraspaninsprojects the evolution of cell-cell interactions from unicellular to multicellular organisms. Genomics 86: 674-684


Kaji K, Oda S, Miyazaki S, Kudo A (2002) Infertility of CD9-deficient mouse eggs is reversed by mouse CD9, human CD9, or mouseCD81; polyadenylated mRNA injection developed for molecular analysis of sperm-egg fusion. Dev Biol 247: 327-334


Karimi M, Bleys A, Vanderhaeghen R, Hilson P (2007) Building blocks for plant gene assembly. Plant Physiol 145: 1183-1191Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis. Plant Cell 17: 2981-2992


Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markovmodel: application to complete genomes. J Mol Biol 305: 567-580


Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls thethermosensory activation of flowering. Nature 484: 242-245


Lieber D, Lora J, Schrempp S, Lenhard M, Laux T (2011) Arabidopsis WIH1 and WIH2 genes act in the transition from somatic toreproductive cell fate. Curr Biol 21: 1009-1017


Lumba S, Tsuchiya Y, Delmas F, Hezky J, Provart NJ, Shi Lu Q, McCourt P, Gazzarrini S (2012) The embryonic leaf identity geneFUSCA3 regulates vegetative phase transitions by negatively modulating ethylene-regulated gene expression in Arabidopsis.BMC Biol 10: 8


Luo X-M, Lin W-H, Zhu S, Zhu J-Y, Sun Y, Fan X-Y, Cheng M, Hao Y, Oh E, Tian M, et al (2010) Integration of light- andbrassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Dev Cell 19: 872-883


Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33-44Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Mejia-Guerra MK, Pomeranz M, Morohashi K, Grotewold E (2012) From plant gene regulatory grids to network dynamics. BiochimBiophys Acta - Gene Regul Mech 1819: 454-465


Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8: 122-128Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Murray JAH, Jones A, Godin C, Traas J (2012) Systems analysis of shoot apical meristem growth and development: integratinghormonal and mechanical signaling. Plant Cell 24: 3907-3919


Nakamichi N, Kita M, Niinuma K, Ito S, Yamashino T, Mizoguchi T, Mizuno T (2007) Arabidopsis clock-associated pseudo-responseregulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol 48: 822-832


http://www.ncbi.nlm.nih.gov/pubmed?term=%28Genomics%5BTitle%5D%29 AND 86%5BVolume%5D AND 674%5BPagination%5D AND Huang S%2C Yuan S%2C Dong M%2C Su J%2C Yu C%2C Shen Y%2C Xie X%2C Yu Y%2C Yu X%2C Chen S%2C et al%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Huang S, Yuan S, Dong M, Su J, Yu C, Shen Y, Xie X, Yu Y, Yu X, Chen S, et al (2005) The phylogenetic analysis of tetraspanins projects the evolution of cell-cell interactions from unicellular to multicellular organisms. Genomics 86: 674-684

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Huang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The phylogenetic analysis of tetraspanins projects the evolution of cell-cell interactions from unicellular to multicellular organisms&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The phylogenetic analysis of tetraspanins projects the evolution of cell-cell interactions from unicellular to multicellular organisms&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Huang&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Infertility%5BTitle%5D%29 AND 9%5BVolume%5D AND human CD9%2C or mouse CD81%3B polyadenylated mRNA injection developed for molecular analysis of sperm%5BPagination%5D AND Kaji K%2C Oda S%2C Miyazaki S%2C Kudo A%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kaji K, Oda S, Miyazaki S, Kudo A (2002) Infertility of CD9-deficient mouse eggs is reversed by mouse CD9, human CD9, or mouse CD81; polyadenylated mRNA injection developed for molecular analysis of sperm-egg fusion. Dev Biol 247: 327-334

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kaji&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kaji&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 145%5BVolume%5D AND 1183%5BPagination%5D AND Karimi M%2C Bleys A%2C Vanderhaeghen R%2C Hilson P%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Karimi M, Bleys A, Vanderhaeghen R, Hilson P (2007) Building blocks for plant gene assembly. Plant Physiol 145: 1183-1191

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Karimi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Building blocks for plant gene assembly&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Building blocks for plant gene assembly&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Karimi&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 17%5BVolume%5D AND 2981%5BPagination%5D AND Kasahara RD%2C Portereiko MF%2C Sandaklie%2DNikolova L%2C Rabiger DS%2C Drews GN%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN (2005) MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17: 2981-2992

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kasahara&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kasahara&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Mol Biol%5BTitle%5D%29 AND 305%5BVolume%5D AND 567%5BPagination%5D AND Krogh A%2C Larsson B%2C von Heijne G%2C Sonnhammer ELL%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Krogh&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Krogh&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nature%5BTitle%5D%29 AND 484%5BVolume%5D AND 242%5BPagination%5D AND Kumar SV%2C Lucyshyn D%2C Jaeger KE%2C Al�s E%2C Alvey E%2C Harberd NP%2C Wigge PA%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kumar SV, Lucyshyn D, Jaeger KE, Al�s E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484: 242-245

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kumar&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Transcription factor PIF4 controls the thermosensory activation of flowering&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Transcription factor PIF4 controls the thermosensory activation of flowering&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kumar&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Biol%5BTitle%5D%29 AND 21%5BVolume%5D AND 1009%5BPagination%5D AND Lieber D%2C Lora J%2C Schrempp S%2C Lenhard M%2C Laux T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lieber D, Lora J, Schrempp S, Lenhard M, Laux T (2011) Arabidopsis WIH1 and WIH2 genes act in the transition from somatic to reproductive cell fate. Curr Biol 21: 1009-1017

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lieber&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis WIH1 and WIH2 genes act in the transition from somatic to reproductive cell fate&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis WIH1 and WIH2 genes act in the transition from somatic to reproductive cell fate&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lieber&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions by negatively modulating ethylene%2Dregulated gene expression in Arabidopsis%2E%5BTitle%5D%29 AND Lumba S%2C Tsuchiya Y%2C Delmas F%2C Hezky J%2C Provart NJ%2C Shi Lu Q%2C McCourt P%2C Gazzarrini S%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lumba S, Tsuchiya Y, Delmas F, Hezky J, Provart NJ, Shi Lu Q, McCourt P, Gazzarrini S (2012) The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions by negatively modulating ethylene-regulated gene expression in Arabidopsis. BMC Biol 10: 8

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lumba&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions by negatively modulating ethylene-regulated gene expression in Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions by negatively modulating ethylene-regulated gene expression in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lumba&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Dev Cell%5BTitle%5D%29 AND 19%5BVolume%5D AND 872%5BPagination%5D AND Luo X%2DM%2C Lin W%2DH%2C Zhu S%2C Zhu J%2DY%2C Sun Y%2C Fan X%2DY%2C Cheng M%2C Hao Y%2C Oh E%2C Tian M%2C et al%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Luo X-M, Lin W-H, Zhu S, Zhu J-Y, Sun Y, Fan X-Y, Cheng M, Hao Y, Oh E, Tian M, et al (2010) Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Dev Cell 19: 872-883

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Luo&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Luo&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Development%5BTitle%5D%29 AND 124%5BVolume%5D AND 33%5BPagination%5D AND Malamy JE%2C Benfey PN%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33-44

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Malamy&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Organization and cell differentiation in lateral roots of Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Organization and cell differentiation in lateral roots of Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Malamy&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Biochim Biophys Acta %2D Gene Regul Mech%5BTitle%5D%29 AND 1819%5BVolume%5D AND 454%5BPagination%5D AND Mejia%2DGuerra MK%2C Pomeranz M%2C Morohashi K%2C Grotewold E%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mejia-Guerra MK, Pomeranz M, Morohashi K, Grotewold E (2012) From plant gene regulatory grids to network dynamics. Biochim Biophys Acta - Gene Regul Mech 1819: 454-465

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Mejia-Guerra&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=From plant gene regulatory grids to network dynamics&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=From plant gene regulatory grids to network dynamics&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mejia-Guerra&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Opin Plant Biol%5BTitle%5D%29 AND 8%5BVolume%5D AND 122%5BPagination%5D AND Moore RC%2C Purugganan MD%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8: 122-128

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Moore&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The evolutionary dynamics of plant duplicate genes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The evolutionary dynamics of plant duplicate genes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Moore&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 24%5BVolume%5D AND 3907%5BPagination%5D AND Murray JAH%2C Jones A%2C Godin C%2C Traas J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Murray JAH, Jones A, Godin C, Traas J (2012) Systems analysis of shoot apical meristem growth and development: integrating hormonal and mechanical signaling. Plant Cell 24: 3907-3919

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Murray&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Systems analysis of shoot apical meristem growth and development: integrating hormonal and mechanical signaling&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Systems analysis of shoot apical meristem growth and development: integrating hormonal and mechanical signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Murray&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1



Nie H, Zhao C, Wu G, Wu Y, Chen Y, Tang D (2012) SR1, a calmodulin-binding transcription factor, modulates plant defense andethylene-induced senescence by directly regulating NDR1 and EIN3. Plant Physiol 158: 1847-1859


Perilli S, Di Mambro R, Sabatini S (2012) Growth and development of the root apical meristem. Curr Opin Plant Biol 15: 17-23Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Riou-Khamlichi C, Menges M, Healy JMS, Murray JAH (2000) Sugar control of the plant cell cycle: differential regulation ofArabidopsis D-type cyclin gene expression. Mol Cell Biol 20: 4513-4521


Rubinstein E, Ziyyat A, Prenant M, Wrobel E, Wolf J-P, Levy S, Le Naour F, Boucheix C (2006) Reduced fertility of female micelacking CD81. Dev Biol 290: 351-358


Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factorsregulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811-814


Schenke D, Böttcher C, Scheel D (2011) Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling inArabidopsis prevents flavonol accumulation in favor of pathogen defence compound production. Plant, Cell and Environment 34:1849-1864


Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathwaysusing global expression analysis. Development 130: 6001-6012


Shoham T, Rajapaksa R, Boucheix C, Rubinstein E, Poe JC, Tedder TF, Levy S (2003) The tetraspanin CD81 regulates theexpression of CD19 during B cell development in a postendoplasmic reticulum compartment. J Immunol 171: 4062-4072


Sparks E, Wachsman G, Benfey PN (2013) Spatiotemporal signalling in plant development. Nat Rev Genet 14: 631-644Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Steffens NO, Galuschka C, Schindler M, Bülow L, Hehl R (2004) AthaMap: an online resource for in silico transcription factorbinding sites in the Arabidopsis thaliana genome. Nucleic Acids Res 32: D368-D372


Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, et al (2008) The auxininflux carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10: 946-954


Thomas-Chollier M, Sand O, Turatsinze J-V, Janky R, Defrance M, Vervisch E, Brohée S, van Helden J (2008) RSAT: regulatorysequence analysis tools. Nucleic Acids Res 36: W119-W127


Van de Velde J, Heyndrickx KS, Vandepoele K (2014) Inference of transcriptional networks in Arabidopsis through conservednoncoding sequence analysis. Plant Cell 26: 2729-2745



http://www.ncbi.nlm.nih.gov/pubmed?term=%28Arabidopsis%5BTitle%5D%29 AND 9%5BVolume%5D AND PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS%5BPagination%5D AND Nakamichi N%2C Kita M%2C Niinuma K%2C Ito S%2C Yamashino T%2C Mizoguchi T%2C Mizuno T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nakamichi N, Kita M, Niinuma K, Ito S, Yamashino T, Mizoguchi T, Mizuno T (2007) Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol 48: 822-832

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Nakamichi&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nakamichi&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28SR%5BTitle%5D%29 AND 1%5BVolume%5D AND Nie H%2C Zhao C%2C Wu G%2C Wu Y%2C Chen Y%2C Tang D%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nie H, Zhao C, Wu G, Wu Y, Chen Y, Tang D (2012) SR1, a calmodulin-binding transcription factor, modulates plant defense and ethylene-induced senescence by directly regulating NDR1 and EIN3. Plant Physiol 158: 1847-1859

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Nie&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nie&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Opin Plant Biol%5BTitle%5D%29 AND 15%5BVolume%5D AND 17%5BPagination%5D AND Perilli S%2C Di Mambro R%2C Sabatini S%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Perilli S, Di Mambro R, Sabatini S (2012) Growth and development of the root apical meristem. Curr Opin Plant Biol 15: 17-23

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Perilli&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Growth and development of the root apical meristem&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Growth and development of the root apical meristem&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Perilli&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mol Cell Biol%5BTitle%5D%29 AND 20%5BVolume%5D AND 4513%5BPagination%5D AND Riou%2DKhamlichi C%2C Menges M%2C Healy JMS%2C Murray JAH%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Riou-Khamlichi C, Menges M, Healy JMS, Murray JAH (2000) Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell Biol 20: 4513-4521

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http://scholar.google.com/scholar?as_q=Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Riou-Khamlichi&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Dev Biol%5BTitle%5D%29 AND 290%5BVolume%5D AND 351%5BPagination%5D AND Rubinstein E%2C Ziyyat A%2C Prenant M%2C Wrobel E%2C Wolf J%2DP%2C Levy S%2C Le Naour F%2C Boucheix C%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rubinstein E, Ziyyat A, Prenant M, Wrobel E, Wolf J-P, Levy S, Le Naour F, Boucheix C (2006) Reduced fertility of female mice lacking CD81. Dev Biol 290: 351-358

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rubinstein&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Reduced fertility of female mice lacking CD81&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Reduced fertility of female mice lacking CD81&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rubinstein&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nature%5BTitle%5D%29 AND 446%5BVolume%5D AND 811%5BPagination%5D AND Sarkar AK%2C Luijten M%2C Miyashima S%2C Lenhard M%2C Hashimoto T%2C Nakajima K%2C Scheres B%2C Heidstra R%2C Laux T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811-814

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Sarkar&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sarkar&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant%2C Cell and Environment%5BTitle%5D%29 AND 34%5BVolume%5D AND 1849%5BPagination%5D AND Schenke D%2C B�ttcher C%2C Scheel D%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schenke D, B�ttcher C, Scheel D (2011) Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production. Plant, Cell and Environment 34: 1849-1864

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schenke&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schenke&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Development%5BTitle%5D%29 AND 130%5BVolume%5D AND 6001%5BPagination%5D AND Schmid M%2C Uhlenhaut NH%2C Godard F%2C Demar M%2C Bressan R%2C Weigel D%2C Lohmann JU%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130: 6001-6012

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schmid&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Dissection of floral induction pathways using global expression analysis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Dissection of floral induction pathways using global expression analysis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schmid&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Immunol%5BTitle%5D%29 AND 171%5BVolume%5D AND 4062%5BPagination%5D AND Shoham T%2C Rajapaksa R%2C Boucheix C%2C Rubinstein E%2C Poe JC%2C Tedder TF%2C Levy S%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Shoham T, Rajapaksa R, Boucheix C, Rubinstein E, Poe JC, Tedder TF, Levy S (2003) The tetraspanin CD81 regulates the expression of CD19 during B cell development in a postendoplasmic reticulum compartment. J Immunol 171: 4062-4072

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Shoham&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The tetraspanin CD81 regulates the expression of CD19 during B cell development in a postendoplasmic reticulum compartment&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The tetraspanin CD81 regulates the expression of CD19 during B cell development in a postendoplasmic reticulum compartment&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shoham&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nat Rev Genet%5BTitle%5D%29 AND 14%5BVolume%5D AND 631%5BPagination%5D AND Sparks E%2C Wachsman G%2C Benfey PN%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sparks E, Wachsman G, Benfey PN (2013) Spatiotemporal signalling in plant development. Nat Rev Genet 14: 631-644

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Sparks&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Spatiotemporal signalling in plant development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Spatiotemporal signalling in plant development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sparks&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nucleic Acids Res%5BTitle%5D%29 AND 32%5BVolume%5D AND D368%5BPagination%5D AND Steffens NO%2C Galuschka C%2C Schindler M%2C B�low L%2C Hehl R%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Steffens NO, Galuschka C, Schindler M, B�low L, Hehl R (2004) AthaMap: an online resource for in silico transcription factor binding sites in the Arabidopsis thaliana genome. Nucleic Acids Res 32: D368-D372

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Steffens&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=AthaMap: an online resource for in silico transcription factor binding sites in the Arabidopsis thaliana genome&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=AthaMap: an online resource for in silico transcription factor binding sites in the Arabidopsis thaliana genome&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Steffens&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nat Cell Biol%5BTitle%5D%29 AND 10%5BVolume%5D AND 946%5BPagination%5D AND Swarup K%2C Benkov� E%2C Swarup R%2C Casimiro I%2C P�ret B%2C Yang Y%2C Parry G%2C Nielsen E%2C De Smet I%2C Vanneste S%2C et al%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Swarup K, Benkov� E, Swarup R, Casimiro I, P�ret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, et al (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10: 946-954

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Swarup&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The auxin influx carrier LAX3 promotes lateral root emergence&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The auxin influx carrier LAX3 promotes lateral root emergence&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Swarup&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nucleic Acids Res%5BTitle%5D%29 AND 36%5BVolume%5D AND W119%5BPagination%5D AND Thomas%2DChollier M%2C Sand O%2C Turatsinze J%2DV%2C Janky R%2C Defrance M%2C Vervisch E%2C Broh�e S%2C van Helden J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Thomas-Chollier M, Sand O, Turatsinze J-V, Janky R, Defrance M, Vervisch E, Broh�e S, van Helden J (2008) RSAT: regulatory sequence analysis tools. Nucleic Acids Res 36: W119-W127

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Thomas-Chollier&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=RSAT: regulatory sequence analysis tools&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=RSAT: regulatory sequence analysis tools&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Thomas-Chollier&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 26%5BVolume%5D AND 2729%5BPagination%5D AND Van de Velde J%2C Heyndrickx KS%2C Vandepoele K%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Van de Velde J, Heyndrickx KS, Vandepoele K (2014) Inference of transcriptional networks in Arabidopsis through conserved noncoding sequence analysis. Plant Cell 26: 2729-2745

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Van&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Inference of transcriptional networks in Arabidopsis through conserved noncoding sequence analysis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Inference of transcriptional networks in Arabidopsis through conserved noncoding sequence analysis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Van&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1


van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in theArabidopsis root meristem. Nature 390: 287-289


Vandepoele K, Quimbaya M, Casneuf T, De Veylder L, Van de Peer Y (2009) Unraveling transcriptional control in Arabidopsis usingcis-regulatory elements and coexpression networks. Plant Physiol 150: 535-546


Wang F, Vandepoele K, Van Lijsebettens M (2012) Tetraspanin genes in plants. Plant Sci 190: 9-15Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Yamamoto A, Kagaya Y, Usui H, Hobo T, Takeda S, Hattori T (2010) Diverse roles and mechanisms of gene regulation by theArabidopsis seed maturation master regulator FUS3 revealed by microarray analysis. Plant Cell Physiol 51: 2031-2046


Yáñez-Mó M, Barreiro O, Gordon-Alonso M, Sala-Valdés M, Sánchez-Madrid F (2009) Tetraspanin-enriched microdomains: afunctional unit in cell plasma membranes. Trends Cell Biol 19: 434-446


Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, et al (2011) A brassinosteroid transcriptionalnetwork revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65: 634-646


Zhang W, Zhang T, Wu Y, Jiang J (2012) Genome-wide identification of regulatory DNA elements and protein-binding footprintsusing signatures of open chromatin in Arabidopsis. Plant Cell 24: 2719-2731


Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of the Arabidopsis MADS domain proteinAGAMOUS-Like15. Plant Cell 21: 2563-2577



http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nature%5BTitle%5D%29 AND 390%5BVolume%5D AND 287%5BPagination%5D AND van den Berg C%2C Willemsen V%2C Hendriks G%2C Weisbeek P%2C Scheres B%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390: 287-289

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=van&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Short-range control of cell differentiation in the Arabidopsis root meristem&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 150%5BVolume%5D AND 535%5BPagination%5D AND Vandepoele K%2C Quimbaya M%2C Casneuf T%2C De Veylder L%2C Van de Peer Y%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Vandepoele K, Quimbaya M, Casneuf T, De Veylder L, Van de Peer Y (2009) Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks. Plant Physiol 150: 535-546

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Vandepoele&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Vandepoele&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Sci%5BTitle%5D%29 AND 190%5BVolume%5D AND 9%5BPagination%5D AND Wang F%2C Vandepoele K%2C Van Lijsebettens M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang F, Vandepoele K, Van Lijsebettens M (2012) Tetraspanin genes in plants. Plant Sci 190: 9-15

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Tetraspanin genes in plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell Physiol%5BTitle%5D%29 AND 51%5BVolume%5D AND 2031%5BPagination%5D AND Yamamoto A%2C Kagaya Y%2C Usui H%2C Hobo T%2C Takeda S%2C Hattori T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yamamoto A, Kagaya Y, Usui H, Hobo T, Takeda S, Hattori T (2010) Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis. Plant Cell Physiol 51: 2031-2046

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yamamoto&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Trends Cell Biol%5BTitle%5D%29 AND 19%5BVolume%5D AND 434%5BPagination%5D AND Y��ez%2DM� M%2C Barreiro O%2C Gordon%2DAlonso M%2C Sala%2DVald�s M%2C S�nchez%2DMadrid F%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Y��ez-M� M, Barreiro O, Gordon-Alonso M, Sala-Vald�s M, S�nchez-Madrid F (2009) Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 19: 434-446

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Y��ez-M�&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 65%5BVolume%5D AND 634%5BPagination%5D AND Yu X%2C Li L%2C Zola J%2C Aluru M%2C Ye H%2C Foudree A%2C Guo H%2C Anderson S%2C Aluru S%2C Liu P%2C et al%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, et al (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65: 634-646

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yu&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 24%5BVolume%5D AND 2719%5BPagination%5D AND Zhang W%2C Zhang T%2C Wu Y%2C Jiang J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang W, Zhang T, Wu Y, Jiang J (2012) Genome-wide identification of regulatory DNA elements and protein-binding footprints using signatures of open chromatin in Arabidopsis. Plant Cell 24: 2719-2731

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 21%5BVolume%5D AND 2563%5BPagination%5D AND Zheng Y%2C Ren N%2C Wang H%2C Stromberg AJ%2C Perry SE%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21: 2563-2577

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1 running head: tetraspanin genes in arabidopsis … · 103 in primary root growth and lateral root...

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