1 running head: del1 affects rice growth and leaf senescence 2 · 4/28/2017 · 97 accumulation of...

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Running Head: DEL1 affects rice growth and leaf senescence 1

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Corresponding authors: 3

Dali Zeng 4

State Key Lab for Rice Biology, China National Rice Research Institute, Hangzhou 5

310006, China 6

Tel: +86 571 6337 0537 7

Fax: +86 571 6337 0537 8

E-mail: [email protected] 9

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Qian qian 11

State Key Lab for Rice Biology, China National Rice Research Institute, Hangzhou 12

310006, China 13

Tel: +86 571 6337 0537 14

Fax: +86 571 6337 0537 15

E-mail: [email protected] 16

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Plant Physiology Preview. Published on April 28, 2017, as DOI:10.1104/pp.16.01625

Copyright 2017 by the American Society of Plant Biologists

www.plantphysiol.orgon October 7, 2020 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

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Title of article: 31

A rice PECTATE LYASE-LIKE gene is required for plant growth and leaf senescence 32

Authors’names: 33

Yujia Leng1, 2, †, Yaolong Yang1, †, Deyong Ren1, †, Lichao Huang1, Liping Dai1, 2, 34

Yuqiong Wang1, Long Chen1, 2, Zhengjun Tu1, Yihong Gao1, Xueyong Li3, Li Zhu1, 35

Jiang Hu1, Guangheng Zhang1, Zhenyu Gao1, Longbiao Guo1, Zhaosheng Kong4, 36

Yongjun Lin2, Qian Qian1,*, Dali Zeng1,* 37

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Addresses: 39 1 State Key Lab for Rice Biology, China National Rice Research Institute, Hangzhou 40

310006, China 41

2 National Key Laboratory of Crop Genetic Improvement and National Centre of 42

Plant Gene Research, Huazhong Agricultural University, Wuhan 430070, China 43

3 National Key Facility for Crop Gene Resources and Genetic Improvement, Institute 44

of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, 45

China, 46

4 Institute of Microbiology, Chinese Academy of Sciences, State Key Laboratory of 47

Plant Genomics, Beijing 100101, China 48

ORCID IDs: 0000-0003-2349-8633 (D.Z.); 0000-0002-0349-4937 (Q.Q.). 49

One-sentence Summary: DEL1 affects rice growth and leaf senescence mediated 50

by PECTATE LYASE-LIKE genes. 51

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Footnotes: 53

The author responsible for the distribution of materials integral to the findings 54

presented in this article in accordance with the policy described in the Instructions 55

for Authors (www.plantphysiol.org) is: Dali Zeng ([email protected]), Qian Qian 56

([email protected]) 57

† contributed equally to the article. 58

Author Contributions: 59

Y.J.L., Y.L.Y., and D.Y.R. performed research. L.C.H., L.P.D., Y.Q.W., L.C., Z.J.T., 60



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Y.H.G., L.Z., J.H., G.H.Z., Z.Y.G., L.B.G., Y.J.L., X.Y.L., and Z.S.K. analyzed the 61

data. Y.J.L. wrote the article. Y.J.L., D.L.Z. and Q.Q. designed the research. D.L.Z. 62

revised the article. 63

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Funding Information: 65

This research was supported by the National Natural Science Foundation of China 66

(Grant No. 31661143006, 91435105, 91535205), National Key Basic Research 67

Program (Grant No. 2013CBA014) and “Science and technology innovation project” 68

of the Chinese Academy of Agriculture Sciences. 69

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ABSTRACT 89

To better understand the molecular mechanisms behind plant growth and leaf 90



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senescence in monocot plants, we identified a mutant exhibiting dwarfism and an 91

early-senescence leaf phenotype, termed dwarf and early-senescence leaf (del1). 92

Histological analysis showed that the abnormal growth was caused by a reduction in 93

cell number. Further investigation revealed that the decline in cell number in del1 94

was affected by the cell cycle. Physiological analysis, transmission electron 95

microscopy, and TUNEL assays showed that leaf senescence was triggered by the 96

accumulation of reactive oxygen species. The DEL1 gene was cloned using a 97

map-based approach. It was shown to encode a pectate lyase (PEL) precursor that 98

contains a PelC domain. DEL1 contains all the conserved residues of PEL and has 99

strong similarity with plant PelC. DEL1 is expressed in all tissues but predominantly 100

in elongating tissues. Functional analysis revealed that mutation of DEL1 decreased 101

the total PEL enzymatic activity, increased the degree of methylesterified 102

homogalacturonan and altered the cell wall composition and structure. In addition, 103

transcriptome assay revealed that a set of cell wall function and senescence related 104

gene expression was altered in del1 plants. Our research indicates that DEL1 is 105

involved in both the maintenance of normal cell division and the induction of leaf 106

senescence. These findings reveal a new molecular mechanism for plant growth and 107

leaf senescence mediated by PECTATE LYASE-LIKE (PLL) genes. 108

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INTRODUCTION 123

The development of higher plants is accompanied by the complex processes of cell 124



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division and cell expansion, and finally the emergence of many specialized organs, 125

tissues, and cells. As part of cell development in plants, cell walls perform essential 126

functions such as tensile strength, providing shape, and protection, as well as helping 127

the cell to maintain its internal pressure (Cosgrove, 2005). In growing plants, the cell 128

wall are both resistant to the high turgor pressure that drives growth and also flexible 129

enough to yield and expand selectively in response to that pressure (Cosgrove, 2005; 130

Xiao et al., 2014). This process involves a series of molecular mechanisms, 131

including disruption of the intermolecular adhesion, polymer lysis, religation and 132

rearrangements, and/or cleavage of polymer glycosyl linkages by enzymes 133

(McQueen-Mason and Cosgrove, 1995; Van Sandt et al., 2007; Anderson et al., 134

2010; Park and Cosgrove, 2012). 135

Pectins are major components of the plant primary cell wall and middle lamella 136

and have several functions, including involvement in maintaining plant growth and 137

development, promoting cell-to-cell adhesion, providing structural support in soft 138

tissues, defense responses, and influencing wall porosity and thickness, etc (Ridley 139

et al., 2001; Iwai et al., 2002; Ogawa et al., 2009; Wolf et al., 2009; Hongo et al., 140

2012). Pectins may be the most complex polysaccharide family in the living world, 141

being composed of as many as 17 different monosaccharides and having more than 142

20 different linkages (Bonnin et al., 2014). According to the current understanding 143

of pectins at the structure/function level, there are two conceptual models of 144

structural modification during plant growth (Atmodjo et al., 2013). First, the large 145

number of linkages and structural motifs allow the domains of pectins to interact 146

indirectly and/or via covalent bonds (Dick-Perez et al., 2011; Tan et al., 2013). 147

Second, pectins can depend on reversible calcium-mediated cross-linking between 148

stretches of demethylated homogalacturonan (HG) to coordinate cell wall networks 149

(Vincken et al., 2003; Xiao et al., 2014). Homogalacturonan is secreted in a highly 150

methylesterified form and selectively demethylesterified by pectin methylesterases 151

(PME) (Hongo et al., 2012). The demethylesterified HG can either form a rigid gel 152

by Ca2+-pectate cross-linked complexes, or become more susceptible to cleavage by 153

two classes of pectin-degrading enzyme, namely pectin/pectate lyase (PL/PEL, EC 154



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4.2.2.10; EC 4.2.2.2) and polygalacturonase (PG, EC 3.2.1.15) (Wolf et al., 2009; 155

Hongo et al., 2012). Hence, the methylesterification status of HG can regulate 156

cellular growth and cell shape, and affect plant growth and development (Wolf et al., 157

2009; Peaucelle et al., 2011). 158

Pectate lyases, a family of endo-acting depolymerizing enzymes, are responsible 159

for the α-1,4-glycosidic linkages in demethylesterified HG by β-elimination and 160

produces 4,5-unsaturated oligogalacturonides (OGs) at their non-reducing ends 161

(Palusa et al., 2007). Pectate lyases have been extensively studied in plant 162

pathogenic bacteria such as Erwinia chrysanthemi, which causes soft-rot diseases 163

(Barras et al., 1994). In plants, multiple functions have been identified for PEL, and 164

there is some suggestion that it is involved in pollen, anthers, pistils, and developing 165

tracheary elements (Wing et al., 1989; Rogers et al., 1992; Wu et al., 1996; 166

Kulikauskas and McCormick, 1997; Domingo et al., 1998; Milioni et al., 2001), fruit 167

softening and ripening (Dominguez-Puigjaner et al., 1997; Medina-Escobar et al., 168

1997; Nunan et al., 2001; Pua et al., 2001), lateral root emergence (Laskowski et al., 169

2006), cotton fiber elongation (Wang et al., 2010), leaf senescence (Wu et al., 2013), 170

and susceptibility to plant pathogens (Vogel et al., 2002). It has also been shown to 171

be expressed in a wide range of tissues (Palusa et al., 2007; Sun and Nocker, 2010). 172

In addition, recent research has revealed that the overexpression of aspen PtxtPL1-27 173

can increase the solubility of wood matrix polysaccharides (Biswal et al., 2014). The 174

modification of pectins may be important in the field of biotechnology for improving 175

woody biomass (Biswal et al., 2014). 176

The large family of PECTATE LYASE-LIKE (PLL) genes all exhibit redundant or 177

unique functions in plant evolution, and this diversity may enhance plasticity in 178

adaptation to changing environments (Sun and Nocker, 2010). In rice, genome 179

prediction has suggested that there are 14 PLL genes, but only one of these (ospse1) 180

has been analyzed genetically (Wu et al., 2013). In this study, we report on the 181

isolation and characterization of a recessive mutant, dwarf and early-senescence leaf 182

1 (del1), in rice (Oryza sativa L.). The mutation of DEL1 led to a phenotype 183

involving abnormal plant growth and leaf senescence. DEL1 encodes a PEL 184



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precursor and is a member of a multi-gene family in rice. The loss of function of 185

DEL1 decreased total PEL activity, increased the degree of methylesterified HG, and 186

perturbed cell wall composition and structure, resulting in a reduced number of cells 187

and triggering reactive oxygen species (ROS) activity. Expression profiling indicated 188

the genes involved in cell wall function and senescence are altered in expression in 189

the del1 plants. Our findings suggest that DEL1 is a critical gene for plant growth 190

and leaf senescence in rice. 191

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RESULTS 193

del1 exhibits significant size reduction in the whole plant 194

The dwarf and early-senescence leaf 1 (del1) mutant was isolated from an 195

EMS-mutagenized japonica cultivar, Nipponbare. del1 exhibited dwarfism at the 196

seedling stage (5 days after germination) and its main root length was clearly 197

reduced, which reached 47.8% of that in the wild-type (Fig. 1a, c). Meanwhile, the 198

number of lateral roots in del1 decreased significantly to just 44.7% of that in the 199

wild-type (Fig. 1b, d). The plant height of del1 was also shorter than that of the 200

wild-type throughout the growth period, being only about 36.8% of that of the 201

wild-type at the mature stage (Fig. 1e, f; Fig. S1, S2), and the internode length, 202

thickness, and diameter of del1 were significantly reduced (Fig. S3). Compared with 203

the wild-type, the tiller number and panicle length were also clearly reduced in del1 204

plants (Fig. 1e, g, h, and k). Moreover, grain development also changed significantly, 205

with grain size and grain weight being diminished in del1 plants (Fig. 1i, j, l; Table 206

S1). Besides these phenotypic findings, the heading date of del1 was also notably 207

retarded, along with decreases in leaf length and leaf width (Table S1). These 208

phenotypes clearly suggest that plant size was significantly lower in del1 plants. 209

Cell number is reduced in del1 plants 210

The size of a plant organ is determined by its cell size and number of cells, which are 211

related to cell expansion and cell division, respectively (Krizek, 2009). To determine 212

the causes of organ size reduction in del1 plants, we conducted microscopic 213

observation on the second culms and compared the findings between the wild-type 214



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and del1 using paraffinized sections. Cross sections of culms revealed that the size of 215

sclerenchyma cells in del1 was less than that in the wild-type (Fig. 2a–d). Statistical 216

analysis showed that the cell number of del1 was only 88.56% of that in the 217

wild-type (Fig. 2e). Moreover, the number of layers of sclerenchyma cells in del1 218

was reduced by two (Fig. 2c, d and f). Longitudinal sections of culms in del1 219

displayed a significant change in cell size (Fig. 2g, h). The cell length in del1 was 220

59.6% longer and the cell width was 20.8% narrower than that in the wild-type (Fig. 221

2i, j). Further investigation of the total number of parenchyma cells showed that del1 222

had only 19% of the number in the wild-type (Fig. 2k). 223

Cell cycle progression is delayed in del1 plants 224

To determine whether the decline in cell number in del1 was affected by the cell 225

cycle, we further investigated the cell cycle progression by flow cytometry. The 226

results of the suspension cell lines of del1 revealed a significant increase in the 227

number of cells in the G1 phase and decreases in the S and G2/M phases of the cell 228

cycle, implying that the cell cycle was delayed at the G1 phase (Fig. 3a–c). We also 229

analyzed the expression of cell-cycle-related genes in wild-type and del1 plants 230

using real-time RT-PCR. The expression levels of genes related to the G1 phase of 231

the cell cycle, CDKA1, CAK1, CAK1A, MCM5, and CYCT1, were down-regulated 232

by approximately 10–45%, while little difference was observed for genes related to 233

the G2 phase of the cell cycle in del1 mutants (Fig. 3d). Therefore, we conclude that 234

the mutation of DEL1 delays cell cycle progression at the G1 phase. 235

del1 displays early leaf senescence 236

del1 also exhibited a phenotype of early senescence, which became increasingly 237

apparent as the plants developed (Fig. 4a–d). The mutant leaf apex and leaf margin 238

exhibited a faint yellow color from 5 days after germination (Fig. 4a). With the 239

development of plants, the young leaves were pale white and then turned green upon 240

maturation, while the old leaves exhibited withering and cracking (Fig. 4b–d). The 241

chlorophyll content in del1 plants was significantly lower, being only 44.0% of that 242

in the wild-type (Fig. 4e). In addition, transmission electron microscopy (TEM) 243

revealed the presence of well-developed mesophyll cells and membrane-intact 244



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chloroplasts in fully developed wild-type leaves, whereas the disordered 245

arrangement of grana thylakoid, and the degradation of chloroplasts, was observed in 246

del1 plants (Fig. 4f, g). Moreover, the photosynthetic rate in del1 plants was only 247

58.5% of that in the wild-type (Fig. 4h). All these results indicate that leaf 248

senescence occurred in del1 plants. 249

Leaf senescence is usually accompanied by a change of expression of many genes 250

including those for transcription factors (Wang et al., 2015). To confirm senescence 251

in the del1 plants, the expression levels of senescence-associated genes (SAGs) and 252

related transcription factors (Osl2, OsH36, SGR, OsNAC2, OsWRKY23, and 253

OsWRKY72) were determined by real-time RT-PCR. The expression levels of Osl2, 254

OsH36, SGR, OsNAC2, OsWRKY23, and OsWRKY72 mRNAs were 2.0 to 8.0 times 255

higher than in wild-type leaves (Fig. 4i). The up-regulated expression patterns of 256

SAGs and transcription factors further support the notion that early leaf senescence 257

occurred in del1 plants. 258

ROS accumulation and programmed cell death are enhanced in del1 plants 259

The accumulation of ROS can lead to leaf senescence (Khanna-Chopra, 2012). 260

Therefore, we performed nitro blue tetrazolium (NBT) staining and 261

3,3′-diaminobenzidine (DAB) staining tests to detect O2− and H2O2 accumulation, 262

respectively. Extensive NBT staining was observed in del1 plants, whereas the 263

staining was minimal in wild-type leaves (Fig. 5a). A brown color was seen for the 264

DAB staining, correlating with the area of leaf senescence, but there was no sign of 265

this in wild-type leaves (Fig. 5b). These results revealed that ROS accumulated in 266

del1 plants. During senescence, plant cell membrane damage can lead to a change in 267

electrolyte leakage (Blum and Ebercon, 1981). In del1 plants, the electrolyte leakage 268

was 45.8% higher than that in the wild-type (Fig. 5c), suggesting that del1 lost more 269

membrane integrity during development than the wild-type. 270

Plant senescence can lead to the synthesis of anti-oxidative enzymes to remove 271

ROS (Miller et al., 2010). Therefore, we quantitatively determined the activity of 272

these enzymes. The results indicated that the activities of superoxide dismutase 273

(SOD) and peroxidase (POD) increased in del1 plants, at 100.3 and 110.4 U/mg 274



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fresh weight (FW) in del1 leaves, which were much higher than the levels of 62.2 275

and 102.3 U/mg FW in the wild-type leaves, respectively (Fig. 5d, e). In the process 276

of leaf senescence, ROS-scavenging systems may play an important role in ROS 277

detoxification (Tan et al., 2014). ROS-scavenging-related genes [alternative oxidases 278

(AOXs), ascorbate peroxidase (APX), superoxide dismutase (SOD), and catalase 279

(CAT)] were up-regulated during leaf senescence (Tan et al., 2014). As expected, the 280

expression levels of ROS-scavenging-related genes (AOX1a, AOX1b, APX1, APX2, 281

SODB, SODA1, catA, and catB) were 2.5 to 13.6 times higher than in the wild-type 282

(Fig. 5f). 283

Leaf senescence is the final stage of leaf development, and it is considered to be a 284

type of PCD (Nooden and Leopold, 1978). Trypan blue (TB) staining revealed that 285

the leaf apex and leaf margin of del1 were colored blue, but the counterpart 286

wild-type remained green (Fig. 5g), suggesting that some of the cells in the leaf apex 287

and leaf margin of the del1 plant were dead. One basic feature of PCD is the 288

condensation of nuclear chromatin, which is caused by endonucleolytic degradation 289

of nuclear DNA (Simeonova et al., 2000). We accordingly used the TUNEL assay to 290

determine whether the del1 plants induced PCD. A few of the nuclei in the wild-type 291

were TUNEL-positive; in contrast, most nuclei in the del1 leaf sections were 292

TUNEL-positive (Fig. 5h–k), indicating that DNA degradation was widespread in 293

the del1 leaves. 294

Map-based cloning of DEL1 295

To determine the molecular basis for the del1 phenotypes, a map-based cloning 296

approach was employed to isolate the corresponding gene. The mapping population 297

was generated by crossing DEL1 with Taichung Native 1, a wild-type indica variety 298

with DNA polymorphism with japonica. All the F1 plants exhibited a normal 299

phenotype matching that of the wild-type. In the F2 segregating populations, normal 300

and mutant phenotypes showed a typical segregation ratio of 3:1 (Table S2). This 301

finding suggests that del1 is controlled by a single recessive nuclear gene. 302

Thirty F2 plants with the del1 phenotype were used for primary mapping, and 303

DEL1 was found to be located on the long arm of chromosome 10 between markers 304



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M1 and M14. Furthermore, by using 1081 homozygous mutant plants, DEL1 was 305

further narrowed down to an approximately 45-kb region with molecular markers as 306

shown in Supplemental Table 5. This 45-kb region is in the BAC AC025905 and 307

contains eight putative open-reading frames (ORFs), as annotated by the MSU Rice 308

Genome Annotation Project (Fig. 6a). Upon sequencing analysis of these eight ORFs, 309

one base-pair mutation was found at position 1940 of ORF LOC_Os10g31910. This 310

change from G to T causes a substitution at the 365th amino acid residue from 311

tryptophan (Trp) to leucine (Leu) (Fig. 6b). By examining this base in six other rice 312

varieties, we found that they all exhibited the wild-type genotype (Fig. S4). 313

To confirm that LOC_Os10g31910 is responsible for the del1 phenotype, a 314

7843-bp wild-type DEL1 DNA fragment, containing the promoter region and the 315

entire ORF, was introduced into del1 plants by Agrobacterium tumefaciens-mediated 316

transformation. Analysis of independent transgenic plants by PCR using primers 317

flanking the mutation site, together with further sequencing, revealed a double peak 318

(G and T) at the mutation site, confirming the presence of normal DEL1 gene 319

sequence (Fig. 6c). The transgenic plants rescued the phenotypes of del1, whereas in 320

all of those transformed by pCAMBIA1300, there was a failure to rescue the mutant 321

phenotype, confirming that disruption of the DEL1 gene was responsible for the del1 322

mutant phenotype (Fig. 6d–i). In addition, RNAi transgenic plants exhibited early 323

senescence leaves and a significantly reduced size (Fig. S5a–e). The expression of 324

DEL1 was significantly decreased in RNAi plants (Fig. S5f). Therefore, we conclude 325

that LOC_Os10g31910 is the DEL1 gene. 326

DEL1 encodes a pectate lyase precursor 327

Sequence analysis indicated that DEL1 cDNA is 1476 bp in length and encodes a 328

protein of 491 amino acid residues (Fig. 7a). A search using SignalP and Pfam 329

revealed that the DEL1 protein contains a 28-amino-acid signal peptide and one 330

predicted PelC domain (Fig. 7a). Multiple sequence alignment analysis revealed that 331

DEL1 contains all the conserved residues of PELs known to be involved in Ca2+ 332

binding, substrate binding, and catalysis, and has stronger similarity with plant PelC 333

than Erwinia chrysanthemi (Fig. S6). 334



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An unrooted phylogenetic tree was built among PEL members of rice, Arabidopsis, 335

and seven known plant PELs using the neighbor-joining method, which revealed that 336

PEL were divided into five major clades, with clade I being further divided into four 337

sub-clades (Fig. 7b). DEL1 belongs to Ic and is in the same clade as PMR6 (a 338

powdery mildew susceptibility) of Arabidopsis (Vogel et al., 2002). 339

DEL1 was highly expressed in elongating tissues 340

To analyze the spatial and developmental expression of the DEL1 genes, we isolated 341

RNA from different tissues, including young roots, young sheaths, young leaves, 342

mature roots, mature sheaths, mature leaves, culms, panicles, and spikelets, and 343

determined the transcript levels of the DEL1 genes by real-time RT-PCR. The results 344

revealed that DEL1 was ubiquitously expressed in all the tissues examined at the 345

young and mature stages, and high levels of DEL1 expression were observed in 346

elongating tissues, such as culms and roots (Fig. 8a). 347

In addition, to analyze the spatial expression pattern of DEL1, we expressed the 348

β-glucuronidase (GUS) gene under the control of the native promoter of the DEL1 349

gene. Six independent DEL1:GUS transgenic lines were analyzed and all of them 350

exhibited similar results. The GUS activity was expressed in all of the tissues and 351

was consistent with the qRT-PCR data (Fig. 8b–j). 352

Mutation of DEL1 decreased total PEL activity and altered cell wall 353

composition and structure 354

Since PelC is the only domain identified in DEL1, it may be critical for its function. 355

Therefore, we determined the total PEL activity. As expected, PEL enzyme activity 356

was significantly decreased in del1 plants. Especially in culms, the PEL activity was 357

only 32.0% of that in the wild-type (Fig. 9a). This result is consistent with the real 358

time RT-PCR (Fig. 8a) and the ProDEL1:GUS expression results (Fig. 8b–j). 359

The morphological phenotypes suggested that the cell wall structure in the mutant 360

plants may also be altered. We therefore analyzed the structure of wild-type and del1 361

plants by TEM. The results revealed that the wall thicknesses of bundle sheath fiber 362

cells in del1 culms were altered (Fig. 9d-g). Specifically, the thicknesses of the 363

middle lamella and secondary cell wall were reduced by 51.6% and 40.6%, 364



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respectively, and that of the primary cell wall was 15.6% higher than those of the 365

wild-type (Fig. 9h-j). Similarly in roots, the thicknesses (sclerenchyma cell) of the 366

middle lamella and secondary cell wall were reduced by 18.5% and 41.4%, 367

respectively, and that of the primary cell wall was 12.7% higher than those of the 368

wild-type (Fig. S7). 369

To determine whether changes in the cell wall structure affected the wall 370

composition, we analyzed the cellulose, hemicellulose, and pectin contents and 371

compared them between wild-type and del1 culms. The cellulose content of del1 was 372

reduced by approximately 20%, while the contents of hemicellulose 1 (HC 1), 373

hemicellulose 2 (HC 2), and pectin were increased by 58.3%, 27.3%, and 117.2%, 374

respectively (Fig. 9b). In addition, the levels of seven neutral monosaccharides were 375

also determined and compared between the wild-type and del1 plants. All the neutral 376

monosaccharides in del1 exhibited significant increases, except for xylose (Fig. 9c). 377

These results suggest that the DEL1 mutation causes complex compositional and 378

structural alterations in cell walls. 379

Mutation of DEL1 increased the degree of HG methylesterification 380

Given that PEL can catalyze the α-1,4 glycosidic linkages of demethylated HG by 381

β-elimination, we used immunohistochemical techniques to discern in situ aspects of 382

cell wall microstructures and locate polymers precisely. The second culms from 383

wild-type and del1 plants were probed using JIM5, LM18, and LM19 antibodies, 384

which are used to recognize partially demethylesterified and unesterified HG; JIM7 385

antibody, which labels moderately high extent of methylesterified HG; and 2F4 386

antibody, which binds to HG with degrees of methylesterification up to 40% 387

(Verhertbruggen et al., 2009; Held et al., 2011). As shown in Fig. 10, 388

immunolabeling of culm sections with JIM7, LM18, LM19, and 2F4 indicated an 389

apparent increase in the recognition of HG epitopes, while JIM5 exhibited a slight 390

increase, suggesting that the degree of methylesterified HG was higher in del1 391

plants. 392

Activation of cell wall and senescence related genes revealed by transcriptome 393

analysis 394



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To further unravel the function of DEL1 in rice, 10-day-old wild-type and del1 plants 395

were used for transcriptome analysis. A total of 491 differentially expressed genes 396

(DEGs) were found, with a P-value <0.05 (Table S3). Among these genes, 332 were 397

up-regulated and 159 were down-regulated in del1 plants (Table S3). Clusters of 398

orthologous groups of proteins (COG) functional catalogue showed that in DEGs 399

were assigned to 39.2% and 50.9% of the up and down-regulated genes, respectively 400

(Table S3). Most of the genes up-regulated in del1 were involved in secondary 401

metabolites biosynthesis, transport and catabolism, carbohydrate transport and 402

metabolism, lipid transport and metabolism (Table S3). The majority of the 403

down-regulated genes were associated with translation, ribosomal structure and 404

biogenesis, secondary metabolites biosynthesis, transport and catabolism and cell 405

wall/membrane/envelope biogenesis (Table S3). Of note, a set of the DEGs 406

associated with cell wall and senescence were significantly altered in del1 plants, 407

such as the pectin methylesterase gene (OsPME1), β-expansin gene (OsEXPB2), 408

peroxidase precursor gene (OsPOX1), protochlorophyllide oxidoreductase B gene 409

(OsPORA), etc (Kim et al., 2012; Sakuraba et al., 2013; Zou et al., 2015; Fang et al., 410

2016) (Table S4). These results suggested that the mutation of DEL1 might affect the 411

expression of cell wall and senescence related genes in an indirect manner. 412

413

DISSCUSSION 414

Pectate lyase is an endogenous pectin-degrading enzyme that is capable of cleaving 415

α-1,4-glycosidic linkages in demethylated pectin by β-elimination (Palusa et al., 416

2007). It is a ubiquitous enzyme in higher plants and is encoded by at least 26, 22, 417

and 14 genes in Arabidopsis, poplar (Populus trichocarpa), and rice (Oryza sativa 418

L.), respectively (Palusa et al., 2007). Although several PLL genes are considered to 419

play potentially diverse physiological roles in plants, such as being expressed in 420

anthers and pollen, and being involved in fruit softening and ripening, pathogen 421

defense, and tissue/plant growth and development, their molecular mechanism in 422

monocots remains largely unknown. Here, we identified DEL1 as a pectate lyase 423

precursor in model monocot rice using a forward genetic approach; it contains a 424



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PelC domain and represents a multi-gene family in rice. DEL1 is crucial for plant 425

growth and leaf senescence. The loss of function of DEL1 reduced the total PEL 426

enzymatic activity, increased the degree of methylesterified HG, and perturbed the 427

cell wall structure and composition, resulting in retardation of the cell cycle and 428

enhancement of ROS activity. These results reveal a dual molecular function of PLL 429

genes in rice. 430

DEL1 impacts plant growth by regulating cell cycle progression 431

Cell division/expansion is a fundamental, dynamic cellular process driving plant 432

growth and development, and enables the plant and various organs to develop to 433

suitable sizes (Duan et al., 2012). The orderly development process involves many 434

genes and pathways that affect plant organ size by altering cell number, cell size, or 435

both (Krizek, 2009). Although recent studies have uncovered some key regulators 436

and genes that affect plant organ size, the intrinsic mechanisms responsible for organ 437

size variation are yet to be fully understood (Krizek, 2009; Duan et al., 2012). In this 438

study, we identified a PLL gene, DEL1, that appeared to play an important role in the 439

control of organ size in rice. In del1 plants, various organs were dramatically 440

reduced in size, including in terms of root length, leaf size, plant height, grain size, 441

and panicle and internode length (Fig. 1; Table 1). Inside the organs, paraffinized 442

sections of internodes revealed that cell number was lower in the del1 plants (Fig. 2), 443

suggesting that cell division is inhibited in the mutant. 444

Cell division requires a range of complicated processes that must be strictly 445

executed in a spatially and temporally controlled manner (Dewitte and Murray, 446

2003). The inhibition of cell division could alter cell cycle progression and affect 447

plant development (Dewitte and Murray, 2003). Our study demonstrates that the cell 448

cycle in the G1 phase was significantly retarded in del1 plants (Fig. 3a–c). Recent 449

evidence has indicated that a variety of cell cycle regulators play roles as targets 450

coupling cell proliferation with development, and their proper functioning is crucial 451

for patterning (Ramirez-Parra et al., 2005). Consistent with the flow cytometric 452

results, the expression levels of genes regulating the G1 phase of the cell cycle were 453

down-regulated in del1, and no significant difference was observed in the G2 phase 454



16

(Fig. 3d). These results strongly suggest that DEL1 controls plant growth by 455

regulating cell cycle progression. 456

DEL1 contributes to early leaf senescence through ROS accumulation 457

Leaf senescence is a complex process that involves many highly organized 458

molecular and cellular changes, such as the disintegration of chloroplasts; 459

down-regulation of photosynthesis; degradation of nucleic acids, proteins, and lipids; 460

and recycling of nutrients (Lim et al., 2007). This process is controlled by both 461

internal and external factors. To date, although many SAGs and/or transcription 462

factors have been identified, the complex mechanisms responsible for leaf 463

senescence in rice remain poorly understood. Recently, Wu et al. (2013) identified 464

the novel leaf senescence gene OsPSE1, which encodes a pectate lyase. Mutation of 465

OsPSE1 displays a premature senescence phenotype. In our study, we identified a 466

PLL gene, DEL1, which also appears to play a general role in leaf senescence. TEM 467

observation, physiological analysis, and TUNEL assays showed that leaf senescence 468

was induced in del1 plants, resulting in the withering and cracking of leaves (Fig. 4). 469

Moreover, the up-regulated expression levels of SAGs and transcription factors also 470

demonstrate leaf senescence in del1 plants (Fig. 4i). 471

Reactive oxygen species are by-products of various metabolic processes such as 472

photosynthesis and respiration in chloroplasts, mitochondria, and peroxisomes (Apel 473

and Hirt, 2004). They can cause oxidative damage to thylakoid membranes and other 474

cellular components, and assume several important roles in leaf senescence (Wang et 475

al., 2015). In the present study, staining by NBT and DAB indicated the 476

accumulation of O2− and H2O2 in del1 plants (Fig. 5a, b), and there was also an 477

elevated level of electrolyte leakage, which is a marker of cell membrane damage 478

(Fig. 5c). Meanwhile, the activities of SOD and POD were increased in del1 plants 479

(Fig. 5d, e). These results indicate that leaf senescence in del1 plants is triggered by 480

the accumulation of ROS. Under normal physiological conditions, cells control ROS 481

levels by balancing the generation of ROS with their elimination by the ROS 482

scavenging system, but the overproduction of ROS can trigger retrograde signaling 483

from chloroplasts to the nucleus, resulting in alteration of the expression of 484



17

nuclear-encoded genes (Tan et al., 2014). Consistent with this, the expression of 485

ROS-scavenging genes was significantly up-regulated (Fig. 5f). In addition, 486

transcriptome analysis also revealed that a set of the DEGs associated with 487

senescence was significantly altered in del1 plants (Table S4). 488

Taking these findings together, it is clear that ROS accumulation-mediated 489

chloroplast membrane breakage and chloroplast degradation play an important role 490

in leaf senescence in the del1 plants. 491

Possible molecular mechanism of DEL1 responsible for the mutant phenotypes 492

Pectate lyase-like genes have been shown to exhibit a broad range of functions in 493

plants, which depend on the degradation of demethylesterified HG and alteration of 494

cell wall composition and structure (Yadav et al., 2009; Biswal et al., 2014). In the 495

process of fruit ripening, the cell wall needs to loosen the xyloglucan-cellulose 496

network and pectin solubilization, this processes increasing the access of degradative 497

enzymes to their substrates (Brummell, 2006). For pathogen defense, the 498

accumulation of pectin increases hydrogen bonding in the extracellular matrix, 499

resulting in decreased nutrient availability to the pathogen (Vogel et al., 2002). The 500

decrease of de-esterified pectin in cotton fiber can promote its elongation (Wang et 501

al., 2010). Our study also demonstrates that the mutant phenotype of del1 depends 502

on the alteration of cell wall composition and structure. Despite our failure to purify 503

the fusion DEL1 protein via prokaryotic expression in E. coli or transient expression 504

in Nicotiana benthamiana (data not shown), the mutant phenotype indicated that 505

DEL1 protein plays an important role in rice growth and leaf senescence. 506

Many cell-wall-related mutants display abnormal growth and morphogenesis 507

(Pien et al., 2001). It has been speculated that cell wall biogenesis and modification 508

are tightly associated with cell growth via key genes at the interface of 509

morphogenesis, the cell cycle, and cell wall biogenesis (Somerville et al., 2004; 510

Zhang et al., 2010). In rice, the Brittle Culm 12 gene, encoding a kinesin-4 protein, 511

has been implicated in cell cycle progression, cellulose microfibril deposition, and 512

wall composition (Zhang et al., 2010). In our study, the del1 mutant exhibited cell 513

wall abnormalities and the retardation of cell cycle progression, which indicates that 514



18

DEL1 is at the interface between the cell cycle and cell wall biogenesis. 515

The dynamic interactions of plant cells depending on the status of pectin in the 516

cell wall form an important regulatory mechanism of growth and development (Wolf 517

et al., 2012). The degree of HG methylesterification has a large effect on the physical 518

properties of the cell wall (Held et al., 2011). A high degree of HG 519

methylesterification impedes the formation of calcium-mediated cross-linking 520

complexes, which is thought to promote cellular expansion by increasing wall 521

flexibility (Wolf et al., 2009). Our findings revealed that the degree of 522

methylesterified HG was increased, as determined by immunohistochemical assay, 523

which indicates that the cell wall loosened and expanded in the del1 plants (Fig. 10). 524

Consistent with this, the cell length was significantly increased and the expression 525

levels of expansion were all dramatically up-regulated in the del1 plants (Fig. 2g, h. 526

Fig. S8). These results indicate that the function of DEL1 affects not only cell 527

number, but also cell expansion. 528

In addition, our findings also revealed an early leaf senescence phenotype in 529

comparison to that in wild-type plants. This initially appears paradoxical, but it could 530

potentially be explained by the alterations of cell wall structure. Pectin OGs are 531

oligomers of α-1,4-linked galacturonosyl residues and are released by PEL and 532

PG-mediated breakdown of HG (Cote et al., 1998). Oligogalacturonides can produce 533

ROS signal molecules and trigger many abiotic stress responses in plants (Ferrari et 534

al., 2013). In our study, mutation in DEL1 significantly increased ROS content. We 535

speculate that DEL1 may participate in the OG-mediated ROS pathway that affects 536

leaf senescence. 537

We hypothesize a conceptual model that by tuning HG methylesterification, cell 538

wall component and structure might act as downstream components of the regulatory 539

networks that control cell cycle and expansion, as well as ROS, enabling normal 540

growth and leaf senescence in rice (Fig. 11). 541

542

MATERIALS AND METHODS 543

Plant materials 544



19

The rice del1 mutant was isolated from ethyl methanesulfonate (EMS)-treated 545

japonica cultivar Nipponbare, as described previously (Guo et al., 2006). An F2 546

mapping population was generated from a cross between del1 and an indica cultivar, 547

Taichung Native 1 (TN1). All plants were cultivated in paddies in Hangzhou (HZ, 548

119°54′ E, 30°04′ N) and Hainan (HN, 110°00′ E, 18°31′ N), during rice-growing 549

seasons. 550

Paraffin sectioning and transmission electron microscopy (TEM) analysis 551

For paraffin sectioning, the samples were fixed in 50% ethanol, 0.9 M glacial acetic 552

acid, and 3.7 % formaldehyde overnight at 4°C, then dehydrated with a graded series 553

of ethanol, infiltrated with xylene, and embedded in paraffin (Sigma). The specimens 554

were sectioned (8 μm thickness) with a Leica RM2245, transferred onto glass slides 555

with poly-L-lysine-coated, deparaffinized with xylene series, and dehydrated 556

through an ethanol series (Ren et al., 2016). The samples section was conducted 557

using a Nikon Eclipse 90i microscope. 558

For TEM, the samples were fixed in 2.5% glutaraldehyde in phosphate-buffered 559

saline (PBS) for at least 4 h and washed in PBS three times. Then, they were 560

post-fixed with 1% (w/v) OsO4 for 2 h after extensive washing in PBS, dehydrated 561

with a graded ethanol series, and infiltrated with Suprr Kit (Sigma). The specimens 562

were then sectioned (70 nm ultra-thin) with a Leica EM UC7 ultratome and the 563

sections was stained by uranyl acetate and alkaline lead citrate for 10 min before 564

being observed by TEM with a Hitachi Model H-7650. 565

Flow cytometric analysis 566

Cell cycle analysis was performed in accordance with the method described by 567

Galbraith et al. (1983). In brief, suspension cells were cut using a razor blade and 568

placed in ice-cold Galbraith’s buffer (45 mM MgCl2, 30 mM sodium citrate, 20 mM 569

MOPS, 0.1% TritonX-100, pH 7.0). The homogenates were then passed through a 570

20-µm mesh to remove cellular debris. After staining with 571

4,6-diamidino-2-phenylindole (DAPI, 2 µg ml−1), the nuclei were analyzed using 572

FACSAria II flow cytometer (BD Bioscience, San Jose, CA, USA). A total of 30,000 573

events were recorded, and three independent flow cytometric experiments were 574



20

carried out and analyzed using the ModFit LT (Verity Software House, Inc., Maine, 575

CA) and FlowJo V10 software (Tree Star Inc., Ashland, OR). 576

Chlorophyll content and net photosynthesis rate 577

A total 0.2 g of samples from wild-type and del1 leaves were extracted with 80% 578

acetone. The chlorophyll content was determined according to the method as 579

previously described (Yang et al., 2015). Net photosynthesis rate was measured 580

using Walz GFS-3000 (Eichenring, Germany). Parameter settings were accordance 581

with the manufacturer’s instructions. 582

Histochemical staining and ROS-scavenging enzyme assays 583

DAB and NBT staining was used to detect the accumulation of ROS, as previously 584

described (Blum and Ebercon, 1981). TB staining was performed as described 585

previously (Koch and Slusarenko, 1990). Electrolyte leakage was determined in 586

accordance with a previous study (Zhou and Guo, 2009). Assays of the activities of 587

SOD and POD were conducted in accordance with previously described methods 588

(Wang et al., 2013). 589

TUNEL assays 590

The TUNEL assays were performed as described previously (Huang et al., 2007). 591

The leaves were fixed in 4% paraformaldehyde in 0.1 M PBS containing 0.1% 592

Tween 20 and Triton X-100 at 4°C overnight and embedded in paraplasts. The 593

sections of leaves (8 μm thickness) were treated using a Fluorescein In Situ Cell 594

Death Detection Kit (Roche, Switzerland). The green fluorescence of fluorescein and 595

blue fluorescence of DAPI was analyzed using a Carl Zeiss LSM 710 laser-scanning 596

confocal microscope (Gottingen, Germany). 597

Gene cloning and complementation 598

For genetic analysis, 1081 F2 mutant plants were used for fine mapping of the DEL1 599

locus. The molecular markers of polymorphism are listed in Table S5. The markers 600

were designed using Primer 5 software (Primer-E Ltd). Gene prediction and 601

sequence analysis were performed using the publicly available rice databases, 602

including Gramene (http://www.gramene.org) and the Rice Genome Annotation 603

Project (http://rice.plantbiology.msu.edu/index.shtml). For the complementation 604



21

construct, a 7843-bp genomic DNA fragment containing the entire DEL1 coding 605

region, a 1998-bp upstream sequence, and an 841-bp downstream region was 606

amplified using KOD FX (Toyobo, Japan) from Nipponbare genomic DNA and 607

inserted into the binary vector pCAMBIA 1300. The recombinant binary vector was 608

introduced into Agrobacterium tumefaciens strain EHA105 by electroporation and 609

transformed into the del1 mutant callus as described previously (Hiei et al., 1994). 610

For the RNAi construct, a 336-bp fragment was amplified by PCR from Nipponbare 611

cDNA and inserted into the vector pTCK303. The recombinant binary vector was 612

transformed into the Nipponbare callus. The primer sequences used in this study are 613

listed in Table S5. 614

Phylogenetic analysis and protein domain identification 615

Annotated proteins of DEL1 domains were identified in the Pfam database 616

(http://pfam.xfam.org/). The signal peptide was predicted using SignalP version 4.1 617

(Petersen et al., 2011). Homologous protein sequences of DEL1 were identified 618

using the NCBI BLAST server (http://www.ncbi.nlm.nih.gov/). Amino acid 619

sequence alignments were conducted using ClustalX 2.1 (http://www.clustal.org/) 620

and DNAMAN version 5.0 (Lynnon Biosoft, San Ramon, CA, USA). A phylogenetic 621

tree was constructed using MEGA4 software (http://www.megasoftware.net/). 622

Gene expression analysis 623

Total RNA from roots, culms, sheaths, leaves and panicles at young and mature 624

stages, was extracted using the RNeasy plant mini kit (Qiagen, Valencia, CA, USA). 625

RNA reverse transcription was performed using ReverTra Ace real time PCR-RT Kit 626

with gDNA remover (Toyobo, Japan). After synthesis, the cDNA reaction was 627

diluted five times in TE buffer, and 1 μl was used for real time RT-PCR using the 628

SYBR Green PCR Master Mix kit (Applied Biosystems, Wellesley, MA, USA) and 629

gene-specific primers (Table S5) in ABI7900 (Applied Biosystems, Foster City, CA, 630

USA). The tissue-level expression pattern of DEL1 was analyzed using the 631

β-glucuronidase (GUS) reporter gene. The promoter of DEL1 (2038 bp upstream of 632

ATG) was amplified from the genome DNA of Nipponbare and inserted into the 633

binary vector pCAMBIA1305 in-frame with the GUS reporter gene. The binary 634



22

vector was introduced into the Nipponbare callus to generate transgenic plants. The 635

positive transgenic plants were used to analyze the GUS reporter gene. Different 636

tissues of T1 plants were incubated at 37°C in 0.1 M X-Gluc in buffer [0.1 M 637

Na2HPO4-NaH2P4, pH 7.0, 10% Triton X-100, 0.5 M EDTA-Na, and 50 mM 638

K3Fe(CN)6] for approximately 12 h to examine GUS activity. After being cleaning in 639

70% ethanol, the tissues were photographed under a light microscope. 640

Enzyme activity assays 641

Pectate lyase enzyme activity assays were routinely performed using a modified 642

version of the method of Collmer et al. (1988). A total of 0.5 g of sample was 643

suspended in 1.5 ml of extraction buffer (20 mM sodium phosphate, pH 7.0, 20 mM 644

cysteine/HCl, 1% polyvinylpyrrolidone (PVP), mw 360,000 and 1 mM 645

phenylmethylsulfonyl fluoride (PMSF) and centrifuged at 10,000g for 30 min. The 646

supernatant was collected as the crude extract for enzyme assays. 647

The enzyme activity system consisted of 0.3% polygalacturonic acid (PGA) in 0.07 648

M Tris-HCl buffer (pH 8.0), 0.1 M CaCl2, crude extract protein, and sterile water. 649

The enzyme reaction was incubated at 37°C for 30 min, and then stopped by the 650

addition of 9% ZnSO4•7H2O and 0.5 M NaOH. The control tubes received the 651

enzyme after the addition of ZnSO4•7H2O and NaOH. One unit of PEL activity was 652

defined as the amount of enzyme that produces 1 mM of 4,5-unsaturated product in 1 653

min under the assay conditions. The activity of PEL is expressed in units per mg of 654

protein. Soluble protein concentrations were determined in accordance with 655

Bradford method (1976), using bovine serum albumin (BSA) as a standard. 656

Immunofluorescence microscopy 657

The culms of wild-type and del1 plant at the same development stage were fixed and 658

embedded in glycol methacrylate. Two-micrometer-thick sections were cut with a 659

Leica RM2265. Immunolabeling was performed in accordance with the 660

methodology of Willats et al., (2001). The primary antibodies JIM5, JIM7, LM18, 661

LM19, and 2F4 were used at a 1:10 dilution in PBS containing 5% (w/v) fat-free 662

milk powder (5% M/PBS) and the secondary antibody (goat anti-rat IgG coupled 663

with fluorescein isothiocyanate, FITC) were used at dilution of 100-fold in 5% 664



23

M/PBS. Sections incubated without primary antibody were used as controls to assess 665

the autofluorescence of the samples. The labeled sections were observed using Carl 666

Zeiss LSM 710 confocal microscope. 667

Compositional analysis of neutral glycosyl residues and cellulose content 668

Alcohol-insoluble residues (AIRs) of culms were prepared as described by Zhang et 669

al., (2012). In briefly, de-starched AIRs samples were hydrolyzed in 2 M 670

trifluoroacetic acid at 121°C for 90 min. The samples were centrifuged to collect the 671

supernatants, air-dried and then dissolved with a 1 M ammonium hydroxide buffer 672

containing NaBH4. The alditol acetate derivatives were analyzed using an Agilent 673

7890 GC system equipped with a 5975C MSD (GC-MS) (Song et al., 2013). To 674

measure the crystalline cellulose content, the pellets remaining after trifluoroacetic 675

acid treatment were hydrolyzed with Updegraff reagent (Updegraff, 1969). The 676

samples were subsequently centrifuged and the supernatant removed. The pellets 677

were then treated with 72% sulfuric acid. The cellulose content was quantified via an 678

anthrone assay, and three replicates were included. 679

Cell wall extraction and measurement of polysaccharide content 680

Cell wall materials and fractionation components were analyzed in accordance with 681

the methods of Zhong and Lauchli (1993). The samples were ground in liquid 682

nitrogen to a fine power and suspended in 75% ethanol for 25 min in an ice-cold 683

water bath. The samples were then centrifuged at 12,000 rpm for 15 min and 684

removed the supernatant. Next, the pellet was suspended and washed with precooled 685

acetone, followed by methanol:chloroform, and then with methanol. The remaining 686

pellet as a crude cell wall fraction was freeze-dried and stored at 4°C for future use. 687

The cell wall extracts were fractionated into three parts: pectin, HC 1 and HC 2. First, 688

the pectin fraction was extracted twice using 0.5% ammonium oxalate buffer 689

containing 0.1% NaBH4 (pH 4) in a boiling water bath for 1 h. Next, the pellets were 690

subjected to triple extractions with 4% KOH containing 0.1% NaBH4 at room 691

temperature for 8 h each, followed by a similar extraction with 24% KOH containing 692

0.1% NaBH4. The HC 1 and HC 2 fractions were referred to as hemicellulose 693

material (Yang et al., 2008). The uronic acid content in the pectin fraction was 694



24

assayed in accordance with the method of Blumenkrantz and Asboe-Hansen (1973) 695

using galacturonic acid (GalA) as a standard. 696

Transcriptome sequencing and data analysis 697

The RNA samples from 10-day-old wild-type and del1 plants were used for 698

transcriptome sequencing, and each sample was pooled for total RNA isolation with 699

three biological replicates. Total RNA was extracted using TRIzol® reagent 700

(Invitrogen Life Technologies, Carlsbad, CA, USA). Transcriptome sequencing was 701

performed in Biomarker Biotechnology Corporation (Beijing, China) using the 702

Illumina system HiSeq2500 (Illumina Inc., San Diego, CA, USA) according to the 703

standard procedure. Transcriptome assembly was performed according to the 704

protocol described previously (Yu et al., 2013). Differentially expressed genes were 705

defined by using IDEG6 (Romualdi et al., 2003), at a significance level of P<0.05. 706

Functional annotation analysis of DEGs in wild-type and del1 plants was performed 707

by DAVID Web tools (Huang et al., 2008). 708

709

Accession Numbers 710

Sequence data from this article can be found in the EMBL/GenBank data libraries 711

under the following accession numbers: DEL1 (LOC_Os10g31910), PMR6 712

(At3g54920), NJJS25 (AF339024), PtxtPL1-27 (EU379971), ZePel (Y09541), 713

MaPel (AAF19195), GhPel (ADB90478), CryjⅠ(BAA05542), SGR 714

(LOC_Os09g36200), OsNAC2 (LOC_Os01g66120), Osl2 (LOC_Os04g52450), 715

OsH36 (LOC_Os05g39770), OsWRKY23 (LOC_Os01g53260), OsWRKY72 716

(LOC_Os11g29870), CDKA1 (LOC_Os03g02680), CAK1 (LOC_Os06g07480), 717

CAK1A (LOC_Os06g22820), CMC5 (LOC_Os02g55410), CYCT1 718

(LOC_Os02g24190), CYCA2.2 (LOC_Os12g31810), CYCA2.3 (LOC_Os01g13260), 719

CYCB2.2 (LOC_Os06g51110), AOX1a (LOC_Os04g51150), AOX1b 720

(LOC_Os04g51160), APX1 (LOC_Os03g17690), APX2 (LOC_Os07g49400), SODB 721

(LOC_Os06g05110), SODA1 (LOC_Os05g25850), catA (LOC_Os02g02400), catB 722

(LOC_Os06g51150), OsEXPA1 (LOC_Os04g15840), OsEXPA2 723

(LOC_Os01g60770), OsEXPA5 (LOC_Os02g51040), OsEXPA10 724



25

(LOC_Os04g49410), OsEXPA32 (LOC_Os08g44790), OsEXPB3 725

(LOC_Os10g40720), OsEXPB5 (LOC_Os04g46650), OsEXPB9 (LOC_Os10g40090) 726

and OsEXPB11 (LOC_Os02g44108). 727

728

ACKNOWLEDGMENTS 729

We are grateful to Dr. Yihua Zhou (Institute of Genetics and Developmental Biology, 730

Chinese Academy of Sciences) for help with the monosaccharide and cellulose 731

analyses; Dr. Yong Hu (Capital Normal University) for help with the flow cytometric 732

analysis; and Dr. Paul Knox (Centre for Plant Science, University of Leeds, UK) for 733

kindly providing the protocol for the immunofluorescence assay. 734

735

Figure legends 736

Figure 1. Comparison of phenotype between wild-type and del1 plants 737

(a) Wild-type (Nipponbare, left) and del1 plants (right) 5 days after sowing. Scale 738

bar = 2 cm. (b) Root length of wild-type (left) and del1 plants (right) 5 days after 739

sowing. Scale bar = 1 cm. (c and d) Statistical analysis of root length and lateral root 740

number between wild-type and del1 plants. Twenty plants were measured. Error bars 741

indicate SD, ** indicates P<0.01 (Student’s t-test). (e) Wild-type (left) and del1 plants 742

(right) at maturity. Scale bar = 10 cm. (f and g) Statistical analysis of plant height 743

and tiller number between wild-type and del1 plants. Twenty plants were measured. 744

Error bars indicate SD, ** indicates P<0.01 (Student’s t-test). (h) Phenotype of 745

panicle between wild-type (left) and del1 (right) plants. Scale bar = 5 cm. (i) Floret 746

with the lemma removed, wild-type (left) and del1 (right). Scale bar = 0.5 cm. (j) 747

Mature seed and brown rice of wild-type (left) and del1 (right). Scale bar = 0.5 cm. 748

(k) and (l) Statistical analysis of panicle length and thousand grain weight between 749

wild-type and del1 plants. Twenty panicles were measured. Error bars indicate SD, ** 750

indicates P<0.01 (Student’s t-test). 751

752

Figure 2. Histological characterization of culms in wild-type and del1 plants 753

(a–d) Cross sections of internode II of wild-type (a) and del1 (b). Scale bar = 500 μm. 754



26

(c) Magnification of (a), (d) magnification of (b); white rectangle shows a 755

magnification of the sclerenchyma cell layer. Scale bar = 50 μm. (e and f) Statistical 756

analysis of cell number and sclerenchyma cell layer number between wild-type and 757

del1 plants, means ± SD of five independent replicates. (g and h) Longitudinal 758

sections of internode II of wild-type (g) and del1 (h). Scale bar = 50 μm. (i and j) 759

Statistical analysis of the cell length and cell width between wild-type and del1 760

plants, mean ± SD of 30 cells. ** indicates P<0.01 (Student’s t-test). (k) Number of 761

parenchyma cells (PCs) for internode II of wild-type and del1 plants, means ± SD of 762

five independent replicates. 763

764

Figure 3. Cell cycle analysis of wild-type and del1 plants 765

(a and b) Flow karyotype histogram of wild-type (a) and del1 (b) leaves. (c) 766

Quantification of the DNA profiles of wild-type and del1 plants. (d) Relative 767

expression levels of cell-cycle-related genes in wild-type and del1 plants, means ± 768

SD of three independent replicates. * indicates P<0.05, ** indicates P<0.01 (Student’s 769

t-test). 770

771

Figure 4. Leaf phenotype and identification of leaf senescence in DEL1 772

(a–d) Leaf phenotype from young (a), tillering (b, c), and heading (d) stages. Scale 773

bars = 1 cm, 5 cm, 5 cm and 1 cm, respectively. (e) Statistical analysis of chlorophyll 774

content between wild-type and del1 plants, means ± SD of five independent 775

replicates. ** indicates P<0.01 (Student’s t-test). (f and g) Transmission electron 776

microscopy analysis of senescence leaves of wild-type (f) and del1 plants (g). Scale 777

bar = 0.5 μm. (h) Statistical analysis of photosynthesis rate between wild-type and 778

del1 plants, means ± SD of five independent replicates. ** indicates P<0.01 779

(Student’s t-test). (i) Relative expression levels of senescence-related genes and 780

transcription factors in wild-type and del1 plants, means ± SD of three independent 781

replicates. * indicates P<0.05, ** indicates P<0.01 (Student’s t-test). 782

Figure 5. ROS accumulation and enhancement of PCD in wild-type and del1 783

leaves 784



27

(a and b) NBT and DAB staining of leaves between the wild-type (left) and del1 785

plants (right). (c–e) Statistical analysis of electrolyte leakage (c), SOD activity (d), 786

and POD activity (e) in leaves between wild-type and del1 plants, means ± SD of 787

five independent replicates. ** indicates P<0.01 (Student’s t-test). (f) Relative 788

expression levels of ROS detoxification-related genes in wild-type and del1 plants, 789

means ± SD of three independent replicates. ** indicates P<0.01 (Student’s t-test). (g) 790

Trypan blue staining of leaves in wild-type (left) and del1 plants (right). (h–k) 791

TUNEL assay of leaves. DAPI staining of wild-type (h) and del1 plants (j). Positive 792

results of wild-type (i) and del1 plants (k), scale bar = 50 μm. 793

794

Figure 6. Map-based cloning and identification of DEL1 795

(a) Fine mapping of DEL1. The del1 locus was mapped to a 45-kb region on 796

chromosome 10. (b) Schematic diagram of DEL1. Black rectangles represent exons. 797

Black inverted triangle represents mutant site. (c) Sequencing analysis of the DEL1 798

transcripts in T0 transgenic lines. (d and e) Phenotype of the complementation 799

transgenic line: wild-type (left), complementation transgenic line (middle) and 800

empty vector control (right). Scale bars = 10 cm and 4 cm, respectively. (f) 801

Expression levels of DEL1 detected by qRT-PCR in wild-type and transgenic plants, 802

means ± SD of three independent replicates. (g–i) Statistical analysis of plant height 803

(g), tiller number (h), and flag leaf length (i) in wild-type and transgenic plants, 804

means ± SD of ten independent replicates. 805

806

Figure 7. Prediction of the primary sequence and phylogenetic analysis of DEL1 807

(a) The deduced amino acid sequence of DEL1. Numbers on the left refer to the 808

positions of amino acid residues. The signal peptide is indicated with an underline; 809

the PelC domain is shown by a dotted line; the conserved residues involved in Ca2+ 810

binding (red background), disulfide bonds (orange background), catalysis (blue 811

background), and substrate binding (purple background) (b) Phylogenetic tree of 812

PEL in Arabidopsis thaliana, Oryza sativa L., and other plants. The numbers at each 813

node represent the bootstrap support (percentage), and scale bar is an indicator of 814



28

genetic distance based on branch length. 815

816

Figure 8. Expression analysis of DEL1 817

(a) Transcription level of DEL1 in various organs, means ± SD of three independent 818

replicates. YR, young root; YL, young leaf; YS, young sheath; MR, mature root; C, 819

culm; ML, mature leaf; MS, mature sheath; P, panicle; S, spikelet. (b–j) GUS 820

analysis of DEL1 expression: (b and c) Four and seven days after germination of 821

the young plant, scale bar = 1 cm; (d) root, scale bar = 500 μm; (e) lateral root, scale 822

bar = 250 μm; (f) mature sheath, scale bar = 1 cm; (g) mature leaf, scale bar = 1 cm; 823

(h) culm, scale bar = 1 cm; (i) spikelet, scale bar = 1 cm; (j) lemma and palea were 824

removed in (i), scale bar = 500 μm. 825

826

Figure 9. The levels of PEL activity and cell wall composition and structure in 827

wild-type and del1 plants 828

(a) Analysis of PEL activity in wild-type and del1 plants, means ± SD of five 829

independent replicates. ** indicates P<0.01 (Student’s t-test). (b) Comparison of cell 830

wall composition between wild-type and del1 plants, means ± SD of five 831

independent replicates. **indicates P<0.01 (Student’s t-test). HC 1: hemicellulose 1, 832

HC 2: hemicellulose 2. (c) Neutral monosaccharide composition between wild-type 833

and del1 plants, means ± SE of five independent replicates, ** indicates P<0.01 834

(Student’s t-test). (d and e) Transmission electron microscopy micrographs of the 835

bundle sheath fiber cells of wild-type (d) and del1 (e) plants, scale bar = 1 μm. (f) 836

Magnification in (d), and (g) magnification in (e), scale bar = 0.2 μm. ml: middle 837

lamella, pw: primary cell wall, sw: secondary cell wall, pm: plasma membrane, c: 838

cytoplasm. (h–j) Statistical analysis of the middle lamella (h) , primary cell wall (i), 839

and secondary cell wall (j) thicknesses of bundle sheath fiber cells between the 840

wild-type and del1 plants, mean ± SD of 30 cells, ** indicates P<0.01 (Student’s 841

t-test). 842

843

Figure 10. Immunohistochemical localization of HG in culm sections of 844



29

wild-type and del1 plants 845

(a–t) Immunolocalization of HG of wild-type (a, c) and del1 plants (b, d) with JIM7, 846

wild-type (e, g) and del1 plants (f, h) with JIM5, wild-type (i, k) and del1 plants (j, l) 847

with LM18, wild-type (m, o) and del1 plants (n, p) with LM19, wild-type (q, s) and 848

del1 plants (r, t) with 2F4. Scale bar = 50 μm. 849

850

Figure 11. A schematic model of DEL1 function in rice 851

Homogalacturonan is secreted in a highly methylesterified form and selectively 852

demethylesterified by PME. The demethylesterified HG might be cleaved by DEL1 853

and other PELs or PGs. The alternative of the cell wall regulated the cell cycle/ 854

expansion and ROS, enabling normal rice growth and leaf senescence process. 855

856

Supplemental Data 857

Supplemental Figure 1. Wild-type (Nipponbare, left) and del1 plants (right) at the 858

tillering stage. 859

Supplemental Figure 2. Statistical analysis of plant height from 30 to 110 days 860

between wild-type and del1 plants. 861

Supplemental Figure 3. Internode assessment of culms in the wild-type and del1 862

plants. 863

Supplemental Figure 4. Mutation position of wild-type, del1 and six other varieties. 864

Supplemental Figure 5. The phenotype of wild-type and RNAi transgenic plants. 865

Supplemental Figure 6. Protein sequence alignment of DEL1 and homologs. 866

Supplemental Figure 7. Cell wall structure in wild-type and del1 roots 867

Supplemental Figure 8. Expression analysis of cell expansion-related genes in 868

culms. 869

Supplemental Table 1. The basic agronomic traits in wild-type and del1 plants. 870

Supplemental Table 2. Segregation analysis of F2 phenotype from crosses of del1 871

and five crop strains (NPB, TN1, ZF802, NJ06, and 93-11). 872

Supplemental Table 3. Clusters of orthologous groups of proteins (COG) functional 873

catalogue of differentially expressed genes in del1 plants 874



30

Supplemental Table 4. Differentially expressed of cell wall and senescence related 875

genes in del1 plants. 876

Supplemental Table 5. Primers used for PCR in this study. 877

878

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1097



1

Figure 1. Comparison of phenotype between wild-type and del1 plants

(a) Wild-type (Nipponbare, left) and del1 plants (right) 5 days after sowing. Scale bar

= 2 cm. (b) Root length of wild-type (left) and del1 plants (right) 5 days after sowing.

Scale bar = 1 cm. (c and d) Statistical analysis of root length and lateral root number

between wild-type and del1 plants. Twenty plants were measured. Error bars indicate

SD, ** indicates P<0.01 (Student’s t-test). (e) Wild-type (left) and del1 plants (right) at

maturity. Scale bar = 10 cm. (f and g) Statistical analysis of plant height and tiller

number between wild-type and del1 plants. Twenty plants were measured. Error bars

indicate SD, ** indicates P<0.01 (Student’s t-test). (h) Phenotype of panicle between

wild-type (left) and del1 (right) plants. Scale bar = 5 cm. (i) Floret with the lemma

removed, wild-type (left) and del1 (right). Scale bar = 0.5 cm. (j) Mature seed and

brown rice of wild-type (left) and del1 (right). Scale bar = 0.5 cm. (k) and (l)

Statistical analysis of panicle length and thousand grain weight between wild-type and

del1 plants. Twenty panicles were measured. Error bars indicate SD, ** indicates

P<0.01 (Student’s t-test).



1

Figure 2. Histological characterization of culms in wild-type and del1 plants

(a–d) Cross sections of internode II of wild-type (a) and del1 (b). Scale bar = 500 μm.

(c) Magnification of (a), (d) magnification of (b); white rectangle shows a

magnification of the sclerenchyma cell layer. Scale bar = 50 μm. (e and f) Statistical

analysis of cell number and sclerenchyma cell layer number between wild-type and

del1 plants, means ± SD of five independent replicates. (g and h) Longitudinal

sections of internode II of wild-type (g) and del1 (h). Scale bar = 50 μm. (i and j)

Statistical analysis of the cell length and cell width between wild-type and del1 plants,

mean ± SD of 30 cells. ** indicates P<0.01 (Student’s t-test). (k) Number of

parenchyma cells (PCs) for internode II of wild-type and del1 plants, means ± SD of

five independent replicates.



1

Figure 3. Cell cycle analysis of wild-type and del1 plants

(a and b) Flow karyotype histogram of wild-type (a) and del1 (b) leaves. (c)

Quantification of the DNA profiles of wild-type and del1 plants. (d) Relative

expression levels of cell-cycle-related genes in wild-type and del1 plants, means ± SD

of three independent replicates. * indicates P<0.05, ** indicates P<0.01 (Student’s

t-test).



1

Figure 4. Leaf phenotype and identification of leaf senescence in DEL1

(a–d) Leaf phenotype from young (a), tillering (b, c), and heading (d) stages. Scale

bars = 1 cm, 5 cm, 5 cm and 1 cm, respectively. (e) Statistical analysis of chlorophyll

content between wild-type and del1 plants, means ± SD of five independent replicates.

** indicates P<0.01 (Student’s t-test). (f and g) Transmission electron microscopy

analysis of senescence leaves of wild-type (f) and del1 plants (g). Scale bar = 0.5 μm.

(h) Statistical analysis of photosynthesis rate between wild-type and del1 plants,

means ± SD of five independent replicates. ** indicates P<0.01 (Student’s t-test). (i)

Relative expression levels of senescence-related genes and transcription factors in

wild-type and del1 plants, means ± SD of three independent replicates. * indicates

P<0.05, ** indicates P<0.01 (Student’s t-test).



1

Figure 5. ROS accumulation and enhancement of PCD in wild-type and del1

leaves

(a and b) NBT and DAB staining of leaves between the wild-type (left) and del1

plants (right). (c–e) Statistical analysis of electrolyte leakage (c), SOD activity (d),

and POD activity (e) in leaves between wild-type and del1 plants, means ± SD of five

independent replicates. ** indicates P<0.01 (Student’s t-test). (f) Relative expression

levels of ROS detoxification-related genes in wild-type and del1 plants, means ± SD

of three independent replicates. ** indicates P<0.01 (Student’s t-test). (g) Trypan blue

staining of leaves in wild-type (left) and del1 plants (right). (h–k) TUNEL assay of

leaves. DAPI staining of wild-type (h) and del1 plants (j). Positive results of wild-type

(i) and del1 plants (k), scale bar = 50 μm.



1

Figure 6. Map-based cloning and identification of DEL1

(a) Fine mapping of DEL1. The del1 locus was mapped to a 45-kb region on

chromosome 10. (b) Schematic diagram of DEL1. Black rectangles represent exons.

Black inverted triangle represents mutant site. (c) Sequencing analysis of the DEL1

transcripts in T0 transgenic lines. (d and e) Phenotype of the complementation

transgenic line: wild-type (left), complementation transgenic line (middle) and empty

vector control (right). Scale bars = 10 cm and 4 cm, respectively. (f) Expression levels

of DEL1 detected by qRT-PCR in wild-type and transgenic plants, means ± SD of

three independent replicates. (g–i) Statistical analysis of plant height (g), tiller number

(h), and flag leaf length (i) in wild-type and transgenic plants, means ± SD of ten

independent replicates.



1

Figure 7. Prediction of the primary sequence and phylogenetic analysis of DEL1

(a) The deduced amino acid sequence of DEL1. Numbers on the left refer to the

positions of amino acid residues. The signal peptide is indicated with an underline; the

PelC domain is shown by a dotted line; the conserved residues involved in Ca2+

binding (red background), disulfide bonds (orange background), catalysis (blue

background), and substrate binding (purple background) (b) Phylogenetic tree of PEL

in Arabidopsis thaliana, Oryza sativa L., and other plants. The numbers at each node

represent the bootstrap support (percentage), and scale bar is an indicator of genetic

distance based on branch length.



1

Figure 8. Expression analysis of DEL1

(a) Transcription level of DEL1 in various organs, means ± SD of three independent

replicates. YR, young root; YL, young leaf; YS, young sheath; MR, mature root; C,

culm; ML, mature leaf; MS, mature sheath; P, panicle; S, spikelet. (b–j) GUS analysis

of DEL1 expression: (b and c) Four and seven days after germination of the young

plant, scale bar = 1 cm; (d) root, scale bar = 500 μm; (e) lateral root, scale bar = 250

μm; (f) mature sheath, scale bar = 1 cm; (g) mature leaf, scale bar = 1 cm; (h) culm,

scale bar = 1 cm; (i) spikelet, scale bar = 1 cm; (j) lemma and palea were removed in

(i), scale bar = 500 μm.



1

Figure 9. The levels of PEL activity and cell wall composition and structure in

wild-type and del1 plants

(a) Analysis of PEL activity in wild-type and del1 plants, means ± SD of five

independent replicates. ** indicates P<0.01 (Student’s t-test). (b) Comparison of cell

wall composition between wild-type and del1 plants, means ± SD of five independent

replicates. **indicates P<0.01 (Student’s t-test). HC 1: hemicellulose 1, HC 2:

hemicellulose 2. (c) Neutral monosaccharide composition between wild-type and del1

plants, means ± SE of five independent replicates, ** indicates P<0.01 (Student’s

t-test). (d and e) Transmission electron microscopy micrographs of the bundle sheath

fiber cells of wild-type (d) and del1 (e) plants, scale bar = 1 μm. (f) Magnification in

(d), and (g) magnification in (e), scale bar = 0.2 μm. ml: middle lamella, pw: primary

cell wall, sw: secondary cell wall, pm: plasma membrane, c: cytoplasm. (h–j)

Statistical analysis of the middle lamella (h) , primary cell wall (i), and secondary cell

wall (j) thicknesses of bundle sheath fiber cells between the wild-type and del1 plants,



2

mean ± SD of 30 cells, ** indicates P<0.01 (Student’s t-test).



1

Figure 10. Immunohistochemical localization of HG in culm sections of wild-type

and del1 plants

(a–t) Immunolocalization of HG of wild-type (a, c) and del1 plants (b, d) with JIM7,

wild-type (e, g) and del1 plants (f, h) with JIM5, wild-type (i, k) and del1 plants (j, l)

with LM18, wild-type (m, o) and del1 plants (n, p) with LM19, wild-type (q, s) and

del1 plants (r, t) with 2F4. Scale bar = 50 μm.



1

Figure 11. A schematic model of DEL1 function in rice Homogalacturonan is secreted in a highly methylesterified form and selectively

demethylesterified by PME. The demethylesterified HG might be cleaved by DEL1

and other PELs or PGs, The alternative of the cell wall regulated the cell cycle/

expansion and ROS, enabling normal rice growth and leaf senescence process.



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are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21: 216-233Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Palusa SG, Golovkin M, Shin SB, Richardson DN, Reddy ASN (2007) Organ-specific, developmental, hormonal and stressregulation of expression of putative pectate lyase genes in Arabidopsis. New Phytol 174: 537-550


Park YB, Cosgrove DJ (2012) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol 158: 1933-1943


Peaucelle A, Braybrook S, Leguillou L, Bron E, Kuhlemeier C, Hofte H (2011) Pectin-induced changes in cell wall mechanicsunderlie organ initiation in Arabidopsis. Curr Biol 21: 1720-1726


Petersen TN, Brunak S, Heijne GV, Nielsen H (2011) SIGNALP 4.0: discriminating signal peptides from transmembrane regions. NatMethods 8: 785-786


Pien S, Wyrzykowska J, Mcqueen-Mason S, Smart C, Fleming A (2001) Local expression of expansin induces the entire process ofleaf development and modifies leaf shape. Proc Natl Acad Sci USA 98: 11812-11817


Pua EC, Ong CK, Liu P, Liu JZ (2001) Isolation and expression of two pectate lyase genes during fruit ripening of banana (Musaacuminata). Physiol Plantarum 113: 92-99


Ramirez-Parra E, Desvoyes B, Gutierrez C (2005) Balance between cell division and differentiation during plant development. Int JDev Biol 49: 467-477


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Ridley BL, O'Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry57: 929-967


Rogers HJ, Harvey A, Lonsdale DM (1992) Isolation and characterization of a tobacco gene with homology to pectate lyase which isspecifically expressed during microsporogenesis. Plant Mol Biol 20: 493-502


Romualdi C, Bortoluzzi S, D'Alessi F, Danieli GA (2003) IDEG6: a web tool for detection of differentially expressed genes inmultiple tag sampling experiments. Physiol Genomics 12: 159-162


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Wang X, Fang G, Li Y, Ding M, Gong HY, Li YS (2013) Differential antioxidant responses to cold stress in cell suspension culturesof two subspecies of rice. Plant Cell Tiss Org 113: 353-361


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http://www.ncbi.nlm.nih.gov/pubmed?term=Sun L%2C Nocker SV %282010%29 Analysis of promoter activity of members of the PECTATE LYASE%2DLIKE %28PLL%29 gene family in cell separation in Arabidopsis%2E BMC Plant Biol 10%3A 152%2D152&dopt=abstract

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1 running head: del1 affects rice growth and leaf senescence 2 · 4/28/2017 · 97 accumulation of...

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