antagonistic actions of fpa and ibm2 regulate transcript … · 2019. 4. 29. · 107 explored. in...

Deremetz et al. 1

Short title: Screening for ibm2 suppressors identified FPA 1

2

Corresponding author: 3

Nicolas BOUCHÉ 4

Tel: +33 1 30 83 31 71 5

E-mail: [email protected] 6

7

Antagonistic actions of FPA and IBM2 regulate transcript processing from 8

genes containing heterochromatin 9

10

Aurélie Deremetz1,2, Clémentine Le Roux3, Yassir Idir1,2, Cécile Brousse1, Astrid Agorio1, 11

Isabelle Gy1, Jane E. Parker3 and Nicolas Bouché1 12

13

Affiliations: 14

1 Institut Jean-Pierre Bourgin, UMR1318, INRA, 78000 Versailles, France 15

2 Université Paris-Sud, Université Paris-Saclay, 91405 Orsay, France 16

3 Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe 17

Interactions, D-50829 Cologne, Germany 18

19

Summary sentence: 20

Intronic heterochromatic marks, associated with alternative polyadenylation sites, are decoded 21

by RNA-binding proteins like FPA and IBM2, to tune the expression of key regulator genes 22

such as IBM1 or RPP7. 23

24

Author contributions: 25

AD, CLR, YI, CB, AA, IG and NB performed the research; AD, CLR, YI and NB analyzed the 26

data; NB designed the research; JP and NB wrote the paper. 27

28

Plant Physiology Preview. Published on February 27, 2019, as DOI:10.1104/pp.18.01106

Copyright 2019 by the American Society of Plant Biologists

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Deremetz et al. 2

ABSTRACT 29

30

Repressive epigenetic marks, such as DNA and histone methylation, are sometimes 31

located within introns. In Arabidopsis (Arabidopsis thaliana), INCREASE IN BONSAI 32

METHYLATION2 (IBM2), an RNA-binding protein containing a BAH domain, is required to 33

process functional transcript isoforms of genes carrying intronic heterochromatin. In a genetic 34

screen for suppressors of the ibm2 mutation, we identified FPA, an RNA-binding protein which 35

promotes use of proximal polyadenylation sites in genes targeted by IBM2, including IBM1 36

encoding an essential H3K9 histone demethylase and the disease resistance gene 37

RECOGNITION OF PERONOSPORA PARASITICA7 (RPP7). Both IBM2 and FPA are 38

involved in the processing of their common mRNA targets: transcription of IBM2 target genes 39

is restored when FPA is mutated in ibm2 and impaired in transgenic plants over-expressing 40

FPA. By contrast, transposons targeted by IBM2 and localised outside introns are not under 41

this antagonistic control. The DNA methylation patterns of some genes and transposons are 42

modified in fpa plants, including the large intron of IBM1, but these changes are rather limited 43

and reversed when the mutant is complemented, indicating that FPA has a restricted role in 44

mediating silencing. These data reveal a complex regulation by IBM2 and FPA pathways in 45

processing mRNAs of genes bearing heterochromatic marks. 46

47

48

Keywords 49

Arabidopsis; 50

FPA; 51

INCREASE IN BONSAI METHYLATION (IBM1 & IBM2); 52

mRNA processing; 53

RECOGNITION OF PERONOSPORA PARASITICA7 (RPP7). 54



Deremetz et al. 3

INTRODUCTION 55

56

DNA and histone methylations are epigenetic marks found in plants and animals that 57

influence chromatin structure and have a direct impact on gene function and transposon 58

mobilization. Chromatin can be modified and remodeled in several ways. In plants, the Jumonji 59

C (JmjC) domain-containing protein INCREASE IN BONSAI METHYLATION1 (IBM1) is a 60

histone demethylase which removes methylation on lysine 9 of histone H3 (H3K9me). IBM1 61

function is essential in plants because it prevents deposition of these heterochromatic silencing 62

marks at transcribed genes (Saze et al., 2008; Miura et al., 2009; Inagaki et al., 2010). H3K9me 63

and CHG DNA methylation (where H = A, T or C) are tightly correlated. Indeed, CHG 64

methylation is controlled by the DNA methyltransferase CHROMOMETHYLASE3 (CMT3) 65

recruited to regions enriched in H3K9me, which it directly binds (Du et al., 2012; Du et al., 66

2014). In a reciprocal manner, H3K9me is catalysed by three histone methyltransferases, 67

SU(VAR)3-9 HOMOLOG4 / KRYPTONITE (SUVH4/KYP), SUVH5, and SUVH6 (Ebbs and 68

Bender, 2006). KYP binds CHG-methylated cytosines through its SRA domain (Johnson et al., 69

2007). Thus, CMT3 and KYP participate in a self-reinforcing loop between DNA and histone 70

methylation, which is needed for silencing transposons and repeat sequences but is deleterious 71

to genes when IBM1 is absent. Consequently, ibm1 mutants accumulate both H3K9me and 72

CHG in coding regions with drastic consequences for development (Saze et al., 2008; Miura et 73

al., 2009). 74

Two other categories of Arabidopsis (Arabidopsis thaliana) mutants share the ibm1 75

developmental and molecular phenotype: mutants of the IBM2 / ANTI-SILENCING1 / SHOOT 76

GROWTH1 gene, hereafter called IBM2 (Saze et al., 2013; Wang et al., 2013; Coustham et al., 77

2014) and mutants of ENHANCED DOWNY MILDEW2 (EDM2) (Tsuchiya and Eulgem, 2013). 78

The IBM1 gene encodes two different transcripts of which only the longest encodes a functional 79

protein (Rigal et al., 2012), and its production is controlled by both IBM2 and EDM2 in a yet 80

unclear manner. IBM2 is a protein of unknown function containing a Bromo-Adjacent 81

Homology (BAH) domain and an RNA-Recognition Motif (RRM) (Saze et al., 2013; Wang et 82

al., 2013; Coustham et al., 2014). EDM2 contains several zinc-finger domains and a region 83

similar to the active domains of certain methyltransferases (Tsuchiya and Eulgem, 2013). Both 84

EDM2 and IBM2 are found in the same protein complex, bridged by the ASI1-85

IMMUNOPRECIPITATED PROTEIN1 (AIPP1) (Duan et al., 2017). In addition to the IBM1 86

gene, EDM2, AIPP1 and IBM2 share another target, the disease resistance gene 87

RECOGNITION OF PERONOSPORA PARASITICA7 (RPP7) (Saze et al., 2013; Tsuchiya and 88



Deremetz et al. 4

Eulgem, 2013; Wang et al., 2013; Lai et al., 2018). Like IBM1, RPP7 contains a 89

heterochromatic domain within a long (>2 kb) intron associated with H3K9me and DNA 90

methylated in all cytosine contexts. The IBM2 complex associates with these methylated 91

intronic regions (Saze et al., 2013; Tsuchiya and Eulgem, 2013; Wang et al., 2013) to produce 92

the full-length functional transcript by an unknown molecular mechanism. One hypothesis is 93

that EDM2/AIPP1/IBM2 function by enhancing the use of distal polyadenylation sites over 94

proximal sites located in large introns. 95

Polyadenylation is one key mRNA processing step, and the choice between alternative 96

polyadenylation sites impacts the regulation of gene expression. FPA is an RNA-binding 97

protein with three RRMs involved in polyadenylation site choice and plays a major role in 98

repressing floral transition by favoring the proximal polyadenylation site of an antisense of the 99

FLOWERING LOCUS C (FLC) transcript (Hornyik et al., 2010; Liu et al., 2010) and more 100

broadly in regulating the 3′-end site choice of diverse mRNAs (Sonmez et al., 2011; Duc et al., 101

2013), including its own transcript (Macknight et al., 2002; Hornyik et al., 2010). So far, FPA 102

has not been identified as a member of any splicing or polyadenylation complexes, and the 103

precise function of FPA and its mode of action are still unclear. fpa mutants have also been 104

identified in a genetic screen aimed at finding components required for RNA-mediated 105

chromatin silencing (Bäurle et al., 2007), but the role played by FPA in silencing has not been 106

explored. In addition, FPA is involved in plant defense responses (Lyons et al., 2013), pointing 107

toward a more general role in addition to flowering. 108

Here, we identify fpa as a suppressor of the ibm2 phenotype. The transcription of both 109

IBM1 and RPP7 is restored in a double fpa ibm2 mutant and impaired when FPA is over-110

expressed. We show that fpa mutants are depleted in CHG methylated cytosine within the 111

largest introns of IBM1, providing evidence that mutating FPA has an effect on chromatin 112

structure that nevertheless seems to be limited to specific regions. We demonstrate that RNA-113

binding proteins, like FPA and IBM2, are involved in an intricate crosstalk between chromatin 114

and RNA processing to regulate the production of key genes such as IBM1 and RPP7. We 115

further show that transposons controlled by IBM2 localised outside introns are unaffected by 116

this mechanism. 117

118

RESULTS 119

120

fpa is a genetic suppressor of ibm2 121



Deremetz et al. 5

To uncover new genes impacting the function of IBM2, we performed a forward genetic 122

screen to isolate suppressors of ibm2-4, an allele previously called sg1-1 (Coustham et al., 123

2014). Approximately 7,000 ibm2-4 seeds were treated with EMS (see Materials & Methods). 124

The genetic screen was performed in two steps on 88,000 M3 seedlings. Because the ibm2 125

phenotype is related to a deficiency in production of the long functional IBM1 mRNA (Saze et 126

al., 2013; Wang et al., 2013; Coustham et al., 2014), we screened for mutants showing a wild-127

type phenotype, aiming to select suppressors in which the function of IBM1 was restored. We 128

postulated that this pool of plants contained suppressors of ibm2, but also suppressors restoring 129

the effects of a non-functional IBM1. Mutations like cmt3 or kyp, for instance, suppress ibm1 130

by preventing the accumulation of heterochromatic marks on a large range of IBM1 targets 131

(Saze et al., 2008). These mutations did not restore the transcription of IBM2 targets such as 132

AT3G05410 or RPP7 (Supplemental Figure S1). Next, to isolate genetic suppressors of ibm2 133

more specifically from the first screen, we determined the level of transcription of AT3G05410 134

(Saze et al., 2013; Wang et al., 2013), a target of IBM2 which is not targeted by IBM1. We 135

isolated three M3 plants (from the same M2 pool) which resembled wild-type plants but had 136

more serrated leaves (Figure 1A) and were late flowering (Supplemental Figure S2). In these 137

plants, mRNA levels of the known IBM2 target AT3G05410 were intermediate between ibm2-138

4 and wild type (Supplemental Figure S3). Therefore, the three mutants are likely progeny from 139

the same M2 plant. By sequencing and comparing the genomes of these plants and the original 140

ibm2-4 mutant, we identified mutations that were homozygous and common to the three plants 141

but not the original mutant. Sequencing revealed that the suppressor of ibm2-4 carries a 142

nucleotide change (C-to-T) in the fifth exon of FPA (AT2G43410) at position 586, creating a 143

premature stop codon. The ibm2-4 suppressor was therefore designated a new fpa allele (fpa-144

11). These results show that fpa is epistatic over ibm2. 145

We then extracted genomic DNA from leaves of fpa-11 ibm2-4 mutants to perform 146

whole-genome bisulfite single-base resolution sequencing (WGBS; Supplemental Table S1) 147

and determine the patterns of methylation for genes. On average, both CG and CHH 148

methylation levels were similar in genes of ibm2-4 and fpa-11 ibm2-4 mutants (Supplemental 149

Figure S4), however, the CHG hypermethylation accumulating in ibm2 genes (Saze et al., 2013; 150

Wang et al., 2013; Coustham et al., 2014) was lost in genes of fpa-11 ibm2-4 (Figure 1B). We 151

confirmed the results by identifying the Differentially-Methylated Regions (DMRs) in ibm2-4 152

or fpa-11 ibm2-4 compared to wild type (Figure 1C). Indeed, the number of ibm2 CHG 153

hyperDMRs (n=4722) was reduced by 35-fold in fpa-11 ibm2-4, implying that mutating FPA 154

in ibm2 suppresses the CHG hypermethylation in genes. 155



Deremetz et al. 6

Next, we quantified mRNA levels of known IBM2 targets (Supplemental Figure S5) in 156

fpa and fpa ibm2 mutants grown in vitro for 21 days. RT-qPCR analyses revealed that the IBM1-157

L transcripts were more abundant compared to wild type in all fpa allelic backgrounds tested, 158

including fpa-3, which is a previously described allele (Hornyik et al., 2010), fpa-11, fpa-3 159

ibm2-4, and fpa-11 ibm2-4 (Figure 2; IBM1-L). The opposite trend was observed for IBM1-S 160

(Figure 2; IBM1-S). We also detected a general increase of IBM1 transcripts in fpa mutants 161

using a set of primers amplifying all IBM1 transcript isoforms (Figure 2; IBM1-total). Together, 162

the expression data show that mutating FPA in both ibm2 and wild-type plants increased IBM1 163

transcripts by ~1.8-fold. Furthermore, in fpa backgrounds, the production of the long IBM1 164

transcript is favored over the shortest one. Levels of two other IBM2 targets (AT3G05410 and 165

AT1G11270) were restored to 40 % of wild type in the double fpa ibm2 mutants (Figure 2; 166

AT3G05410-L and AT1G11270-L). Finally, RPP7 (AT1G58602) mRNA levels were restored 167

to 80% of wild type in the suppressor fpa ibm2 backgrounds (Figure 2; RPP7-L). Altogether, 168

the genetic screen for ibm2 suppressors, the methylome sequencing of fpa ibm2 mutants, and 169

the RT-qPCR analyses of IBM2 targets demonstrate that a mutation in fpa counterbalances the 170

absence of IBM2 by restoring the production of its target transcripts. 171

172

FPA contributes to processing of IBM2 target genes containing intronic heterochromatin 173

To understand better the links between FPA and the processing of IBM2 targets, the 174

levels of their transcripts were monitored when FPA was over-expressed. Compared to wild 175

type, the production of IBM1-L, RPP7-L, AT1G11270-L, and AT3G05410-L mRNAs was 176

reduced by 29%, 60%, 47%, and 54%, respectively, in plants expressing 35S:FPA-YFP 177

constructs in a fpa-8 background (Figure 3 and Supplemental Figure S6). Therefore, the long 178

RPP7, IBM1, AT1G11270, and AT3G05410 transcripts are produced incorrectly in these 179

transgenic plants, confirming the role played by FPA in their processing. 180

Next, we assessed the function of the Col-0 RPP7 gene in race-specific disease 181

resistance against the biotrophic oomycete Hyaloperonospora parasitica isolate Hiks1 (Hpa 182

Hiks1) (Slusarenko and Schlaich, 2003). The triple suvh456 mutant, which has lost the RPP7 183

intragenic methylation, and two ibm2 alleles (ibm2-1 and ibm2-4) displayed reduced RPP7 184

resistance, indicated by increased growth of Hpa Hiks1 in leaves (Figure 4), whereas fpa-3 and 185

fpa-11 mutants were as resistant as Col-0 (Figure 4). In agreement with the partial restoration 186

of RPP7-L transcript levels in fpa-11 ibm2-4 (Figure 2), this double mutant also exhibited 187

partially restored RPP7-mediated resistance (Figure 4). Therefore, FPA controls the resistance 188

function of RPP7. 189



Deremetz et al. 7

Direct RNA sequencing (DRS) helps to define polyadenylation sites by direct 190

sequencing of RNAs in the absence of reverse transcription and is therefore a method of choice 191

to localise regions where FPA promotes polyadenylation. We used the DRS data published 192

previously for fpa mutants to identify polyadenylated 3’ ends in fpa-7 and Col-0 (Duc et al., 193

2013). We found that distant polyadenylation sites of AT3G05410, IBM1, and RPP7 were more 194

frequently used in fpa mutants at the expense of proximal polyadenylation sites (Figure 5). 195

Indeed, the number of normalized DRS reads corresponding to distal polyadenylated sites 196

increased in the fpa-7 background by 2.4, 1.9, and 1.7 fold for IBM1, AT3G05410, and RPP7, 197

respectively. By contrast, the number of DRS reads corresponding to proximal sites decreased 198

by 28.8 and 3.4 fold for IBM1 and AT3G05410, respectively. Hence, polyadenylation of IBM2 199

targets is mediated by FPA. The data indicate that FPA and IBM2 pathways are interconnected 200

in processing of their common targets, including IBM1 and RPP7 transcripts. 201

IBM2 promotes the transcription of the methylated Copia element AT4G16870 (Duan 202

et al., 2017), which is a non-intronic transposon localized upstream of the RPP4 resistant gene 203

(Figure 6A). A chimeric RPP4-AT4G16870 mRNA consisting of both RPP4 and this Copia 204

element (Wang and Warren, 2010) was detected in the wild type but not in ibm2-4, aipp1-1, 205

edm2-4, or suvh456 (Figure 6B and Supplemental Figure S7A), confirming that the 206

transcription of RPP4-AT4G16870 is promoted by an EDM2/AIPP1/IBM2 complex and relies 207

on the presence of heterochromatic marks controlled by SUVH proteins. Similarly, RPP4-208

AT4G16870 mRNAs were not detected in fpa-11 ibm2-4 mutants but were expressed in fpa-11 209

(Figure 6B). Thus, the loss of FPA does not restore the transcription of RPP4-AT4G16870 210

mRNAs in ibm2. We verified that the RPP4-mediated resistance to Hpa isolate EMWA1 was 211

not compromised in ibm2, edm2, fpa ibm2, or fpa mutants (Supplemental Figure S8). To 212

identify additional non-intronic IBM2 targets, transposons differently expressed in ibm2, edm2 213

and aipp1, compared to wild-type plants, were listed using published RNA-seq data (Duan et 214

al., 2017). We found a total of 18 transposons that were significantly (FDR threshold ≤ 0.05) 215

downregulated (log2FC(ibm2 and edm2 and aipp1/WT) < -2) in ibm2, edm2, and aipp1 216

(Supplemental Table S2). Six transposons corresponded to known IBM2 targets like the 217

intronic RPP7 transposons or the Copia element AT4G16870. In addition, we found that 218

AT4TE21110 is another non-intronic IBM2 target expressed in Col-0 and fpa mutants but not 219

in ibm2 or fpa ibm2 mutants (Figure 6C and Supplemental Figure S7B), as observed for RPP4-220

AT4G16870. Altogether, our data show that FPA and IBM2 pathways are antagonistic at genes 221

containing heterochromatin within their introns, like IBM1 or RPP7, but not at non-intronic 222

IBM2 targets such as the Copia element AT4G16870 or AT4TE21110. 223



Deremetz et al. 8

224

Intronic DNA methylation of IBM1 decreases in fpa 225

The genes targeted by IBM2 contain introns carrying heterochromatic marks which 226

regulate their transcription. Since FPA was previously identified in a mutant screen for genes 227

required for the silencing of an inverted repeat (Bäurle et al., 2007), we tested whether the DNA 228

methylation patterns of IBM2 targets were modified in an fpa background. For this, we 229

monitored methylation levels of the large IBM1 intron in the fpa mutants. After bisulfite 230

conversion, we sequenced the corresponding IBM1 region in ibm2-4, fpa-11 ibm2-4, and fpa-231

3. Compared to wild type or to ibm2 controls, CHG methylation was reduced by almost half in 232

the fpa-11 ibm2-4 and the fpa-3 mutants (Figure 7A and Supplemental Figure S9). We 233

examined the methylation patterns of the same IBM1 region in mutants for which the whole 234

methylomes were sequenced (Stroud et al., 2013), and we found reduced CHG methylation in 235

both fpa-7 and fca-9 fpa-7 plants (Supplemental Figure S10). Therefore, the methylation of 236

IBM1 is modified in fpa backgrounds. 237

To explain the reduction of CHG methylation observed at IBM1 in fpa, we hypothesized 238

that IBM1 could control the production of its own mRNA by removing intronic epigenetic 239

marks contained within the largest intron of the IBM1 gene. If this hypothesis was correct, 240

increased levels of IBM1-L transcript – as observed in fpa – would result in the demethylation 241

of the IBM1 intron. To test whether such a feedback loop exists, we monitored patterns of DNA 242

methylation in the intron of IBM1 when IBM1-L was over-expressed ectopically (Supplemental 243

Figure S6). Indeed, IBM1 controls methylation of H3K9 which cross-regulates the levels of 244

mCHG (Johnson et al., 2007; Du et al., 2012; Du et al., 2014). Our data show that cytosine 245

methylation levels of the IBM1 intron were comparable between wild type and ibm1 mutants 246

that over-express the IBM1-L cDNA (Figure 7A and Supplemental Figure S9). As the 247

methylation patterns of the IBM1 intron remained unchanged when IBM1-L was more 248

abundant, we concluded that the hypomethylation of IBM1 in fpa is likely not associated with 249

the increased production of IBM1-L transcripts observed in this mutant background. 250

251

The absence of FPA induces transient methylation changes 252

To understand whether the decrease of methylation we observed for IBM1 was 253

widespread or limited to specific regions of the genome, we sequenced the whole methylome 254

of fpa mutants. Levels of methylation per cytosine confirmed that biological replicates were 255

closely correlated (Pairwise Pearson correlation values between biological replicates 0.97 for 256

CGs, 0.98 for CHG and 0.94 for CHH). When the average methylation levels were calculated 257



Deremetz et al. 9

in 100-bp windows partitioning the genome, we observed no broad changes between wild-type 258

plants and fpa-3 (Figure 8A), confirming results obtained with the fpa-7 T-DNA allele (Stroud 259

et al., 2013). Next, we identified the DMRs in fpa-3 and compared them to the wild type and to 260

the transgenic fpa-8 line complemented by a 35S:FPA-YFP construct (Bäurle et al., 2007) that 261

was also sequenced. The spontaneous DMRs naturally occurring within the Arabidopsis Col-0 262

accession were filtered (Zhang et al., 2018). We identified 61 CG hypoDMRs, 73 CG 263

hyperDMRs, 7 CHG hypoDMRs, 7 CHG hyperDMRs, 2 CHH hypoDMRs, and 6 CHH 264

hyperDMRs arising in fpa-3 and returning to wild-type methylation patterns when the function 265

of FPA was restored (Supplemental Table S3). Most of the CG hyperDMRs were found in 266

genes (Figure 8B) and were de novo methylated in fpa (Figure 8C; CGhyper), while CG 267

hypoDMRs overlapped with transposons (Figure 8B) that were demethylated in fpa (Figure 8C; 268

CGhypo). The IBM1 intronic region carrying the heterochromatic marks (Figure 7B) was 269

identified among the 7 CHG hypoDMRs, confirming the results obtained by targeted bisulfite 270

sequencing (Figure 7A and Supplemental Figure S9). A limited number of other regions 271

remained differentially methylated in both fpa-3 and the fpa complemented line compared to 272

their respective wild-type controls: 12 CG hypoDMRs, 9 CG hyperDMRs, 2 CHG hypoDMRs, 273

2 CHG hyperDMRs and 1 CHH hypoDMR. Therefore, most of the changes of methylation 274

patterns in fpa, including those at IBM1, are reversible when the mutant is complemented by a 275

construct overexpressing FPA. 276

Next, we examined the methylation profiles of transposable elements that are 277

derepressed in fpa. Previous studies have revealed that transposons like AtSN1, which is a SINE 278

retroelement, AtMu1, which is a DNA transposon, and the helitron AT1TE93275 are expressed 279

in the fpa backgrounds in contrast to wild type (Bäurle et al., 2007; Sonmez et al., 2011). No 280

changes in DNA methylation were observed for AtMu1 in fpa-3 or for AtSN1 (Supplemental 281

Figure S11). We confirmed that AT1TE93275 is demethylated in all cytosine contexts in fpa-3 282

(Supplemental Figure S11), matching one of the 4 CHG DMRs that remained hypomethylated 283

when fpa was complemented. These results indicate that some transposons, which are up-284

regulated in fpa, are associated with differences in DNA methylation patterns, but their number 285

is low because we found no widespread changes of transposon methylation patterns in fpa. 286

287

DISCUSSION 288

289

Here we identify fpa as a genetic suppressor of the ibm2 mutation. The IBM2 protein 290

complex interacts with heterochromatic marks localized within the large introns of IBM2 target 291



Deremetz et al. 10

genes to promote production of their long transcripts. FPA, by promoting polyadenylation of 292

shorter transcripts, antagonizes the function of IBM2. In addition, FPA affects methylation of 293

the largest intron of IBM1 and a limited number of other regions. 294

295

Crosstalk between FPA and IBM2 in polyadenylation site choice 296

Our forward genetic screen to isolate suppressors of ibm2-4 revealed that FPA is 297

involved in the processing of IBM2 targets. Levels of AT1G11270 and AT3G05410 long 298

transcripts were restored to 40% of wild-type levels in a double fpa-11 ibm2-4 mutant, and 299

levels of RPP7 long mRNAs were restored to 80% (Figure 2; RPP7-L). In addition, IBM1 long 300

mRNAs were ~1.8-fold more abundant in fpa compared to wild type (Figure 2; IBM1-L). 301

Consequently, we found that the most distant polyadenylation sites of IBM2 target genes are 302

favored in an fpa background (Figure 5). At the same time, the large intron of IBM1 contained 303

less methylation in fpa mutants (Figure 7, Supplemental Figure S9 and Table S3), although 304

both CHG and H3K9 methylation within introns appear to be crucial for processing IBM2 target 305

transcripts. First, these transcripts are incorrectly processed when intronic transposons are 306

depleted of CHG methylation (Le et al., 2015). Indeed, RT-qPCR analyses revealed that levels 307

of long RPP7 and AT3G05410 transcripts are reduced in cmt3 (Le et al., 2015), confirming 308

results obtained for IBM1 long transcripts (Rigal et al., 2012). Second, compromising the 309

functions of H3K9 histone methyltransferases has similar consequences. Northern blot analyses 310

show that kyp/suvh4 mutants produce lower levels of IBM1 long transcripts compared to wild 311

type (Rigal et al., 2012). If methylation marks are necessary to correctly transcribe IBM2 target 312

genes, how then can IBM2 targets be transcribed in an fpa background in which intragenic 313

heterochromatic marks are reduced? Because fpa is epistatic to ibm2, it is likely that IBM2 is 314

important for the production of its target transcripts only when FPA is functional. A possible 315

explanation is that FPA promotes the recruitment of the polyadenylation complex at proximal 316

sites, while IBM2 antagonizes this binding. We suggest that IBM2 prevents the polyadenylation 317

of short transcripts only when FPA is active. Whether IBM2 and/or its partners interact directly 318

with proteins of the polyadenylation complex remains to be determined. This mechanism might 319

apply to other plant species. In oil palm (Elaeis guineensis), for instance, the transcription of 320

an essential homeotic gene is regulated by methylation of an intronic LINE retroelement (Ong-321

Abdullah et al., 2015). Levels of transcription also correlate with the size of heterochromatic 322

regions. Expression of genes with long methylated introns, such as RPP7, AT3G05410, or 323

AT1G11270, is decreased by more than 70% in ibm2 and partially rescued in fpa ibm2 (Figure 324

2). However, the transcription of IBM1, which contains a shorter methylated intronic region, is 325



Deremetz et al. 11

decreased by only 50% in ibm2 and restored in fpa ibm2 (Figure 2) in which IBM1 is fully 326

functional (Figure 1B and 1C). By inserting into introns, transposons introduce alternative 327

polyadenylation sites, making the targeted gene regulated by both the IBM2 and FPA pathways. 328

By contrast, FPA does not antagonize IBM2 for IBM2 transposon targets localized outside 329

genic regions (Figure 6). 330

331

Links between RNA processing and methylation changes 332

The role played by FPA in controlling silencing remains controversial. The fpa mutants 333

were first retrieved from a forward genetic screen to identify genes involved in RNA silencing 334

(Bäurle et al., 2007). Even if some transposons are strongly reactivated in fpa (Bäurle et al., 335

2007; Sonmez et al., 2011), the analysis of DRS data showed no widespread differences of 336

expression for transposons between fpa-7 and the wild type (Duc et al., 2013). In addition, fpa-337

7 methylome analyses revealed no major differences in methylation patterns (Stroud et al., 338

2013). fpa-7 is a T-DNA allele, and recent studies have demonstrated that fpa mutations can 339

rescue T-DNA insert mutants (Zhang et al., 2016), possibly explaining the phenotypic 340

discrepancies existing between T-DNA and point mutation fpa alleles (Duc et al., 2013). By 341

sequencing the methylome of the point mutation fpa-3 allele, we confirmed that no major 342

changes of DNA methylation patterns were observed genome-wide (Figure 8A), but we found 343

that CG methylation was gained in some genes and lost in some transposons of fpa (Figure 8B 344

and 8C). Most of these changes revert to wild-type patterns when the function of FPA is 345

restored, indicating that the changes of methylation are rather limited and transient. 346

Mutating FPA more specifically disturbs DNA methylation of heterochromatic regions 347

localised within the largest intron of IBM1 in contrast to other IBM2 targets. By sequencing the 348

methylome of fpa-3, the largest intron of IBM1 was identified as a CHG hypomethylated DMR 349

(out of 7 in total) (Supplemental Table S3), confirming results obtained by targeted bisulfite 350

sequencing in fpa-11 ibm2-4 (Figure 7A). Likewise, the CHG methylation, localized at the 351

endogenous phytoene desaturase (PDS) locus silenced by an inverse repeat introduced 352

transgenically in trans, is compromised in the fpa-8 background (Bäurle et al., 2007). 353

Hypomethylation of IBM1 observed in fpa is probably not coupled to an increase of IBM1-L 354

production, since transgenic ibm1 plants overexpressing IBM1-L ectopically show no alteration 355

of methylation at IBM1 (Figure 7A and Supplemental Figure S9). Moreover, the limited number 356

of CHG DMRs found in an fpa background (Supplemental Table S3) argue against FPA directly 357

controlling the activity of CMTs at transposons localized near or within genes. Therefore, the 358

loss of methylation at IBM1 in fpa is probably independent of IBM1 activity. Other factors 359



Deremetz et al. 12

might account for this hypomethylation, such as those associated with the changes of 360

polyadenylation site in fpa mutants and the subsequent effects on IBM1 mRNA processing. 361

Previous studies have demonstrated that transcription initiation and/or the Pol II elongation 362

rates are influenced by choice of polyadenylation sites at FLC (Wu et al., 2016). Similarly, Pol 363

II occupancy is increased near the proximal polyadenylation sites of RPP7 in edm2, aipp1 and 364

suvh456 plants, indicating that the enzyme is probably pausing in this region (Lai et al., 2018). 365

Therefore, changes of polyadenylation sites in fpa also very likely modify the rates of 366

transcription for many genes, including IBM1 and transposons, which might impact their 367

methylation patterns. Furthermore, the recent discovery that human RBM15 proteins, related 368

to FPA, direct methylation to specific non-coding RNAs (Patil et al., 2016), is consistent with 369

a role for FPA in mRNA methylation, implying that a previously unrecognized interplay exists 370

between epigenetic silencing marks and methylation of IBM2 target RNAs. 371

372

Conclusion 373

We show that FPA and IBM2 pathways are crucial for controlling the transcription of 374

their common targets and provide evidence that they act antagonistically when transposons are 375

inserted in introns. The tight regulatory control of RPP7 mRNA levels is likely critical to limit 376

the accumulation of a long functional RPP7 transcript in pathogen-unchallenged conditions and 377

to prevent autoimmunity. In the presence of Hpa Hiks1, the fine regulation of RPP7 transcripts 378

mediated by both IBM2 and FPA favors accumulation of a long transcript to induce a rapid and 379

specific immune response (Tsuchiya and Eulgem, 2013). Similarly, the importance of H3K9 380

methylation in resistance to viruses has been described (Sun et al., 2015), and the virulence of 381

geminiviruses requires a viral protein that inhibits expression of the main plant H3K9 382

methyltransferase, KYP. To reinforce the action of KYP, rapid modulation of IBM1 gene 383

expression, mediated by both FPA and IBM2, is likely essential. Our data suggest that intronic 384

heterochromatic marks associated with alternative polyadenylation sites can be decoded by 385

RNA-binding proteins like FPA and IBM2 to tune the expression of key regulator genes such 386

as IBM1 or RPP7. 387

388

MATERIALS AND METHODS 389

390

Plant materials and growth conditions 391

Arabidopsis (Arabidopsis thaliana) accession Ksk-1 was described previously 392

(Slusarenko and Schlaich, 2003). All other plants were in the Arabidopsis Col-0 background. 393



Deremetz et al. 13

The ibm2-4 point mutation was previously named sg1-1, and ibm2-5 (SAIL_310B06) was sg1-394

2 (Coustham et al., 2014). The following mutants were previously described: edm2-4 395

SALK_142563 (Eulgem et al., 2007), fpa-3 (Hornyik et al., 2010), fpa-7 (Michaels and 396

Amasino, 2001; Veley and Michaels, 2008), fpa-8 (Bäurle et al., 2007), ibm1-1 (Saze et al., 397

2008), ibm2-1 (Saze et al., 2013), the triple suvh456 mutant (Ebbs and Bender, 2006), cmt3-11 398

ibm2-5 (Coustham et al., 2014), and kyp ibm2-5 (Coustham et al., 2014). The following lines 399

were previously described: the transgenic fpa-8 line (Col-0 background) carrying a 35S:FPA-400

YFP construct (Bäurle et al., 2007) and the ibm1-3 complemented lines expressing a 35S:YFP-401

IBM1-L cDNA (Fan et al., 2012). 402

For ethylmethane sulfonate (EMS) mutagenesis, ~ 7,000 ibm2-4 seeds were incubated 403

in water containing 0.1% (v/v) EMS for 15 hours at room temperature and washed several times 404

with water. Plants were then grown in pools of 16 (440 M1 pools in total) in greenhouses in 405

long-day conditions at 20°C. The next generation was obtained by growing 200 M2 plants per 406

pool that were selfed to obtain the M3 generation. The genetic screen was performed on M3s. 407

Seeds of plants grown in vitro were first surface sterilized and then sown on Gamborg 408

B5 medium containing 1% (w/v) Sucrose. Plants were cultivated in growth chambers at 21°C 409

in long day conditions. 410

411

Gene expression analyses 412

Total RNA was isolated from the aerial parts of 21-day-old seedlings grown in vitro 413

using the RNeasy Plant Mini kit (Qiagen) followed by a DNAse treatment (Fermentas). RT-414

PCR was performed on 500 ng (except for RPP7 amplifications where 1 µg was used) of total 415

RNAs with the M-MLV reverse transcriptase (Fermentas), and cDNAs were diluted 10 times. 416

Five µl was used for RT-qPCR using a CFX96 real-time PCR machine (BioRad) with a SYBR 417

solution (Eurogentec) and primers listed in Supplemental Table S4. Expression levels were 418

normalized against the Arabidopsis UBC21 gene (AT5G25760). 419

420

Pathogen infection assays 421

To test RPP7 disease resistance function, plants were inoculated with 422

Hyaloperonospora arabidopsidis (Hpa) isolate Hiks1, which is an oomycete pathogen 423

specifically recognized by RPP7 in Arabidopsis accession Col-0 and virulent on accession Ksk-424

1 (Slusarenko and Schlaich, 2003). The function of another Hpa resistance gene, RPP4, was 425

assessed by inoculating the plants with Hpa isolate EMWA1, which is specifically recognized 426

by RPP4 in Arabidopsis accession Col-0 and virulent on the Col-0 eds1-2 mutant (García et al., 427



Deremetz et al. 14

2010). Briefly, 14-day-old plants were sprayed with water containing 4 x 104 Hpa Hiks1 spores 428

per ml. Plant cell necrosis and Hiks1 or EMWA1 hyphal development were monitored by 429

staining leaves with lactophenol trypan blue as described (Koch and Slusarenko, 1990). Stained 430

leaves were viewed under a binocular light microscope. Infection assays were repeated 431

independently at least three times with similar results. 432

433

Whole-genome sequencing and bioinformatic analyses 434

The genomes of fpa-11 ibm2-4 and ibm2-4 were sequenced using HiSeq technology 435

(Illumina). Mutations were identified using the MutDetect pipeline described previously 436

(Girard et al., 2014). 437

For fpa-3, fpa-8 35S:FPA-YFP, and fpa-11 ibm2-4 methylome sequencings, bisulfite 438

treatment, library preparation, and whole-genome sequencing (final depth of 20X) were 439

performed by the BGI (China) using HiSeq technology (Illumina) producing 100 bp paired-end 440

reads (Supplemental Table S1). Reads were trimmed with Trim_Galore (Babraham 441

Bioinformatics) and aligned to the Col-0 Arabidopsis TAIR10 reference genome with Bismark 442

version 0.14.5 (Babraham Bioinformatics) using standard options (Bowtie2; 1 mismatch 443

allowed). Identical pairs were collapsed. Subsequent analyses were done using the following R 444

packages: bsseq version 1.7.7 (Hansen et al., 2012) and DSS version 2.11.3 (Wu et al., 2015) 445

to call Differentially-Methylated Regions (DMRs) as previously described (Corem et al., 2018). 446

The hcDMR pipeline was used as indicated (Zhang et al., 2018) to filter spontaneous DMRs 447

occurring in Arabidopsis Col-0 bisulfite sequencings. DMRs arising in fpa and restored to wild-448

type patterns in fpa complemented lines corresponded to DMRs found between fpa-3 and the 449

corresponding Col-0 controls that overlapped with DMRs found between fpa-3 and the fpa 450

complemented line but not with DMRs found between the fpa complemented line and its Col-451

0 control. DMRs that remained differentially methylated when the FPA function was restored 452

corresponded to DMRs found between fpa-3 and the corresponding Col-0 controls that 453

overlapped with DMRs found between the fpa complemented line and its Col-0 control. 454

For DRS analyses, we retrieved the data corresponding to the study PRJEB3993 455

deposited at the ENA (Duc et al., 2013). Raw DRS reads were aligned using TopHat2 (Kim et 456

al., 2013), allowing a maximum of two mismatches and no gaps. 457

For transposon expression analyses, we used ibm2 and aipp1 RNA-seq data described 458

previously (Stroud et al., 2012; Saze et al., 2013; Wang et al., 2013; Duan et al., 2017). Reads 459

were trimmed with Trim_Galore (Babraham Bioinformatics) and aligned to the Col-0 460

Arabidopsis TAIR10 reference genome with HISAT2 version 2.1.0 (Kim et al., 2015) using 461



Deremetz et al. 15

standard options. Differential expression analyses were done with DESeq2 version 1.20.0 (Love 462

et al., 2014) in R version 3.5.1. To define transposon transcripts differently expressed, we used 463

a significance cut-off of 0.05 and a 2-fold change relative to wild type. RNA-seq read coverage 464

files were produced and normalized with deepTools2 (Ramírez et al., 2018). 465

466

Targeted bisulfite sequencing 467

For each sample, 1 to 2 µg of genomic DNA was extracted from leaves corresponding 468

to bulks of 10 to 15 plants, using the NucleoSpin Plant II kit (Macherey-Nagel). DNA was 469

treated with bisulfite using the EpiTect Bisulfite Kit (Qiagen). Treated DNA was amplified 470

using primers listed in Supplemental Table S4. PCR fragments were then cloned in pTOPO 471

(Life Technologies) and sequenced individually. Results were analyzed with the Kismeth tool 472

(Gruntman et al., 2008). 473

474

ACCESSION NUMBERS 475

WGBS data described in this study are available from the ENA database under the accession 476

number PRJEB28432. 477

478

SUPPLEMENTAL DATA 479

Supplemental Figure S1. Expression analysis of two IBM2 targets in cmt3 ibm2 and kyp ibm2 480

Supplemental Figure S2. Late flowering phenotype of fpa-11 ibm2-4 and fpa-3 ibm2-4 481

mutants 482

Supplemental Figure S3. ibm2-4 suppressor screen 483

Supplemental Figure S4. CG and CHH methylation levels of genes in ibm2 and fpa ibm2 484

mutants. 485

Supplemental Figure S5. Schematic representation of the IBM2 target genes and localization 486

of the regions amplified by qPCR 487

Supplemental Figure S6. Characterization of plants overexpressing FPA or IBM1 488

Supplemental Figure S7. Expression of IBM2 non-intronic target transposons 489

Supplemental Figure S8. Host responses and Hpa EMWA1 growth in Arabidopsis mutant 490

lines 491

Supplemental Figure S9. Methylation patterns of the IBM1 intron in ibm2 and fpa mutants 492

Supplemental Figure S10. Methylation of IBM1 intron in fpa determined by whole-genome 493

sequencing after bisulfite conversion 494

Supplemental Figure S11. Methylation profiles of transposons derepressed in fpa 495



Deremetz et al. 16

Supplemental Table S1. Bisulfite sequencing statistics 496

Supplemental Table S2. List of transposons differentially expressed in ibm2, edm2, and aipp1 497

Supplemental Table S3. DMRs identified between fpa-3 and the wild type in CG, CHG, and 498

CHH contexts 499

Supplemental Table S4. List of primers 500

501

ACKNOWLEDGMENTS 502

The authors wish to thank Eric Kemen (MPIPZ) for providing Ksk-1 seeds, Thomas Eulgem 503

(UC Riverside) for Hpa isolate Hiks1, Caroline Dean for the 35S:FPA-YFP line, and Ligeng 504

Ma for the 35S:YFP-IBM1 line. We acknowledge funding from the Agence Nationale de la 505

Recherche (Project 11-JSV7-0013) to NB, the Max-Planck Society and a H2020-Marie 506

Skłodowska-Curie Actions Individual Fellowship (705631-CHERI) to CLR and JEP. The 507

Institut Jean-Pierre Bourgin benefits from the support of the LabEx Saclay Plant Sciences-SPS 508

(Project 10-LABX-0040-SPS). We are grateful to the Genotoul bioinformatics platform 509

Toulouse Midi-Pyrénées for providing help and computing resources. 510



Deremetz et al. 17

LEGENDS OF FIGURES 511

512

Figure 1. Phenotype of the ibm2 suppressor 513

(A) Wild type (Col-0), ibm2-4, and the ibm2 suppressor (fpa-11 ibm2-4) plants were grown in 514

the greenhouse and pictured after 25 days. Scale bar = 1 cm. 515

(B) CHG methylation levels of genes in ibm2-4 and fpa-11 ibm2-4 mutants. The average 516

methylation levels of genes were determined by dividing the genes into 100 bp bins. Regions 517

located 1 kb upstream and 1 kb downstream are shown. 518

(C) Total number of DMRs found in the three methylation contexts (mCG, mCHG, and 519

mCHH). Hypo- and hypermethylated DMRs are shown. 520

521

Figure 2. Expression analyses of IBM2 target genes in fpa mutants 522

The expression of IBM2 targets were determined by RT-qPCR in ibm2-4, fpa-3, and fpa-11 523

back-crossed twice to Col-0 and the double ibm2-4 fpa-11 and ibm2-4 fpa-3 mutants. Results 524

were normalized to Col-0 (expression fixed at 1 for each experiment). The PCR fragments 525

amplified are shown in Supplemental Figure S5. Error bars represent SD (n=9). The asterisks 526

indicate a significant difference between the sample and the corresponding Col-0 control 527

determined by Student’s t-test (* p<0.05; ** p<0.01; *** p<0.001). 528

529

Figure 3. Reduced expression of IBM2 target genes in plants over-expressing FPA 530

Expression analysis of RPP7, IBM1, AT1G11270, and AT3G05410 transcript isoforms in an 531

fpa-8 mutant complemented by a 35S:YFP-FPA construct resulting in the over-expression of 532

FPA (Supplemental Figure S6). The expression was determined by RT-qPCR using primers 533

(Supplemental Table S4) specific of IBM2 targets as shown in Supplemental Figure S5. Error 534

bars represent SD (n=9). The asterisks indicate a significant difference between the sample and 535

the corresponding Col-0 control determined by Student’s t-test (*** p<0.001). 536

537

Figure 4. Host RPP7 resistance and Hpa Hiks1 growth in Arabidopsis mutant lines 538

Two-week-old seedlings of the indicated genotypes were inoculated with Hpa Hiks1 (see 539

Materials and Methods). At 4 days after inoculation, the two first true leaves of >10 plants per 540

genotype were stained with lactophenol trypan blue to reveal necrotic plant cells and pathogen 541

structures. Hpa Hiks1 is recognized by resistance gene RPP7. Col-0 expressing RPP7 is 542

resistant and Ksk-1 lacking RPP7 is susceptible to Hpa Hiks1 infection. Hpa Hiks1 hyphal 543

growth is restricted at HR sites in Col-0 whereas hyphae ramify through Ksk-1 leaves. Col-0 544



Deremetz et al. 18

ibm2-1 or ibm2-4 and Col-0 suvh456 display reduced RPP7 resistance to Hpa Hiks1. EDM2 is 545

regulating RPP7 transcript levels and Col-0 edm2-4 mutants are therefore susceptible to Hpa 546

Hiks1 (Eulgem et al., 2007). fpa-11 ibm2-4 double mutant exhibits intermediate RPP7 547

resistance. Col-0 fpa-3 or fpa-11 mutants and Col-0 ibm1-1 are not affected in RPP7 resistance. 548

Plants shown were grown and inoculated at the same time. Similar results were obtained in 549

three independent experiments. HR, host hypersensitive response; h, Hpa Hiks1 hyphae; Sp, 550

Hpa Hiks1 sporangiophore. Scale bars = 1 mm. 551

552

Figure 5. Polyadenylation of IBM2 intronic targets 553

Reads corresponding to the direct RNA sequencing (DRS) of fpa-7 and the Col-0 wild type 554

(Duc et al., 2013) were aligned to the sequence of Col-0 (TAIR10 version). 555

(A) DRS reads for IBM1, AT3G05410, and RPP7 loci were visualized using the Integrated 556

Genome Browser (IGB). Proximal (Prox.) and distal (Dist.) polyadenylation sites are indicated. 557

Each biological repeat is presented individually (rep#1 to #3). The scale is identical for all 558

repeats presented for a given gene. The gene model is shown with exons represented by black 559

boxes. 560

(B) DRS reads mapping the proximal or distal polyadenylation site regions were counted and 561

normalized in reads per million mapped reads (RPM). Error bars represent SD (n=3). The 562

asterisks indicate a significant difference between the sample and the Col-0 control determined 563

by Student’s t-test (* p<0.05; ** p<0.01). 564

565

Figure 6. Expression analysis of IBM2 non-intronic target transposons 566

(A) Schematic representation of the Copia (AT4G16870) - RPP4 (AT4G16860) locus targeted 567

by IBM2. The exons of RPP4 are in blue, and the Copia element is in green. 568

(B) Expression analysis of RPP4, AT4G16870, and the chimeric RPP4-AT4G16870 transcripts 569

in Col-0 and different mutant backgrounds. cDNAs were amplified using primers indicated in 570

(A) and described previously (Wang and Warren, 2010). ATEF cDNA amplifications served as 571

controls. 572

(C) Expression analysis of AT4TE21110 in Col-0 wild type and different mutant backgrounds. 573

AT4TE21110 is localized in the pericentromeric region of chromosome 4. RNAs were extracted 574

from bulks (#1 and #2) of 20 plants grown in vitro for 15 days and cDNAs were amplified using 575

primers described in Supplemental Table S4. ACTIN cDNA amplifications served as controls. 576

577

Figure 7. Methylation of IBM1 intron in fpa mutants and an IBM1 overexpressing line 578



Deremetz et al. 19

(A) The methylation levels within the large intron of IBM1, in the region containing the 579

heterochromatic marks (chromosome 3, position 2,430,285 to 2,430,595), are indicated. Data 580

were obtained by amplifying the region after bisulfite conversion and correspond to the average 581

methylation ratio determined between the repeats (Supplemental Figure S9). 582

(B) Methylation on top (positive values) and bottom (negative values) strands across the coding 583

sequence of IBM1 in fpa-3. The IBM1 gene model is shown according to TAIR10. Mean 584

methylation levels per cytosine are plotted on a 0 to 100% scale for each strand. Data 585

correspond to the combination of two biological repeats for each genotype. CG methylation is 586

in red, CHG in blue, and CHH in green. The CHG hypoDMR identified between fpa-3 and Col-587

0 is represented by a blue rectangle. 588

589

Figure 8. Patterns of methylation in fpa 590

(A) Pairwise comparison of methylation in wild type and fpa-3 mutants. Each dot represents a 591

100 bp-window, and their methylation levels were determined as follows. The Arabidopsis 592

genome (TAIR10 release) was partitioned in 100 bp-tiles and methylation levels correspond to 593

the ratios of methylated cytosines over the total number of cytosines. Only cytosines covered 594

by at least five reads were considered. The average methylation levels were determined by 595

combining the two biological replicates for each genotype. The color scale measures the density 596

of points (red being very dense). The Pearson correlation coefficients between the samples are 597

0.97 for mCG, 0.98 for mCHG and 0.94 for mCHH. 598

(B) Nature of CG hypo- and hyperDMRs identified in fpa-3. ‘gene+TE’ corresponds to DMRs 599

overlapping with both genes and transposons, ‘gene’ corresponds to DMRs overlapping with 600

genes, and ‘TE’ corresponds to DMRs overlapping with transposons. All other DMRs were 601

classified as ‘Intergenic’. 602

(C) Methylation levels of CG hypo- and hyperDMRs. The average methylation levels of the 603

DMRs were determined by dividing the DMR into 100 bp bins. Regions located 1 kb upstream 604

and 1 kb downstream are shown. 605



Deremetz et al. 20

LEGENDS OF SUPPLEMENTARY MATERIALS 606

607

Supplemental Figure S1. Expression analysis of two IBM2 targets in cmt3 ibm2 and kyp 608

ibm2 609

RT-qPCR analyses of RPP7-L and AT3G05410-L expression in Col-0, ibm2-4, cmt3-11 ibm2-610

5 (Coustham et al., 2014) and kyp ibm2-5 (Coustham et al., 2014). Results were normalized to 611

Col-0 (expression fixed at 1 for each experiment). Error bars represent SD (n=4). 612

613

Supplemental Figure S2. Late flowering phenotype of fpa-11 ibm2-4 and fpa-3 ibm2-4 614

mutants 615

616

Supplemental Figure S3. ibm2-4 suppressor screen 617

Expression analyses of an IBM2 target in 9 M3 plants (#1 to #9) retrieved from the ibm2-4 618

suppressor screen. RNAs of plants were extracted and cDNAs were amplified using primers 619

corresponding to AT3G05410-L (Supplemental Figure S5). ATEF amplifications served as 620

controls. The GeneRuler DNA Ladder Mix (Ref SM0331, Thermo) is the DNA ladder used. 621

622

Supplemental Figure S4. CG and CHH methylation levels of genes in ibm2 and fpa ibm2 623

mutants 624

The average methylation levels of genes were determined by dividing the genes into 100 bp 625

bins. Regions located 1 kb upstream and 1 kb downstream are shown. 626

627

Supplemental Figure S5. Schematic representation of the IBM2 target genes and 628

localization of the regions amplified by RT-qPCR 629

Schematic representation of the IBM2 target gene drawn to scale. The region (chromosome 3, 630

position 2,430,285 to 2,430,595) containing intronic heterochromatic marks in IBM1 is 631

represented by a blue bar. 632

633

Supplemental Figure S6. Characterization of plants overexpressing FPA or IBM1 634

RNAs were extracted from bulks of plants carrying the 35S:FPA-YFP or 35S:YFP-IBM1 635

constructs. Both FPA (A) or IBM1-L (B) cDNAs were amplified using specific primers 636

(Supplemental Table S4). ATEF or ACTIN cDNA amplifications served as controls. 637

638

Supplemental Figure S7. Expression of IBM2 non-intronic target transposons 639



Deremetz et al. 21

RNA-seq data were retrieved from the following GEO projects: GSE38286 for suvh456 and 640

the three corresponding wild-type repeats (Stroud et al., 2012), GSE98655 for aipp1-1, edm2-641

4, ibm2/asi1-2 and the two wild-type repeats (Duan et al., 2017), GSE48026 for asi1-1 and the 642

corresponding wild type (Wang et al., 2013) and PRJDB2180 for ibm1-4, ibm2-2 and the wild 643

type (Saze et al., 2013). The methylation levels for mCG, mCHG and mCHH are shown for the 644

wild type and fpa-3 plants. The screenshots were obtained with Integrative Genome Browser 645

(IGB). The scales indicated on the left are identical for all RNA-seq or methylation tracks, 646

respectively. RPKM; Reads Per Kilobase per Million mapped reads. (A) RPP4 locus, (B) 647

AT4TE21110 locus. 648

649

Supplemental Figure S8. Host responses and Hpa EMWA1 growth in Arabidopsis mutant 650

lines 651

Two-week-old seedlings of the indicated genotypes were inoculated with Hpa EMWA1 (see 652

Materials & Methods). At 4 days after inoculation, the two first true leaves of >10 plants per 653

genotype were stained with lactophenol trypan blue to reveal necrotic plant cells and pathogen 654

structures. Hpa EMWA1 is specifically recognized by RPP4. Col-0 expressing RPP4 is 655

resistant and eds1-2 mutants (García et al., 2010) are susceptible to Hpa EMWA1 infection. 656

Hpa EMWA1 hyphal growth is restricted at HR sites in Col-0 whereas hyphae ramify through 657

eds1-2 leaves. None of the mutants (in the Col-0 background) are affected in RPP4 resistance. 658

Plants were grown and inoculated at the same time. Similar results were obtained in three 659

independent experiments. 660

661

Supplemental Figure S9. Methylation patterns of the IBM1 intron in ibm2 and fpa 662

mutants 663

After bisulfite conversion of DNAs, the region indicated in Supplemental Figure S5 (IBM1, 664

blue bar) was amplified in the large intron of IBM1 using primers described in Supplemental 665

Table S4. Samples are corresponding to leaves from 10 to 15 plants bulked together. The 666

number of clones sequenced (n) is indicated. Sequences were aligned and the methylation 667

quantified using the Kismeth tool (Gruntman et al., 2008). Cytosines are represented by circles 668

(red for CGs, blue for CHGs, green for CHHs; solid circles: methylated cytosines). 669

670

Supplemental Figure S10. Methylation of IBM1 intron in fpa determined by whole-671

genome sequencing after bisulfite conversion 672



Deremetz et al. 22

The methylation levels within the large intron of IBM1, in the region containing 673

heterochromatic marks (chromosome 3, position 2,430,285 to 2,430,595), are indicated. Data 674

for three wild-type (Col-0) repetitions, fpa-7, fca-9 fpa-7 and suvh4 were obtained from raw 675

data publicly available (Stroud et al., 2013). Data for ibm2-4 and the corresponding wild type 676

(Col-0) were obtained from our previous methylome sequencing data (Coustham et al., 2014). 677

678

Supplemental Figure S11. Methylation profiles of transposons derepressed in fpa 679

Mean methylation levels for mCG, mCHG and mCHH were obtained by combining the two 680

biological replicates for the wild type or fpa-3, respectively. The screenshots were obtained 681

with Integrative Genome Browser (IGB). HypoDMRs between the mutant and the wild type 682

are contained in the boxed area. The scale is identical for all tracks. 683

684

Supplemental Table S1. Bisulfite sequencing statistics 685

Col #1, biological replicate #1 Col-0 methylome sequencing; Col #2, biological replicate #2 686

Col-0 methylome sequencing; fpa-3 #1, biological replicate #1 fpa-3 mutant methylome 687

sequencing; fpa-3 #2, biological replicate #1 fpa-3 mutant methylome sequencing; 35S:FPA-688

YFP, 35S:FPA-YFP methylome sequencing ; Col-0 (35S:FPA-YFP control), Col-0 methylome 689

sequencing; fpa-11 ibm2-4, fpa ibm2 methylome sequencing. To determine the bisulfite 690

conversion rates, reads were aligned to the TAIR10 Arabidopsis chloroplast sequence. 691

692

Supplemental Table S2. Transposons differentially expressed in ibm2, edm2 and aipp1 693

compared to wild type 694

The IBM2 targets previously identified are in red. 695

696

Supplemental Table S3. DMRs identified between fpa-3 and the wild type in CG, CHG 697

and CHH contexts 698

DMRs were defined using two biological repeats per genotype with the bsseq and DSS R 699

packages (see Materials & Methods). 700

701

Supplemental Table S4. List of primers 702



Deremetz et al. 23

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Coustham V, Vlad D, Deremetz A, Gy I, Cubillos FA, Kerdaffrec E, Loudet O, Bouché N (2014) SHOOT GROWTH1 maintains Arabidopsisepigenomes by regulating IBM1. PLoS One 9: e84687


Du J, Johnson LM, Groth M, Feng S, Hale CJ, Li S, Vashisht AA, Gallego-Bartolome J, Wohlschlegel JA, Patel DJ, Jacobsen SE (2014)Mechanism of DNA methylation-directed histone methylation by KRYPTONITE. Mol Cell 55: 495-504


Du J, Zhong X, Bernatavichute YV, Stroud H, Feng S, Caro E, Vashisht AA, Terragni J, Chin HG, Tu A, Hetzel J, Wohlschlegel JA,Pradhan S, Patel DJ, Jacobsen SE (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNAmethylation in plants. Cell 151: 167-180


Duan CG, Wang X, Zhang L, Xiong X, Zhang Z, Tang K, Pan L, Hsu CC, Xu H, Tao WA, Zhang H, Zhu JK (2017) A protein complexregulates RNA processing of intronic heterochromatin-containing genes in Arabidopsis. Proc Natl Acad Sci U S A 114: E7377-e7384


Duc C, Sherstnev A, Cole C, Barton GJ, Simpson GG (2013) Transcription termination and chimeric RNA formation controlled byArabidopsis thaliana FPA. PLoS Genet 9: e1003867


Ebbs ML, Bender J (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell18: 1166-1176


Eulgem T, Tsuchiya T, Wang XJ, Beasley B, Cuzick A, Tor M, Zhu T, McDowell JM, Holub E, Dangl JL (2007) EDM2 is required for RPP7-dependent disease resistance in Arabidopsis and affects RPP7 transcript levels. Plant J 49: 829-839


Fan D, Dai Y, Wang X, Wang Z, He H, Yang H, Cao Y, Deng XW, Ma L (2012) IBM1, a JmjC domain-containing histone demethylase, isinvolved in the regulation of RNA-directed DNA methylation through the epigenetic control of RDR2 and DCL3 expression inArabidopsis. Nucleic Acids Res 40: 8905-8916


García AV, Blanvillain-Baufumé S, Huibers RP, Wiermer M, Li G, Gobbato E, Rietz S, Parker JE (2010) Balanced Nuclear andCytoplasmic Activities of EDS1 Are Required for a Complete Plant Innate Immune Response. PLoS Pathog 6


Girard C, Crismani W, Froger N, Mazel J, Lemhemdi A, Horlow C, Mercier R (2014) FANCM-associated proteins MHF1 and MHF2, butnot the other Fanconi anemia factors, limit meiotic crossovers. Nucleic Acids Res 42: 9087-9095


Gruntman E, Qi Y, Slotkin RK, Roeder T, Martienssen RA, Sachidanandam R (2008) Kismeth: Analyzer of plant methylation statesthrough bisulfite sequencing. In BMC Bioinformatics, Vol 9. BioMed Central Ltd, p 371


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https://www.ncbi.nlm.nih.gov/pubmed?term=B�urle I%2C Smith L%2C Baulcombe DC%2C Dean C %282007%29 Widespread role for the flowering%2Dtime regulators FCA and FPA in RNA%2Dmediated chromatin silencing%2E Science&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Ong%2DAbdullah M%2C Ordway JM%2C Jiang N%2C Ooi SE%2C Kok SY%2C Sarpan N%2C Azimi N%2C Hashim AT%2C Ishak Z%2C Rosli SK%2C Malike FA%2C Bakar NA%2C Marjuni M%2C Abdullah N%2C Yaakub Z%2C Amiruddin MD%2C Nookiah R%2C Singh R%2C Low ET%2C Chan KL%2C Azizi N%2C Smith SW%2C Bacher B%2C Budiman MA%2C Van Brunt A%2C Wischmeyer C%2C Beil M%2C Hogan M%2C Lakey N%2C Lim CC%2C Arulandoo X%2C Wong CK%2C Choo CN%2C Wong WC%2C Kwan YY%2C Alwee SS%2C Sambanthamurthi R%2C Martienssen RA %282015%29 Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm%2E Nature&dopt=abstract

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antagonistic actions of fpa and ibm2 regulate transcript … · 2019. 4. 29. · 107 explored. in...

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