h3k4me3 is crucial for chromatin condensation and mitotic …€¦ · 28/04/2017 · 62...

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1 2 Running head: 3 Crucial function of SDG2 in male gametogenesis 4 5 6 Corresponding author: 7 Wen-Hui Shen 8 Université de Strasbourg 9 CNRS, IBMP UPR2357 10 F-67000 Strasbourg 11 France 12 13 Phone +33 3 67 15 53 26 14 Fax +33 3 67 15 53 00 15 email [email protected] 16 17

Plant Physiology Preview. Published on April 28, 2017, as DOI:10.1104/pp.17.00306

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SDG2-mediated H3K4me3 is crucial for chromatin condensation and mitotic division during 18 male gametogenesis in Arabidopsis [1] 19 20 Violaine Pinon 2, Xiaozhen Yao2, Aiwu Dong , Wen-Hui Shen * 21 22 Université de Strasbourg, CNRS UPR2357, F-67000 Strasbourg, France (V.P., W.-H.S.); State 23 Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and 24 Development, International Associated Laboratory of CNRS-Fudan-HUNAU on Plant 25 Epigenome Research, Department of Biochemistry, Institute of Plant Biology, School of Life 26 Sciences, Fudan University, Shanghai 20043, PR China (X.Y., A.D. W.-H.S.); College of Life and 27 Environment Sciences, Shanghai Normal University, Shanghai 200234, PR China (X.Y.) 28 29 30 Footnotes: 31 32 1 This work was supported by the French Agence Nationale de la Recherche (ANR-12-BSV2-33 0013-02), the National Basic Research Program of China (973 Program, 2012CB910500 and 34 2011CB944600), the National Natural Science Foundation of China (grant no. 31571319, 35 31371304 and 31300263), the Science and Technology Commission of Shanghai Municipality 36 (grant no. 13JC1401000), and the French Centre National de la Recherche Scientifique 37 (CNRS, LIA PER) 38 39 2 These authors contributed equally to this work. 40 41 42 *Corresponding author; e-mail [email protected] 43 44 45



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Authors' contributions: W.-H.S. conceived the original research plans and supervised the 46 experiments; V.P. and X.Y. performed the experiments and analyzed the data with equal 47 contribution; A.D. provided assistance to X.Y. and supervised some of the experiments; V.P., 48 X.Y. and W.-H.S. wrote the article with contributions of all the authors. 49 50 One-sentence summary: Active H3K4me3 deposition is essential for gametophyte chromatin 51 landscape, playing critical roles in gamete mitotic cell cycle progression and pollen 52 vegetative cell function. 53 54



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ABSTRACT 55 56 Epigenetic reprogramming occurring during reproduction is crucial for both animal and plant 57 development. Histone H3 lysine 4 trimethylation (H3K4me3) is an evolutionarily conserved 58 epigenetic mark of transcriptional active euchromatin. While much has been learned in 59 somatic cells, H3K4me3 deposition and function in gametophyte is poorly studied. Here we 60 demonstrate that SDG2-mediated H3K4me3 deposition participates in epigenetic 61 reprogramming during Arabidopsis male gametogenesis. We show that loss of SDG2 barely 62 affects meiosis and cell fate establishment of haploid cells. However, we found that SDG2 is 63 critical for postmeiotic microspore development. Mitotic cell division progression is partly 64 impaired in the loss-of-function sdg2-1 mutant, particularly at the second mitosis setting up 65 the two sperm cells. We demonstrate that SDG2 is involved in promoting chromatin 66 decondensation in the pollen vegetative nucleus, likely through its role in H3K4me3 67 deposition, which prevents ectopic heterochromatic H3K9me2 speckle formation. Moreover, 68 we found that derepression of the LTR retrotransposon ATLANTYS1 is compromised in the 69 vegetative cell of the sdg2-1 mutant pollen. Consistent with chromatin condensation and 70 compromised transcription activity, pollen germination and pollen tube elongation, 71 representing the key function of the vegetative cell in transporting sperm cells during 72 fertilization, are inhibited in the sdg2-1 mutant. Taken together, we conclude that SDG2-73 mediated H3K4me3 is an essential epigenetic mark of the gametophyte chromatin 74 landscape, playing critical roles in gamete mitotic cell cycle progression and pollen 75 vegetative cell function during male gametogenesis and beyond. 76



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INTRODUCTION 77 78 In animals and plants, epigenetic reprogramming during reproduction is believed to play 79 crucial roles in maintaining genome integrity, in potentiating genetic and epigenetic 80 variation, in resetting gene-expression program, and in contributing to the embryo 81 totipotency at fertilization (Sasaki and Matsui 2008; Feng et al. 2010; Kawashima and Berger 82 2014; Lesch and Page 2014). In animals, a diploid germline arises early during embryogenesis 83 and remains as a distinct niche of stem cells (primordial germ cells) throughout life (Sasaki 84 and Matsui 2008). In flowering plants, however, the germline is differentiated from somatic 85 cells within specialized organs of the flower, which is formed late in development, after a 86 long postembryonic phase of plant growth (Ma 2005). Furthermore, while in animals 87 gametes are direct products of meiosis, in plants multicellular haploid gametophytes are 88 formed through rounds of postmeiotic cell divisions. Thus, in many flowering plants 89 including the model plant Arabidopsis thaliana, the male gametophyte is characterized by a 90 3-celled pollen and the female gametophyte by a 7-celled embryo sac (Berger and Twell 91 2011; Schmid et al. 2015). Upon double fertilization, one of the two haploid sperm cells from 92 the pollen fuses with the egg cell of the embryo sac to form the diploid zygote, which 93 develops into embryo. The other sperm cell fuses with the central cell of the embryo sac to 94 produce the triploid endosperm, a tissue providing nourishment to the developing embryo 95 (Hamamura et al. 2012). These differences of reproductive strategies used by plants as 96 compared to animals are driving intense interest on epigenetic reprogramming mechanisms 97 associated with complex cell fate establishment and maintenance during plant reproduction. 98

Cell-type specificities lay in distinctive transcriptomes that are controlled by the 99 activity of transcription factors, and by the chromatin structure, which can impede the 100 accessibility and activity of the transcriptional machinery. In mammals, an erasure of almost 101 all DNA methylation states is observed before fertilization (Feng et al. 2010). In plants, 102 however, such extreme reprogramming event does not seem to occur at fertilization 103 (Ingouff et al. 2017; Saze et al. 2003; Jullien et al. 2012; Calarco et al. 2012). Moreover, over 104 85% of mammalian histones are replaced by sperm-specific protamine proteins enabling 105 extensive compaction of DNA in male gametes, and upon fertilization the paternal 106 chromatin is deprived of the protamines and loaded with variant histone H3.3 provided by 107 the female gametes (Ooi and Henikoff 2007; Saitou and Kurimoto 2014). However, plants do 108



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not contain protamines, and in Arabidopsis germ cells the canonical histone H3.1 is replaced 109 by the H3.3 variant, HISTONE THREE RELATED10 (HTR10), which is subsequently removed 110 from the zygote nucleus upon fertilization (Ingouff et al. 2007; Ingouff et al. 2010). Within 111 pollen, chromatin is less condensed in the vegetative cell nucleus than in the two sperm cell 112 nuclei. Interestingly, during microsporogenesis, DNA demethylation occurs in the pollen 113 vegetative cell nucleus and activation of transposable elements (TEs) in the vegetative cell 114 has been proposed to generate small RNAs to reinforce silencing of complementary TEs in 115 sperm cells (Ibarra et al. 2012; Slotkin et al. 2009; Calarco et al. 2012). Moreover, the 116 heterochromatin mark H3K9me2 specifically accumulates in the two sperm cell nuclei while 117 it is greatly absent from the vegetative cell nucleus (Schoft et al. 2009), and the other 118 histone methylations including H3K4me2/me3, H3K36me2/me3 and H3K27me3 are 119 detected abundantly in the vegetative cell nucleus (Cartagena et al. 2008; Sano and Tanaka 120 2010; Houben et al. 2011; Pandey et al. 2013). 121

Methylation of histone lysine residues depends on the activity of Histone 122 Methyltransferases (HMTases): most of them contain an evolutionarily conserved catalytic 123 SET-domain (Huang et al. 2011; Thorstensen et al. 2011; Herz et al. 2013). So far, various 124 HMTases have been characterized in animals and plants, primarily in somatic cells but rarely 125 in germ cells. In Arabidopsis, several SET DOMAIN GROUP (SDG) proteins, including 126 ATX1/SDG27, ATX2/SDG30, ATXR7/SDG25 and ATXR3/SDG2, have been reported to catalyze 127 H3K4 methylation. Disruption of ATX1 causes pleiotropic phenotypes including homeotic 128 transformation, root and leaf defects, and early flowering, whereas loss of ATX2 alone does 129 not have an obvious phenotype but can enhance atx1 mutant defects (Alvarez-Venegas et al. 130 2003; Pien et al. 2008; Saleh et al. 2008). The loss-of-function sdg25/atxr7 mutant has an 131 early flowering phenotype associated with suppression of FLOWERING LOCUS C (FLC) 132 expression (Berr et al. 2009; Tamada et al. 2009). Remarkably, ATXR3/SDG2 is broadly 133 expressed and its disruption leads to severe and pleiotropic phenotypes including dwarfism, 134 short-root, impaired fertility and altered circadian clock, as well as the misregulation of a 135 large number of genes (Berr et al. 2010; Guo et al. 2010; Malapeira et al. 2012; Yun et al. 136 2012; Yao et al. 2013). 137

In this study, we investigate the function of SDG2 in chromatin reprogramming 138 during male gametophyte development. While loss of SDG2 does not show detectable effect 139 on meiosis and cell fate acquisition, the loss-of-function sdg2-1 mutant displays a pause or 140



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delay of developmental progression at bicellular pollen stage. Chromatin condensation was 141 found elevated in the pollen vegetative cell nucleus, which is in association with a reduction 142 of H3K4me3 and an ectopic speckle formation of the heterochromatin mark H3K9me2 143 detected in the sdg2-1 pollen grains. Remarkably, in the sdg2-1 mutant, the activation of 144 retrotransposon ATLANTYS1 in the pollen vegetative cell is impaired, and pollen germination 145 as well as pollen tube elongation is inhibited. Our study thus establishes a crucial role of 146 SDG2-mediated H3K4me3 in chromatin landscape regulation and postmeiotic microspore 147 development and function. 148 149 RESULTS 150 151 Loss of SDG2 barely affects male meiosis 152 Arabidopsis SDG2 has been shown to be essential in sporogenous tissues during specification 153 of floral organs, as well as in gametophytic function (Berr et al. 2010; Guo et al. 2010). In 154 these previous studies, several independent sdg2 mutant alleles had been characterized to 155 display similar loss-of-function mutant phenotype, and the mutant phenotype could be fully 156 rescued to wild-type phenotype in complementation test. It was reported that 157 independently from flower developmental defects, the probability of the sdg2-1, sdg2-2 or 158 sdg2-3 allele transmission from the selfing population in heterozygous (+/-) mutant plants is 159 reduced roughly to 55-75%. Furthermore, analyses of reciprocal crosses between the control 160 wild-type Columbia-0 (Col-0) and the heterozygous mutant sdg2-1(+/-) plants or between 161 Col-0 and sdg2-3(+/-) plants showed that both male and female transmission are affected 162 (Berr et al. 2010). The decreased transmission of mutant alleles does not result from an 163 increase in embryo lethality (Berr et al. 2010). This phenotype might rather result from 164 defects in meiosis progression and/or gametophyte development. To investigate those 165 possibilities, we first monitored the different stages of meiosis in sdg2-1 mutant using 4, 6-166 diamidino-2-phenylindole (DAPI) staining of microspore mother cells. Meiosis consists of two 167 rounds of cell divisions after a single round of DNA replication, producing haploid gametes. 168 The meiosis events have been clearly described previously (Ross et al. 1996; Ma 2005); the 169 different meiotic stages observed in the control Col-0 plants are shown in Fig. 1A to 1J. 170 During meiosis I in sdg2-1, the condensed homologous chromosomes form an array on the 171 nuclear plate following synapsis and pairing in prophase I (Fig. 1K to 1M), similarly as in Col-0 172



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(Fig. 1A to 1C). The homologous chromosomes then migrate to opposite poles in sdg2-1 (Fig. 173 1N and 1O) similarly as in Col-0 (Fig. 1D and 1E), and after meiosis II, individual sister 174 chromatids are separated to form tetrad of haploid nuclei in sdg2-1 (Fig. 1P and 1T) similarly 175 as in Col-0 (Fig.1F to 1J). Based on the observation of more than 50 meiocytes at each 176 meiotic stage, we found that the meiosis events in the sdg2-1 mutant show no significant 177 differences compared to Col-0. To conclude we could not detect any abnormal chromosome 178 configuration during meiosis in sdg2-1, suggesting that SDG2 activity rather regulates 179 postmeiotic gametogenesis in Arabidopsis. 180 181 SDG2 is not essential for establishment of pollen vegetative and sperm cell identity 182 To further characterize SDG2 function during postmeiotic gametogenesis, we investigated 183 the establishment of gametophytic cell fate in sdg2-1 mutant. We analyzed postmeiotic 184 events using specific vegetative and sperm cell nuclei reporters, respectively AC26-mRFP and 185 HTR10-mRFP, combined with nuclear DAPI staining. The living-cell reporter HTR10-mRFP 186 represents a fusion between the H3.3 variant HTR10 protein and the fluorescent protein 187 mRFP under the control of the native HTR10 promoter (Ingouff et al. 2007); and AC26-mRFP 188 is associated with the expression of HISTONE H2B-mRFP fusion protein under the control of 189 ACTIN11 promoter (Rotman et al. 2005). Analyses under the confocal microscope revealed 190 that HTR10-mRFP specifically marks the generative cell nucleus of bicellular pollen (Fig. 2A) 191 and the two sperm cell nuclei of tricellular pollen (Fig. 2B) in a way similar between Col-0 192 and sdg2-1. Also the vegetative cell marker AC26-mRFP was observed specifically marking 193 the vegetative cell within the mature pollen in a way similar between Col-0 and sdg2-1 (Fig. 194 2C). Our data thus indicate that the establishment of sperm and vegetative cell fate can 195 occur normally in sdg2-1 pollen. Furthermore our observation also indicates that specific 196 incorporation of the HTR10 variant before fertilization in the chromatin of generative and 197 sperm cell nuclei (Ingouff et al. 2007) is unaffected in sdg2-1, as compared to wild-type. 198 199 SDG2 is involved in the timing of pollen development 200 To further understand sdg2-1 pollen defects that lead to a reduced transmission of the 201 mutant allele, we analyzed the developmental timing of pollen maturation. Anther 202 formation in Arabidopsis is divided into 14 developmental stages (Sanders et al. 1999). The 203 meiosis that will generate the microspores occurs around stage 6 of anther development. 204



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While the first mitotic division takes place at stages 11, the second division that will produce 205 tricellular pollen is observed at anther developmental stages 12. We first examined bicellular 206 stage pollen (anther stage 11) using HTR10-mRFP marker to count the number of 207 generative/sperm nuclei per pollen. In both Col-0 and sdg2-1, more than 94% of pollen 208 grains contained one generative nucleus per pollen as expected for normal development 209 (Fig. 3A). Later at development, in tricellular stage pollen (anther stages 12-13), 82% of the 210 Col-0 pollen grains had two sperm nuclei per pollen marked with HTR10-mRFP, while only 211 65% of the sdg2-1 pollen grains showed two sperm nuclei per pollen, and 24% of the sdg2-1 212 pollen grains showed one sperm nucleus per pollen (versus 11% in Col-0) (Fig. 3B). To verify 213 that sdg2-1 pollen from anther stages 12-13 with one HTR10-mRFP positive nucleus is 214 indeed at bicellular stage, we also used DAPI staining in examination. We found that sdg2-1 215 pollen with one nucleus marked with HTR10-mRFP is always a bicellular pollen and never a 216 tricellular pollen (Fig. 3C). Therefore we conclude that the transition from bicellular to 217 tricellular stage of pollen development is slowing down or paused in sdg2-1. 218 219 SDG2 is involved in maintenance of decondensed chromatin state of pollen vegetative cell 220 In both male and female gametophytes, specific cell types are characterized by specific 221 chromatin organization. In wild-type Arabidopsis pollen, the vegetative cell nucleus contains 222 a relatively decondensed chromatin whereas the sperm nuclei contain highly condensed 223 chromatin (Schoft et al. 2009). In sdg2-1 mutant, global chromatin organization might be 224 impaired, and would then affect pollen development. To verify this hypothesis, we analyzed 225 DNA condensation in pollen vegetative and sperm cell nuclei using DAPI staining. Confocal 226 analyses showed that at early stage of gametophyte development, DNA in haploid 227 microspore is more condensed in sdg2-1 than in Col-0 (Fig. 4A, upper panels). At the 228 following bicellular and tricellular stages of pollen development, we found that DNA 229 condensation remained obviously higher in the vegetative cell nuclei of sdg2-1 as compared 230 to those of Col-0 (Fig. 4A, middle and lower panels; and Fig. 4B and 4C). In contrast, 231 significant differences in DNA condensation were undetectable in generative or sperm cell 232 nuclei between sdg2-1 and Col-0 (Fig. 4). Together, our data indicate that SDG2 is required 233 for proper chromatin decondensation in the microspore and later on in the vegetative cell 234 nucleus at bicellular and tricellular stages of pollen development. 235 236



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SDG2-mediated H3K4me3 prevents ectopic heterochromatic H3K9me2 speckle formation 237 in pollen nuclei 238 To confirm that SDG2 is indeed involved in regulating H3K4me3 in pollen, we utilized anti-239 H3H4me3 antibodies to immunolocalize the histone mark in wild-type versus mutant pollen. 240 We found that H3K4me3 is present in both vegetative and sperm nuclei of Col-0 pollen (Fig. 241 5A, upper panels) and its signal intensity are greatly reduced in both vegetative and sperm 242 nuclei of the sdg2-1 mutant pollen (Fig. 5A, lower panels) compared to Col-0 pollen (Fig. 5B). 243 Western blot analysis revealed that H3K4me3 level is globally reduced in the sdg2-1 244 inflorescence (Fig. 5C). These data are consistent with the previous reports showing that 245 SDG2 encodes a major H3K4-methyltransferase in Arabidopsis (Berr et al. 2010; Guo et al. 246 2010). In contrast to the euchromatin marker H3K4me3, H3K9me2 represents the 247 heterochromatin marker in Arabidopsis. Our western blot analysis failed to detect any clear 248 changed level of H3K9me2 in the sdg2-1 inflorescence (Fig. 5C). Our immunolocalization 249 analysis showed that H3K9me2 is detected in speckles in the sperm cell nuclei but barely in 250 the vegetative nucleus (<9%, n=56) of Col-0 pollen (Fig. 5D and 5E; Supplemental Fig. S1), 251 which is in agreement with a previous study (Schoft et al. 2009). Interestingly, the sdg2-1 252 mutant pollen showed clearly detectable H3K9me2 speckles in the vegetative nucleus 253 (>30%, n=52) as well as an increase of speckles in the sperm nuclei (Fig. 5D and 5E; 254 Supplemental Fig. S1). Examination of pollen at bicellular stage also revealed an increase of 255 H3K9me2 speckles in both vegetative and generative nuclei in sdg2-1 as compared to Col-0 256 (Fig. 5F; Supplemental Fig. S1). From those data, we conclude that SDG2-mediated H3K4me3 257 prevents ectopic heterochromatic H3K9me2 speckle formation, and that the reduced level 258 of H3K4me3 together with H3K9me2 redistribution likely has caused high chromatin 259 compaction observed in the vegetative nucleus of the sdg2-1 mutant. 260 261 SDG2 is required for active expression of retrotransposon ATLANTYS1 in pollen 262 Previous studies have revealed that global DNA demethylation specifically occurs in the 263 pollen vegetative cell nucleus, and active transcription and production of mobile siRNAs 264 from TEs in the vegetative cell are proposed to act on complementary TE silencing 265 associated with compact chromatin in the sperm cell nuclei (Ibarra et al. 2012; Slotkin et al. 266 2009; Calarco et al. 2012). The presence of a more condensed DNA together with the 267 decreased H3K4me3 in sdg2-1 might affect TEs derepression in the pollen vegetative cell. To 268



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directly analyze the functional effect of chromatin condensation defect in sdg2-1 pollen, we 269 crossed sdg2-1/+ with a GUS enhancer trap line ET5729, which contains an insertion of β-270 glucuronidase (GUS) coding sequence in an endogenous retrotransposon ATLANTYS1 271 (Sundaresan et al. 1995; Slotkin et al. 2009). To eliminate possible mixed genetic background 272 effect, we also crossed Col-0 with ET5729 (Landsberg erecta, Ler background) and used as 273 control. GUS staining analysis revealed that wild-type Col-0 pollen is absent of staining (Fig. 274 6A) and pollen from F2 plants of Col-0 x ET5729 shows clear blue GUS staining (Fig. 6B). 275 Interestingly, pollen from F2 plants of sdg2-1 (Col-0 background) x ET5729 showed barely 276 detectable GUS blue staining (Fig. 6C). Consistently, at later generation, with the GUS 277 reporter allele at homozygous state, strong blue staining was detected in ET5729 (Col-0) 278 control pollen (Fig. 6D) but not in ET5729 (sdg2-1) mutant pollen (Fig. 6E). Thus, our data 279 indicate that ATLANTYS1 activation is impaired in sdg2-1. Analysis of the previously 280 published microarray data (Berr et al. 2010) revealed that 20 TE genes are down-regulated 281 by more than 2-fold in sdg2-1 compared to Col-0 flower buds (Supplemental Table S1). 282 Transcripts of the majority of these TE genes are detectable in the male meiocyte (Yang et al. 283 2011) and/or in pollen (Loraine et al. 2013) by RNA sequencing (RNA-seq) analysis. More 284 notably, among these TE genes At5g28626 corresponds to a full-length SADHU element, 285 which is disrupted by an ATLANTYS2-like retrotransposon LTR sequence and controlled in 286 silencing by DNA methylation in some Arabidopsis accessions (Rangwala et al. 2006). 287 Collectively, the data indicate that transcription activation of various TE genes relies on 288 SDG2, which is in agreement with the reduced H3K4me3 and high chromatin compaction 289 observed in the vegetative cell of sdg2-1 pollen. 290 291 SDG2 plays a critical role in pollen germination and pollen tube elongation 292 A major function of pollen vegetative cell activity is to assure pollen germination and 293 subsequent pollen tube elongation to deliver sperm cells for fertilization. Lastly, we 294 addressed the question whether or not SDG2 plays a role in these processes. Thus we 295 carried out in vitro pollen germination assays. After 8 hours incubation on appropriate 296 culture medium, nearly 77% of the Col-0 pollen grains produced pollen tubes (n=300), while 297 the germination ratio of the sdg2-1 mutant pollen grains arrived only to about 10% (n=300) 298 (Fig. 6F,G). Moreover, the length of the mutant pollen tube was drastically inhibited, as 299 compared to the good length of wild-type pollen tube (Fig. 6F). These data clearly 300



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demonstrate that loss of SDG2 impairs pollen germination and pollen tube elongation, which 301 is in line with high chromatin compaction and compromised transcription activity observed 302 in the sdg2-1 pollen vegetative cell. 303 304 DISCUSSION 305 306 In this study we show that SDG2-mediated H3K4me3 participates to the epigenetic 307 reprogramming observed during Arabidopsis male gametogenesis. Although male meiosis 308 and cell fate acquisition can occur normally in the sdg2-1 mutant, SDG2-mediated H3K4me3 309 is crucial in promoting postmeiotic microspore chromatin decondensation, mitotic cell 310 division, and activation of retrotransposon ATLANTYS1. Consistent with a compromised 311 vegetative cell function, pollen germination and pollen tube elongation are found inhibited 312 in the sdg2-1 mutant. 313

In wild-type Arabidopsis, as compared to surrounding somatic cells, both 314 megaspore and microspore mother cells display more decondensed chromatin with higher 315 levels of H3K4me2 and H3K4me3 (She et al. 2013; She and Baroux 2015). The MALE 316 MEIOCYTE DEATH 1 (MMD1, also known as DUET) gene encodes a PHD-finger protein 317 essential for male meiosis (Reddy et al. 2003; Yang et al. 2003). Loss of MMD1/DUET 318 function causes multiple defects including cytoplasmic collapse and cell death of meiocytes 319 with possible DNA fragmentation, delay in progression and arrest at metaphase I, and 320 formation of aberrant meiotic products such as dyads and triads (Reddy et al. 2003; Yang et 321 al. 2003; Andreuzza et al. 2015). More recent studies demonstrate that the MMD1/DUET 322 PHD-finger exhibits binding activities to modified histone H3 peptides including H3K4me2 323 and H3K4me3 and that its mutation compromises MMD1/DUET biological function 324 (Andreuzza et al. 2015; Wang et al. 2016). Based on these previous studies, one can predict 325 that H3K4me2/me3 might play crucial roles in Arabidopsis male meiosis. In contrast, 326 however, depletion of the Arabidopsis major H3K4me2/me3-methyltransferase SDG2 in the 327 sdg2-1 mutant (Berr et al. 2010; Guo et al. 2010) showed normal male meiosis without any 328 detectable chromosomal abnormality throughout different meiotic phases (Fig. 1). The 329 female meiosis also occurs normally in the sdg2-1 mutant, albeit reduced H3K4me3 in 330 megaspore mother cells (She et al. 2013). It seems that Arabidopsis meiosis is rather tolerant 331 to H3K4me3 reduction. Nevertheless, cautions are necessary because Arabidopsis contains 332



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multiple H3K4-methyltransferases that may have overlap/redundant function in meiosis. 333 Transcripts of SDG2 as well as those of ATX1, ATX2 and SDG4 have been detected in male 334 meiocytes (Yang et al. 2011). Moreover, SDG4 has been reported to contribute to pollen 335 function, likely through methylation of H3K4 and H3K36 (Cartagena et al. 2008). Future 336 studies will be required to verify possible overlap/redundant functions of these different 337 HMTase genes to better understand the role of H3K4me2/me3 deposition in Arabidopsis 338 meiosis. 339

After meiosis II, sister chromatids are separated to form tetrad of haploid cells in 340 sdg2-1 as in Col-0 (Fig. 1P and 1T). Nevertheless, tetrad analysis had revealed significant loss 341 of nuclei in sdg2-1 (Berr et al. 2010), indicating that chromatin in the mutant might be 342 unstable and DNA degradation might have occurred in some mutant microspores. During 343 gametogenesis, the first haploid cell division leads to establishment of the vegetative cell 344 and the generative cell at bicellular pollen stage, and the second mitotic cell division occurs 345 specifically from the generative cell resulting in tricellular pollen containing the vegetative 346 cell and two sperm cells. Our analysis of living pollen grains shows that cell fate acquisition 347 can occur normally in the sdg2-1 mutant (Fig. 2). However, SDG2-depletion prevents the 348 second pollen mitosis, generating a fraction of pollen grains comprising a vegetative cell and 349 a single sperm cell (Fig. 3). One major regulator of sperm cell identity and cell cycle 350 progression is the transcription factor DUO POLLEN1 (DUO1) (Rotman et al. 2005; Borg et al. 351 2011; Borg et al. 2014). In the loss-of-function mutant duo1, the generative cell fails to 352 divide to generate two sperm cells, and the mutant pollen cannot fertilize the female egg 353 cell or central cell. Specific expression of the histone variant gene HTR10 in sperm cells is 354 under the direct control of DUO1 (Borg et al. 2014). Our study shows that HTR10-mRFP 355 expression is unaffected in the sdg2-1 pollen (Fig. 2 and Fig. 3), suggesting that SDG2 acts 356 independently from the DUO1-pathway. The more condensed chromatin observed in the 357 vegetative cell (Fig. 4) might have affected its genome function and indirectly impairs 358 generative cell division in the sdg2-1 pollen. The histone chaperone CHROMATIN ASSEMBLY 359 FACTOR1 (CAF1), which is involved in de novo assembly of nucleosomes in a replication-360 dependent manner, is also required for mitotic cell division but not for cell fate maintenance 361 during pollen development (Chen et al. 2008). Together those data suggest the existence of 362 a strong link between the chromatin landscape and cell cycle progression for proper pollen 363 development. 364



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Highly condensed chromatin of sperm cells is thought to serve as a mechanism to 365 insure genome integrity, e.g. by suppression of TE transposition because uncontrolled TE 366 transposition could cause insertions, deletions and/or other rearrangements of the genome 367 (Slotkin et al. 2009). Distinct from sperm cells, the pollen vegetative cell does not transfer its 368 genomic DNA to the fertilization products during plant reproduction. The less condensed 369 chromatin allows active TE transcription, and production of mobile siRNAs from TEs in the 370 pollen vegetative cell has been proposed to move to promote TE silencing associated with 371 DNA methylation in the pollen sperm cell nuclei (Ibarra et al. 2012; Slotkin et al. 2009; 372 Calarco et al. 2012). Genome-wide analysis using Arabidopsis seedlings reveals that 373 H3K4me2/3 and DNA methylation are mutually exclusive (Zhang et al. 2009). The sdg2-1 374 mutant has reduced H3K4me3 levels and its pollen vegetative cell exhibits more condensed 375 chromatin (Fig. 4 and 5). Consistent with the role of H3K4me3 in promoting 376 euchromatinization and transcription activation, expression of the retrotransposon 377 ATLANTYS1 and likely also some other TE genes is impaired in the sdg2-1 pollen (Fig. 6, Table 378 S1). Remarkably, the sdg2-1 pollen nuclei display ectopic speckles of H3K9me2, the main 379 histone modification associated with DNA methylation in heterochromatinization in somatic 380 tissues of Arabidopsis (Stroud et al. 2013). It is currently unknown whether or not H3K9me2 381 heterochromatinization is associated with TE silencing and/or whether the H3K4me3 382 reduction directly or indirectly causes the impaired TE expression in the sdg2-1 mutant 383 pollen. 384

In wild-type Arabidopsis pollen, H3K4me3 is found in both the vegetative cell 385 nucleus and the sperm nuclei, whereas H3K9me2 is present specifically in the sperm cell 386 nuclei (Fig. 5; Schoft et al. 2009). Remarkably, a recent study demonstrates that H3K4me3 is 387 present at similar levels in vegetative, generative and sperm nuclear extracts of lily (Lilium 388 davidii) pollen, whereas H3K9me2 and H3K9me3 are detected at higher levels in vegetative 389 than in generative or sperm nuclear extract (Yang et al. 2016). Thus, pollen cell-type-specific 390 pattern of H3K9me2 accumulation is likely plant species-dependent. Nevertheless, H3K9me2 391 in the lily (Lilium longiflorum) pollen vegetative cell nucleus is co-localized with DAPI-staining 392 regions (Sano and Tanaka 2010), indicating that the heterochromatic nature of H3K9me2 393 remains similar in lily as in Arabidopsis. Our study showed that albeit reduced H3K4me3, 394 chromatin compaction remains largely unaffected in the sdg2-1 pollen sperm nuclei. It 395 becomes evident that future studies are required to further investigate histone methylation 396



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function in chromatin condensation in pollen sperm cells. Distinctively, our data clearly 397 establish a crucial function of H3K4me3 deposition in the pollen vegetative cell. SDG2-398 dependent H3K4me3 deficiency prevents pollen germination and pollen tube elongation. 399 Chromatin landscape seems to be tightly associated with the active transcriptional genome 400 program of the pollen vegetative cell, which is key for pollen tube growth to guide the 401 delivery of sperm cells to the ovule for fertilization. 402 403 MATERIALS AND METHODS 404 405 Plant material 406 sdg2-1 mutant has been described previously (Berr et al. 2010). Seeds from the reporters 407 AC26-mRFP and HTR10-mRFP were kindly provided by Frederic Berger (Chen et al. 2008). 408 sdg2-1 mutant and the two reporter lines mentioned previously are in the Col-0 background. 409 Both reporter lines were crossed with sdg2-1/+. Plants homozygous for the fluorescent 410 marker and heterozygous for sdg2-1/+ were selected in F2 population by analyzing RFP 411 segregation in mature pollen, and PCR-based genotyping (Berr et al. 2010) to identify sdg2-1 412 allele. Then F3 plants homozygous for both the fluorescent reporter and sdg2-1 were 413 identified based on sdg2-1 phenotype (Berr et al. 2010). The GUS enhancer trap line ET5729 414 was kindly provided by Mathieu Ingouff. ET5729 is in the Landsberg erecta (Ler) background 415 and was crossed to wild-type Col-0 plants (controls) and sdg2-1/+ plants to generate in F3 416 progeny plants homozygous for sdg2-1 and ET5729. Seedlings (until one week old) were 417 grown at 21-22°C under continuous white light and on Murashige and Skoog medium 418 supplemented with 0.8% of Plant agar (Sigma). Then seedlings were transferred on standard 419 potting soil at 21-22°C under a 12h light/12h dark cycle for 3 weeks, and then to a 420 photoperiod of 16h light/8h dark. 421 422 Chromosome spreading analysis and immunostaining 423 Microspores from all stages of meiosis were collected from fresh floral buds, fixed in 424 Carnoy’s fixative solution (ethanol:chloroform:acetic acid = 6:3:1), prepared for chromosome 425 spreads as described previously (Ross et al. 1996), and stained with 4, 6-diamidino-2-426 phenylindole (DAPI) (0.1 μg/mL). Immunostainings of histone modifications were performed 427 on bicellular and tricellular pollen collected after anther dissection from floral stages 10 to 428



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12. The collected pollens were fixed in 4% paraformaldehyde in PBS for 30 min, and then 429 keep in 1% sucrose solution overnight at 4°C. After washing, the samples were incubated 430 with the anti-H3K4me3 antibody (Millipore), or the anti-H3K9me2 antibody (Millipore) at 431 1:200 dilution. Alexa Fluor 488-conjugated anti-rabbit IgG antibodies (Invitrogen) and 594-432 conjugated anti-mouse IgG antibodies (Invitrogen) were used specifically as the secondary 433 antibody. 434 435 Microscopy 436 DAPI staining of pollen grains was performed according to a previous report (Park et al. 437 1998). Epifluoresce images (mRFP-fusion proteins and DAPI-stained DNA) were acquired 438 using Zeiss Imager A2 microscope (Fig. 1 and Fig. 5) and Zeiss LSM710 confocal laser-439 scanning microscopy (Fig. 2, Fig. 3, Fig. 4, and Fig. 6). GUS staining was performed following 440 the protocol described previously (Johnson et al. 2004). Here pollen grains were incubated 441 with X-Gluc overnight at 37°C, and imaged under a phase-contrast microscope. 442 443 Histone extraction and western blot analysis 444 Histone-enriched proteins were extracted from inflorescence according a previously 445 described method (Yu et al. 2004). Western blot assays were performed to detect the 446 covalent modification status of H3 tails (Yu et al. 2004). Antibodies against histone 447 H3K4me3, H3K9me2, and H3 (Millipore) were used at 1:2000 dilution. 448 449 Quantification and statistic test 450 Densitometry quantification of western blots and fluorescent intensity quantification of 451 microscopy images were performed by using ImageJ software (https://imagej.nih.gov/ij/). 452 For each pollen grain, confocal image with maximum fluorescence intensity was used in 453 measurement at individual nucleus level, divided by nuclear area size, and normalized using 454 a similar size area in the cytoplasm as background. Statistical analysis was performed by 455 unpaired t-test using GraphPad InStat v. 3.05 (GraphPad Software; 456 http://www.graphpad.com). 457 458 In vitro pollen germination assay 459



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In vitro pollen tube growth assay was performed as described previously (Li et al. 1999). 460 Briefly, pollen grains from dehiscent anthers were carefully plated onto the surface of agar 461 plates. The plates were than immediately transferred to a chamber at 25°C and 100% 462 relative humidity. Pollen grains were cultured for 8h, and the germination ratio was 463 calculated by counting 300 pollen grains under a light microscope. This experiment was 464 repeated three times with three plates per repeat. 465 ACKNOWLEDGMENTS 466 The authors thank Zhihao Cheng for technical assistance in chromosome spreading 467 experiments, Hongxing Yang, Yingxiang Wang and Hong Ma for providing male meiocytes 468 transcriptome data and helpful discussions. 469 470 SUPPLEMENTAL DATA 471 Supplemental Figure 1. Immunofluorescence-staining analysis of the wild-type control Col-0 472 and the sdg2-1 mutant pollen. 473 Supplemental Table 1. List of transposable element genes down-regulted by more than 2-474 fold sdg2-1 as compared to wild-type flower buds. 475 476 FIGURE LEGENDS 477 478 Fig. 1. Male meiosis proceeds normally in the loss-of-function mutant sdg2-1. A to J, DAPI 479 staining showing different stages of meiosis in the wild-type control Col-0. K to T, DAPI 480 staining showing different stages of meiosis in sdg2-1. The shown stages correspond to 481 Zygotene (A, K), Diakinesis (B, L), Metaphase I (C, M), Anaphase I (D, N), Telophase I (E, O), 482 Interphase II (F, P), Metaphase II (G, Q), Anaphase II (H, R), Telophase II (I, S), and newly 483 formed tetrad (J, T). Scale bar = 10 µm for all images (A to T). 484 485 Fig. 2. Male cell fate acquisition is unaffected in the loss-of-function mutant sdg2-1. A and B, 486 DAPI (upper panels) and HTR10-mRFP (lower panels) fluorescent signals in pollen at 487 bicellular and tricellular developmental stage, respectively. In (B) but not in (A), the HTR10-488 mRFP fluorescence is shown together with its corresponding transmitted light reference 489



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image to visualize the entire mature pollen grain. Note for specific HTR10-mRFP expression 490 in the generative (A) and sperm (B) cells within pollen grains in sdg2-1 similarly as in the 491 wild-type control Col-0. C, DAPI (upper panels) and AC26-mRFP (lower panels) fluorescent 492 signals in tricellular stage pollen in Col-0 and sdg2-1. Note for specific AC26-mRFP signal 493 detected in the vegetative cell nucleus but not in the sperm cells, similarly in sdg2-1 and Col-494 0. Scale bars = 10 µm for all images. 495 496 Fig. 3. Loss of SDG2 prevents mitotic division of pollen generative cell in the sdg2-1 mutant. 497 A, Graphic representation of pollen grains containing the indicated number of generative cell 498 (GC) determined using HTR10-mRFP marker in sdg2-1 and the wild-type control Col-0 at 499 bicellular pollen developmental stage. Pollen was examined from anthers at developmental 500 stage 11 from over ten individual plants for each genotype. The difference between sdg2-1 501 and Col-0 is not significant according to unpaired t-test (p-value > 0.05). B, Graphic 502 representation of pollen grains containing the indicated number of sperm cell (SC) 503 determined using HTR10-mRFP marker in sdg2-1 and Col-0 at tricellular pollen 504 developmental stage. Pollen was examined from anthers at developmental stage 12-13 from 505 over ten individual plants for each genotype. Unpaired t-test indicates that the difference 506 between sdg2-1 and Col-0 is statistically significant for 1 SC and 2 SC categories (indicated by 507 *, p-values < 0.05) but not for 0 SC category (p-value > 0.05). C, HTR10-mRFP (left panel) and 508 DAPI (right panel) fluorescent signals in sdg2-1 pollen grains at tricellular pollen 509 developmental stage. Pollen was examined from anthers at developmental stage 12-13. 510 Arrows indicate pollen grains arrested at bicellular stage without GC division. Scale bars = 10 511 µm. 512 513 Fig. 4. SDG2 is involved in promoting chromatin decondensation in microspore and in pollen 514 vegetative cell nuclei. A, DAPI fluorescent signals in microspores and in pollen grains at 515 bicellular or tricellular stage in the wild-type control Col-0 and the loss-of-function mutant 516 sdg2-1, as indicated. Note for more condensed chromatin in sdg2-1 than in Col-0 in 517 microspore and in the vegetative cell of bicellular or tricellular pollen. Dashed arrow 518 indicates the vegetative cell nucleus and solid arrows indicate sperm cells in the tricelluar 519 pollen. Scale bars = 10 µm. B, Graphic representation of the nuclei area from sperm cells and 520 vegetative cells of mature tricellular stage pollen. The area was measured using ImageJ 521



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software from DAPI-staining microscopy images at the largest scan surface. C, Graphic 522 representation of the DAPI fluorescence intensity per µm2 from sperm and vegetative cell 523 nuclei of mature tricellular stage pollen. The fluorescence intensity was measured using 524 ImageJ software from the image scan displaying the brightest signal. Data shown in B and C 525 represent mean together with error bar based on 40 pollen grains for each genotype per 526 experiment from three independent experiments. The symbol * indicates where the 527 difference between Col-0 and sdg2-1 is significant in statistic test (p-value < 0.05). 528 529 Fig. 5. SDG2 contributes to H3K4me3 and H3K9me2 patterning in pollen. A, 530 Immunofluorescence staining performed with anti-H3K4me3 antibody in tricellular pollen in 531 the wild-type control Col-0 (upper panels) and the sdg2-1 mutant (lower panels). DAPI 532 staining of the same pollen is shown on left panel. Note for drastically reduced H3K4me3 533 signal in the vegetative cell nucleus and the two sperm nuclei of the sdg2-1 pollen as 534 compared to the Col-0 pollen. B, Graphic representation of the relative H3K4me3 535 fluorescence intensity, after normalization using DAPI, in sperm cell and vegetative cell 536 nuclei of Col-0 and sdg2-1 (set as 1 for sdg2-1 vegetative cell nuclei). The fluorescence 537 intensity was measured using ImageJ software, and mean values from 10 pollen grains are 538 shown together with error bars. The symbol * indicates where the difference between Col-0 539 and sdg2-1 is significant in statistic test (p-value < 0.05). C, Western blot analysis of 540 H3K4me3 and H3K9me2 levels in sdg2-1. Histone-enriched protein were extracted from 541 inflorescence of Col-0 and sdg2-1 plants grown under a 16h light / 8h dark photoperiod. 542 H3K9me2, H3K4me3 and total H3 proteins were detected using specific antibodies. Numbers 543 indicate 'mean (± standard error)' of relative densitometry values measured from 3 544 independent experiments, in sdg2-1 and Col-0 (set as 1). D, Immunofluorescence staining 545 performed with anti-H3K9me2 antibody in tricellular pollen in Col-0 (upper panels) and 546 sdg2-1 (lower panels). DAPI staining of the same pollen is shown on left panel. Note for 547 H3K9me2 speckles detected in the sdg2-1 pollen vegetative cell nucleus but not in the Col-0 548 pollen vegetative cell nucleus. E, Close-up images showing H3K9me2 speckles in the sdg2-1 549 but not in the Col-0 pollen vegetative nucleus (dashed circle) as well as in the sperm nuclei 550 (circles) of both sdg2-1 and Col-0 pollen. F, Images showing H3K9me2 speckles in the 551 vegetative nucleus (dashed circle) and in the generative nucleus (circles) of bicellular pollen 552 in Col-0 and sdg2-1. Scale bars = 10 µm for A and D, and 5 µm for E and F. 553



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554 Fig. 6. SDG2 is involved in activation of retransposon ATLANTYS1 transcription and in 555 promoting pollen germination and pollen tube growth. A-C, GUS staining of tricellular stage 556 pollen in bright field microscopy from Col-0 (A), from a F2 plant generated by the cross 557 between the wild-type control Col-0 and the enhancer trap line ET5729 (B), or between 558 sdg2-1 and ET5729 (C). D and E, GUS staining of tricellular stage pollen from plants 559 homozygous for ET5729 in respectively Col-0 (D) and sdg2-1 (E) backgrounds. The lower 560 panels show the corresponding DAPI stained pollen. Arrows indicate the sperm cell nuclei. F, 561 Representative images showing in vitro germination of pollen from Col-0 and sdg2-1. Red 562 arrows indicate germinated sdg2-1 pollen but with pollen tube elongation inhibited. G, 563 Graphic representation of sdg2-1 and Col-0 pollen germination rate. Scale bars = 10 µm for 564 A-E, and 200 µm for F. 565 566 567 LITERATURE CITED 568 Alvarez-Venegas R, Pien S, Sadder M, Witmer X, Grossniklaus U, Avramova Z (2003) 569 ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes. 570 Curr Biol 13 (8):627-637 571 Andreuzza S, Nishal B, Singh A, Siddiqi I (2015) The Chromatin Protein DUET/MMD1 572 Controls Expression of the Meiotic Gene TDM1 during Male Meiosis in 573 Arabidopsis. PLoS Genet 11 (9):e1005396. doi:10.1371/journal.pgen.1005396 574 Berger F, Twell D (2011) Germline specification and function in plants. Annu Rev Plant 575 Biol 62:461-484. doi:10.1146/annurev-arplant-042110-103824 576 Berr A, McCallum EJ, Menard R, Meyer D, Fuchs J, Dong AW, Shen WH (2010) 577 Arabidopsis SET DOMAIN GROUP2 Is Required for H3K4 Trimethylation and Is 578 Crucial for Both Sporophyte and Gametophyte Development. Plant Cell 22 579 (10):3232-3248. doi:10.1105/tpc.110.079962 580 Berr A, Xu L, Gao J, Cognat V, Steinmetz A, Dong A, Shen WH (2009) SET DOMAIN 581 GROUP25 encodes a histone methyltransferase and is involved in FLOWERING 582 LOCUS C activation and repression of flowering. Plant Physiol 151 (3):1476-583 1485. doi:10.1104/pp.109.143941 584 Borg M, Brownfield L, Khatab H, Sidorova A, Lingaya M, Twell D (2011) The R2R3 MYB 585 transcription factor DUO1 activates a male germline-specific regulon essential for 586 sperm cell differentiation in Arabidopsis. Plant Cell 23 (2):534-549. 587 doi:10.1105/tpc.110.081059 588 Borg M, Rutley N, Kagale S, Hamamura Y, Gherghinoiu M, Kumar S, Sari U, Esparza-589 Franco MA, Sakamoto W, Rozwadowski K, Higashiyama T, Twell D (2014) An 590 EAR-Dependent Regulatory Module Promotes Male Germ Cell Division and Sperm 591 Fertility in Arabidopsis. Plant Cell 26 (5):2098-2113. 592 doi:10.1105/tpc.114.124743 593



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Fig. 1.Malemeiosisproceedsnormally in the loss-of-functionmutantsdg2-1.A to J,DAPI

staining showing different stages of meiosis in the wild-type control Col-0. K to T, DAPI

staining showing different stages of meiosis in sdg2-1. The shown stages correspond to

Zygotene(A,K),Diakinesis(B,L),MetaphaseI(C,M),AnaphaseI(D,N),TelophaseI(E,O),

Interphase II (F, P),Metaphase II (G,Q), Anaphase II (H, R), Telophase II (I, S), and newly

formedtetrad(J,T).Scalebar=10µmforallimages(AtoT).

Col-0 Col-0 Col-0 Col-0 Col-0

Col-0 Col-0 Col-0 Col-0 Col-0

sdg2-1 sdg2-1 sdg2-1 sdg2-1 sdg2-1

sdg2-1 sdg2-1 sdg2-1 sdg2-1 sdg2-1



Fig.2.Malecellfateacquisitionisunaffectedintheloss-of-functionmutantsdg2-1.AandB,

DAPI (upper panels) and HTR10-mRFP (lower panels) fluorescent signals in pollen at

bicellularandtricellulardevelopmentalstage,respectively.In(B)butnotin(A),theHTR10-

mRFP fluorescence is shown together with its corresponding transmitted light reference

imagetovisualizetheentirematurepollengrain.NoteforspecificHTR10-mRFPexpression

in the generative (A) and sperm (B) cellswithin pollen grains in sdg2-1 similarly as in the

wild-type controlCol-0.C,DAPI (upperpanels) andAC26-mRFP (lowerpanels) fluorescent

signals in tricellular stage pollen in Col-0 and sdg2-1. Note for specific AC26-mRFP signal

detectedinthevegetativecellnucleusbutnotinthespermcells,similarlyinsdg2-1andCol-

0.Scalebars=10µmforallimages.

Col-0 sdg2-1

HTR10-mRFP

Col-0 sdg2-1

AC26-mRFP

ACol-0 sdg2-1

HTR10-mRFP

B C



Fig.3.LossofSDG2preventsmitoticdivisionofpollengenerativecellinthesdg2-1mutant.

A,Graphicrepresentationofpollengrainscontainingtheindicatednumberofgenerativecell

(GC) determined using HTR10-mRFP marker in sdg2-1 and the wild-type control Col-0 at

bicellularpollendevelopmentalstage.Pollenwasexaminedfromanthersatdevelopmental

stage11fromovertenindividualplantsforeachgenotype.Thedifferencebetweensdg2-1

and Col-0 is not significant according to unpaired t-test (p-value > 0.05). B, Graphic

representation of pollen grains containing the indicated number of sperm cell (SC)

determined using HTR10-mRFP marker in sdg2-1 and Col-0 at tricellular pollen

developmentalstage.Pollenwasexaminedfromanthersatdevelopmentalstage12-13from

over ten individualplants for eachgenotype.Unpaired t-test indicates that thedifference

betweensdg2-1andCol-0isstatisticallysignificantfor1SCand2SCcategories(indicatedby

*,p-values<0.05)butnotfor0SCcategory(p-value>0.05).C,HTR10-mRFP(leftpanel)and

DAPI (right panel) fluorescent signals in sdg2-1 pollen grains at tricellular pollen

developmental stage. Pollen was examined from anthers at developmental stage 12-13.

ArrowsindicatepollengrainsarrestedatbicellularstagewithoutGCdivision.Scalebars=10

µm.

ColTricellularstage

(n=311)

8%2SC1SC0SC

ColBicellularstage

6%

94%

(n=284)

sdg2-1

(n=266)

2%

98%

1GC0GC

Col-0 Col-0sdg2-1A

DAPIHTR10-mRFP

TricellularstageC

sdg2-1

(n=325)

24%*

11%sdg2-1

82% 65%*

11%

B



Fig.4.SDG2isinvolvedinpromotingchromatindecondensationinmicrosporeandinpollen

vegetative cell nuclei. A, DAPI fluorescent signals in microspores and in pollen grains at

bicellularor tricellularstage in thewild-typecontrolCol-0andthe loss-of-functionmutant

sdg2-1, as indicated. Note for more condensed chromatin in sdg2-1 than in Col-0 in

microspore and in the vegetative cell of bicellular or tricellular pollen. Dashed arrow

indicates thevegetative cell nucleusand solidarrows indicate spermcells in the tricelluar

pollen.Scalebars=10µm.B,Graphicrepresentationofthenucleiareafromspermcellsand

vegetative cells of mature tricellular stage pollen. The area was measured using ImageJ

software from DAPI-staining microscopy images at the largest scan surface. C, Graphic

representationof theDAPI fluorescence intensityperµm2 fromspermandvegetative cell

nuclei of mature tricellular stage pollen. The fluorescence intensity was measured using

ImageJsoftwarefromtheimagescandisplayingthebrightestsignal.DatashowninBandC

representmean togetherwith error bar basedon40pollen grains for each genotypeper

experiment from three independent experiments. The symbol * indicates where the

differencebetweenCol-0andsdg2-1issignificantinstatistictest(p-value<0.05).

C

Fluo

rescen

ceIntensity

/µm

2

*

sdg2-1

Col-0 sdg2-1

Microspore

Bicellularstage

Tricellularstage

A B

Nucleiarea(µm

2 )

*

sdg2-10"

2000"

4000"

6000"

8000"

10000"

Col" sdg2.1"

Sperm"cell"nuclei"

Vegeta;ve"cell"nuclei"

C

Fluo

resc

ence

Inte

nsity

/ µm

2

*

sdg2-1

Col-0 Col-00"

2000"

4000"

6000"

8000"

10000"

Col" sdg2.1"

Sperm"cell"nuclei"

Vegeta;ve"cell"nuclei"

C

Fluo

resc

ence

Inte

nsity

/ µm

2

*

sdg2-1



Fig. 5. SDG2 contributes to H3K4me3 and H3K9me2 patterning in pollen. A,Immunofluorescencestainingperformedwithanti-H3K4me3antibodyintricellularpolleninthe wild-type control Col-0 (upper panels) and the sdg2-1 mutant (lower panels). DAPIstainingof the samepollen is shownon leftpanel.Note fordrastically reducedH3K4me3signal in the vegetative cell nucleus and the two sperm nuclei of the sdg2-1 pollen ascompared to the Col-0 pollen. B, Graphic representation of the relative H3K4me3fluorescence intensity, after normalization using DAPI, in sperm cell and vegetative cellnuclei of Col-0 and sdg2-1 (set as 1 for sdg2-1 vegetative cell nuclei). The fluorescenceintensitywasmeasuredusing ImageJsoftware,andmeanvaluesfrom10pollengrainsareshowntogetherwitherrorbars.Thesymbol*indicateswherethedifferencebetweenCol-0and sdg2-1 is significant in statistic test (p-value < 0.05). C, Western blot analysis ofH3K4me3 and H3K9me2 levels in sdg2-1. Histone-enriched protein were extracted frominflorescence of Col-0 and sdg2-1plants grown under a 16h light / 8h dark photoperiod.H3K9me2,H3K4me3andtotalH3proteinsweredetectedusingspecificantibodies.Numbersindicate 'mean (± standard error)' of relative densitometry values measured from 3independent experiments, in sdg2-1 and Col-0 (set as 1). D, Immunofluorescence stainingperformed with anti-H3K9me2 antibody in tricellular pollen in Col-0 (upper panels) andsdg2-1 (lower panels). DAPI staining of the same pollen is shown on left panel. Note forH3K9me2specklesdetectedinthesdg2-1pollenvegetativecellnucleusbutnotintheCol-0pollenvegetativecellnucleus.E,Close-upimagesshowingH3K9me2specklesinthesdg2-1butnotintheCol-0pollenvegetativenucleus(dashedcircle)aswellasinthespermnuclei(circles) of both sdg2-1 and Col-0 pollen. F, Images showing H3K9me2 speckles in thevegetativenucleus(dashedcircle)andinthegenerativenucleus(circles)ofbicellularpolleninCol-0andsdg2-1.Scalebars=10µmforAandD,and5µmforEandF.

A DAPI H3K4me3

Col-0 sdg2-1

H3K9me2

H3

H3K4me3

C

Col-0

sdg2-1

D DAPI H3K9me2

Col-0

sdg2-1

H3K9me2E

Col-0

H3K9me2

sdg2-1

Col-0

sdg2-1

F

B

1

1

1 0.21±0.06

0.95±0.09

0.80±0.10

Vegeta=vecellnucleiSpermcellnuclei

Col-0 sdg2-1

Rela=veintensity

*

*



Fig. 6. SDG2 is involved in activation of retransposon ATLANTYS1 transcription and in

promotingpollengerminationandpollentubegrowth.A-C,GUSstainingoftricellularstage

pollen in bright field microscopy from Col-0 (A), from a F2 plant generated by the cross

between the wild-type control Col-0 and the enhancer trap line ET5729 (B), or between

sdg2-1 and ET5729 (C). D and E, GUS staining of tricellular stage pollen from plants

homozygous for ET5729 in respectively Col-0 (D) and sdg2-1 (E) backgrounds. The lower

panelsshowthecorrespondingDAPIstainedpollen.Arrowsindicatethespermcellnuclei.F,

Representative images showing in vitrogerminationof pollen fromCol-0 and sdg2-1. Red

arrows indicate germinated sdg2-1 pollen but with pollen tube elongation inhibited. G,

Graphicrepresentationofsdg2-1andCol-0pollengerminationrate.Scalebars=10µmfor

A-E,and200µmforF.

Col-0Col-0

xET5729sdg2-1

xET5729

A B C

(n=300)

(n=300)

Germ

ina9

onra

te(%

)

G

Col-0

F

Col-0

sdg2-1

ET5729(Col-0)

DAPI

D E

ET5729(sdg2-1)

DAPI



Parsed CitationsAlvarez-Venegas R, Pien S, Sadder M, Witmer X, Grossniklaus U, Avramova Z (2003) ATX-1, an Arabidopsis homolog of trithorax,activates flower homeotic genes. Curr Biol 13 (8):627-637

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Andreuzza S, Nishal B, Singh A, Siddiqi I (2015) The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic GeneTDM1 during Male Meiosis in Arabidopsis. PLoS Genet 11 (9):e1005396. doi:10.1371/journal.pgen.1005396


Berger F, Twell D (2011) Germline specification and function in plants. Annu Rev Plant Biol 62:461-484. doi:10.1146/annurev-arplant-042110-103824


Berr A, McCallum EJ, Menard R, Meyer D, Fuchs J, Dong AW, Shen WH (2010) Arabidopsis SET DOMAIN GROUP2 Is Required forH3K4 Trimethylation and Is Crucial for Both Sporophyte and Gametophyte Development. Plant Cell 22 (10):3232-3248.doi:10.1105/tpc.110.079962


Berr A, Xu L, Gao J, Cognat V, Steinmetz A, Dong A, Shen WH (2009) SET DOMAIN GROUP25 encodes a histone methyltransferaseand is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol 151 (3):1476-1485.doi:10.1104/pp.109.143941


Borg M, Brownfield L, Khatab H, Sidorova A, Lingaya M, Twell D (2011) The R2R3 MYB transcription factor DUO1 activates a malegermline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell 23 (2):534-549.doi:10.1105/tpc.110.081059


Borg M, Rutley N, Kagale S, Hamamura Y, Gherghinoiu M, Kumar S, Sari U, Esparza-Franco MA, Sakamoto W, Rozwadowski K,Higashiyama T, Twell D (2014) An EAR-Dependent Regulatory Module Promotes Male Germ Cell Division and Sperm Fertility inArabidopsis. Plant Cell 26 (5):2098-2113. doi:10.1105/tpc.114.124743


Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, Lopes T, Gardner R, Berger F, Feijo JA, Becker JD, Martienssen RA(2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151 (1):194-205.doi:10.1016/j.cell.2012.09.001


Cartagena JA, Matsunaga S, Seki M, Kurihara D, Yokoyama M, Shinozaki K, Fujimoto S, Azumi Y, Uchiyama S, Fukui K (2008) TheArabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in maturepollen. Dev Biol 315 (2):355-368. doi:10.1016/j.ydbio.2007.12.016


Chen Z, Tan JL, Ingouff M, Sundaresan V, Berger F (2008) Chromatin assembly factor 1 regulates the cell cycle but not cell fateduring male gametogenesis in Arabidopsis thaliana. Development 135 (1):65-73. doi:10.1242/dev.010108


Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330 (6004):622-627.doi:10.1126/science.1190614


Guo L, Yu YC, Law JA, Zhang XY (2010) SET DOMAIN GROUP2 is the major histone H3 lysie 4 trimethyltransferase in Arabidopsis.Proceedings of the National Academy of Sciences of the United States of America 107 (43):18557-18562.doi:10.1073/pnas.1010478107

Pubmed: Author and TitleCrossRef: Author and Title https://plantphysiol.orgDownloaded on December 9, 2020. - Published by


http://www.ncbi.nlm.nih.gov/pubmed?term=Alvarez%2DVenegas R%2C Pien S%2C Sadder M%2C Witmer X%2C Grossniklaus U%2C Avramova Z %282003%29 ATX%2D1%2C an Arabidopsis homolog of trithorax%2C activates flower homeotic genes%2E Curr Biol 13 %288%29%3A627%2D637&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Alvarez-Venegas R, Pien S, Sadder M, Witmer X, Grossniklaus U, Avramova Z (2003) ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes. Curr Biol 13 (8):627-637

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Alvarez-Venegas&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Andreuzza S%2C Nishal B%2C Singh A%2C Siddiqi I %282015%29 The Chromatin Protein DUET%2FMMD1 Controls Expression of the Meiotic Gene TDM1 during Male Meiosis in Arabidopsis%2E PLoS Genet 11 %289%29%3Ae1005396%2E doi%3A10%2E1371%2Fjournal%2Epgen%2E1005396&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Andreuzza S, Nishal B, Singh A, Siddiqi I (2015) The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene TDM1 during Male Meiosis in Arabidopsis. PLoS Genet 11 (9):e1005396. doi:10.1371/journal.pgen.1005396

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Andreuzza&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene TDM1 during Male Meiosis in Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene TDM1 during Male Meiosis in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Andreuzza&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Berger F%2C Twell D %282011%29 Germline specification and function in plants%2E Annu Rev Plant Biol 62%3A461%2D484%2E doi%3A10%2E1146%2Fannurev%2Darplant%2D042110%2D103824&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Berger F, Twell D (2011) Germline specification and function in plants. Annu Rev Plant Biol 62:461-484. doi:10.1146/annurev-arplant-042110-103824

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Berger&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Germline specification and function in plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Berr A%2C McCallum EJ%2C Menard R%2C Meyer D%2C Fuchs J%2C Dong AW%2C Shen WH %282010%29 Arabidopsis SET DOMAIN GROUP2 Is Required for H3K4 Trimethylation and Is Crucial for Both Sporophyte and Gametophyte Development%2E Plant Cell 22 %2810%29%3A3232%2D3248%2E doi%3A10%2E1105%2Ftpc%2E110%2E079962&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Berr A, McCallum EJ, Menard R, Meyer D, Fuchs J, Dong AW, Shen WH (2010) Arabidopsis SET DOMAIN GROUP2 Is Required for H3K4 Trimethylation and Is Crucial for Both Sporophyte and Gametophyte Development. Plant Cell 22 (10):3232-3248. doi:10.1105/tpc.110.079962

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Berr&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Berr&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Berr A%2C Xu L%2C Gao J%2C Cognat V%2C Steinmetz A%2C Dong A%2C Shen WH %282009%29 SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering%2E Plant Physiol 151 %283%29%3A1476%2D1485%2E doi%3A10%2E1104%2Fpp%2E109%2E143941&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Berr A, Xu L, Gao J, Cognat V, Steinmetz A, Dong A, Shen WH (2009) SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol 151 (3):1476-1485. doi:10.1104/pp.109.143941

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Berr&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Berr&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Borg M%2C Brownfield L%2C Khatab H%2C Sidorova A%2C Lingaya M%2C Twell D %282011%29 The R2R3 MYB transcription factor DUO1 activates a male germline%2Dspecific regulon essential for sperm cell differentiation in Arabidopsis%2E Plant Cell 23 %282%29%3A534%2D549%2E doi%3A10%2E1105%2Ftpc%2E110%2E081059&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Borg M, Brownfield L, Khatab H, Sidorova A, Lingaya M, Twell D (2011) The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell 23 (2):534-549. doi:10.1105/tpc.110.081059

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http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Borg&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Borg M%2C Rutley N%2C Kagale S%2C Hamamura Y%2C Gherghinoiu M%2C Kumar S%2C Sari U%2C Esparza%2DFranco MA%2C Sakamoto W%2C Rozwadowski K%2C Higashiyama T%2C Twell D %282014%29 An EAR%2DDependent Regulatory Module Promotes Male Germ Cell Division and Sperm Fertility in Arabidopsis%2E Plant Cell 26 %285%29%3A2098%2D2113%2E doi%3A10%2E1105%2Ftpc%2E114%2E124743&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Borg M, Rutley N, Kagale S, Hamamura Y, Gherghinoiu M, Kumar S, Sari U, Esparza-Franco MA, Sakamoto W, Rozwadowski K, Higashiyama T, Twell D (2014) An EAR-Dependent Regulatory Module Promotes Male Germ Cell Division and Sperm Fertility in Arabidopsis. Plant Cell 26 (5):2098-2113. doi:10.1105/tpc.114.124743

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Borg&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Borg&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Calarco JP%2C Borges F%2C Donoghue MT%2C Van Ex F%2C Jullien PE%2C Lopes T%2C Gardner R%2C Berger F%2C Feijo JA%2C Becker JD%2C Martienssen RA %282012%29 Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA%2E Cell 151 %281%29%3A194%2D205%2E doi%3A10%2E1016%2Fj%2Ecell%2E2012%2E09%2E001&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, Lopes T, Gardner R, Berger F, Feijo JA, Becker JD, Martienssen RA (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151 (1):194-205. doi:10.1016/j.cell.2012.09.001

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Calarco&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Calarco&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cartagena JA%2C Matsunaga S%2C Seki M%2C Kurihara D%2C Yokoyama M%2C Shinozaki K%2C Fujimoto S%2C Azumi Y%2C Uchiyama S%2C Fukui K %282008%29 The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen%2E Dev Biol 315 %282%29%3A355%2D368%2E doi%3A10%2E1016%2Fj%2Eydbio%2E2007%2E12%2E016&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cartagena JA, Matsunaga S, Seki M, Kurihara D, Yokoyama M, Shinozaki K, Fujimoto S, Azumi Y, Uchiyama S, Fukui K (2008) The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev Biol 315 (2):355-368. doi:10.1016/j.ydbio.2007.12.016

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Cartagena&hl=en&c2coff=1


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http://www.ncbi.nlm.nih.gov/pubmed?term=Chen Z%2C Tan JL%2C Ingouff M%2C Sundaresan V%2C Berger F %282008%29 Chromatin assembly factor 1 regulates the cell cycle but not cell fate during male gametogenesis in Arabidopsis thaliana%2E Development 135 %281%29%3A65%2D73%2E doi%3A10%2E1242%2Fdev%2E010108&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Chen Z, Tan JL, Ingouff M, Sundaresan V, Berger F (2008) Chromatin assembly factor 1 regulates the cell cycle but not cell fate during male gametogenesis in Arabidopsis thaliana. Development 135 (1):65-73. doi:10.1242/dev.010108

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http://www.ncbi.nlm.nih.gov/pubmed?term=Feng S%2C Jacobsen SE%2C Reik W %282010%29 Epigenetic reprogramming in plant and animal development%2E Science 330 %286004%29%3A622%2D627%2E doi%3A10%2E1126%2Fscience%2E1190614&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330 (6004):622-627. doi:10.1126/science.1190614

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Yang H, Yang N, Wang T (2016) Proteomic analysis reveals the differential histone programs between male germline cells andvegetative cells in Lilium davidii. Plant J 85 (5):660-674. doi:10.1111/tpj.13133


Yang X, Makaroff CA, Ma H (2003) The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is requiredfor male meiosis. Plant Cell 15 (6):1281-1295


Yao X, Feng H, Yu Y, Dong A, Shen WH (2013) SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growthand development. PLoS One 8 (2):e56537. doi:10.1371/journal.pone.0056537


Yu Y, Dong A, Shen WH (2004) Molecular characterization of the tobacco SET domain protein NtSET1 unravels its role in histonemethylation, chromatin binding, and segregation. Plant J 40 (5):699-711. doi:10.1111/j.1365-313X.2004.02240.x


Yun JY, Tamada Y, Kang YE, Amasino RM (2012) Arabidopsis trithorax-related3/SET domain GROUP2 is required for the winter-annual habit of Arabidopsis thaliana. Plant Cell Physiol 53 (5):834-846. doi:10.1093/pcp/pcs021


Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation ofhistone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10 (6):R62. doi:10.1186/gb-2009-10-6-r62



http://www.ncbi.nlm.nih.gov/pubmed?term=Wang J%2C Niu B%2C Huang J%2C Wang H%2C Yang X%2C Dong A%2C Makaroff C%2C Ma H%2C Wang Y %282016%29 The PHD Finger Protein MMD1%2FDUET Ensures the Progression of Male Meiotic Chromosome Condensation and Directly Regulates the Expression of the Condensin Gene CAP%2DD3%2E Plant Cell 28 %288%29%3A1894%2D1909%2E doi%3A10%2E1105%2Ftpc%2E16%2E00040&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang J, Niu B, Huang J, Wang H, Yang X, Dong A, Makaroff C, Ma H, Wang Y (2016) The PHD Finger Protein MMD1/DUET Ensures the Progression of Male Meiotic Chromosome Condensation and Directly Regulates the Expression of the Condensin Gene CAP-D3. Plant Cell 28 (8):1894-1909. doi:10.1105/tpc.16.00040

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wang&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yang H%2C Lu P%2C Wang Y%2C Ma H %282011%29 The transcriptome landscape of Arabidopsis male meiocytes from high%2Dthroughput sequencing%3A the complexity and evolution of the meiotic process%2E Plant J 65 %284%29%3A503%2D516%2E doi%3A10%2E1111%2Fj%2E1365%2D313X%2E2010%2E04439%2Ex&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang H, Lu P, Wang Y, Ma H (2011) The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J 65 (4):503-516. doi:10.1111/j.1365-313X.2010.04439.x

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yang&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yang H%2C Yang N%2C Wang T %282016%29 Proteomic analysis reveals the differential histone programs between male germline cells and vegetative cells in Lilium davidii%2E Plant J 85 %285%29%3A660%2D674%2E doi%3A10%2E1111%2Ftpj%2E13133&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang H, Yang N, Wang T (2016) Proteomic analysis reveals the differential histone programs between male germline cells and vegetative cells in Lilium davidii. Plant J 85 (5):660-674. doi:10.1111/tpj.13133




http://www.ncbi.nlm.nih.gov/pubmed?term=Yang X%2C Makaroff CA%2C Ma H %282003%29 The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD%2Dfinger protein that is required for male meiosis%2E Plant Cell 15 %286%29%3A1281%2D1295&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang X, Makaroff CA, Ma H (2003) The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 15 (6):1281-1295




http://www.ncbi.nlm.nih.gov/pubmed?term=Yao X%2C Feng H%2C Yu Y%2C Dong A%2C Shen WH %282013%29 SDG2%2Dmediated H3K4 methylation is required for proper Arabidopsis root growth and development%2E PLoS One 8 %282%29%3Ae56537%2E doi%3A10%2E1371%2Fjournal%2Epone%2E0056537&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yao X, Feng H, Yu Y, Dong A, Shen WH (2013) SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development. PLoS One 8 (2):e56537. doi:10.1371/journal.pone.0056537

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yao&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yao&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yu Y%2C Dong A%2C Shen WH %282004%29 Molecular characterization of the tobacco SET domain protein NtSET1 unravels its role in histone methylation%2C chromatin binding%2C and segregation%2E Plant J 40 %285%29%3A699%2D711%2E doi%3A10%2E1111%2Fj%2E1365%2D313X%2E2004%2E02240%2Ex&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yu Y, Dong A, Shen WH (2004) Molecular characterization of the tobacco SET domain protein NtSET1 unravels its role in histone methylation, chromatin binding, and segregation. Plant J 40 (5):699-711. doi:10.1111/j.1365-313X.2004.02240.x

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yu&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yu&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yun JY%2C Tamada Y%2C Kang YE%2C Amasino RM %282012%29 Arabidopsis trithorax%2Drelated3%2FSET domain GROUP2 is required for the winter%2Dannual habit of Arabidopsis thaliana%2E Plant Cell Physiol 53 %285%29%3A834%2D846%2E doi%3A10%2E1093%2Fpcp%2Fpcs021&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yun JY, Tamada Y, Kang YE, Amasino RM (2012) Arabidopsis trithorax-related3/SET domain GROUP2 is required for the winter-annual habit of Arabidopsis thaliana. Plant Cell Physiol 53 (5):834-846. doi:10.1093/pcp/pcs021

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yun&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yun&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang X%2C Bernatavichute YV%2C Cokus S%2C Pellegrini M%2C Jacobsen SE %282009%29 Genome%2Dwide analysis of mono%2D%2C di%2D and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana%2E Genome Biol 10 %286%29%3AR62%2E doi%3A10%2E1186%2Fgb%2D2009%2D10%2D6%2Dr62&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10 (6):R62. doi:10.1186/gb-2009-10-6-r62

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h3k4me3 is crucial for chromatin condensation and mitotic …€¦ · 28/04/2017 · 62...

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