Gibberellin induces diploid pollen formation by interfering · PDF file1 Gibberellin induces...

Gibberellin induces diploid pollen formation by interfering with meiotic 1

cytokinesis 2

Bing Liu, Nico De Storme, and Danny Geelen* 3 Department of Plant Production, Faculty of Bioscience Engineering, University of Ghent, 4 9000 Ghent, Belgium 5 6 This work was supported by the FWO PostDoc grant 1293014N, by the LiMiD-Hercules 7 Foundation project AUGE/013, and by China Scholarship Council. 8 Corresponding author Danny Geelen: [email protected]. 9 B. L. and N. D. S. conceived and designed the project; B. L. performed the experiment and 10 wrote the draft manuscript; N. D. S provided technical assistance to B. L. and helped with 11 manuscript edition; D. G. supervised the project, contributed to the experimental design and 12 to the interpretation of results, edited the manuscript, and provided the funding. 13 14

Abstract 15

The plant hormone gibberellic acid (GA) controls many physiological processes including 16 cell differentiation, cell elongation, seed germination and response to abiotic stress. In this 17 study, we report that exogenous treatment of flowering Arabidopsis thaliana plants with GA 18 specifically affects the process of male meiotic cytokinesis leading to meiotic restitution and 19 the production of diploid (2n) pollen grains. Similar defects in meiotic cell division and 20 reproductive ploidy stability occur in Arabidopsis plants depleted of RGA and GAI, two 21 members of the DELLA family that function as suppressor of GA signaling. Cytological 22 analysis of the double rga-24 gai-t6 mutant revealed that defects in male meiotic cytokinesis 23 are not caused by alterations in MI or MII chromosome dynamics, but instead result from 24 aberrations in the spatial organization of the phragmoplast-like radial microtubule arrays 25 (RMAs) at the end of meiosis II. In line with a role for GA in the genetic regulation of the 26 male reproductive system we additionally show that DELLA downstream targets MYB33 and 27 MYB65 are redundantly required for functional RMA biosynthesis and male meiotic 28 cytokinesis. By analyzing the expression of pRGA::GFP-RGA in the wild type Ler 29 background, we demonstrate that the GFP-RGA protein is specifically expressed in the anther 30 cell layers surrounding the meiocytes and microspores, suggesting that appropriate GA 31 signaling in the somatic anther tissue is critical for male meiotic cell wall formation and thus 32 plays an important role in consolidating the male gametophytic ploidy consistency. 33 34

Introduction 35

Polyploidization repeatedly occurred in the history of plant evolution creating a basis for 36 genetic diversification and speciation (Adams and Wendel, 2005). Different mechanisms may 37 contribute to the formation of polyploid species (Ramsey and Schemske, 1998), yet the 38 production of unreduced gametes is considered the main cause of polyploid induction 39 (Bretagnolle and Thompson, 1995). Generally, both pre- and post-meiotic genome duplication 40

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events, as well as meiotic restitution can lead to 2n gamete formation (Bretagnolle and 41 Thompson, 1995; Ramsey and Schemske, 1998). In the tomato pmcd1 mutant, for example, 42 ectopic defects in cell wall formation during mitotic cell division in meiotic founder cells 43 lead to pre-meiotic genome duplication and the associated formation of tetraploid meiocytes 44 and diploid pollen grains (De Storme and Geelen, 2013). As the main cellular process driving 45 sexual polyploidization, meiotic restitution can be classified into three types of mechanisms: 46 omission of meiosis I or II, alteration in spindle organization and unsuccessful or incomplete 47 meiotic cytokinesis (Ramanna and Jacobsen, 2003). 48 49 Meiotic cell division and gametophytic ploidy stability are strictly controlled at the molecular 50 level and several factors operating in this process have already been identified (De Storme 51 and Mason, 2014). In Arabidopsis, DYAD/SWITCH1 regulates meiotic chromatid cohesion 52 and chromosome structure, and loss of function of this gene has been found to fully convert 53 the reductional meiotic cell division into a mitotic one, eventually yielding clonal, diploid 54 gametes in female sporogenesis (Ravi et al., 2008). The Arabidopsis OSD1/GIG1 and 55 TAM/CYCA1;2 proteins promote the transition of meiosis I into meiosis II, and loss of 56 function of each of them causes omission of the second meiotic cell division, resulting in 2n 57 gamete formation in both male and female gametogenesis (d'Erfurth et al., 2009; d'Erfurth et 58 al., 2010). Mutation in ps in potato, and loss of function of JASON or AtPS1 in Arabidopsis 59 cause an altered spindle configuration in male meiosis II, with parallel, tripolar and fused 60 spindles giving rise to restituted dyads and triads that contain 2n male gametes (Mok and 61 Peloquin, 1975; d'Erfurth et al., 2008; De Storme and Geelen, 2011). Meiotic restitution may 62 also result from defects in meiotic cytokinesis, either following MI or MII, with either a full 63 or partial elimination of meiotic cell wall formation leading to 2n or polyploid gamete 64 formation (De Storme and Geelen, 2013). In Arabidopsis, a specific MAPK signaling cascade 65 controls male meiotic cytokinesis (Takahashi et al., 2004; Takahashi et al., 2010). Loss of 66 function of either TES, MKK6 and MPK4 causes defects in male meiotic cell wall formation 67 and eventually leads to the ectopic production of diploid or polyploid male gametes 68 (Spielman et al., 1997; Kosetsu et al., 2010; Zeng et al., 2011). Besides induced by genetic 69 defects, meiotic restitution and alterations in the consistency of the gametophytic ploidy may 70 also result from environmental stresses, such as heat and cold (Pécrix et al., 2011; De Storme 71 et al., 2012; De Storme and Mason, 2014; Zhou et al., 2015). Although progress has been 72 made in understanding the cellular mechanisms and genetic factors involved in 2n gamete 73 formation, the molecular factors and signaling pathways involved remain largely unknown. 74 75 Gibberellins (GAs) are endogenous plant hormones that play an important role in many 76 aspects of plant growth and development; including seed germination, leaf expansion, 77 trichome development, pollen maturation and floral transition (Debeaujon and Koornneef, 78 2000; Daviere and Achard, 2013; Claeys et al., 2014). The Arabidopsis GA biosynthetic 79 mutant ga1-3 displays defects in stem elongation, flowering time, and leaf abaxial trichome 80 initiation (Silverstone et al., 1998). Besides mediating somatic tissue growth and development, 81 GA is also involved in the control of reproductive system growth and floral morphogenesis 82 (Fleet and Sun, 2005). GA positively regulates the development of the Arabidopsis stamen 83 and petal by promoting cell elongation, and also regulates microsporogenesis and pollen 84



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development (Cheng et al., 2004; Plackett et al., 2014). In multiple species, GA signaling 85 regulates both the development and programmed cell death of tapetal cells, which is required 86 for the growth and maturation of the developing microspores. Moreover, GA is also known to 87 operate as a stress signaling molecule upon exposure to abiotic stresses (cold, salt and osmotic 88 stresses) either triggered by alterations in GA biosynthesis or its downstream signaling 89 pathway. For example, cold stress inhibits root growth and disrupts pollen development by 90 reducing the plant’s endogenous GA levels (Achard et al., 2008; Sakata et al., 2014). However, 91 although various significances of GA in both vegetative and reproductive growth and 92 development have been identified, it is unknown whether GA plays a role in the control of 93 meiotic cell division. 94 95 The DELLA family, which consists of five members (RGA, GAI, RGL1, RGL2 and RGL3), 96 acts as the main repressor of the GA signaling pathway by negatively regulating the 97 expression of GA responsive genes (Daviere and Achard, 2013). The positive effect of GA on 98 plant growth is achieved by stimulating the degradation of DELLAs, and hence by 99 counteracting their growth-suppressive effect (Silverstone et al., 2001; Xu et al., 2014). The 100 majority of GA-dependent growth and development processes are mediated by DELLAs and 101 their promiscuous interaction with transcription factors (Fleet and Sun, 2005; Daviere and 102 Achard, 2015). The GA receptor GID1-DELLA complex constitutes an important regulatory 103 pathway in GA signaling. GA stimulates the formation of GA-GID1-DELLA complex that is 104 a target for ubiquitination and subsequent 26S proteasome (Sun, 2010, 2011). 105 106 In barley and rice, GA positively regulates the expression of a specific group of MYB 107 transcription factors, sometimes referred to as GAMYB, by relieving the repressive action of 108 DELLAs (Gubler et al., 2002; Huang et al., 2015). Arabidopsis MYB33 and MYB65 are two of 109 the GAMYB-like DELLA downstream target genes that are essential for anther development 110 (Millar and Gubler, 2005; Cheng et al., 2009) and are involved in various other development 111 processes (Jin and Martin, 1999; Gocal et al., 2001; Stracke et al., 2001). Several studies have 112 shown that MYB33 and MYB65 are negatively controlled by miRNA159 (Millar and Gubler, 113 2005; Millar and Gubler, 2005; Alonso-Peral et al., 2010; Alonso-Peral et al., 2010), whose 114 expression is suppressed by DELLAs (Achard et al., 2004), suggesting a positive role of 115 DELLA in regulating MYB33 and MYB65. 116 117 In this study, we demonstrate that exogenous GA treatment of flowering Arabidopsis plants 118 induces meiotic restitution in male sporogenesis and subsequently generates viable 2n pollen. 119 Using a combination of genetic and cytological analyses, we found that the combined loss of 120 the DELLA transcription factors RGA and GAI causes defective cytokinesis and aberrant 121 callosic cell wall formation at the male meiotic tetrad stage, yielding a subset of diploid, 122 bean-shaped microspores. In agreement with the cytokinesis defects, the formation of the 123 radial microtubule arrays (RMA) at the end of male meiosis is altered or absent between 124 adjacent nuclei. In addition, combined loss of function of the downstream DELLA targets 125 MYB33 and MYB65 causes similar defects in male meiotic cytokinesis and gametophytic 126 ploidy stability as observed in the DELLA double mutant, suggesting that MYB33 and 127 MYB65 are downstream targets of DELLA in controlling male meiotic cytokinesis. Based on 128



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our findings we propose that gametophytic ploidy consistency depends on a functional 129 GA-DELLA-MYBs regulatory module. 130 131

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Results 133

134 GA3 treatment induces diploid pollen formation in Arabidopsis 135 136 To determine the effect of the plant hormone gibberellin on male sporogenesis in Arabidopsis, 137 we sprayed wild type Colombia-0 plants with 100µM GA3 and water respectively. To assess 138 for putative alterations in male spore formation, the ploidy of Arabidopsis pollen was 139 analyzed during the 14 days following GA3 treatment (Fig. 1A). The ploidy level of resulting 140 pollen grains was monitored by assessing pollen diameter which is a proxy for the 141 gametophytic ploidy level (De Storme et al., 2013). During the first five days following GA 142 treatment, pollen grains appeared normally sized, similar as pollen isolated from non-treated 143 control plants. However, from the sixth day (2.61%) to the thirteenth day (0.13%) after GA3 144 treatment a variable number of oversized mature pollen grains was found, with the highest 145 frequency of larger pollen (4.31%) at day eight post treatment (dpt) (Fig. 1A, C and E). In 146 order to monitor whether GA-induced larger pollen resulted from enlarged microspores, spore 147 size at the early microspore stage was analyzed during the first seven days following GA3 148 treatment. Three to four days post treatment, a subpopulation of microspores at the unicellular 149 stage (4.45%) appeared larger than similar stage spores isolated from a non-treated control 150 (Fig. 1B, D and F). These findings demonstrate that GA induces the formation of larger pollen 151 grains, indicating for an increased gametophytic ploidy level, and that the GA-induced larger 152 pollen grains originate from a cellular defect occurring before pollen mitosis I (PMI). 153 154 To determine the gametophytic ploidy level of the GA3-induced enlarged microspores, the 155 chromosome number in male gametes at the unicellular microspore stage was quantified 156 using the pWOX2::CENH3-GFP reporter line (De Storme et al., 2016). Under control 157 conditions, unicellular microspores isolated from diploid Arabidopsis plants (2x = 10) 158 harboring the pWOX2::CENH3-GFP construct consistently show five distinct GFP foci, 159 reflecting the haploid chromosome number in their gametophytic nucleus (Fig. 1G and H). In 160 contrast, the enlarged microspores in GA3-treated plants revealed an increased number of GFP 161 dots; specifically showing 10 distinct foci organized in two spatially separated but syncytial 162 clusters of five GFP dots (Fig. 1I and J). The occurrence of 10 CENH3-GFP dots provides 163 evidence for a doubled chromosome number, indicating that the enlarged pollen grains are 164 diploid. The specific localization pattern of the centromeric CENH3-GFP foci in GA3-induced 165 enlarged spores suggests for the presence of two syncytial haploid nuclei, either indicating 166 that diploid microspores either result from a nuclear duplication event (endomitosis) during 167 early microgametogenesis or alternatively from of meiotic non-reduction through defects in 168 meiotic cell wall formation. 169 170 Constitutive GA signalling in the Arabidopsis DELLA rga-24 gai-t6 mutant leads 171 to diploid pollen formation 172 173 GA3-mediated activation of the GA signaling pathway generally occurs through degradation 174 of DELLA proteins that mainly act as negative transcriptional regulators of the GA response. 175



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To determine whether GA3-induced formation of diploid pollen is mediated by DELLAs, we 176 further analyzed a series of single, double, quadruple and pentuple null DELLA mutants for 177 alterations in pollen morphology. In contrast to the single rga-24 and gai-t6 Arabidopsis 178 mutants, which only produce a very low number of larger pollen grains (Fig. 2A), the double 179



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null rga-24 gai-t6 mutant generates a significant number of larger pollen (3.38%), similar to 180 the frequency of larger pollen grains induced by exogenous GA3 treatment (Fig. 2A, B-G). 181 Similar frequencies of larger pollen grains were observed in the quadruple rga-t2 gai-t6 182 rgl1-1 rgl2-1 mutant (3.30%) and the pentuple rga-t2 gai-t6 rgl1-1 rgl2-1 rgl3-1 mutant 183



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(3.07%) (Fig. 2A, H-K; Supplement Fig. S1F), indicating that except for RGA and GAI, the 184 mutations in other DELLA genes (e.g. RGL1, RGL2 and RGL3) do not contribute to the larger 185 pollen phenotype. 186 187 To analyze the size and organization of the gametophytic nuclei in the larger pollen grains of 188 the DELLA double and quadruple mutants, nuclei were stained and visualized using DAPI 189 (4’,6-diamidino-2-phenylindole). The nuclear configuration of the enlarged pollen in both 190 types of DELLA mutants appears highly similar to that of wild type haploid pollen, displaying 191 one less-condensed vegetative nucleus and two highly-condensed sperm nuclei. However, 192 both the vegetative nucleus and the sperm nuclei in rga-24 gai-t6 and rga-t2 gai-t6 rgl1-1 193 rgl2-1 larger pollen appear significantly larger compared to their corresponding counterparts 194 in wild type haploid pollen, indicating that the enlarged pollen have a higher nuclear DNA 195 content. These findings, together with relative pollen size increase, suggest that the enlarged 196 pollen grains in both types of DELLA mutants are diploid (Fig. 2D, E, H and I) or triploid 197 (Fig. 2F, G, J and K). In addition to this ectopic induction of gametophytic instability, it was 198 also noted that all pollen in both DELLA double and quadruple mutants display a defective 199 pollen wall morphology (Fig. 2D, F, H and J), typically lacking the thick protein-rich outer 200 cell wall. A similar defect has been observed in the enlarged pollen isolated from wild type 201 Ler plants sprayed with 100 µM GA3 (Supplement Fig. S2), indicating that alterations in GA 202 signalling not only interfere with male gametophytic ploidy stability but also affect processes 203 in pollen wall formation. . 204 205 The gametophytic ploidy level of the larger pollen in the rga-24 gai-t6 double mutant was 206 accurately determined by quantifying the chromosome number in early stage microspores 207 using the pWOX2::CENH3-GFP. Contrary to the haploid unicellular microspores from 208 control plants, which consistently show five distinct centromeric GFP dots (Fig. 2L), the 209 oversized microspores in the rga-24 gai-t6 double mutant either harbor two or three nuclei 210 that each exhibits five distinct GFP foci (Fig. 2M and O) or alternatively contain one single 211 enlarged nucleus with 10 GFP dots reflecting a fusion of two haploid nuclei (Fig. 2N). These 212 observations demonstrate that the rga-24 gai-t6 double mutant generates a subset of 213 microspores containing two or more sets of haploid nuclei, that subsequently fuse to yield 214 diploid or triploid pollen grains. 215 216 To determine the viability of the diploid pollen grains induced by RGA and GAI mutation, we 217 evaluated cellular activity of mature pollen grains by fluorescein diacetate (FDA) staining 218 (Heslop-Harrison and Heslop-Harrison, 1970; Trognitz, 1991; Abdul-Baki, 1992) 219 (Supplement Fig. S3A-F). FDA staining of both mature haploid Ler pollen grains 220 (Supplement Fig. S3C and D) and enlarged rga-24 gai-t6 mutant pollen (Supplement Fig. S3E 221 and F) showed clear cytoplasmic fluorescence, indicating that both haploid, diploid and 222 polyploid pollen grains were biologically active, and thus viable. In addition, the germination 223 ability of the larger pollen grains in the rga-24 gai-t6 double mutant plants was examined in 224 vitro (Supplement Fig. S3G-J). Following soiling on pollen growth medium and incubation in 225 the dark for 24 hours, enlarged rga-24 gai-t6 pollen grains germinated and produced pollen 226 tubes (Supplement Fig. S3H and J; red dot labels larger pollen grains in J) similar as the 227



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control Ler haploid pollen (Supplement Fig. S3G and I). Altogether, these data indicate that 228 diploid pollen grains produced by rga-24 gai-t6 Arabidopsis plants are viable and may evoke 229 sexual polyploidization events. 230 231 GA3 induces the formation of diploid pollen by promoting DELLA degradation 232 233 To determine whether GA induces diploid pollen formation through degradation of DELLA, 234 we next examined the GA response of male sporogenesis in the GA-insensitive gai mutant 235 and in the DELLA rga-24 gai-t6 double mutant. In contrast to the gai-t6 loss-of-function 236 mutation, the allelic gai mutation is localized in the N-terminal DELLA domain of GAI and 237 thus acts as a gain-of-function mutation, impairing the GA response in multiple GA-mediated 238 processes (seed germination, stem elongation and onset of flowering), even under exogenous 239 GA treatment conditions (Wilson and Somerville, 1995; Willige et al., 2007). After spraying 240 both wild type Ler plants and gai mutant plants with 100 µM GA3, the frequency of enlarged 241 uninuclear stage microspore was quantified 4 dpt. Under normal growth conditions, gai plants 242 produce normal sized haploid microspores (Fig. 1B), indicating that an impaired GA response 243 ability in Arabidopsis does not affect male sporogenesis. However, in contrast to GA-treated 244 wild type Ler plants, which produce a subset of enlarged unicellular-stage microspores 245 (3.06%) (Fig. 1B), no oversized microspores were observed in gai plants after GA treatment 246 (Fig. 1B). As male sporogenesis in gai plants is not responsive to exogenous GA application, 247 these findings demonstrate that GA-induced production of 2n pollen in Arabidopsis requires a 248 functional, targetable GAI DELLA domain, and thus indicate that GA-based induction of 2n 249 pollen in Arabidopsis is mediated through GA-based degradation of the DELLA GAI protein. 250 251 In support of this, we found that exogenous GA3 treatment of the double rga-24 gai-t6 mutant 252 plants does not enhance the frequency of enlarged uninuclear microspores compared with the 253 untreated rga-24 gai-t6 plants or GA-treated wild type Ler plants (Fig. 1B), indicating that 254 exogenous GA3 treatment has no additive effect on diploid male gamete formation in the 255 double rga-24 gai-t6 mutant background. Collectively, these data demonstrate that exogenous 256 GA3 treatment induces diploid pollen formation in Arabidopsis by promoting DELLA protein 257 degradation. 258 259 Diploid pollen in rga-24 gai-t6 mutant and GA3-treated wild type Arabidopsis 260 plants result from a restitution of male meiotic cell division 261 262 In order to determine whether GA3-induced formation of diploid pollen is caused by meiotic 263 alterations, male meiocytes were examined at the tetrad stage using orcein staining (Fig. 264 3B-F). Male meiosis in wild type Arabidopsis plants typically results in balanced tetrads 265 containing four haploid sporocytes (Fig. 3B). Similarly, upon GA3 treatment, the majority of 266 tetrad stage meiocytes appear normal, showing four equally sized microspores in a meiotic 267 tetrad (Fig. 3C). However, at 36-48 hours after GA3 treatment, a subset of meiotically 268 restituted triad (Fig. 3D and E) and dyad microspores (Fig. 3F) were observed, indicating that 269 GA3 interferes with one or more processes during male meiotic cell division. Similarly, three 270 or four days post GA3 treatment (100µM), qrt1-2-/- plants (Fig. 3G-K) were also found to 271



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produce a sub-population of triad (Fig. 3H and I) and dyad microspore configurations 272 (balanced dyad, Fig. 3J and unbalanced dyad, Fig. 3K) in agreement with GA3-induced male 273 meiotic restitution. The rga-24 gai-t6 double mutant also revealed a subset of triads (4.71 %; 274



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Fig. 3N and O) and dyads (Fig. 3M; balanced dyad 0.4% and unbalanced dyad 0.13%), 275 indicating for meiotic non-reduction similar as in GA3-treated plants. 276 277 Further nuclear analysis of orcein stained tetrad stage meiocytes additionally revealed that 278 enlarged sporocytes in restituted rga-24 gai-t6 meiocytes either carry two equally sized nuclei 279 (Fig. 3N) or alternatively harbor one single enlarged nucleus (Fig. 3O), closely according with 280 diploid microspores either showing two distinct groups of five GFP foci (Fig. 2M) or 281 exhibiting one fused nucleus with 10 GFP dots (Fig. 2N), respectively. Further confirmation 282 of binuclear and higher ploidy mononuclear microspores in GA3-treated plants and untreated 283 rga-24 gai-t6 mutant was obtained by DAPI staining of tetrad-stage meiocytes and 284 unicellular-stage microspores (Fig. 3T-Y). Both the rga-24 gai-t6 mutant and GA3-treated 285 plants show syncytial co-localization of two or more nuclei in tetrad-stage male meiocytes 286 (Fig. 3U and V) and in the unicellular microspore stage (Fig. 3X and Y). 287 288 Collectively, these data suggest that diploid pollen both in GA3-treated wild type plants and in 289 the rga-24 gai-t6 Arabidopsis mutant result from a similar defect in meiotic cell division, with 290 ectopic events of meiotic non-reduction leading to the syncytial co-localization of two or 291 more haploid nuclei in one microsporocyte. 292 293 The rga-24 gai-t6 mutant displays normal male meiotic chromosome segregation 294 295 Meiotically restituted dyads and triads generally result from defective meiotic chromosome 296 segregation, omission of either meiosis I or II, or alterations in spindle orientation. To 297 determine which of these cellular processes is affected, male meiotic chromosome spreads of 298 both the rga-24 gai-t6 double mutant and wild type Ler plants were examined (Supplement 299 Fig. S4A-L). In both wild type and rga-24 gai-t6 mutant plants, four distinct sets of five 300 chromosomes (haploid nuclei), were consistently observed in all telophase II meiocytes, 301 indicating that male meiotic chromosome segregation in the rga-24 gai-t6 double mutant is 302 not affected (Supplement Fig. S4J). Following nucleation at the tetrad stage, haploid nuclei in 303 rga-24 gai-t6 male meiocytes occasionally display an irregular spatial organization with two 304 or more nuclei in close proximity to each other. Under normal conditions, tetrad-stage wild 305 type male meiocytes always exhibit two distinct perpendicularly oriented internuclear 306 organelle bands, which physically separate the resulting nuclei in four distinct cytoplasmic 307 domains and additionally determine the spatial positioning of the future cell walls 308 (Supplement Fig. S4K). In contrast, in the rga-24 gai-t6 double mutant, some tetrad stage 309 meiocytes showed a clear absence of the internuclear organelle band between two or more 310 haploid nuclei, typically resulting in the physical clustering of two or more nuclei in one 311 single cytoplasmic domain (Supplement Fig. S4L). Hence, since the rga-24 gai-t6 mutant 312 does not show any defect in chromosome segregation during male MI or MII, the cellular 313 defect causing meiotic restitution and diploid pollen formation occurs in a later stage of 314 sporogenesis; i.e. after telophase II. 315 316 Meiotic restitution in the rga-24 gai-t6 mutant and in GA3-treated Arabidopsis 317 plants results from defects in male meiotic cytokinesis 318



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319 Both the normal meiotic chromosome dynamics and the eventual co-localization of haploid 320 nuclei at the tetrad stage suggest that meiotically restituted dyads and triads in the rga-24 321 gai-t6 double mutant result from defects in male meiotic cytokinesis. In Arabidopsis male 322 meiosis, the accumulation of intermediate callosic material at the end of MII reflects proper 323 cell wall formation and cytokinesis. Aniline blue staining of GA3-treated wild type Ler plants 324 and DELLA double rga-24 gai-t6 and quadruple rga-t2 gai-t6 rgl1-1 rgl2-1 mutants revealed 325 alterations in the deposition of callosic cell walls (Fig. 4). In most cases, GA3-treated plants 326 (Fig. 4B) and DELLA mutants (Fig. 4G and L) produce normal tetrads, similar as seen in 327 wild-type Ler, typically showing the presence of a distinct ‘cross’-shaped callosic cell wall 328 that separates all four haploid spores (Fig. 4A). However, in GA3-treated plants, a subset of 329 tetrad stage meiocytes was found to produce partial or incomplete callosic cell walls at the 330 end of MII, leading to the formation of balanced and unbalanced dyads and triads (Fig. 4C-E). 331 In this pool of altered meiotic products, a great variation in defect severity was observed, with 332 some cells not forming any callosic wall whereas others produce cell wall stubs or cell plates 333 with small gaps (Fig. 4F). Callose staining revealed similar defects in male meiotic cell wall 334 formation in the DELLA double and quadruple mutants (Fig. 4H-K and M-P). 335 336 Combined DAPI and aniline blue staining on tetrad stage male meiocytes additionally 337 revealed that aberrations in rga-24 gai-t6 MII cell wall positioning lead to the co-localization 338 and occasional clustering of two or more nuclei in one single microsporocyte (Fig. 4R and S). 339 Moreover, in a few rare events, tetrad stage rga-24 gai-t6 meiocytes were found to form 340 ectopic callosic cell walls (Fig. 4T), suggesting that one or more processes determining the 341 spatial positioning of cytokinesis and the associated deposition of cell wall components is 342 affected. Collectively, these data demonstrate that meiotic restitution in both GA3-treated 343 plants and DELLA mutants is caused by defects in male meiotic cytokinesis. 344 345 As both the DELLA RGA and GAI genes are actively transcribed ubiquitously (Silverstone et 346 al., 1998), the question rises whether cell wall formation in other tissues is also affected. To 347 monitor for putative defects in somatic cell wall formation, epidermal cells and associated cell 348 wall patterning of mature rga-24 gai-t6 petals was assessed using bright field microscopy. 349 Somatic nuclei were concomitantly visualized using DAPI staining. A thorough scanning 350 revealed that rga-24 gai-t6 petals exhibit normal epidermal cell wall morphology 351 (Supplement Fig. S5E-G) and consistently show nuclei of equal size (Supplement Fig. S5H), 352 similar as in wild type Ler plants (Supplement Fig. S5A-D), indicating that somatic cell wall 353 formation is not affected. Furthermore, propidium iodide staining of root tips did not reveal 354 altered or incomplete cell walls in both wild type Ler and rga-24 gai-t6 mutant plants 355 (Supplement Fig. S5I and J). Hence, both the observations in root and petal tissues indicate 356 that rga-24 gai-t6 somatic tissues do not show any defect in cell wall formation, suggesting 357 that the DELLA proteins RGA and GAI specifically mediate cytokinesis in male meiotic cell 358 division. 359 360 Cell wall defects in rga-24 gai-t6 male meiotic tetrads are caused by structural 361 alterations in the radial microtubule array (RMA) 362



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363 The positioning of the cell wall and associated deposition of cell wall material, such as 364 intermediate callose, in somatic plant cells is guided by the phragmoplast (De Storme and 365 Geelen, 2013). In male meiosis, cytokinesis also depends on microtubular phragmoplast-like 366



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structures, however, due to their specific spatial intercellular organization, i.e. formed at the 367 intersection of microtubules (MT) emanating from syncytial telophase II nuclei, they are 368 referred to as radial microtubule arrays (RMAs) (Peirson et al., 1997; Brown and Lemmon, 369 2001). Since RMAs are crucial for the formation and positioning of the meiotic cell wall 370



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(Otegui and Staehelin, 2003), we next performed immunocytological analysis of the MT 371 subunit tubulin-α in male meiocytes of the rga-24 gai-t6 double mutant (Fig. 5). In wild type 372 Ler plants, TII male meiocytes show a microtubular structure that consists of six RMAs that 373 are organized between the four haploid nuclei (Fig. 5A). Although most rga-24 gai-t6 male 374 meiocytes show a similar TII cytoskeletal configuration, with distinct RMAs in between each 375 of the four haploid nuclei, a subset of TII male meiocytes in the rga-24 gai-t6 double mutant 376 were found to exhibit clear alterations in the biogenesis and organization of the RMAs (Fig. 377 5B-H). In some instances, adjacent nuclei in a single TII meiocyte were found to completely 378 lack the presence of internuclear microtubules, hence causing a physical clustering of haploid 379 nuclei in a triad figure (Fig. 5B-D). Moreover, besides TII meiocytes that show partial or 380 complete loss of RMA formation, some of the rga-24 gai-t6 tetrads with regularly separated 381 nuclei display a reduced level of internuclear MT labeling, indicating for minor aberrations in 382 RMA biogenesis or MT stability (Fig. 5E and F). In these slightly altered TII meiocytes, a 383 subset of MTs of the RMA appears bent and exhibits a randomly organized pattern (Fig. 5G 384 and H). Moreover, fluorescent dots in some cells suggest that microtubules did not elongate 385 properly or were depolymerized (Fig. 5H: see arrow), indicating for defects in RMA 386 microtubule dynamics. 387 388 Overall, the RMA defects observed in rga-24 gai-t6 TII meiocytes are consistent with the 389 aberrations in male meiotic cell wall formation, and form the structural basis for events of 390 male meiotic restitution and the associated production of higher ploidy male gametes. 391 392 DELLA downstream factors MYB33 and MYB65 are redundantly required for 393 male meiotic cytokinesis in Arabidopsis 394 395 MYB33 and MYB65 are downstream factors of DELLA in regulating GA responsive 396 processes (Gubler et al., 2002; Kaneko et al., 2003), and are well known in regulating anther 397 development (Millar and Gubler, 2005). To investigate whether these two MYB factors 398 participate in DELLA-mediated male meiotic cytokinesis in Arabidopsis, we monitored both 399 sporogenesis and gametogenesis in the single and double myb33 myb65 mutant plants. Both 400 single myb33 and myb65 mutant plants produce normal tetrads, haploid microspores and 401 haploid pollen grains, similar as in wild type Col-0 plants (Fig. 6A-C, D-F and G-I). In 402 contrast, double myb33 myb65 mutant plants were found to produce a subset of meiotically 403 restituted triads, together with the associated formation of enlarged spores and mature pollen 404 grains (Fig. 6J-L). Oversized microspores at the unicellular stage (Fig. 6K) and larger pollen 405 grains (Fig. 6L) occurred at a frequency of 4.35% and 4.64%, respectively. Similar to 406 GA-treated wild type plants and double rga-24 gai-t6 mutant plants, mature pollen from the 407 double myb33 myb65 mutant also show aberrant pollen wall morphology with lack of the 408 thick protein-rich outer cell wall (Fig. 6L). These data indicate that MYB33 and MYB65 409 operate redundantly in regulating male sporogenesis in Arabidopsis, with a loss of function of 410 both genes resulting in male meiotic restitution and the associated formation of larger, higher 411 ploidy male gametes. 412 413



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Aniline blue staining revealed that single myb33 and myb65 mutants produce tetrad stage 414 male meiocytes with regular callosic cell walls (Fig. 7B and C) whereas male meiotic 415 products in the myb33 myb65 double mutant display defects in cytokinesis with formation of 416 incomplete or misshapen callosic cell walls (Fig. 7F-I). Combined aniline blue and DAPI 417



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staining further revealed a co-localization of nuclei in the enlarged spore that results from lack 418 of cell wall formation (Fig. 7J-N). Tubulin-ɑ immunolocalization of myb33 myb65 TII male 419 meiocytes revealed a complete loss of RMA formation between co-localized nuclei (Fig. 7S 420 and T) and additionally displayed fluorescent dots in some male meiocytes, suggesting for 421



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defects in microtubule polymerization or stability (Fig. 7U). MI and MII spindle organization 422 in myb33 myb65 male meiotic cells appeared normal (Fig. 7V and W), similar to those in wild 423 type Col-0 cells (Fig. 7Q and R), indicating that other microtubular structures in earlier stages 424 of male meiosis are not affected, allowing normal chromosome segregation. Collectively, 425 these findings indicate that the RMA biosynthesis and/or polymerization stability are affected 426 in the double myb33 myb65 mutant, leading to defects in male meiotic cell wall formation. 427 428 GA-induced defects in male meiotic cytokinesis correlate with DELLA signaling 429 in the somatic anther tissue 430 431 In order to assess the specific expression pattern of DELLAs during male sporogenesis, we 432 analyzed expression of RGA in the Arabidopsis anther by using a pRGA::GFP-RGA marker 433 in the Ler background. To stabilize the GFP-RGA signals in the developing flowers, we 434 sprayed flowering pRGA::GFP-RGA plants with 1mM Paclobutrazol and monitored 435 GFP-RGA expression/localization six hours post treatment using both confocal laser scanning 436 (Fig. 8) and epi-fluorescence microscopy (Supplement Fig. S6). No GFP signal was detected 437 in the anthers isolated from wild type Ler control plants (Fig. 8A-D; Supplement Fig. S6A-C). 438 Contrary, in the plants harboring the pRGA::GFP-RGA construct, GFP-RGA expression was 439 clearly visible in the anther, showing a distinct dotted pattern that is strictly confined to the 440 somatic tissue surrounding the male meiocytes and/or microspores during anther development 441 (Fig. 8E and Supplement Fig. S6D, pre-cytokinesis stage; Fig. 8F and Supplement Fig. S6E, 442 tetrad stage; Fig. 8G and H and Supplement Fig. S6F, microspore stage), indicating that RGA 443 is not expressed in the male reproductive tract, i.e. in the meiocytes and developing 444 microspores, but instead appears specifically expressed in the somatic cell layer including the 445 tapetum that surrounds the meiotic and gametophytic cells. 446 447 To examine whether exogenous GA treatment reduces RGA expression in the tapetal cell layer 448 during male sporogenesis, we next sprayed flowering pRGA::GFP-RGA plants with 100 µM 449 GA3 (24h post 1mM PAC treatment, 0.06% Tween-20), and subsequently monitored the 450 RGA-GFP signal 2 hours post GA treatment. In the absence of exogenous GA treatment, a 451 distinct pattern of RGA-GFP fluorescent signals was observed in the tapetal cell layer that 452 surrounds the male meiocytes and young microspores during progressive anther development 453 (Supplement Fig. S7A-C). However, two hours post GA treatment, a significant decrease in 454 RGA-GFP signal intensity in developing anthers was observed (Supplement Fig. S7D-F), 455 indicating that exogenous GA treatment suppresses the expression of RGA in the tapetal cell 456 layer during male meiosis and early gametogenesis. 457

458

459



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Discussion 460

461



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GA-DELLA-MYB signaling module regulates male meiotic cytokinesis in Arabidopsis 462 463 In this study, we report that exogenous GA3 treatment induces 2n pollen formation in 464 Arabidopsis by causing defects in male meiotic cytokinesis. Using genetic studies we 465 additionally demonstrate that combined loss-of-function of two downstream GA factors, i.e. 466 the DELLA proteins RGA and GAI, causes a phenotype highly reminiscent to external GA 467 treatment, suggesting that the transcriptional regulators RGA and GAI control the expression 468 of proteins that either promote or interfere with regular meiotic cytokinesis. Altogether, our 469 observations indicate that ectopic GA induces male meiotic restitution and 2n gamete 470 formation in Arabidopsis by promoting the degradation of the DELLA RGA and GAI proteins. 471 Cytological studies additionally revealed that combined loss of MYB33 and MYB65, i.e. two 472 downstream DELLA targets, leads to similar male meiotic defects and associated formation of 473 enlarged male gametes, suggesting for a role of the GA-DELLA-MYB33/MYB65 regulatory 474 pathway in controlling male meiotic cytokinesis in Arabidopsis. Moreover, as the double 475 myb33 myb65 mutant displays similar RMA defects as the DELLA rga-24 gai-t6 mutant, we 476 postulate that specific, yet unknown DELLA-MYB downstream factors directly control RMA 477 biogenesis and associated microtubule dynamics in tetrad-stage male meiocytes. However, the 478 identity of these downstream regulators and their specific mode of action in controlling male 479 meiotic RMA formation remains largely elusive. Strikingly, in both GA3-treated wild type 480 plants as well as all DELLA mutants analyzed, cytokinesis defects only occurred in a minority 481 of male meiocytes (around 4%) indicating that male meiotic RMA formation and cytokinesis 482 is largely resilient to GA deregulation. Nevertheless, maintaining ploidy consistency is critical 483 to regular sexual reproduction, with even small deviations in gametophytic ploidy level (e.g. 484 diploid and aneuploid gametes) being highly relevant when considered in an ecophysiological 485 perspective or on a larger evolutionary time scale. 486 487 A role for GA in integrating environmental stress and reproductive genome instability? 488 489 During growth and development plants suffer from various stresses, and the reproductive 490 system is particularly sensitive to adverse environmental conditions (De Storme and Geelen, 491 2014). Previously, we reported that a short period of severe cold (1–40 h at 4–5°C) induces 492 male meiotic restitution and 2n gamete formation by causing defects in male meiotic 493 cytokinesis. More specifically, low temperatures were found to specifically affect the RMA 494 cytoskeletal network at the telophase II stage, consequently impairing male meiotic cell plate 495 formation and cell wall deposition. In contrast, other microtubular structures in the 496 developing meiocytes, such as MI and MII spindles and the cortical MT array, were not 497 affected by low temperature stress, as reflected by the regular chromosome segregation 498 dynamics in MI and MII (De Storme et al., 2012). Based on these findings it is suggested that 499 cold-induced formation of 2n pollen is governed by specific regulators and signaling 500 pathways that specifically interfere with RMA biogenesis and/or MT dynamics during male 501 meiotic cytokinesis. 502 503 Here, in this study, we demonstrate that perturbation of endogenous GA levels mimics the 504 cold-induced defects in Arabidopsis male sporogenesis, causing highly similar defects in male 505



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meiotic RMA biogenesis and cell wall formation. Based on this similarity, we hypothesize 506 that GA may putatively play an important regulatory role in (cold) stress-induced restitution 507 of male meiosis and associated production of 2n pollen. Previous studies have demonstrated 508 that GA signaling plays a prominent role in the plants’ response to cold stress through 509 transient activation of CBF1/DREB1b; i.e. a transcriptional regulator controlling downstream 510 cold-responsive genes (Colebrook et al., 2014). However, the putative role for GA in 511 mediating cold-induced 2n gamete formation is probably indirect since cold has been found to 512 reduce endogenous GA levels, which is incongruent with the observation that increased GA 513 levels induce events of male meiotic restitution. For example, in Arabidopsis seedlings, cold 514 reduces endogenous bioactive GA levels by repressing expression of the GA-biosynthetic 515 GA20 oxidase and by stimulating the expression of the GA-catabolizing GA2-oxidase, 516 thereby enabling cellular accumulation of DELLAs and associated reduction of tissue growth 517 (Achard et al., 2008). Similarly, in rice, endogenous GA levels in developing anthers were 518 found to decrease upon exposure to low temperatures (Sakata et al., 2014), suggesting that 519 cold generally reduces endogenous GA levels, instead of accumulating it. 520 521 Whether low temperature-induced disorders in male meiotic RMA structure are mediated by 522 increased GA levels, and whether this occurs in a direct or indirect manner, remains to be 523 determined. In plants, microtubules are notoriously sensitive to cold shock, with each species 524 having a specific critical temperature underneath which MTs become highly unstable and 525 disassemble. However, despite numerous reports of cold-induced effects on MT stability, it is 526 yet unknown how this is mechanistically controlled and whether and how this is regulated at 527 the molecular level. A recent study by Locascio et al. (2013) provides preliminary evidence 528 for mechanistic link of GA signaling and microtubule organization. These authors reported 529 that cortical MT reorganization in elongating hypocotyls strongly depends on the availability 530 of the prefoldin complex in the cytosol, and that this availability is regulated by the 531 nuclear-localized DELLA proteins RGA and GAI which bind and inactivate prefoldin 532 (Locascio et al., 2013). However, despite this mechanistic insight into the regulatory role of 533 DELLAs in cortical MT stability, it is yet unknown whether male meiotic RMA formation is 534 controlled by a similar regulatory mechanism, and whether cold stress may interfere with this 535 to cause defects in male meiotic cell wall formation. In both GA treated plants and the double 536 rga-24 gai-t6 mutant, we have not observed aberrant organization of cortical microtubules in 537 somatic cells or defects in cell division that could be caused by faulty mitotic cytoskeletal 538 configurations. Hence, the different response of MT structures in somatic and male meiotic 539 cells suggests there may exist different mechanisms by which GA mediates microtubular 540 dynamics in somatic and reproductive tissues, putatively reflecting the differences in the 541 structural organization and molecular regulation of the MT structures in male meiosis (RMAs) 542 and in somatic cell division (phragmoplast and cortical MT arrays) (De Storme and Geelen, 543 2013). 544 545 Different roles of GA in microsporogenesis and gametogenesis 546 547 Several studies demonstrated that GA is required for floral development by repressing the 548 activity of DELLAs (Cheng et al., 2004; Tyler et al., 2004). In the GA-deficient ga1-3 mutant, 549



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male meiocytes display normal MI and MII chromosome segregation and cell wall formation 550 (Cheng et al., 2004), indicating that GA is not required for the meiotic cell division program. 551 This is confirmed in our study by monitoring the sporogenesis of GA-insensitive gai mutant. 552 On the other hand, ga1-3 plants show clear defects in microspore development and pollen 553 maturation because of impaired tapetum development (Cheng et al., 2004; Aya et al., 2009; 554 Mutasa-Gottgens and Hedden, 2009), indicating that GA is essential for microspore 555 development and pollen maturation through its promotive role in tapetum development. 556 Several studies have provided accumulating evidence that GA plays an important role in the 557 developmental regulation of the tapetal cell layer; a nourishing tissue that promotes 558 microspore development and the outer cell wall formation. In rice, for example, impaired GA 559 signaling causes alterations in the programmed cell death (PCD) of tapetal cells (Aya et al., 560 2009), a process which is vital for microspore development through the supplementation of 561 nutrients, hence causing major gametophytic defects such as spore abortion and male sterility. 562 A conserved family of transcription factors, called GAMYBs, which are controlled by the GA 563 signaling pathway have been linked with tapetum functioning and pollen outer cell wall 564 formation (Aya et al., 2011). The GAMYB members MYB33 and MYB65 are redundantly 565 required for the development and persistence of the tapetum cell layer during male 566 reproductive development (Millar and Gubler, 2005; Plackett et al., 2011). In this report, we 567 demonstrate that the combined loss of MYB33 and MYB65 in Arabidopsis not only affects 568 male gametogenesis, but also causes defects in male meiotic cell division, similar as in the 569 DELLA rga-24 gai-t6 double mutant, indicating that the GA-DELLA-MYB pathway plays an 570 important role in the developmental control of both male sporogenesis and gametogenesis. 571 572 The regulatory role of GA signaling (e.g. DELLAs-MYBs) in male meiotic cytokinesis, as 573 shown in this study, together with fact that GA plays an essential role in tapetum and 574 microspore development, corroborates with a previous report by Chhun et al. (2007), who 575 reported that GA biosynthesis genes are expressed at a relatively low level in early stages of 576 anther development (i.e. before meiotic cytokinesis) compared with that of GA-signaling 577 genes, and that the situation reversely alters at later stages in anther development (Chhun et 578 al., 2007). Although the role of GA in regulating male gametophyte development and 579 maintaining plant male fertility has been widely investigated, our data further clarify that a 580 restriction of GA signaling and associated maintenance of DELLA activity in Arabidopsis is 581 critical for successful male meiotic cell division and gametophytic ploidy stability. 582 583 Male meiotic cytokinesis - regulated by GA signaling in the surrounding somatic tissue? 584 585 The GAMYB transcription factor family is conserved in land plants and seems to regulate a 586 range of reproductive processes (Aya et al., 2011). In agreement with GA being involved in 587 the control of tapetum and microspore development, several members of the GAMYB 588 transcription factor family (MYB33 and MYB65 in Arabidopsis, HvGAMYB in barley, and 589 OSGAMYB in rice) have been shown to be expressed in young anthers prior to flower 590 anthesis (Kaneko et al., 2003; Murray et al., 2003; Millar and Gubler, 2005). Although 591 MYB33 transcripts were reported to occur in a wide range of tissues, translational fusions 592 showed that expression of MYB33 is mainly confined to the somatic cell layers of young 593



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anthers, likely due to MIR159-controlled restriction of mRNA translation. Lower expression 594 levels were detected in developing microspores (Millar and Gubler, 2005). In this study, RGA 595 expression analysis using a GFP translational fusion indicated that basal RGA levels are very 596 low in young flower buds. Upon treatment with paclobutrazol, however, GFP expression 597 strongly increases in most anther tissues including the four outer somatic cell layers, except 598 for meiocytes and microspores. This thus demonstrate that there is certain level of 599 endogenous GA biosynthesis present in young anther tissues, that restricts the expression of 600 the DELLA RGA protein to a certain limit, however, up till a level that still allows full 601 completion of male meiotic cell wall formation. 602 603 Based on these findings, we conclude that the DELLA-GAMYB module is predominantly 604 expressed in the somatic tissue surrounding the developing meiocytes, playing a putative 605 important role in the appropriate functioning of the tapetum, possibly in cooperation with the 606 other anther outer cell layers. Since expression of DELLAs and GAMYBs in meiocytes and 607 developing microspores is generally low, the observed defects in male meiotic cytokinesis and 608 cell wall formation in corresponding mutants and GA treated plants may indirectly result from 609 tapetal dysfunctioning rather than from a cell-autonomous male meiotic deregulation of the 610 DELLA-GAMYB module. Our data therefore provide preliminary evidence for molecular 611 communication between the somatic anther cells and enclosed meiocytes/microspores to 612 guide and to generate not only pollen outer cell wall maturation but also MT cytoskeletal 613 dynamics and cell wall formation during the final stage of meiosis. 614

615

MATERIALS AND METHODS 616

617

Plant Materials and Growth Conditions 618 619 Arabidopsis (Arabidopsis thaliana) Columbia-0 and Landsberg erecta accessions were 620 obtained from the Nottingham Arabidopsis Stock Centre. For GA3 treatment analysis, the 621 qrt1-2-/- mutant (Preuss et al., 1994; Francis et al., 2006) was ordered from Nottingham 622 Arabidopsis Stock Centre; The gai mutant was kindly provided by Patrick Achard. For the in 623 vivo gametophytic ploidy determination, Arabidopsis plants containing 624 pWOX2::CENH3-GFP (De Storme and Geelen, 2011) were used. The DELLA double mutant 625 rga-24 gai-t6 and the quadruple mutant rga-t2 gai-t6 rgl1-1 rgl2-1 were previously described 626 (Achard et al., 2006) and were kindly provided by Patrick Achard and Nicholas Harberd. The 627 rga-24 gai-t6 double mutant plants harboring pWOX2::CENH3-GFP were isolated in F2 628 population from the rga-24 gai-t6 double mutant intercrossing with pWOX2::CENH3-GFP 629 transgenic line, according to the phenotype of pWOX2::CENH3-GFP transgenic line and 630 genotyping of rga-24 and gai-t6 mutation. The rga-24 and gai-t6 single mutants were 631 acquired from F2 population from the rga-24 gai-t6 double mutant intercrossing with 632 pWOX2::CENH3-GFP transgenic line by genotyping rga-24 and gai-t6 mutation respectively. 633 The pentuple rga-t2 gai-t6 rgl1-1 rgl2-1 rgl3-1 mutant was kindly shared by M. Höfte. The 634



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single and double myb33 myb65 mutants were kindly provided by Anthony Millar. The 635 pRGA::GFP-RGA transgenic plants were obtained from Nicholas Harberd. Primers used for 636 genotyping are listed in Supplemental tables S1. 637 638 Seeds were germinated on K1 medium for 6-8 days and then seedlings were transferred to soil 639 and cultivated in growth chambers at 12 h day/12 h night, 20°C, and less than 70% humidity. 640 Upon flowering, the photoperiod was changed to a 16-h-day/8-h-night regime. For GA3 641 treatment, flowering plants were sprayed by water (+0.02% Tween) and 100 µM GA3 (+0.02% 642 Tween) respectively. 643 644 GA3 and PAC Treatment Analysis 645 646 To determine the effect of GA3 treatment on male meiotic products, tetrads and microspores 647 were observed at 36-48 h and 72-96 h later after GA3 and water spraying respectively. To 648 monitor the effect of GA3 treatment on larger pollen formation, mature pollen grains were 649 analyzed in the 14 days following GA3 treatment. For pRGA::GFP-RGA expression analysis, 650 to stabilize the GFP-RGA signals in Arabidopsis flowers, flowering pRGA::GFP-RGA plants 651 were sprayed with PAC (1mM, 0.06% Tween-20) and water respectively. Anthers at different 652 developmental stages were isolated to glass slides with a drop of diluted water and analyzed 653 by microscopy. 654 655 Pollen viability examination 656 657 For performing FDA staining, mature pollen grains from newly opened flowers are released 658 in a drop of FDA buffer (2 mg/mL in acetone) on a glass slide, and the fluorescence is 659 observed after10 min staining. For pollen germination, mature pollen grains from newly 660 opened flowers are soiled on pollen growth medium (5 mM CaCl2, 1 mM MgSO4, 5mM KCl, 661 0.01 mM H3BO3, 18% sucrose, 1.5% agarose, pH at 7.5 modified by 0.1 M NaOH), and the 662 pollen tube is observed after incubation in humid chamber under dark for 24 h. 663 664 Cytology 665 666 Pollen DAPI staining, callosic cell wall staining and analysis of the male meiotic products 667 (tetrad-stage analysis by orcein and DAPI staining) was performed as described previously 668 (De Storme et al., 2012). Buds producing significant numbers of mature meiotic products 669 were used for quantification and monitoring assays. DAPI and aniline blue-combined staining 670 of male meiotic products was performed by releasing spores in a drop of DAPI solution (1 671 mg/ mL; Sigma) and aniline blue solution (0.1% [m/v] in 0.033% K3PO4 [m/v]) mixture. 672 Visualization of pWOX2::CENH3-GFP constructs was performed by releasing spores in a 673 0.05 M NaPO4 (pH 7.0) and 0.5% Triton X-100 (v/v) solution. Male meiotic spreads were 674 performed as described previously (De Storme and Geelen, 2011). Visual assessment of petal 675 leaves was performed according to the method of Carland et al. (Carland et al., 2002). For 676 observation of the cell wall in root tip, roots were cut from 5 days old seedlings and mounted 677 on a glass slide with 10 μg/ml PI solution for 5 min, followed by three times washing using 678



25

diluted water before observation. 679 680 Tubulin Immunolocalization 681 682 ɑ-tubulin immunolocalization analysis was performed as described previously (De Storme et 683 al., 2012). 684 685 Microscopy 686 687 Both bright-field and fluorescence microscopy were performed using an Olympus IX81 688 inverted fluorescence microscope equipped with an X-Cite Series 120Q UV lamp and an 689 Olympus XM10 camera. Fluorescence from pRGA::GFP-RGA transgenic line and propidium 690 iodide staining was captured using Nikon A1r confocal laser scanning microscope equipped 691 with Axiovision software (LiMiD). Bifluorescent images and Z-stacks were processed using 692 ImageJ. Brightness and contrast settings were adjusted using Photoshop CS6. 693 694 Figure 1. GA3 treatment induces the formation of diploid pollen in Arabidopsis. A, Histogram showing 695 the frequency of larger pollen produced in Arabidopsis Col-0 plants one to fourteen days after 696 exogenous GA3 treatment (100µM); see exact numbers in the histogram. B, Histogram showing the 697 frequency of enlarged unicellular-stage microspores yielded 3-4 days after GA3 treatment (100µM). C 698 and D, Bright field image of haploid mature pollen grain (C) and unicellular-stage microspore (D) 699 produced in untreated Arabidopsis plants. E and F, Enlarged mature pollen grain (E) and 700 unicellular-stage microspore (F) from Arabidopsis plants treated by 100µM GA3. G and H, Haploid 701 microspore displaying five centromeric GFP dots in control, untreated plants harboring the 702 pWOX2::CENH3-GFP reporter construct. I and J, Diploid microspores in pWOX2::CENH3-GFP 703 transgenic plants treated by 100 µM GA3, exhibiting two syncytial groups of five CENH3-GFP dots. 704 Scale bars = 10 µm. 705 706 Figure 2. The DELLA double rga-24 gai-t6, quadruple rga-t2 gai-t6 rgl1-1 rgl2-1 and pentuple rga-t2 707 gai-t6 rgl1-1 rgl2-1 rgl3-1 mutants produce a subset of diploid pollen. A, Histogram showing the 708 percentage of larger pollen grains produced in rga-24 and gai-t6 single and double mutants, rga-t2 709 gai-t6 rgl1-1 rgl2-1 quadruple mutant and in the rga-t2 gai-t6 rgl1-1 rgl2-1 rgl3-1 pentuple mutant. 710 B-K, DAPI staining of mature pollen grains isolated from wild type Ler plants(B and C), the rga-24 711 gai-t6 double mutant (D-G) and the rga-t2 gai-t6 rgl1-1 rgl2-1 quadruple mutant (H-K). L-O, 712 unicellular microspores of control plants (L) and the rga-24 gai-t6 double mutant (M-O) harboring the 713 pWOX2::CENH3-GFP reporter construct. Enlarged spores in the rga-24 gai-t6 double mutant either 714 show 10 (M and N) or 15 (O) centromeric GFP foci. Enlarged GFP dots in picture N result from an 715 overlay of two single GFP foci. Scale bars = 10 µm. 716 717 Figure 3. Male meiotic restitution in GA3-treated plants and in the rga-24 gai-t6 double mutant. A, 718 Histograms showing the frequency of meiotic non-reduction events in the rga-24 gai-t6 double mutant. 719 B-F, Orcein staining of tetrad stage male meiocytes in control (B) and GA3-treated plants (C-F). G-K, 720 Orcein staining of unicellular stage microspores in control (G) and in GA3-treated qrt1-2-/- plants (H-K). 721 L-O, Orcein staining of tetrad stage meiocytes in wild-type Ler plants (L) and in the rga-24 gai-t6 722



26

double mutant (M-O). P-S, Orcein staining of unicellular stage microspores in control (P), GA3-treated 723 plants (Q) and in the rga-24 gai-t6 double mutant (R and S). T-Y, DAPI staining of tetrad stage male 724 meiocytes and unicellular microspores in control (T and W), GA3-treated plants (U and X) and in the 725 rga-24 gai-t6 double mutant (V and Y). Scale bars = 10 µm. 726 727 Figure 4. Aniline blue staining reveals male meiotic cytokinesis defects in GA3-treated plants and 728 DELLA double and quadruple Arabidopsis mutants. A-P, Aniline blue staining of callosic cell walls in 729 tetrad stage meiocytes of wild type Ler plants (A), wild type Ler plants sprayed with 100µM GA3 730 (B-F), the rga-24 gai-t6 double mutant (G-K) and the rga-t2 gai-t6 rgl1-1 rgl2-1 quadruple mutant 731 (L-P). Q-T, Combined aniline blue and DAPI staining of tetrad stage male meiocytes in wild type Ler 732 (Q) and rga-24 gai-t6 plants (R-T). Scale bars = 10 µm. 733 734 Figure 5. Tubulin-ɑ immunolocalization in TII male meiocytes of wild-type Ler and rga-24 gai-t6 735 double mutant plants. A-H, Structure of the RMAs in TII male meiocytes of wild-type Ler plants (A) 736 and the rga-24 gai-t6 double mutant (B-H). Green: α-tubulin, cyan: DAPI. Scale bars = 10 µm. 737 738 Figure 6. Sporogenesis and gametogenesis in the single and double myb33 myb65 mutant. A-C, Tetrad 739 (A), haploid unicellular stage microspore (B) and haploid pollen grain (C) in wild type Col-0 plant. D-F, 740 Tetrad (D), haploid unicellular stage microspore (E) and haploid pollen grain (F) in single myb33 741 mutant plant. G-I, Tetrad (G), haploid unicellular stage microspore (H) and haploid pollen grain (I) in 742 single myb65 mutant plant. J-L, Triad (J), enlarged unicellular stage microspore (K) and enlarged 743 pollen grain (L) in double myb33 myb65 mutant plant. Scale bars = 10 µm. 744 745 Figure 7. Male meiotic cytokinesis defects in myb33 myb65 Arabidopsis plants. A-C, Aniline blue 746 staining of tetrads in wild type Col-0 (A) and single myb33 (B) and myb65 (C) mutant plants. D, 747 Combined aniline blue/DAPI staining of tetrad-stage male meiocytes in wild type Col-0 plant. E, DAPI 748 staining of haploid unicellular stage microspore in wild type Col-0 plants. F-I, Aniline blue staining of 749 defective tetrad stage male meiocytes in double myb33 myb65 mutant plants. J-N, Combined aniline 750 blue/DAPI staining of defective tetrad-stage male meiocytes in double myb33 myb65 mutant plants. O, 751 DAPI staining of an enlarged unicellular stage microspore isolated from myb33 myb65 mutant plant. 752 P-R, RMA (P) and MI and MII spindles (Q and R) in wild type Col-0 plants. S-W, Defective RMA 753 (S-U) and normal MI and MII spindles (V and W) in the double myb33 myb65 mutant. Green: 754 α-tubulin, cyan: DAPI. Scale bars = 10 µm. 755 756 Figure 8. Confocal laser scanning microscopy of pRGA::GFP-RGA during different stages of 757 Arabidopsis anther development. A-D, Anthers of wild type Ler plants at during meiosis (A), tetrad 758 stage (B) and early microspore development (C and D). E-H, Anthers of Ler plants harboring the 759 pRGA::GFP-RGA constructs during meiosis (E), tetrad stage (F) and early microspore development (G 760 and H). Scale bars = 50 µm. 761 762 763 764 Supplemental Data 765 766



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The following materials are available in the online version of this article. 767 Supplemental Figure S1. Male meiotic restitution and enlarged male gametes in rga-t2 768 gai-t6 rgl1-1 rgl2-1 rgl3-1 mutant plants. 769 Supplemental Figure S2. Mature pollen grain in GA3-treated wild type Ler plant. 770 Supplemental Figure S3. Viability determination of enlarged mature pollen grains in the 771 double rga-24 gai-t6 mutant plants. 772 Supplemental Figure S4. The Arabidopsis rga-24 gai-t6 mutant displays regular 773 chromosome dynamics during male meiosis I and II. 774 Supplemental Figure S5. Microscopy analysis of cell wall and nuclei in somatic tissues. 775 Supplemental Figure S6. Expression pattern of pRGA::GFP-RGA in Arabidopsis anther. 776 Supplemental Figure S7. Exogenous GA treatment induces decrease of pRGA::GFP-RGA 777 signals in Arabidopsis anther. 778 Supplemental Table S1. Primers for genotyping. 779 780

ACKNOWLEDGMENTS 781

We thank Patrick Achard for sharing the double rga-24 gai-t6 and quadruple rga-t2 gai-t6 782 rgl1-1 rgl2-1 mutant seeds, as well as gai mutant seeds. We thank Nicholas Harberd for 783 providing the double rga-24 gai-t6 and quadruple rga-t2 gai-t6 rgl1-1 rgl2-1 mutant seeds, as 784 well as the pRGA::GFP-RGA transgenic plants. We thank Monica Höfte for sharing the 785 DELLA pentuple rga-t2 gai-t6 rgl1-1 rgl2-1 rgl3-1 mutant. Many thanks to Anthony Millar 786 for providing the single and double myb33 myb65 mutants. We also thank G. Meesen for his 787 support in confocal microscopy. We thank FWO PostDoc grant 1293014N (personal grant 788 Nico De Storme) for supporting the research. We thank LiMiD-Hercules Foundation project 789 AUGE/013 funding for confocal microscope. We thank China Scholarship Council for 790 providing partial funding (personal grant Bing Liu) for this research. 791 792 793



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http://www.ncbi.nlm.nih.gov/pubmed?term=d%27Erfurth I%2C Jolivet S%2C Froger N%2C Catrice O%2C Novatchkova M%2C Mercier R %282009%29 Turning Meiosis into Mitosis%2E PLoS Biol 7%3A e1000124&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=d%27Erfurth I%2C Jolivet S%2C Froger N%2C Catrice O%2C Novatchkova M%2C Simon M%2C Jenczewski E%2C Mercier R %282008%29 Mutations in AtPS1 %28Arabidopsis thaliana Parallel Spindle 1%29 Lead to the Production of Diploid Pollen Grains%2E PLoS Genet 4%3A e1000274&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Daviere JM%2C Achard P %282013%29 Gibberellin signaling in plants%2E Development 140%3A 1147%2D1151&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Daviere JM%2C Achard P %282015%29 A Pivotal Role of DELLAs in Regulating Multiple Hormone Signals%2E Mol Plant&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=De Storme N%2C Copenhaver GP%2C Geelen D %282012%29 Production of diploid male gametes in Arabidopsis by cold%2Dinduced destabilization of postmeiotic radial microtubule arrays%2E Plant Physiol 160%3A 1808%2D1826&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=De Storme N%2C Mason A %282014%29 Plant speciation through chromosome instability and ploidy change%3A Cellular mechanisms%2C molecular factors and evolutionary relevance%2E Current Plant Biology 1%3A 10%2D33&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Debeaujon I%2C Koornneef M %282000%29 Gibberellin Requirement for Arabidopsis Seed Germination Is Determined Both by Testa Characteristics and Embryonic Abscisic Acid%2E Plant Physiology 122%3A 415%2D424&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Fleet CM%2C Sun TP %282005%29 A DELLAcate balance%3A the role of gibberellin in plant morphogenesis%2E Curr Opin Plant Biol 8%3A 77%2D85&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Francis KE%2C Lam SY%2C Copenhaver GP %282006%29 Separation of Arabidopsis Pollen Tetrads Is Regulated by QUARTET1%2C a Pectin Methylesterase Gene%2E Plant Physiology 142%3A 1004%2D1013&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis Pollen Tetrads Is Regulated by QUARTET1, a Pectin Methylesterase Gene. Plant Physiology 142: 1004-1013

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http://www.ncbi.nlm.nih.gov/pubmed?term=Gocal GFW%2C Sheldon CC%2C Gubler F%2C Moritz T%2C Bagnall DJ%2C MacMillan CP%2C Li SF%2C Parish RW%2C Dennis ES%2C Weigel D%2C King RW %282001%29 GAMYB%2Dlike Genes%2C Flowering%2C and Gibberellin Signaling in Arabidopsis%2E Plant Physiology 127%3A 1682%2D1693&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Gubler F%2C Chandler PM%2C White RG%2C Llewellyn DJ%2C Jacobsen JV %282002%29 Gibberellin signaling in barley aleurone cells%2E Control of SLN1 and GAMYB expression%2E Plant Physiol 129%3A 191%2D200&dopt=abstract

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Locascio A, Blázquez Miguel A, Alabadí D (2013) Dynamic Regulation of Cortical Microtubule Organization through Prefoldin-DELLA Interaction. Current Biology 23: 804-809


Millar AA, Gubler F (2005) The Arabidopsis GAMYB-Like Genes, MYB33 and MYB65, Are MicroRNA-Regulated Genes ThatRedundantly Facilitate Anther Development. The Plant Cell 17: 705-721


Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes thatredundantly facilitate anther development. Plant Cell 17: 705-721


Mok DWS, Peloquin SJ (1975) THREE MECHANISMS OF 2n POLLEN FORMATION IN DIPLOID POTATOES. Canadian Journal ofGenetics and Cytology 17: 217-225


Murray F, Kalla R, Jacobsen J, Gubler F (2003) A role for HvGAMYB in anther development. Plant J 33: 481-491Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Mutasa-Gottgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60: 1979-1989Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Otegui MS, Staehelin LA (2003) Electron tomographic analysis of post-meiotic cytokinesis during pollen development inArabidopsis thaliana. Planta 218: 501-515


Pécrix Y, Rallo G, Folzer H, Cigna M, Gudin S, Le Bris M (2011) Polyploidization mechanisms: temperature environment can inducediploid gamete formation in Rosa sp. Journal of Experimental Botany


Peirson BN, Bowling SE, Makaroff CA (1997) A defect in synapsis causes male sterility in a T-DNA-tagged Arabidopsis thalianamutant. Plant J 11: 659-669


Plackett AR, Ferguson AC, Powers SJ, Wanchoo-Kohli A, Phillips AL, Wilson ZA, Hedden P, Thomas SG (2014) DELLA activity isrequired for successful pollen development in the Columbia ecotype of Arabidopsis. New Phytol 201: 825-836


Plackett AR, Thomas SG, Wilson ZA, Hedden P (2011) Gibberellin control of stamen development: a fertile field. Trends Plant Sci16: 568-578


Preuss D, Rhee S, Davis R (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science264: 1458-1460


Ramanna MS, Jacobsen E (2003) Relevance of sexual polyploidization for crop improvement - A review. Euphytica 133: 3-8Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review ofEcology and Systematics 29: 467-501



http://www.ncbi.nlm.nih.gov/pubmed?term=Locascio A%2C Bl�zquez Miguel A%2C Alabad� D %282013%29 Dynamic Regulation of Cortical Microtubule Organization through Prefoldin%2DDELLA Interaction%2E Current Biology 23%3A 804%2D809&dopt=abstract

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Ravi M, Marimuthu MP, Siddiqi I (2008) Gamete formation without meiosis in Arabidopsis. Nature 451: 1121-1124Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Sakata T, Oda S, Tsunaga Y, Shomura H, Kawagishi-Kobayashi M, Aya K, Saeki K, Endo T, Nagano K, Kojima M, Sakakibara H,Watanabe M, Matsuoka M, Higashitani A (2014) Reduction of gibberellin by low temperature disrupts pollen development in rice.Plant Physiol 164: 2011-2019


Silverstone AL, Ciampaglio CN, Sun T-p (1998) The Arabidopsis RGA Gene Encodes a Transcriptional Regulator Repressing theGibberellin Signal Transduction Pathway. The Plant Cell 10: 155-169


Silverstone AL, Jung H-S, Dill A, Kawaide H, Kamiya Y, Sun T-p (2001) Repressing a Repressor: Gibberellin-Induced RapidReduction of the RGA Protein in Arabidopsis. The Plant Cell 13: 1555-1566


Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG (1997) TETRASPORE is required for male meiotic cytokinesis inArabidopsis thaliana. Development 124: 2645-2657


Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4: 447-456Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Sun TP (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154: 567-570Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Sun TP (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21: R338-345Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Takahashi Y, Soyano T, Kosetsu K, Sasabe M, Machida Y (2010) HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, whichphosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant CellPhysiol 51: 1766-1776


Takahashi Y, Soyano T, Sasabe M, Machida Y (2004) A MAP kinase cascade that controls plant cytokinesis. J Biochem 136: 127-132Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Trognitz BR (1991) Comparison of different pollen viability assays to evaluate pollen fertility of potato dihaploids. Euphytica 56:143-148


Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun TP (2004) Della proteins and gibberellin-regulated seed germinationand floral development in Arabidopsis. Plant Physiol 135: 1008-1019


Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EMN, Maier A, Schwechheimer C (2007) The DELLA Domain of GAINSENSITIVE Mediates the Interaction with the GA INSENSITIVE DWARF1A Gibberellin Receptor of Arabidopsis. The Plant Cell 19:1209-1220


Wilson RN, Somerville CR (1995) Phenotypic Suppression of the Gibberellin-Insensitive Mutant (gai) of Arabidopsis. PlantPhysiology 108: 495-502

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon May 12, 2018 - Published by Downloaded from

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ravi M%2C Marimuthu MP%2C Siddiqi I %282008%29 Gamete formation without meiosis in Arabidopsis%2E Nature 451%3A 1121%2D1124&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Sakata T, Oda S, Tsunaga Y, Shomura H, Kawagishi-Kobayashi M, Aya K, Saeki K, Endo T, Nagano K, Kojima M, Sakakibara H, Watanabe M, Matsuoka M, Higashitani A (2014) Reduction of gibberellin by low temperature disrupts pollen development in rice. Plant Physiol 164: 2011-2019

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http://search.crossref.org/?page=1&rows=2&q=Silverstone AL, Ciampaglio CN, Sun T-p (1998) The Arabidopsis RGA Gene Encodes a Transcriptional Regulator Repressing the Gibberellin Signal Transduction Pathway. The Plant Cell 10: 155-169

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http://search.crossref.org/?page=1&rows=2&q=Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG (1997) TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124: 2645-2657

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http://search.crossref.org/?page=1&rows=2&q=Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EMN, Maier A, Schwechheimer C (2007) The DELLA Domain of GA INSENSITIVE Mediates the Interaction with the GA INSENSITIVE DWARF1A Gibberellin Receptor of Arabidopsis. The Plant Cell 19: 1209-1220

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http://www.ncbi.nlm.nih.gov/pubmed?term=Wilson RN%2C Somerville CR %281995%29 Phenotypic Suppression of the Gibberellin%2DInsensitive Mutant %28gai%29 of Arabidopsis%2E Plant Physiology 108%3A 495%2D502&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wilson RN, Somerville CR (1995) Phenotypic Suppression of the Gibberellin-Insensitive Mutant (gai) of Arabidopsis. Plant Physiology 108: 495-502

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Xu H, Liu Q, Yao T, Fu X (2014) Shedding light on integrative GA signaling. Curr Opin Plant Biol 21C: 89-95Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zeng Q, Chen JG, Ellis BE (2011) AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis. Plant J 67: 895-906Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zhou X, Mo X, Gui M, Wu X, Jiang Y, Ma L, Shi Z, Luo Y, Tang W (2015) Cytological, molecular mechanisms and temperature stressregulating production of diploid male gametes in Dianthus caryophyllus L. Plant Physiology and Biochemistry 97: 255-263



http://www.ncbi.nlm.nih.gov/pubmed?term=Xu H%2C Liu Q%2C Yao T%2C Fu X %282014%29 Shedding light on integrative GA signaling%2E Curr Opin Plant Biol 21C%3A 89%2D95&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zeng Q%2C Chen JG%2C Ellis BE %282011%29 AtMPK4 is required for male%2Dspecific meiotic cytokinesis in Arabidopsis%2E Plant J 67%3A 895%2D906&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Zhou X, Mo X, Gui M, Wu X, Jiang Y, Ma L, Shi Z, Luo Y, Tang W (2015) Cytological, molecular mechanisms and temperature stress regulating production of diploid male gametes in Dianthus caryophyllus L. Plant Physiology and Biochemistry 97: 255-263

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

http://scholar.google.com/scholar?as_q=Cytological, molecular mechanisms and temperature stress regulating production of diploid male gametes in Dianthus caryophyllus L&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=Cytological, molecular mechanisms and temperature stress regulating production of diploid male gametes in Dianthus caryophyllus L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1


Gibberellin induces diploid pollen formation by interfering · PDF file1 Gibberellin induces...

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Transcript of Gibberellin induces diploid pollen formation by interfering · PDF file1 Gibberellin induces...