Meiosis produces haploid cells essential for sexual reproduction. In yeast, entry into meiosis activates transcription factors which trigger a transcriptional cascade that results in sequential co-expression of early, middle and late meiotic genes. However, these factors are not conserved, and the factors and regulatory mechanisms that ensure proper meiotic gene expression in multicellular eukaryotes are poorly understood. Here, we report that DUET/MMD1, a PHD finger protein essential for Arabidopsis male meiosis, functions as a transcriptional regulator in plant meiosis. We find that DUET-PHD binds H3K4me2 in vitro, and show that this interaction is critical for function during meiosis. We also show that DUET is required for proper microtubule organization during meiosis II, independently of its function in meiosis I. Remarkably, DUET protein shows stage-specific expression, confined to diplotene. We identify two genes TDM1 and JAS with critical functions in cell cycle transitions and spindle organization in male meiosis, as DUET targets, with TDM1 being a direct target. Thus, DUET is required to regulate microtubule organization and cell cycle transitions during male meiosis, and functions as a direct transcription activator of the meiotic gene TDM1. Expression profiling showed reduced expression of a subset comprising about 12% of a known set of meiosis preferred genes in the duet mutant. Our results reveal the action of DUET as a transcriptional regulator during male meiosis in plants, and suggest that transcription of meiotic genes is under stagewise control in plants as in yeast.
References
[1]
Winter E. The Sum1/Ndt80 Transcriptional Switch and Commitment to Meiosis in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 2012;76: 1–15. doi: 10.1128/MMBR.05010-11. pmid:22390969
[2]
Werven FJ van, Amon A. Regulation of entry into gametogenesis. Philos Trans R Soc B Biol Sci. 2011;366: 3521–3531. doi: 10.1098/rstb.2011.0081.
[3]
Bolcun-Filas E, Bannister LA, Barash A, Schimenti KJ, Hartford SA, Eppig JJ, et al. A-MYB (MYBL1) transcription factor is a master regulator of male meiosis. Development. 2011;138: 3319–3330. doi: 10.1242/dev.067645. pmid:21750041
[4]
Hayashi K, Yoshida K, Matsui Y. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature. 2005;438: 374–378. doi: 10.1038/nature04112. pmid:16292313
[5]
White-Cooper H. Molecular mechanisms of gene regulation during Drosophila spermatogenesis. Reproduction. 2010;139: 11–21. doi: 10.1530/REP-09-0083. pmid:19755484
[6]
Yamaguchi S, Hong K, Liu R, Shen L, Inoue A, Diep D, et al. Tet1 controls meiosis by regulating meiotic gene expression. Nature. 2012;492: 443–447. doi: 10.1038/nature11709. pmid:23151479
[7]
Zhou A, Pawlowski WP. Regulation of meiotic gene expression in plants. Front Plant Sci. 2014;5: 413. doi: 10.3389/fpls.2014.00413. pmid:25202317
[8]
Qin Y, Zhao L, Skaggs MI, Andreuzza S, Tsukamoto T, Panoli A, et al. ACTIN-RELATED PROTEIN 6 regulates female meiosis by modulating meiotic gene expression in Arabidopsis. Plant Cell. 2014; doi: 10.1105/tpc.113.120576.
[9]
Zhao L, He J, Cai H, Lin H, Li Y, Liu R, et al. Comparative expression profiling reveals gene functions in female meiosis and gametophyte development in Arabidopsis. Plant J. 2014; n/a–n/a. doi: 10.1111/tpj.12657.
[10]
Reddy TV, Kaur J, Agashe B, Sundaresan V, Siddiqi I. The DUET gene is necessary for chromosome organization and progression during male meiosis in Arabidopsis and encodes a PHD finger protein. Development. 2003;130: 5975–5987. doi: 10.1242/dev.00827. pmid:14573517
[11]
Yang X, Makaroff CA, Ma H. The Arabidopsis MALE MEIOCYTE DEATH1 Gene Encodes a PHD-Finger Protein That Is Required for Male Meiosis. Plant Cell Online. 2003;15: 1281–1295. doi: 10.1105/tpc.010447.
[12]
Storme ND, Geelen D. The Arabidopsis mutant jason produces unreduced first division restitution male gametes through a parallel/fused spindle mechanism in meiosis II. Plant Physiol. 2011;155: 1403–1415. doi: 10.1104/pp.110.170415. pmid:21257792
[13]
Cromer L, Heyman J, Touati S, Harashima H, Araou E, Girard C, et al. OSD1 promotes meiotic progression via APC/C inhibition and forms a regulatory network with TDM and CYCA1;2/TAM. PLoS Genet. 2012;8: e1002865. doi: 10.1371/journal.pgen.1002865. pmid:22844260
[14]
Musselman CA, Kutateladze TG. Handpicking epigenetic marks with PHD fingers. Nucleic Acids Res. 2011;39: 9061–9071. doi: 10.1093/nar/gkr613. pmid:21813457
[15]
Ali M, Rincón-Arano H, Zhao W, Rothbart SB, Tong Q, Parkhurst SM, et al. Molecular basis for chromatin binding and regulation of MLL5. Proc Natl Acad Sci. 2013;110: 11296–11301. doi: 10.1073/pnas.1310156110. pmid:23798402
[16]
Kim T, Buratowski S. Dimethylation of H3K4 by Set1 Recruits the Set3 Histone Deacetylase Complex to 5′ Transcribed Regions. Cell. 2009;137: 259–272. doi: 10.1016/j.cell.2009.02.045. pmid:19379692
[17]
Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature. 2006;442: 86–90. doi: 10.1038/nature04815. pmid:16728976
[18]
Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature. 2006;442: 96–99. doi: 10.1038/nature04835. pmid:16728974
[19]
Ruthenburg AJ, Allis CD, Wysocka J. Methylation of Lysine 4 on Histone H3: Intricacy of Writing and Reading a Single Epigenetic Mark. Mol Cell. 2007;25: 15–30. doi: 10.1016/j.molcel.2006.12.014. pmid:17218268
[20]
Alexander MP. Differential staining of aborted and nonaborted pollen. Stain Technol. 1969;44: 117–122. pmid:4181665 doi: 10.3109/10520296909063335
[21]
D’ Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Simon M, et al. Mutations in AtPS1 (Arabidopsis thaliana Parallel Spindle 1) lead to the production of diploid pollen grains. PLoS Genet. 2008;4: e1000274. doi: 10.1371/journal.pgen.1000274. pmid:19043546
[22]
Armstrong SJ, Caryl AP, Jones GH, Franklin FCH. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci. 2002;115: 3645–3655. doi: 10.1242/jcs.00048. pmid:12186950
[23]
Jackson N, Sanchez-Moran E, Buckling E, Armstrong SJ, Jones GH, Franklin FCH. Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO J. 2006;25: 1315–1323. doi: 10.1038/sj.emboj.7600992. pmid:16467846
[24]
D’ Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R. Turning meiosis into mitosis. PLoS Biol. 2009;7: e1000124. doi: 10.1371/journal.pbio.1000124. pmid:19513101
[25]
Iwata E, Ikeda S, Matsunaga S, Kurata M, Yoshioka Y, Criqui M-C, et al. GIGAS CELL1, a Novel Negative Regulator of the Anaphase-Promoting Complex/Cyclosome, Is Required for Proper Mitotic Progression and Cell Fate Determination in Arabidopsis. Plant Cell Online. 2011;23: 4382–4393. doi: 10.1105/tpc.111.092049.
[26]
Wang Y, Magnard J-L, McCormick S, Yang M. Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant Physiol. 2004;136: 4127–4135. doi: 10.1104/pp.104.051201. pmid:15557098
[27]
D’ Erfurth I, Cromer L, Jolivet S, Girard C, Horlow C, Sun Y, et al. The CYCLIN-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLoS Genet. 2010;6: e1000989. doi: 10.1371/journal.pgen.1000989. pmid:20585549
[28]
Glover J, Grelon M, Craig S, Chaudhury A, Dennis E. Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis. Plant J. 1998;15: 345–356. doi: 10.1046/j.1365-313X.1998.00216.x. pmid:9750346
[29]
Aarts MGM, Hodge R, Kalantidis K, Florack D, Wilson ZA, Mulligan BJ, et al. The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J. 1997;12: 615–623. doi: 10.1046/j.1365-313X.1997.00615.x. pmid:9351246
[30]
Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ. The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J. 2001;28: 27–39. doi: 10.1046/j.1365-313X.2001.01125.x. pmid:11696184
[31]
Libeau P, Durandet M, Granier F, Marquis C, Berthomé R, Renou JP, et al. Gene expression profiling of Arabidopsis meiocytes: Gene expression profiling of Arabidopsis meiocytes. Plant Biol. 2011;13: 784–793. doi: 10.1111/j.1438-8677.2010.00435.x. pmid:21815983
[32]
Qin Z, Zhang X, Zhang X, Xin W, Li J, Hu Y. The Arabidopsis transcription factor IIB-related protein BRP4 is involved in the regulation of mitotic cell-cycle progression during male gametogenesis. J Exp Bot. 2014;65: 2521–2531. doi: 10.1093/jxb/eru140. pmid:24723406
[33]
Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 2009;10: R62. doi: 10.1186/gb-2009-10-6-r62. pmid:19508735
[34]
Roudier F, Ahmed I, Bérard C, Sarazin A, Mary‐Huard T, Cortijo S, et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 2011;30: 1928–1938. doi: 10.1038/emboj.2011.103. pmid:21487388
[35]
Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu Y-C, Lee PY, et al. Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod. 1999;11: 297–322. doi: 10.1007/s004970050158.
[36]
Bulankova P, Riehs-Kearnan N, Nowack MK, Schnittger A, Riha K. Meiotic progression in Arabidopsis is governed by complex regulatory interactions between SMG7, TDM1, and the meiosis I–specific cyclin TAM. Plant Cell. 2010;22: 3791–3803. doi: 10.1105/tpc.110.078378. pmid:21119056
[37]
Handel MA, Schimenti JC. Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat Rev Genet. 2010;11: 124–136. doi: 10.1038/nrg2723. pmid:20051984
[38]
Ross KJ, Fransz P, Armstrong SJ, Vizir I, Mulligan B, Franklin FC, et al. Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA-transformed lines. Chromosome Res Int J Mol Supramol Evol Asp Chromosome Biol. 1997;5: 551–559.
[39]
Chu S, Herskowitz I. Gametogenesis in Yeast Is Regulated by a Transcriptional Cascade Dependent on Ndt80. Mol Cell. 1998;1: 685–696. doi: 10.1016/S1097-2765(00)80068-4. pmid:9660952
[40]
Mata J, Wilbrey A, B？hler J. Transcriptional regulatory network for sexual differentiation in fission yeast. Genome Biol. 2007;8: R217. doi: 10.1186/gb-2007-8-10-r217. pmid:17927811
[41]
Horie S, Watanabe Y, Tanaka K, Nishiwaki S, Fujioka H, Abe H, et al. The Schizosaccharomyces pombe mei4 + Gene Encodes a Meiosis-Specific Transcription Factor Containing a forkhead DNA-Binding Domain. Mol Cell Biol. 1998;18: 2118–2129. pmid:9528784
[42]
Abe H, Shimoda C. Autoregulated Expression of Schizosaccharomyces pombe Meiosis-Specific Transcription Factor Mei4 and a Genome-Wide Search for Its Target Genes. Genetics. 2000;154: 1497–1508. pmid:10747048
[43]
Buratowski S, Kim T. The role of cotranscriptional histone methylations. Cold Spring Harb Symp Quant Biol. 2010;75: 95–102. doi: 10.1101/sqb.2010.75.036. pmid:21447819
[44]
Orford K, Kharchenko P, Lai W, Dao MC, Worhunsky DJ, Ferro A, et al. Differential H3K4 Methylation Identifies Developmentally Poised Hematopoietic Genes. Dev Cell. 2008;14: 798–809. doi: 10.1016/j.devcel.2008.04.002. pmid:18477461
[45]
Pekowska A, Benoukraf T, Ferrier P, Spicuglia S. A unique H3K4me2 profile marks tissue-specific gene regulation. Genome Res. 2010;20: 1493–1502. doi: 10.1101/gr.109389.110. pmid:20841431
[46]
Pinskaya M, Morillon A. Histone H3 Lysine 4 di-methylation: A novel mark for transcriptional fidelity? Epigenetics. 2009;4: 302–306. doi: 10.4161/epi.4.5.9369. pmid:19633430
[47]
Yang SY, Baxter EM, Van Doren M. Phf7 Controls Male Sex Determination in the Drosophila Germline. Dev Cell. 2012;22: 1041–1051. doi: 10.1016/j.devcel.2012.04.013. pmid:22595675
[48]
Katz DJ, Edwards TM, Reinke V, Kelly WG. A C. elegans LSD1 Demethylase Contributes to Germline Immortality by Reprogramming Epigenetic Memory. Cell. 2009;137: 308–320. doi: 10.1016/j.cell.2009.02.015. pmid:19379696
[49]
Vielle-Calzada J-P, Baskar R, Grossniklaus U. Delayed activation of the paternal genome during seed development. Nature. 2000;404: 91–94. doi: 10.1038/35003595. pmid:10716449
