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The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene during Male Meiosis in

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Meiosis is a critical event in sexual reproduction. During meiosis, chromosomes recombine and segregate twice consecutively to produce haploid daughter cells, which differentiate into gametes. In humans, errors in meiosis are the leading causes of congenital birth defects. In plants, bypassing the meiotic program can lead to production of clonal seeds that retain hybrid traits that otherwise segregate. Thus, understanding the controls of meiosis has major implications for both health and crop improvement. How meiotic gene expression is regulated in multicellular eukaryotes to promote entry into and progression through the meiotic program is poorly understood. Here we identify DUET, a protein essential for male meiosis in the model plant Arabidopsis thaliana, as a regulator of meiotic gene expression. We found that DUET is required for proper expression of JAS and TDM1. These genes function in male meiosis, and regulate spindle organization during meiosis II and cell cycle transitions, respectively. Expression of DUET at the end of prophase coincides with the onset of TDM1 expression, and DUET directly binds TDM1, indicating TDM1 is a direct target of DUET. Our results provide an initial framework for further elucidating the developmental and molecular controls of meiotic gene expression in plants.

Vyšlo v časopise: The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene during Male Meiosis in. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005396
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005396

Souhrn

Meiosis is a critical event in sexual reproduction. During meiosis, chromosomes recombine and segregate twice consecutively to produce haploid daughter cells, which differentiate into gametes. In humans, errors in meiosis are the leading causes of congenital birth defects. In plants, bypassing the meiotic program can lead to production of clonal seeds that retain hybrid traits that otherwise segregate. Thus, understanding the controls of meiosis has major implications for both health and crop improvement. How meiotic gene expression is regulated in multicellular eukaryotes to promote entry into and progression through the meiotic program is poorly understood. Here we identify DUET, a protein essential for male meiosis in the model plant Arabidopsis thaliana, as a regulator of meiotic gene expression. We found that DUET is required for proper expression of JAS and TDM1. These genes function in male meiosis, and regulate spindle organization during meiosis II and cell cycle transitions, respectively. Expression of DUET at the end of prophase coincides with the onset of TDM1 expression, and DUET directly binds TDM1, indicating TDM1 is a direct target of DUET. Our results provide an initial framework for further elucidating the developmental and molecular controls of meiotic gene expression in plants.

Zdroje

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 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 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 16292313

5. White-Cooper H. Molecular mechanisms of gene regulation during Drosophila spermatogenesis. Reproduction. 2010;139 : 11–21. doi: 10.1530/REP-09-0083 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 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 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 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 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 22844260

14. Musselman CA, Kutateladze TG. Handpicking epigenetic marks with PHD fingers. Nucleic Acids Res. 2011;39 : 9061–9071. doi: 10.1093/nar/gkr613 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 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 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 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 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 17218268

20. Alexander MP. Differential staining of aborted and nonaborted pollen. Stain Technol. 1969;44 : 117–122. 4181665

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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 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 9660952

40. Mata J, Wilbrey A, Bähler J. Transcriptional regulatory network for sexual differentiation in fission yeast. Genome Biol. 2007;8: R217. doi: 10.1186/gb-2007-8-10-r217 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. 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. 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 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 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 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 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 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 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 10716449

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