An ARID Domain-Containing Protein within Nuclear Bodies Is Required for Sperm Cell Formation in
For all eukaryotes, gamete formation is an essential aspect of sexual reproduction. Unlike in animals, where meiotic products directly become gametes, the germline in plants is established by two consecutive mitotic divisions after meiosis is completed. The first mitosis is asymmetric, forming a larger vegetative cell and a smaller generative cell. The smaller generative cell then divides to produce two sperm cells. Current knowledge indicates DUO1 (DUO POLLEN 1), a transcription factor, plays a key role in this process by controlling expression of other germline genes. But how DUO1 is activated in the generative cell is unknown. To better understand the mechanisms that govern sperm cell formation and activate DUO1 expression, we characterized, ARID1, encoding an ARID (AT-Rich Interacting Domain)-containing protein. We show that ARID1 is required for DUO1 activation and sperm cell formation in Arabidopsis. Furthermore, ARID1 physically associates with a histone deacetylase, facilitating the maintenance of histone acetylation between the vegetative nucleus and sperm nuclei. Thus, our study shows that a pollen-specific ARID protein plays an important role during sperm cell formation in a dual manner: as a transcription factor to activate DUO1 and as a potential component of the histone modification machinery to maintain epigenetic status in pollen.
Vyšlo v časopise:
An ARID Domain-Containing Protein within Nuclear Bodies Is Required for Sperm Cell Formation in. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004421
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004421
Souhrn
For all eukaryotes, gamete formation is an essential aspect of sexual reproduction. Unlike in animals, where meiotic products directly become gametes, the germline in plants is established by two consecutive mitotic divisions after meiosis is completed. The first mitosis is asymmetric, forming a larger vegetative cell and a smaller generative cell. The smaller generative cell then divides to produce two sperm cells. Current knowledge indicates DUO1 (DUO POLLEN 1), a transcription factor, plays a key role in this process by controlling expression of other germline genes. But how DUO1 is activated in the generative cell is unknown. To better understand the mechanisms that govern sperm cell formation and activate DUO1 expression, we characterized, ARID1, encoding an ARID (AT-Rich Interacting Domain)-containing protein. We show that ARID1 is required for DUO1 activation and sperm cell formation in Arabidopsis. Furthermore, ARID1 physically associates with a histone deacetylase, facilitating the maintenance of histone acetylation between the vegetative nucleus and sperm nuclei. Thus, our study shows that a pollen-specific ARID protein plays an important role during sperm cell formation in a dual manner: as a transcription factor to activate DUO1 and as a potential component of the histone modification machinery to maintain epigenetic status in pollen.
Zdroje
1. McCormickS (2004) Control of male gametophyte development. Plant Cell 16 Suppl: S142–153.
2. OkadaT, EndoM, SinghMB, BhallaPL (2005) Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44: 557–568.
3. RotmanN, DurbarryA, WardleA, YangWC, ChaboudA, et al. (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15: 244–248.
4. IwakawaH, ShinmyoA, SekineM (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J 45: 819–831.
5. MoriT, KuroiwaH, HigashiyamaT, KuroiwaT (2006) GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8: 64–71.
6. KimHJ, OhSA, BrownfieldL, HongSH, RyuH, et al. (2008) Control of plant germline proliferation by SCF(FBL17) degradation of cell cycle inhibitors. Nature 455: 1134–1137.
7. BrownfieldL, HafidhS, DurbarryA, KhatabH, SidorovaA, et al. (2009) Arabidopsis DUO POLLEN3 is a key regulator of male germline development and embryogenesis. Plant Cell 21: 1940–1956.
8. ZhengB, ChenX, McCormickS (2011) The anaphase-promoting complex is a dual integrator that regulates both MicroRNA-mediated transcriptional regulation of cyclin B1 and degradation of Cyclin B1 during Arabidopsis male gametophyte development. Plant Cell 23: 1033–1046.
9. BrownfieldL, HafidhS, BorgM, SidorovaA, MoriT, et al. (2009) A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet 5: e1000430.
10. EngelML, Holmes-DavisR, McCormickS (2005) Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol 138: 2124–2133.
11. BorgM, BrownfieldL, KhatabH, SidorovaA, LingayaM, et al. (2011) The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell 23: 534–549.
12. PalatnikJF, WollmannH, SchommerC, SchwabR, BoisbouvierJ, et al. (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13: 115–125.
13. WilskerD, ProbstL, WainHM, MaltaisL, TuckerPW, et al. (2005) Nomenclature of the ARID family of DNA-binding proteins. Genomics 86: 242–251.
14. OkadaY, ScottG, RayMK, MishinaY, ZhangY (2007) Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis. Nature 450: 119–123.
15. WuRC, JiangM, BeaudetAL, WuMY (2013) ARID4A and ARID4B regulate male fertility, a functional link to the AR and RB pathways. Proc Natl Acad Sci U S A 110: 4616–4621.
16. LaiA, KennedyBK, BarbieDA, BertosNR, YangXJ, et al. (2001) RBP1 recruits the mSIN3-histone deacetylase complex to the pocket of retinoblastoma tumor suppressor family proteins found in limited discrete regions of the nucleus at growth arrest. Mol Cell Biol 21: 2918–2932.
17. FleischerTC, YunUJ, AyerDE (2003) Identification and characterization of three new components of the mSin3A corepressor complex. Mol Cell Biol 23: 3456–3467.
18. TakeuchiT, WatanabeY, Takano-ShimizuT, KondoS (2006) Roles of jumonji and jumonji family genes in chromatin regulation and development. Dev Dyn 235: 2449–2459.
19. TakahashiM, KojimaM, NakajimaK, Suzuki-MigishimaR, TakeuchiT (2007) Functions of a jumonji-cyclin D1 pathway in the coordination of cell cycle exit and migration during neurogenesis in the mouse hindbrain. Dev Biol 303: 549–560.
20. PengJC, ValouevA, SwigutT, ZhangJ, ZhaoY, et al. (2009) Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139: 1290–1302.
21. ShenX, KimW, FujiwaraY, SimonMD, LiuY, et al. (2009) Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 139: 1303–1314.
22. PasiniD, CloosPA, WalfridssonJ, OlssonL, BukowskiJP, et al. (2010) JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464: 306–310.
23. LiG, MargueronR, KuM, ChambonP, BernsteinBE, et al. (2010) Jarid2 and PRC2, partners in regulating gene expression. Genes Dev 24: 368–380.
24. ZhuH, ChenT, ZhuM, FangQ, KangH, et al. (2008) A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus. Plant Physiol 148: 337–347.
25. HonysD, TwellD (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5: R85.
26. BorgesF, GomesG, GardnerR, MorenoN, McCormickS, et al. (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148: 1168–1181.
27. DingZ, GillespieLL, PaternoGD (2003) Human MI-ER1 alpha and beta function as transcriptional repressors by recruitment of histone deacetylase 1 to their conserved ELM2 domain. Mol Cell Biol 23: 250–258.
28. WangL, CharrouxB, KerridgeS, TsaiCC (2008) Atrophin recruits HDAC1/2 and G9a to modify histone H3K9 and to determine cell fates. EMBO Rep 9: 555–562.
29. Alandete-SaezM, RonM, LeiboffS, McCormickS (2011) Arabidopsis thaliana GEX1 has dual functions in gametophyte development and early embryogenesis. Plant J 68: 620–632.
30. RonM, Alandete SaezM, Eshed WilliamsL, FletcherJC, McCormickS (2010) Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev 24: 1010–1021.
31. BorgM, TwellD (2010) Life after meiosis: patterning the angiosperm male gametophyte. Biochem Soc Trans 38: 577–582.
32. HaerizadehF, SinghMB, BhallaPL (2006) Transcriptional repression distinguishes somatic from germ cell lineages in a plant. Science 313: 496–499.
33. LiH, SorianoM, CordewenerJ, MuinoJM, RiksenT, et al. (2014) The histone deacetylase inhibitor trichostatin a promotes totipotency in the male gametophyte. Plant Cell 26: 195–209.
34. HarbourJW, DeanDC (2000) The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev 14: 2393–2409.
35. WildwaterM, CampilhoA, Perez-PerezJM, HeidstraR, BlilouI, et al. (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123: 1337–1349.
36. EbelC, MaricontiL, GruissemW (2004) Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429: 776–780.
37. ChenZ, HafidhS, PohSH, TwellD, BergerF (2009) Proliferation and cell fate establishment during Arabidopsis male gametogenesis depends on the Retinoblastoma protein. Proc Natl Acad Sci U S A 106: 7257–7262.
38. LoraineAE, McCormickS, EstradaA, PatelK, QinP (2013) RNA-seq of Arabidopsis pollen uncovers novel transcription and alternative splicing. Plant Physiol 162: 1092–1109.
39. SlotkinRK, VaughnM, BorgesF, TanurdzicM, BeckerJD, et al. (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461–472.
40. ScarpinR, SigautL, PietrasantaL, McCormickS, ZhengB, et al. (2013) Cajal Bodies Are Developmentally Regulated during Pollen Development and Pollen Tube Growth in Arabidopsis thaliana. Mol Plant 6: 1355–1357.
41. VertG, ChoryJ (2006) Downstream nuclear events in brassinosteroid signalling. Nature 441: 96–100.
42. LiCF, PontesO, El-ShamiM, HendersonIR, BernatavichuteYV, et al. (2006) An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126: 93–106.
43. BoavidaLC, McCormickS (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52: 570–582.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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