Emerging roles for non-coding RNAs in male reproductive development in flowering plants

Biomolecules

Volumn 2, Issue 4, 2012, Pages 608-621

  Grant Downton, Robert ^a   Rodriguez Enriquez, Josefina ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSIDAD DE LA LAGUNA   (Spain)

Author keywords

Cytoplasmic male sterility; Fertility; Flowering plant; Gametophyte; Non coding RNA; Pollen; Reproduction; Small RNA

Indexed keywords

MICRORNA; UNTRANSLATED RNA;

ANGIOSPERM; BIOGENESIS; DNA SEQUENCE; EPIGENETICS; FERTILIZATION; MALE FERTILITY; MALE GAMETOPHYTE; MALE STERILITY; MEIOSIS; MITOSIS; NONHUMAN; PLANT BREEDING; PLANT REPRODUCTION; POLLEN; POLLEN GERMINATION; REVIEW; SOMATIC CELL; TRANSCRIPTION REGULATION;

EID: 85016378054     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom2040608     Document Type: Review

References (65)

1. Feng, X.; Dickinson, H.G. Packaging the male germline in plants. Trends Genetics 2007, 23, 503-510.
2. Dickinson, H.G.; Grant-Downton, R. Bridging the generation gap: Flowering plant gametophytes and animal germlines reveal unexpected similarities. Biol. Rev. Cambridge Philos. Soc. 2009, 84, 589-615.
3. Berger, F.; Twell, D. Germline specification and function in plants. Annual Rev. Plant Biol. 2011, 62, 461-484.
4. Twell, D. Male gametogenesis and germline specification in flowering plants. Sexual Plant Reprod. 2011, 24, 149-160.
5. Taylor, L.P.; Hepler, P.K. Pollen Germination and Tube Growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997, 48, 461-491.
6. Takeuchi, H.; Higashiyama, T. Attraction of tip-growing pollen tubes by the female gametophyte. Curr. Opin. Plant Biol. 2011, 14, 614-621.
7. Hamamura, Y.; Nagahara, S.; Higashiyama, T. Double fertilization on the move. Curr. Opin. Plant Biol. 2012, 15, 70-77.
8. Faure, J.E. Double fertilization in flowering plants: discovery, study methods and mechanisms. Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie 2001, 324, 551-558.
9. Costa, L.M.; Gutierrez-Marcos, J.F.; Dickinson, H.G. More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci. 2004, 9, 507-514.
10. Golden, T.A.; Schauer, S.E.; Lang, J.D.; Pien, S.; Mushegian, A.R.; Grossniklaus, U.; Meinke, D.W.; Ray, A. Short integuments1/suspensor1/carpel factory, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol. 2002, 130, 808-822.
11. Vaucheret, H.; Vazquez, F.; Crete, P.; Bartel, D.P. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 2004, 18, 1187-1197.
12. Nodine, M.D.; Bartel, D.P. MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev. 2010, 24, 2678-2692.
13. Nonomura, K.; Morohoshi, A.; Nakano, M.; Eiguchi, M.; Miyao, A.; Hirochika, H.; Kurata, N. A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 2007, 19, 2583-2594.
14. Yang, H.; Lu, P.; Wang, Y.; Ma, H. The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J. 2011, 65, 503-516.
15. Grant-Downton, R.; Hafidh, S.; Twell, D.; Dickinson, H.G. Small RNA pathways are present and functional in the angiosperm male gametophyte. Mol. Plant 2009, 2, 500-512.
16. Slotkin, R.K.; Vaughn, M.; Borges, F.; Tanurdzic, M.; Becker, J.D.; Feijo, J.A.; Martienssen, R.A. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 2009, 136, 461-472.
17. Borges, F.; Gomes, G.; Gardner, R.; Moreno, N.; McCormick, S.; Feijo, J.A.; Becker, J.D. Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol. 2008, 148, 1168-1181.
18. Russell, S.D.; Gou, X.; Wong, C.E.; Wang, X.; Yuan, T.; Wei, X.; Bhalla, P.L.; Singh, M.B. Genomic profiling of rice sperm cell transcripts reveals conserved and distinct elements in the flowering plant male germ lineage. New Phytol. 2012, 195, 560-573.
19. Lu, C.; Tej, S.S.; Luo, S.; Haudenschild, C.D.; Meyers, B.C.; Green, P.J. Elucidation of the small RNA component of the transcriptome. Science 2005, 309, 1567-1569.
20. Nobuta, K.; Venu, R.C.; Lu, C.; Belo, A.; Vemaraju, K.; Kulkarni, K.; Wang, W.; Pillay, M.; Green, P.J.; Wang, G.L.; Meyers, B.C. An expression atlas of rice mRNAs and small RNAs. Nat. Biotech.2007, 25, 473-477.
21. Grant-Downton, R.; Le Trionnaire, G.; Schmid, R.; Rodriguez-Enriquez, J.; Hafidh, S.; Mehdi, S.; Twell, D.; Dickinson, H. MicroRNA and tasiRNA diversity in mature pollen of Arabidopsis thaliana. BMC Genomics 2009, 10, 643-658.
22. Chambers, C.; Shuai, B. Profiling microRNA expression in Arabidopsis pollen using microRNA array and real-time PCR. BMC Plant Biol. 2009, 9, 87.
23. Borges, F.; Pereira, P.A.; Slotkin, R.K.; Martienssen, R.A.; Becker, J.D. MicroRNA activity in the Arabidopsis male germline. J. Exp. Bot. 2011, 62, 1611-1620.
24. Wei, L.Q.; Yan, L.F.; Wang, T. Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol. 2011, 12, R53.
25. Peng, H.; Chun, J.; Ai, T.B.; Tong, Y.A.; Zhang, R.; Zhao, M.M.; Chen, F.; Wang, S.H. MicroRNA profiles and their control of male gametophyte development in rice. Plant Mol. Biol. 2012, 80, 85-102.
26. Peragine, A.; Yoshikawa, M.; Wu, G.; Albrecht, H.L.; Poethig, R.S. SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev. 2004, 18, 2368-2379.
27. Allen, E.; Howell, M.D. miRNAs in the biogenesis of trans-acting siRNAs in higher plants. Seminars Cell Dev. Biol. 2010, 21, 798-804.
28. Song, X.; Li, P.; Zhai, J.; Zhou, M.; Ma, L.; Liu, B.; Jeong, D.H.; Nakano, M.; Cao, S.; Liu, C.; Chu, C.; Wang, X.J.; Green, P.J.; Meyers, B.C.; Cao, X. Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. 2012, 69, 462-474.
29. Honys, D.; Twell, D. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 2004, 5, R85.
30. Zheng, B.; Chen, X.; McCormick, S. 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. The Plant Cell 2011, 23, 1033-1046.
31. Rotman, N.; Durbarry, A.; Wardle, A.; Yang, W.C.; Chaboud, A.; Faure, J.E.; Berger, F.; Twell, D. A novel class of MYB factors controls sperm-cell formation in plants. Curr. Biol. 2005, 15, 244-248.
32. Borg, M.; Brownfield, L.; Khatab, H.; Sidorova, A.; Lingaya, M.; Twell, D. The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. The Plant Cell 2011, 23, 534-549.
33. Allen, R.S.; Li, J.; Alonso-Peral, M.M.; White, R.G.; Gubler, F.; Millar, A.A. MicroR159 regulation of most conserved targets in Arabidopsis has negligible phenotypic effects. Silence 2010, 1, 18.
34. Russell, S.D.; Cass, D.D. Ultrastructure of the sperms of Plumbago zeylanica 1. Cytology and association with the vegetative nucleus. Protoplasma 1981, 107, 85-107.
35. Eady, C.; Lindsey, K.; Twell, D. The Significance of Microspore Division and Division Symmetry for Vegetative Cell-Specific Transcription and Generative Cell Differentiation. The Plant Cell 1995, 7, 65-74.
36. Matzke, M.A.; Birchler, J.A. RNAi-mediated pathways in the nucleus. Nat. Rev. Genetics 2005, 6, 24-35.
37. Engel, M.L.; Chaboud, A.; Dumas, C.; McCormick, S. Sperm cells of Zea mays have a complex complement of mRNAs. Plant J. 2003, 34, 697-707.
38. Vicient, C.M. Transcriptional activity of transposable elements in maize. BMC Genomics 2010, 11, 601.
39. Grant-Downton, R.T. Through a generation darkly: small RNAs in the gametophyte. Biochem. Soc. Trans. 2010, 38, 617-621.
40. Becker, C.; Hagmann, J.; Muller, J.; Koenig, D.; Stegle, O.; Borgwardt, K.; Weigel, D. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nat. 2011, 480, 245-249.
41. McCue, A.D.; Nuthikattu, S.; Reeder, S.H.; Slotkin, R.K. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genetics 2012, 8, doi:10.1371/journal.pgen.1002474.
42. Wright, D.A.; Voytas, D.F. Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res. 2002, 12, 122-131.
43. Ron, M.; Alandete Saez, M.; Eshed Williams, L.; Fletcher, J.C.; McCormick, S. Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev. 2010, 24, 1010-1021.
44. Song, J.H.; Cao, J.S.; Yu, X.L.; Xiang, X. BcMF11, a putative pollen-specific non-coding RNA from Brassica campestris ssp. chinensis. J. Plant Physiol. 2007, 164, 1097-1100.
45. Dai, X.-Y.; Yu, J.-I.; Zhao, Q.; Zhu, D.-Y.; Ao, G.-M. Non-coding RNA for ZM401, a Pollen-specific Gene of Zea Mays. Acta Botanica Sinica 2004, 46 497-504.
46. Ma, J.; Yan, B.; Qu, Y.; Qin, F.; Yang, Y.; Hao, X.; Yu, J.; Zhao, Q.; Zhu, D.; Ao, G. Zm401, a short-open reading-frame mRNA or noncoding RNA, is essential for tapetum and microspore development and can regulate the floret formation in maize. J. Cell. Biochem. 2008, 105, 136-146.
47. Shi, D.Q.; Liu, J.; Xiang, Y.H.; Ye, D.; Sundaresan, V.; Yang, W.C. SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 2005, 17, 2340-2354.
48. Li, H.J.; Liu, N.Y.; Shi, D.Q.; Liu, J.; Yang, W.C. YAO is a nucleolar WD40-repeat protein critical for embryogenesis and gametogenesis in Arabidopsis. BMC Plant Biol. 2010, 10, 169.
49. Wang, S.Q.; Shi, D.Q.; Long, Y.P.; Liu, J.; Yang, W.C. GAMETOPHYTE DEFECTIVE 1, a putative subunit of RNases P/MRP, is essential for female gametogenesis and male competence in Arabidopsis. PloS One 2012, 7, doi:10.1371/journal.pone.0033595.
50. Pelletier, G.; Budar, F. The molecular biology of cytoplasmically inherited male sterility and prospects for its engineering. Curr. Opin. Biotech. 2007, 18, 121-125.
51. Zhou, H.; Liu, Q.; Li, J.; Jiang, D.; Zhou, L.; Wu, P.; Lu, S.; Li, F.; Zhu, L.; Liu, Z.; Chen, L.; Liu, Y.G.; Zhuang, C. Photoperiod-and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res. 2012, 22, 649-660.
52. Ding, J.; Lu, Q.; Ouyang, Y.; Mao, H.; Zhang, P.; Yao, J.; Xu, C.; Li, X.; Xiao, J.; Zhang, Q. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc. Nat. Acad. Sci. USA 2012, 109, 2654-2659.
53. Chen, H.M.; Li, Y.H.; Wu, S.H. Bioinformatic prediction and experimental validation of a microRNA-directed tandem trans-acting siRNA cascade in Arabidopsis. Proc. Nat. Acad. Sci. USA 2007, 104, 3318-3323.
54. Howell, M.D.; Fahlgren, N.; Chapman, E.J.; Cumbie, J.S.; Sullivan, C.M.; Givan, S.A.; Kasschau, K.D.; Carrington, J.C. Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA-and tasiRNA-directed targeting. Plant Cell 2007, 19, 926-942.
55. Frankel, R. Graft-Induced Transmission to Progeny of Cytoplasmic Male Sterility in Petunia. Science 1956, 124, 684-685.
56. Frankel, R. Further Evidence on Graft Induced Transmission to Progeny of Cytoplasmic Male Sterility in Petunia. Genetics 1962, 47, 641-646.
57. van Marrewijk, G.A.M. Cytoplasmic male sterility in petunia. II. A discussion on male sterility transmission by means of grafting. Euphytica 1970, 19, 25-32.
58. Edwardson, J.R.; Corbett, M.K. Asexual transmission of cytoplasmic male sterility. Proc. Nat. Acad. Sci. USA 1961, 47, 390-396.
59. Curtis, C.L. Graft-trasmission of male sterility in sugar beet(Beta vulgaris L.). Euphytica 1967, 16, 419-424.
60. Melnyk, C.W.; Molnar, A.; Baulcombe, D.C. Intercellular and systemic movement of RNA silencing signals. EMBO J. 2011, 30, 3553-3563.
61. Sorefan, K.; Pais, H.; Hall, A.E.; Kozomara, A.; Griffiths-Jones, S.; Moulton, V.; Dalmay, T. Reducing sequencing bias of small RNAs. Silence 2012, 3, 4.
62. Vaucheret, H. Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev. 2006, 20, 759-771.
63. Yang, J.S.; Lai, E.C. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol. Cell 2011, 43, 892-903.
64. Chen, C.; Farmer, A.D.; Langley, R.J.; Mudge, J.; Crow, J.A.; May, G.D.; Huntley, J.; Smith, A.G.; Retzel, E.F. Meiosis-specific gene discovery in plants: RNA-Seq applied to isolated Arabidopsis male meiocytes. BMC Plant Biol. 2010, 10, 280.
65. van der Heijden, G.W.; Bortvin, A. Transient relaxation of transposon silencing at the onset of mammalian meiosis. Epigenetics 2009, 4, 76-79.