Plant Growth Regulation

, Volume 61, Issue 1, pp 11–20 | Cite as

The molecular mechanisms of male reproductive organogenesis in rice (Oryza sativa L.)

  • Yun Tian
  • Hui Yang
  • Hai wen Zhang
  • Qian Dai
  • Jun Fang
  • Xian guo Qing
  • Xiang yang Lu
Original paper
First Online:
Received:
Accepted:

Abstract

Stamen is the male reproductive organ of rice (Oryza sativa L.), and the development is a considerably significant stage during the sexual reproduction. It is very important to reveal what is the molecular mechanisms which controlling the development of stamen, and will be helpful in producing hybrid seeds by manipulating the male sterility. This article reviews the progress on the molecular mechanisms of male reproductive organogenesis in rice, which would facilitate the further studies on male sterile genes in rice.

Keywords

Stamen Anther Male sterility Oryza sativa L. 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This research was supported by the National Natural Science Foundation of China (30871336), the Key Project of Chinese Ministry of Education, the Hunan Provincial Natural Science Foundation of China (09JJ3043) and the Key Scientific Research Fund of Hunan Provincial Education Department (09A038).

References

  1. Armstrong SJ, Caryl AP, Jones GH, Franklin FC (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115:3645–3655CrossRefPubMedGoogle Scholar
  2. Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21:1453–1472CrossRefPubMedGoogle Scholar
  3. Bishop DK, Park D, Xu L, Kleckner N (1992) DMC1: a meiosis-specific yeast homolog of E.coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:439–456CrossRefPubMedGoogle Scholar
  4. Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727CrossRefPubMedGoogle Scholar
  5. Chen R, Zhao X, Shao Z, Wei Z, Wang Y, Zhu L, Zhao J, Sun M, He R, He G (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19:847–861CrossRefPubMedGoogle Scholar
  6. Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY (2007) Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot (Lond) 100:959–966CrossRefGoogle Scholar
  7. Chhun T, Aya K, Asano K, Yamamoto E, Morinaka Y, Watanabe M, Kitano H, Ashikari M, Matsuoka M, Ueguchi-Tanaka M (2007) Gibberellin regulates pollen viability and pollen tube growth in rice. Plant Cell 19:3876–3888CrossRefPubMedGoogle Scholar
  8. Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen JL, Zhang Q, Wang S (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–1255CrossRefPubMedGoogle Scholar
  9. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11:1623–1634CrossRefPubMedGoogle Scholar
  10. Deng ZY, Wang T (2007) OsDMC1 is required for homologous pairing in Oryza sativa. Plant Mol Biol 65:31–42CrossRefPubMedGoogle Scholar
  11. Endo M, Tsuchiya T, Saito H, Matsubara H, Hakozaki H, Masuko H, Kamada M, Higashitani A, Takahashi H, Fukuda H, Demura T, Watanabe M (2004) Identification and molecular characterization of novel anther-specific genes in Oryza sativa L. by using cDNA microarray. Genes Genet Syst 79:213–226CrossRefPubMedGoogle Scholar
  12. Fujioka T, Kaneko F, Kazama T, Suwabe K, Suzuki G, Makino A, Mae T, Endo M, Kawagishi-Kobayashi M, Watanabe M (2008) Identification of small RNAs in late developmental stage of rice anthers. Genes Genet Syst 83:281–284CrossRefPubMedGoogle Scholar
  13. Fukuda A, Nemoto K, Chono M, Yamaguchi S, Nakajima M, Yamagishi J, Maekawa M, Yamaguchi I (2004) Expression pattern of the coparyl diphosphate synthase gene in developing rice anthers. Biosci Biotechnol Biochem 68:1814–1816CrossRefPubMedGoogle Scholar
  14. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100CrossRefPubMedGoogle Scholar
  15. Han MJ, Jung KH, Yi G, Lee DY, An G (2006) Rice Immature Pollen 1 (RIP1) is a regulator of late pollen development. Plant Cell Physiol 47:1457–1472CrossRefPubMedGoogle Scholar
  16. Hirano K, Aya K, Hobo T, Sakakibara H, Kojima M, Shim RA, Hasegawa Y, Ueguchi-Tanaka M, Matsuoka M (2008) Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol 49:1429–1450CrossRefPubMedGoogle Scholar
  17. Hobo T, Suwabe K, Aya K, Suzuki G, Yano K, Ishimizu T, Fujita M, Kikuchi S, Hamada K, Miyano M, Fujioka T, Kaneko F, Kazama T, Mizuta Y, Takahashi H, Shiono K, Nakazono M, Tsutsumi N, Nagamura Y, Kurata N, Watanabe M, Matsuoka M (2008) Various spatiotemporal expression profiles of anther-expressed genes in rice. Plant Cell Physiol 49:1417–1428CrossRefPubMedGoogle Scholar
  18. Holweg C, Nick P (2004) Arabidopsis myosin XI mutant is defective in organelle movement and polar auxin transport. Proc Natl Acad Sci USA 101:10488–10493CrossRefPubMedGoogle Scholar
  19. Huang MD, Wei FJ, Wu CC, Hsing YI, Huang AH (2009) Analyses of advanced rice anther transcriptomes reveal global tapetum secretory functions and potential proteins for lipid exine formation. Plant Physiol 149:694–707CrossRefPubMedGoogle Scholar
  20. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  21. Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47CrossRefPubMedGoogle Scholar
  22. Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc Natl Acad Sci USA 105:2220–2225CrossRefPubMedGoogle Scholar
  23. Jiang SY, Cai M, Ramachandran S (2007) ORYZA SATIVA MYOSIN XI B controls pollen development by photoperiod-sensitive protein localizations. Dev Biol 304:579–592CrossRefPubMedGoogle Scholar
  24. Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722CrossRefPubMedGoogle Scholar
  25. Jung KH, Han MJ, Lee DY, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, Hwang I, An G (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18:3015–3032CrossRefPubMedGoogle Scholar
  26. Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M, Matsuoka M (2004) Loss-of-function mutations of the rice GAMYB gene impair α-amylase expression in aleurone and flower development. Plant Cell 16:33–44CrossRefPubMedGoogle Scholar
  27. Kerim T, Imin N, Weinman JJ, Rolfe BG (2003) Proteome analysis of male gametophyte development in rice anthers. Proteomics 3:738–751CrossRefPubMedGoogle Scholar
  28. Lan L, Chen W, Lai Y, Suo J, Kong Z, Li C, Lu Y, Zhang Y, Zhao X, Zhang X, Zhang Y, Han B, Cheng J, Xue Y (2004) Monitoring of gene expression profiles and isolation of candidate genes involved in pollination and fertilization in rice (Oryza sativa L.) with a 10K cDNA microarray. Plant Mol Biol 54:471–487CrossRefPubMedGoogle Scholar
  29. Lee S, Jung KH, An G, Chung YY (2004) Isolation and characterization of a rice cysteine protease gene, OsCP1, using T-DNA gene-trap system. Plant Mol Biol 54:755–765CrossRefPubMedGoogle Scholar
  30. Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014CrossRefPubMedGoogle Scholar
  31. Li T, Gong C, Wang T (2009) RA68 is required for postmeiotic pollen development in Oryza sativa. Plant Mol Biol. doi: 10.1007/s11103-009-9566-y Google Scholar
  32. Luo H, Lee JY, Hu Q, Nelson-Vasilchik K, Eitas TK, Lickwar C, Kausch AP, Chandlee JM, Hodges TK (2006) RTS, a rice anther-specific gene is required for male fertility and its promoter sequence directs tissue-specific gene expression in different plant species. Plant Mol Biol 62:397–408CrossRefPubMedGoogle Scholar
  33. Mascarenhas JP (1990) Gene activity during pollen development. Ann Rev Plant Physiol Plant Mol Biol 41:317–338CrossRefGoogle Scholar
  34. Moritoh S, Miki D, Akiyama M, Kawahara M, Izawa T, Maki H, Shimamoto K (2005) RNAi-mediated silencing of OsGEN-L (OsGEN-like), a new member of the RAD2/XPG nuclease family, causes male sterility by defect of microspore development in rice. Plant Cell Physiol 46:699–715CrossRefPubMedGoogle Scholar
  35. Mu H, Ke J, Liu W, Zhuang C, Yip W (2009) UDP-glucose pyrophosphorylase 2 (OsUgp2), a pollen-preferential gene in rice, plays a critical role in starch accumulation during pollen maturation. Chinese Sci Bull 54:234–243CrossRefGoogle Scholar
  36. Ngampanya B, Sobolewska A, Takeda T, Toyofuku K, Narangajavana J, Ikeda A, Yamaguchi J (2003) Characterization of rice functional monosaccharide transporter, OsMST5. Biosci Biotechnol Biochem 67:556–562CrossRefPubMedGoogle Scholar
  37. Nonomura K, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15:1728–1739CrossRefPubMedGoogle Scholar
  38. Nonomura K, Nakano M, Fukuda T, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004a) The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis. Plant Cell 16:1008–1020CrossRefPubMedGoogle Scholar
  39. Nonomura KI, Nakano M, Murata K, Miyoshi K, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004b) An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis. Mol Genet Genomics 271:121–129CrossRefPubMedGoogle Scholar
  40. Nonomura K, Nakano M, Eiguchi M, Suzuki T, Kurata N (2006) PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J Cell Sci 119:217–225CrossRefPubMedGoogle Scholar
  41. Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, Kurata N (2007) 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 19:2583–2594CrossRefPubMedGoogle Scholar
  42. Park JI, Hakozaki H, Endo M, Takada Y, Ito H, Uchida M, Okabe T, Watanabe M (2006) Molecular characterization of mature pollen-specific genes encoding novel small cysteine-rich proteins in rice (Oryza sativa L.). Plant Cell Rep 25:466–474CrossRefPubMedGoogle Scholar
  43. Peng HF, Zhang ZF, Wu B, Chen XH, Zhang GQ, Zhang ZM, Wan BH, Lu YP (2008) Molecular mapping of two reverse photoperiod-sensitive genic male sterility genes (rpms1 and rpms2) in rice (Oryza sativa L.). Theor Appl Genet 118:77–83CrossRefPubMedGoogle Scholar
  44. Raghavan V (1988) Anther and pollen development in rice (Oryza sativa L.). Am J Bot 75:183–196CrossRefGoogle Scholar
  45. Raghavan V (1997) Anther developmental biology in molecular embryology of flowering plants. Cambridge University Press, Cambridge, pp 17–60Google Scholar
  46. Sanchez-Moran E, Santos JL, Jones GH, Franklin FC (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21:2220–2233CrossRefPubMedGoogle Scholar
  47. Sorensen AM, Kröber S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423CrossRefPubMedGoogle Scholar
  48. Suwabe K, Suzuki G, Takahashi H, Shiono K, Endo M, Yano K, Fujita M, Masuko H, Saito H, Fujioka T, Kaneko F, Kazama T, Mizuta Y, Kawagishi-Kobayashi M, Tsutsumi N, Kurata N, Nakazono M, Watanabe M (2008) Separated transcriptomes of male gametophyte and tapetum in rice: validity of a laser microdissection (LM) microarray. Plant Cell Physiol 49:1407–1416CrossRefPubMedGoogle Scholar
  49. Tao J, Zhang L, Chong K, Wang T (2007) OsRAD21–3, an orthologue of yeast RAD21, is required for pollen development in Oryza sativa. Plant J 51:919–930CrossRefPubMedGoogle Scholar
  50. Toyoda Y, Furuya K, Goshima G, Nagao K, Takahashi K, Yanagida M (2002) Requirement of chromatid cohesion proteins rad21/scc1 and mis4/scc2 for normal spindle-kinetochore interaction in fission yeast. Curr Biol 12:347–358CrossRefPubMedGoogle Scholar
  51. Tsuchiya T, Toriyama K, Nasrallah ME, Ejiri S (1992) Isolation of genes abundantly expressed in rice anthers at the microspore stage. Plant Mol Biol 20:1189–1193CrossRefPubMedGoogle Scholar
  52. Tsuchiya T, Toriyama K, Ejiri S, Hinata K (1994) Molecular characterization of rice genes specifically expressed in the anther tapetum. Plant Mol Biol 26:1737–1746CrossRefPubMedGoogle Scholar
  53. Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R, Nishizawa NK, Gomi K, Shimada A, Kitano H, Ashikari M, Matsuoka M (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47:427–444CrossRefPubMedGoogle Scholar
  54. Wang Z, Liang Y, Li C, Xu Y, Lan L, Zhao D, Chen C, Xu Z, Xue Y, Chong K (2005) Microarray analysis of gene expression involved in anther development in rice (Oryza sativa L.). Plant Mol Biol 58:721–737CrossRefPubMedGoogle Scholar
  55. Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464CrossRefPubMedGoogle Scholar
  56. Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492CrossRefPubMedGoogle Scholar
  57. Woo MO, Ham TH, Ji HS, Choi MS, Jiang W, Chu SH, Piao R, Chin JH, Kim JA, Park BS, Seo HS, Jwa NS, McCouch S, Koh HJ (2008) Inactivation of the UGPase1 gene causes genic male sterility and endosperm chalkiness in rice (Oryza sativa L.). Plant J 54:190–204CrossRefPubMedGoogle Scholar
  58. Xiao X, Yang Y, Yang Y, Lin J, Tang D, Liu X (2009) Comparative analysis of young panicle proteome in thermo-sensitive genic male-sterile rice Zhu-1S under sterile and fertile conditions. Biotechnol Lett 31:157–161CrossRefPubMedGoogle Scholar
  59. Xu F, Li X, Ruan Y (2008) RNAi-mediated suppression of hexokinase gene OsHXK10 in rice leads to non-dehiscent anther and reduction of pollen germination. Plant Sci 175:674–684CrossRefGoogle Scholar
  60. Yamaguchi T, Hayashi T, Nakayama K, Koike S (2006) Expression analysis of genes for callose synthases and Rho-type small GTP-binding proteins that are related to callose synthesis in rice anther. Biosci Biotechnol Biochem 70:639–645CrossRefPubMedGoogle Scholar
  61. Yang WQ, Lai Y, Li MN, Xu WY, Xue YB (2008) A novel C2-domain phospholipid-binding protein, OsPBP1, is required for pollen fertility in rice. Mol Plant 1:770–785CrossRefPubMedGoogle Scholar
  62. Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Huang X, Li W, Li J, Liu Z, Li L, Liu J, Qi Q, Liu J, Li L, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Zhang J, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Ren X, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Wang J, Zhao W, Li P, Chen W, Wang X, Zhang Y, Hu J, Wang J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Li G, Liu S, Tao M, Wang J, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92PubMedGoogle Scholar
  63. Yuan W, Li X, Chang Y, Wen R, Chen G, Zhang Q, Wu C (2009) Mutation of the rice gene PAIR3 results in lack of bivalent formation in meiosis. Plant J 59:303–315CrossRefPubMedGoogle Scholar
  64. Zhang Q (2007) Strategies for developing Green Super Rice. Proc Natl Acad Sci USA 104:16402–16409CrossRefPubMedGoogle Scholar
  65. Zhang L, Tao J, Wang S, Chong K, Wang T (2006a) The rice OsRad21–4, an orthologue of yeast Rec8 protein, is required for efficient meiosis. Plant Mol Biol 60:533–554CrossRefPubMedGoogle Scholar
  66. Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006b) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095CrossRefPubMedGoogle Scholar
  67. Zhang DS, Liang WQ, Yuan Z, Li N, Shi J, Wang J, Liu YM, Yu WJ, Zhang DB (2008) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant 1:599–610CrossRefPubMedGoogle Scholar
  68. Zhao DZ, Wang GF, Speal B, Ma H (2002) The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16:2021–2031CrossRefPubMedGoogle Scholar
  69. Zhao X, de Palma J, Oane R, Gamuyao R, Luo M, Chaudhury A, Hervé P, Xue Q, Bennett J (2008) OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J 54:375–387CrossRefPubMedGoogle Scholar
  70. Zhu QH, Ramm K, Shivakkumar R, Dennis ES, Upadhyaya NM (2004) The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice. Plant Physiol 135:1514–1525CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Yun Tian
    • 1
    • 2
    • 3
  • Hui Yang
    • 1
    • 2
  • Hai wen Zhang
    • 5
    • 6
  • Qian Dai
    • 1
    • 2
  • Jun Fang
    • 1
    • 2
  • Xian guo Qing
    • 3
    • 4
  • Xiang yang Lu
    • 1
    • 2
  1. 1.College of Bioscience and Biotechnology, Hunan Agricultural UniversityChangshaChina
  2. 2.Hunan Agricultural Bioengineering Research InstituteChangshaChina
  3. 3.Yuan Long Ping High-Tech Agriculture CO., LTDChangshaChina
  4. 4.National Hybrid Rice Research and Development CenterChangshaChina
  5. 5.Biotechnology Research Institute, Chinese Academy of Agricultural SciencesBeijingChina
  6. 6.National Key Facility of Crop Gene Resources and Genetic ImprovementBeijingChina

Personalised recommendations