Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB

Plant Cell

Volumn 21, Issue 5, 2009, Pages 1453-1472

  Aya, Koichiro ^a,b   Tanaka, Miyako Ueguchi ^a   Kondo, Maki ^c   Hamada, Kazuki ^d   Yano, Kentaro ^d   Nishimura, Mikio ^c   Matsuoka, Makoto ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^d MEIJI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ORYZA SATIVA;

EID: 67651111748     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.062935     Document Type: Article

References (71)

1. Achard, P., Herr, A., Baulcombe, D.C., and Harberd, N.P. (2004). Modulation of floral development by a gibberellin-regulated micro-RNA. Development 131: 3357-3365. (Pubitemid 39139882)
2. Ahlers, F., Bubert, H., Steuernagel, S., and Wiermann, R. (2000). The nature of oxygen in sporopollenin from the pollen of Typha angustifolia L. Z. Naturforsch. [C] 55: 129-136. (Pubitemid 30254784)
3. 1H NMR analysis of sporopollenin from Typha angustifolia. Phytochemistry 50: 1095-1098. (Pubitemid 29156261)
4. Ariizumi, T., Murase, K., Sun, T.-P., and Steber, C.M. (2008). Proteolysis-independent downregulation of DELLA repression in Arabidopsis by the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1. Plant Cell 20: 2447-2459. (Pubitemid 352844610)
5. Bagnall, D.J. (1992). Control of flowering in Arabidopsis thaliana by light, vernalisation and gibberellins. Aust. J. Plant Physiol. 19: 401-409.
6. Beers, E.P., Jones, A.M., and Dickerman, A.W. (2004). The S8 serine, C1A cysteine and A1 aspartic protease families in Arabidopsis. Phytochemistry 65: 43-58. (Pubitemid 38155891)
7. Beers, E.P., Woffenden, B.J., and Zhao, C. (2000). Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol. Biol. 44: 399-415. (Pubitemid 32139553)
8. Breitling, R., Armengaud, P., Amtmann, A., and Herzyk, P. (2004). Rank products: A simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 573: 83-92. (Pubitemid 39141040)
9. Bubert, H., Lambert, J., Steuernagel, S., Ahlers, F., and Wiermann, R. (2002). Continuous decomposition of sporopollenin from pollen of Typha angustifolia L. by acidic methanolysis. Z. Naturforsch. [C] 57: 1035-1041. (Pubitemid 36137348)
10. Cao, D., Cheng, H., Wu, W., Soo, H.M., and Peng, J. (2006). Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol. 142: 509-525. (Pubitemid 44583123)
11. Chandler, P.M., Marion-Poll, A., Ellis, M., and Gubler, F. (2002). Mutants at the Slender1 locus of barley cv Himalaya: Molecular and physiological characterization. Plant Physiol. 129: 181-190. (Pubitemid 34527318)
12. Cheng, H., Qin, L., Lee, S., Fu, X., Richards, D.E., Cao, D., Luo, D., Harberd, N.P., and Peng, J. (2004). Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131: 1055-1064. (Pubitemid 38380459)
13. Chhun, T., Aya, K., Asano, K., Yamamoto, E., Morinaka, Y., Watanabe, M., Kitano, H., Ashikari, M., Matsuoka, M., and Ueguchi-Tanaka, M. (2007). Gibberellin regulates pollen viability and pollen tube growth in rice. Plant Cell 19: 3876-3888. (Pubitemid 351253108)
14. Cleveland, W. (1979). Robust locally weighted regression and smoothing scatter plots. J. Am. Stat. Assoc. 74: 829-836.
15. de Lucas, M., Davière, J.M., Rodríguez-Falcó n, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blá zquez, M.A., Titarenko, E., and Prat, S. (2008). A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480-484. (Pubitemid 351158891)
16. Dill, A., Thomas, S.G., Hu, J., Steber, C.M., and Sun, T.-P. (2004). The Arabidopsis F-box protein SLEEPY1 targets GA signaling repressors for GA-induced degradation. Plant Cell 16: 1392-1405. (Pubitemid 38774237)
17. Edlund, A.F., Swanson, R., and Preuss, D. (2004). Pollen and stigma structure and function: The role of diversity in pollination. Plant Cell 16 (suppl.): S84-S97. (Pubitemid 38774219)
18. Feng, S., et al. (2008). Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475-479. (Pubitemid 351158880)
19. Fleet, C.M., and Sun, T.-P. (2005). A DELLAcate balance: The role of gibberellin in plant morphogenesis. Curr. Opin. Plant Biol. 8: 77-85.
20. SLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16: 1406-1418. (Pubitemid 38774238)
21. Gentleman, R.C., et al. (2004). Bioconductor: Open software development forcomputational biology and bioinformatics.GenomeBiol. 5:R80.
22. Goto, N., and Pharis, R.P. (1999). Role of gibberellin in the development of floral organs of the gibberellin-deficient mutant, ga1-1, of Arabidopsis thaliana. Can. J. Bot. 77: 944-954. (Pubitemid 30233673)
23. Griffiths, J., Murase, K., Rieu, I., Zentella, R., Zhang, Z.L., Powers, S.J., Gong, F., Phillips, A.L., Hedden, P., Sun, T.-P., and Thomas, S.G. (2006). Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399-3414. (Pubitemid 46464901)
24. Gubler, F., Kalla, R., Roberts, J.K., and Jacobsen, J.V. (1995). Gibberellin-regulated expression of a myb gene in barley aleurone cells: Evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. Plant Cell 7: 1879-1891. (Pubitemid 3019808)
25. Gubler, F., Raventos, D., Keys, M., Watts, R., Mundy, J., and Jacobsen, J.V. (1999). Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J. 17: 1-9. (Pubitemid 129517860)
26. Hara-Nishimura, I., Takeuchi, Y., and Nishimura, M. (1993). Molecular characterization of a vacuolar processing enzyme related to a putative cysteine proteinase of Schistosoma mansoni. Plant Cell 5: 1651-1659. (Pubitemid 2021817)
27. Hiei, Y., Ohta, S., Komari, T., and Kumashiro, T. (1994). Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6: 271-282. (Pubitemid 2120909)
28. Hong, F., Breitling, R., McEntee, C.W., Wittner, B.S., Nemhauser, J.L., and Chory, J. (2006). RankProd: A bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22: 2825-2827. (Pubitemid 44742407)
29. Huysmans, S., El-Ghazaly, G., and Smets, E. (1998). Orbicules in angiosperms: Morphology, function, distribution, and relation with tapetum types. Bot. Rev. 64: 240-272. (Pubitemid 128440906)
30. Ikeda, A., Ueguchi-Tanaka, M., Sonoda, Y., Kitano, H., Koshioka, M., Koshioka, M., Futsuhara, Y., Matsuoka, M., and Yamaguchi, J. (2001). slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the heightregulating gene GAI/RGA/RHT/D8. Plant Cell 13: 999-1010. (Pubitemid 32480637)
31. Itoh, J., Nonomura, K., Ikeda, K., Yamaki, S., Inukai, Y., Yamagishi, H., Kitano, H., and Nagato, Y. (2005). Rice plant development: from zygote to spikelet. Plant Cell Physiol. 46: 23-47. (Pubitemid 40307199)
32. Itoh, H., Ueguchi-Tanaka, M., Sato, Y., Ashikari, M., and Matsuoka, M. (2002). The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14: 57-70. (Pubitemid 34140398)
33. Izhaki, A., Borochov, A., Zamski, E., and Weiss, D. (2002). Gibberellin regulates post-microsporogenesis processes in petunia anthers. Physiol. Plant. 115: 442-447. (Pubitemid 34776003)
34. Jacobsen, S.E., and Olszewski, N.E. (1991). Characterization of the arrest in anther development associated with gibberellin deficiency of the gib-1 mutant of tomato. Plant Physiol. 97: 409-414.
35. Jung, K.H., Han, M.J., Lee, D.Y., Lee, Y.S., Schreiber, L., Franke, R., Faust, A., Yephremov, A., Saedler, H., Kim, Y.W., Hwang, I., and 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: 3015-3032. (Pubitemid 46013273)
36. Kaneko, M., Inukai, Y., Ueguchi-Tanaka, M., Itoh, H., Izawa, T., Kobayashi, Y., Hattori, T., Miyao, A., Hirochika, H., Ashikari, M., and Matsuoka, M. (2004). Loss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development. Plant Cell 16: 33-44. (Pubitemid 38162352)
37. King, R.W., and Evans, L.T. (2003). Gibberellins and flowering of grasses and cereals: Prizing open the lid of the "florigen" black box. Annu. Rev. Plant Biol. 54: 307-328.
38. Koornneef, M., and van der Veen, J.H. (1980). Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.). Theor. Appl. Genet. 58: 257-263.
39. Ku, S., Yoon, H., Suh, H.S., and Chung, Y.Y. (2003). Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum. Planta 217: 559-565. (Pubitemid 37056758)
40. Langridge, J. (1957). Effect of day-length and gibberellic acid on the flowering of Arabidopsis. Nature 180: 36-37.
41. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., and Thompson, J.D. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. (Pubitemid 350162903)
42. Li, N., et al. (2006). The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18: 2999-3014. (Pubitemid 46013272)
43. McGinnis, K.M., Thomas, S.G., Soule, F.D., Strader, L.C., Zale, J.M., Sun, T.-P., and Steber, C.M. (2003). The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15: 1120-1130.
44. Millar, A.A., and Gubler, F. (2005). The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17: 705-721. (Pubitemid 43138215)
45. Morant, M., Jørgensen, K., Schaller, H., Pinot, F., Møller, B.L., Werck-Reichhart, D., and Bak, S. (2007). CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell 19: 1473-1487. (Pubitemid 47025371)
46. Murray, F., Kalla, R., Jacobsen, J., and Gubler, F. (2003). A role for HvGAMYB in anther development. Plant J. 33: 481-491. (Pubitemid 36251189)
47. Nakajima, M., et al. (2006). Identification and characterization of Arabidopsis gibberellin receptors. Plant J. 46: 880-889. (Pubitemid 43780632)
48. Nester, J.E., and Zeevaart, J.A.D. (1988). Flower development innormal tomato and a gibberellin-deficient (ga-2) mutant. Am. J.Bot. 75: 45-55.
49. Peng, J., Carol, P., Richards, D.E., King, K.E., Cowling, R.J., Murphy, G.P., and Harberd, N.P. (1997). The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 11: 3194-3205. (Pubitemid 27528059)
50. Peng, J., Richards, D.E., Hartley, N.M., Murphy, G.P., Devos, K.M., Flintham, J.E., Beales, J., Fish, L.J., Worland, A.J., Pelica, F., Sudhakar, D., and Christou, P. (1999). 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400: 256-261.
51. Pharis, R.P., and King, R.W. (1985). Gibberellins and reproductive development in seed plants. Annu. Rev. Plant Physiol. 36: 517-568.
52. Piffanelli, P., Ross, J.H.E., and Murphy, D.J. (1998). Biogenesis and function of the lipidic structures of pollen grains. Sex. Plant Reprod. 11: 65-80. (Pubitemid 28278548)
53. Sakamoto, T., Miura, K., Itoh, H., Tatsumi, T., Ueguchi-Tanaka, M., Ishiyama, K., Kobayashi, M., Agrawal, G.K., Takeda, S., Abe, K., Miyao, A., and Hirochika, H. (2004). An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol. 134: 1642-1653. (Pubitemid 38527372)
54. Sasaki, A., Itoh, H., Gomi, K., Ueguchi-Tanaka, M., Ishiyama, K., Kobayashi, M., Jeong, D.H., An, G., Kitano, H., Ashikari, M., and Matsuoka, M. (2003). Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299: 1896-1898. (Pubitemid 36356658)
55. Silverstone, A.L., Ciampaglio, C.N., and Sun, T.-P. (1998). The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10: 155-169.
56. Singh, D.P., Jermakow, A.M., and Swain, S.M. (2002). Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell 14: 3133-3147.
57. Sun, T.-P., and Kamiya, Y. (1994). The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. Plant Cell 6: 1509-1518. (Pubitemid 24976505)
58. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599. (Pubitemid 47236692)
59. Thornsberry, J.M., Goodman, M.M., Doebley, J., Kresovich, S., Nielsen, D., and Buckler IV, E.S. (2001). Dwarf8 polymorphisms associate with variation in flowering time. Nat. Genet. 28: 286-289. (Pubitemid 32626034)
60. Toomey, R.E., and Wakil, S.J. (1966). Studies on the mechanism of fatty acid synthesis XV. Preparation and general properties of b-ketoacyl acyl carrier protein reductase from Escherichia coli. Biochim. Biophys. Acta 116: 189-197.
61. Tsuji, H., Aya, K., Ueguchi-Tanaka, M., Shimada, Y., Nakazono, M., Watanabe, R., Nishizawa, N.K., Gomi, K., Shimada, A., Kitano, H., Ashikari, M., and Matsuoka, M. (2006). GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J. 47: 427-444. (Pubitemid 44036411)
62. Ueguchi-Tanaka, M., Ashikari, M., Nakajima, M., Itoh, H., Katoh, E., Kobayashi, M., Chow, T.-Y., Hsing, Y.C., Kitano, H., Yamaguchi, I., and Matsuoka, M. (2005). GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693-698. (Pubitemid 41486533)
63. Ueguchi-Tanaka, M., Hirano, K., Hasegawa, Y., Kitano, H., and Matsuoka, M. (2008). Release of the repressive activity of rice DELLA protein SLR1 by gibberellin does not require SLR1 degradation in the gid2 mutant. Plant Cell 20: 2437-2446. (Pubitemid 352844609)
64. Ueguchi-Tanaka, M., Nakajima, M., Ashikari, M., and Matsuoka, M. (2007a). Gibberellin receptor and its role in gibberellin signaling in plants. Annu. Rev. Plant Biol. 58: 183-198. (Pubitemid 46986322)
65. Ueguchi-Tanaka, M., Nakajima, M., Katoh, E., Ohmiya, H., Asano, K., Saji, S., Hongyu, X., Ashikari, M., Kitano, H., Yamaguchi, I., and Matsuoka, M. (2007b). Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19: 2140-2155. (Pubitemid 47347458)
66. Viti, R., Bartolini, S., and Vitagliano, C. (1990). Growth regulators on pollen germination in olive. Acta Hortic. 286: 227-230.
67. Wang, A., Xia, Q., Xie, W., Datla, R., and Selvaraj, G. (2003). The classical Ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development. Proc. Natl. Acad. Sci. USA 100: 14487-14492. (Pubitemid 37499263)
68. Wijeratne, A.J., Zhang, W., Sun, Y., Liu, W., Albert, R., Zheng, Z., Oppenheimer, D.G., Zhao, D., and Ma, H. (2007). Differential gene expression in Arabidopsis wild-type and mutant anthers: Insights into anther cell differentiation and regulatory networks. Plant J. 52: 14-29. (Pubitemid 47476165)
69. Willige, B.C., Ghosh, S., Nill, C., Zourelidou, M., Dohmann, E.M., Maier, A., and Schwechheimer, C. (2007). The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19: 1209-1220. (Pubitemid 46941649)
70. Wilson, R., Heckman, J.W., and Somerville, C. (1992). Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol. 100: 403-408.
71. Yui, R., Iketani, S., Mikami, T., and Kubo, T. (2003). Antisense inhibition of mitochondrial pyruvate dehydrogenase E1a subunit in anther tapetum causes male sterility. Plant J. 34: 57-66. (Pubitemid 36524307)