Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function

Development

Volumn 131, Issue 5, 2004, Pages 1055-1064

  Cheng, Hui ^a,b   Qin, Lianju ^c   Lee, Sorcheng ^a   Fu, Xiangdong ^a   Richards, Donald E ^d   Cao, Dongni ^a   Luo, Da ^c   Harberd, Nicholas P ^d   Peng, Jinrong ^a,b  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^d JOHN INNES CENTRE   (United Kingdom)

Author keywords

DELLA proteins; Floral development; Gibberellin; Stamen development

Indexed keywords

ARABIDOPSIS PROTEIN; GIBBERELLIN; PHYTOHORMONE; PROTEIN DELLA; UNCLASSIFIED DRUG;

ANTHER; ARABIDOPSIS; CELL DIVISION; CELL ELONGATION; CELL MATURATION; CONTROLLED STUDY; GENETIC ANALYSIS; GRAIN; MICROSPORE; NONHUMAN; PETAL; PLANT DEVELOPMENT; POLLEN DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FAMILY; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; STAMEN;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; GENES, PLANT; GIBBERELLINS; MICROSCOPY, ELECTRON, SCANNING; MITOSIS; MUTATION; PHENOTYPE; PLANT GROWTH REGULATORS; PLANT PROTEINS; POLLEN; RAL GUANINE NUCLEOTIDE EXCHANGE FACTOR; TRANSCRIPTION FACTORS;

ARABIDOPSIS;

EID: 1642408616     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00992     Document Type: Review

References (52)

1. Azumi, Y., Liu, D., Zhao, D. Z., Li, W., Wang, G. F., Hu, Y. and Ma, H. (2002). Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein. EMBO J. 21, 3081-3095.
2. Boss, P. K. and Thomas, M. R. (2002). Association of dwarfism and floral induction with a grape 'green revolution' mutation. Nature 416, 847-850.
3. Bowman, J. (1994). Arabidopsis: An Atlas of Morphology and Development. New York: Springer-Verlag.
4. Bozzola, J. J. and Russell, L. D. (1999). In Electron Microscopy: Principles and Techniques for Biologists, pp. 50-71. Sudbury, MA: John and Bartlett.
5. Chandler, P. M., Marion-Poll, A., Ellis, M. and Gubler, F. (2002). Mutants at the Slender1 locus of 'Himalaya' barley: Molecular and physiological characterization. Plant Physiol. 129, 181-190.
6. Chen, Y. S. and McCormick, S. (1996). Sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development. Development 122, 3243-3252.
7. Dill, A. and Sun, T.-p. (2001). Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159, 777-785.
8. Fleck, B. and Harberd, N. P. (2002). Evidence that the Arabidopsis nuclear gibberellin signaling protein GAI is not destabilized by gibberellin. Plant J. 32, 935-947.
9. Fu, X., Richards, D. E., Ait-Ali, T., Hynes, L. W., Ougham, H., Peng, J. R. and Harberd, N. P. (2002). Gibberellin-Mediated Proteasome-Dependent Degradation of the Barley DELLA Protein SLN1 Repressor. Plant Cell 14, 3191-3200.
10. Fu, X. and Harberd, N. P. (2003). Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421, 740-743.
11. Goldberg, R. B., Beals, T. P. and Sanders, P. M. (1993). Anther development: Basic principle and practical applications. Plant Cell 5, 1217-1229.
12. 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.
13. Gubler, F., Chandler, P., White, R., Llewellyn, D. and Jacobsen, J. (2002). GA signalling in barley aleurone cells: Control of SLN1 and GAMYB expression. Plant Physiol. 129, 191-200.
14. Harberd, N. P. (2003). Relieving DELLA restraint. Science 299, 1853-1854.
15. Huang, S., Cerny, R. E., Qi, Y. L., Bhat, D., Aydt, C. M., Hanson, D. D., Malloy, K. P. and Ness, L. A. (2003). Transgenic studies on the involvement of cytokinin and gibberellin in male development. Plant Physiol. 131, 1270-1282.
16. Hynes, L. W., Peng, J., Richards, D. E. and Harberd, N. P. (2003). Transgenic expression of the Arabidopsis DELLA proteins GAI and gai confers altered gibberellin response in tobacco. Transgenic Res. 12, 707-714.
17. Ikeda, A., Ueguchi-Tanaka, M., Sonoda, Y., Kitano, H., 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 height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13, 999-1010.
18. 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.
19. Izhaki, A., Borochov, A., Zamski, E. and Weiss, D. (2002). Gibberellin regulates post-microsporogenesis processes in petunia anthers. Physiol. Plant. 115, 442-447.
20. 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.
21. Jacobsen, S. E., Binkowski, K. A. and Olszewski, N. E. (1996). SPINDLY, a tetratricopetide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc. Natl. Acad. Sci. USA 93, 9292-9296.
22. King, K. E., Moritz, T. and Harberd, N. P. (2001). Gibberellins are not required for stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159, 767-776.
23. Koornneef, M. and van der Veen, J. H. (1980). Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh. Theor. Appl. Genet. 58, 257-263.
24. Lee, S. C., Cheng, H., King, K. E., Wang, W., He, Y., Hussain, A., Lo, J., Harberd, N. P. and Peng, J. R. (2002). Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev. 16, 646-658.
25. Luo, D., Carpenter, R., Vincent, C., Copsey, L. and Coen, E. (1996). Origin of floral asymmetry in Antirrhinum. Nature 383, 794-799.
26. McCormick, S. (1993). Male gametophyte development. Plant Cell 5, 1265-1275.
27. McGinnis, K. M., Thomas, S. G., Soule, J. D., Strader, L. C., Zale, J. M., Sun, T. P. and Steber, C. M. (2003). The Arabidopsis SLEEPY gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15, 1120-1130.
28. Nester, J. E. and Zeevaart, J. A. D. (1988). Flower development in normal tomato and a gibberellin-deficient (ga-2) mutant. Am. J. Bot. 75, 45-55.
29. Park, S. K. and Twell, D. (2001). Novel patterns of ectopic cell plate growth and lipid body distribution in the Arabidopsis Gemini pollens mutant. Plant Physiol. 126, 899-909.
30. Peng, J. R., 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.
31. Peng, J. R. and Harberd, N. P. (1997). Gibberellin deficiency and response mutations suppress the stem elongation phenotype of phytochrome-deficient mutants of Arabidopsis. Plant Physiol. 113, 1051-1058.
32. Peng, J. R., 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. et al. (1999). 'Green Revolution' genes encode mutant gibberellin response modulators. Nature 400, 256-261.
33. Peng, J. R., Richards, D. E., Moritz, T., Ezura, H., Carol, P. and Harberd, N. P. (2002). Molecular and physiological characterization of Arabidopsis GAI alleles obtained in targeted Ds-tagging experiments. Planta 214, 591-596.
34. Pharis, R. P. and King, R. W. (1985). Gibberellins and reproductive development in seed plants. Annu. Rev. Plant Physiol. 36, 517-568.
35. Preuss, D., Lemieux, B., Yen, G. and Davis, R. W. (1993). A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes Dev. 7, 974-985.
36. Pysh, L. D., Wysocka-Diller, J. W., Camilleri, C., Bouchez, D. and Benfey, P. N. (1999). The GRAS family in Arabidopsis: Sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J. 18, 111-119.
37. Regan, S. M. and Moffatt, B. A. (1990). Cytochemical analysis of pollen development in wild-type Aarabidopsis and a male-sterile mutant. Plant Cell 2, 877-889.
38. Richards, D. E., Peng, J. and Harberd, N. P. (2000). Plant GRAS and metazoan STATs: One family? BioEssays 22, 573-577.
39. Richards, D. E., King, K. E., Ait-ali, T. and Harberd, N. P. (2001). How gibberellin regulates plant growth and development: A molecular genetic analysis of gibberellin signaling. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 67-88.
40. Ross, K. J., Fransz, P. and Jones, G. H. (1996). A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res. 4, 507-516.
41. Rubinelli, P., Hu, Y. and Ma, H. (1998). Identification, sequence analysis and expression studies of novel anther-specific genes of Arabidopsis thaliana. Plant Mol. Biol. 37, 607-619.
42. Sanders, P. M., Bui, A. Q., Weterings, K., McIntire, K. N., Hsu, Y. C., Lee, P. Y., Truong, M. T., Beals, T. P. and Goldberg, R. B. (1999). Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11, 297-322.
43. Sasaki, A., Itoh, H., Gomi, K., Ueguchi-Tanaka, M., Ishiyama, K., Kobayashi, M., Jeong, D. H., An, G., Kiitano, H., Ashikari, M. and Matsuoka, M. (2003). Accumulation of phosphorylated repressors for gibberellin signaling in an F-box mutant. Science 299, 1896-1898.
44. 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.
45. Silverstone, A. L., Jung, H.-S., Dill, A., Kawaide, H., Kamiya, Y. and Sun, T.-p. (2001). Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13, 1555-1565.
46. Simpson, G. G. and Dean, C. (2002). Arabidopsis, the Rosetta stone of flowering time? Science 296, 285-289.
47. Smyth, D. R., Bowman, J. L. and Meyerowitz, E. M. (1990). Early flower development in Arabidopsis. Plant Cell 2, 755-767.
48. Steiner-Lange, S., Unte, U. S., Eckstein, L., Yang, C., Wilson, Z. A., Schmelzer, E., Dekker, K. and Saedler, H. (2003). Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant J. 34, 519-528.
49. Unte, U. S., Sorensen, A. M., Pesaresi, P., Gandikota, M., Leister, D., Saedler, H. and Huijser, P. (2003). SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15, 1009-1019.
50. Wen, C. K. and Chang, C. (2002). Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14, 87-100.
51. 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.
52. Zhao, D. Z., Wang, G. F., Speal, B. and 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, 2021-2031.