Fruit growth in Arabidopsis occurs via DELLA-dependent and DELLA-independent gibberellin responses

Plant Cell

Volumn 24, Issue 10, 2012, Pages 3982-3996

  Fuentes, Sara ^a,d   Ljung, Karin ^b   Sorefan, Karim ^a,e   Alvey, Elizabeth ^a,f   Harber, Nicholas P ^c   Østergaard, Lars ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b Umea Plant Science Center   (Sweden)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84870683131     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.103192     Document Type: Article

References (89)

1. Achard, P., and Genschik, P. (2009). Releasing the brakes of plant growth: How GAs shutdown DELLA proteins. J. Exp. Bot. 60: 1085-1092.
2. Achard, P., Gusti, A., Cheminant, S., Alioua, M., Dhondt, S., Coppens, F., Beemster, G.T., and Genschik, P. (2009). Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr. Biol. 19: 1188-1193.
3. Alvarez, J., and Smyth, D.R. (1999). CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126: 2377-2386.
4. Alvarez, J., and Smyth, D.R. (2002). CRABS CLAW and SPATULA genes regulate growth and pattern formation during gynoecium development in Arabidopsis thaliana. Int. J. Plant Sci. 163: 17-41.
5. Ariizumi, T., Murase, K., Sun, T.P., and Steber, C.M. (2008). Proteolysisindependent downregulation of DELLA repression in Arabidopsis by the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1. Plant Cell 20: 2447-2459.
6. Arnaud, N., Girin, T., Sorefan, K., Fuentes, S., Wood, T.A., Lawrenson, T., Sablowski, R., and Østergaard, L. (2010). Gibberellins control fruit patterning in Arabidopsis thaliana. Genes Dev. 24: 2127-2132.
7. Bolle, C. (2004). The role of GRAS proteins in plant signal transduction and development. Planta 218: 683-692.
8. Cao, D., Hussain, A., Cheng, H., and Peng, J. (2005). Loss of function of four DELLA genes leads to light-and gibberellin-independent seed germination in Arabidopsis. Planta 223: 105-113.
9. Carbonell-Bejerano, P., Urbez, C., Carbonell, J.J., Granell, A., and Perez-Amador, M.A. (2010). A fertilization-independent developmental program triggers partial fruit development and senescence processes in pistils of Arabidopsis. Plant Physiol. 154: 163-172.
10. 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.
11. 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.
12. Chiang, H.H., Hwang, I., and Goodman, H.M. (1995). Isolation of the Arabidopsis GA4 locus. Plant Cell 7: 195-201.
13. Cox, C.M., and Swain, S.M. (2006). Goldacre paper. Localised and non-localised promotion of fruit development in Arabidopsis. Funct. Plant Biol. 33: 1-8.
14. Davidonis, G.H. (1990). Gibberellic acid-induced cell elongation in cotton suspension-cultures. J. Plant Growth Regul. 9: 243-246.
15. de Lucas, M., Davière, J.M., Rodríguez-Falcón, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blázquez, M.A., Titarenko, E., and Prat, S. (2008). A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480-484.
16. Del Pozo, J.C., and Estelle, M. (2000). F-box proteins and protein degradation: An emerging theme in cellular regulation. Plant Mol. Biol. 44: 123-128.
17. 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.
18. Dill, A., Thomas, S.G., Hu, J., Steber, C.M., and Sun, T.P. (2004). The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16: 1392-1405.
19. Dorcey, E., Urbez, C., Blázquez, M.A., Carbonell, J., and Perez-Amador, M.A. (2009). Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J. 58: 318-332.
20. Feng, S., et al. (2008). Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475-479.
21. Ficcadenti, N., Sestili, S., Pandolfini, T., Cirillo, C., Rotino, G.L., and Spena, A. (1999). Genetic engineering of parthenocarpic fruit development in tomato. Mol. Breed. 5: 463-470.
22. Fu, X., Richards, D.E., Ait-Ali, T., Hynes, L.W., Ougham, H., Peng, J., and Harberd, N.P. (2002). Gibberellin-mediated proteasomedependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14: 3191-3200.
23. Fu, X., Richards, D.E., Fleck, B., Xie, D., Burton, N., and Harberd, N.P. (2004). The Arabidopsis mutant sleepy1gar2-1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16: 1406-1418.
24. Gagne, J.M., Downes, B.P., Shiu, S.H., Durski, A.M., and Vierstra, R.D. (2002). The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc. Natl. Acad. Sci. USA 99: 11519-11524.
25. Gallego-Bartolomé, J., Minguet, E.G., Marín, J.A., Prat, S., Blázquez, M.A., and Alabadí, D. (2010). Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Mol. Biol. Evol. 27: 1247-1256.
26. Gao, X.H., Xiao, S.L., Yao, Q.F., Wang, Y.J., and Fu, X.D. (2011). An updated GA signaling 'relief of repression' regulatory model. Mol. Plant 4: 601-606.
27. Girin, T., Paicu, T., Stephenson, P., Fuentes, S., Körner, E., O'Brien, M., Sorefan, K., Wood, T.A., Balanzá, V., Ferrándiz, C., Smyth, D.R., and Østergaard, L. (2011). INDEHISCENT and SPATULA interact to specify carpel and valve margin tissue and thus promote seed dispersal in Arabidopsis. Plant Cell 23: 3641-3653.
28. Gillaspy, G., Ben-David, H., and Gruissem, W. (1993). Fruits: A developmental perspective. Plant Cell 5: 1439-1451.
29. 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.
30. Groszmann, M., Paicu, T., Alvarez, J.P., Swain, S.M., and Smyth, D.R. (2011). SPATULA and ALCATRAZ, are partially redundant, functionally diverging bHLH genes required for Arabidopsis gynoecium and fruit development. Plant J. 68: 816-829.
31. Gustafson, F.G. (1936). Inducement of fruit development by growthpromoting chemicals. Proc. Natl. Acad. Sci. USA 22: 628-636.
32. Harberd, N.P. (2003). Botany. Relieving DELLA restraint. Science 299: 1853-1854.
33. Hedden, P., and Phillips, A.L. (2000). Gibberellin metabolism: New insights revealed by the genes. Trends Plant Sci. 5: 523-530.
34. Heisler, M.G., Atkinson, A., Bylstra, Y.H., Walsh, R., and Smyth, D.R. (2001). SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein. Development 128: 1089-1098.
35. Ichihashi, Y., Horiguchi, G., Gleissberg, S., and Tsukaya, H. (2010). The bHLH transcription factor SPATULA controls final leaf size in Arabidopsis thaliana. Plant Cell Physiol. 51: 252-261.
36. Inada, S., and Shimmen, T. (2000). Regulation of elongation growth by gibberellin in root segments of Lemna minor. Plant Cell Physiol. 41: 932-939.
37. Josse, E.M., Gan, Y., Bou-Torrent, J., Stewart, K.L., Gilday, A.D., Jeffree, C.E., Vaistij, F.E., Martínez-García, J.F., Nagy, F., Graham, I.A., and Halliday, K.J. (2011). A DELLA in disguise: SPATULA restrains the growth of the developing Arabidopsis seedling. Plant Cell 23: 1337-1351.
38. King, G.N. (1947). Artificial parthenocarpy in Lycopersicum esculentum; Tissue development. Plant Physiol. 22: 572-581.
39. King, K.E., Moritz, T., and Harberd, N.P. (2001). Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159: 767-776.
40. Koini, M.A., Alvey, L., Allen, T., Tilley, C.A., Harberd, N.P., Whitelam, G.C., and Franklin, K.A. (2009). High temperaturemediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19: 408-413.
41. Lee, S., Cheng, H., King, K.E., Wang, W., He, Y., Hussain, A., Lo, J., Harberd, N.P., and Peng, J. (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.
42. Magnus, V., Ozga, J.A., Reinecke, D.M., Pierson, G.L., Larue, T.A., Cohen, J.D., and Brenner, M.L. (1997). 4-Chloroindole-3-acetic acid and indole-3-acetic acid in Pisum sativum. Phytochemistry 46: 675-681.
43. Martí, C., Orzáez, D., Ellul, P., Moreno, V., Carbonell, J., and Granell, A. (2007). Silencing of DELLA induces facultative parthenocarpy in tomato fruits. Plant J. 52: 865-876.
44. 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 SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15: 1120-1130.
45. Mezzetti, B., Landi, L., Pandolfini, T., and Spena, A. (2004). The defH9-iaaM auxin-synthesizing gene increases plant fecundity and fruit production in strawberry and raspberry. BMC Biotechnol. 4: 4.
46. Murase, K., Hirano, Y., Sun, T.P., and Hakoshima, T. (2008). Gibberellininduced DELLA recognition by the gibberellin receptor GID1. Nature 456: 459-463.
47. Nakajima, M., et al. (2006). Identification and characterization of Arabidopsis gibberellin receptors. Plant J. 46: 880-889.
48. Ngo, P., Ozga, J.A., and Reinecke, D.M. (2002). Specificity of auxin regulation of gibberellin 20-oxidase gene expression in pea pericarp. Plant Mol. Biol. 49: 439-448.
49. Oh, E., Yamaguchi, S., Hu, J., Yusuke, J., Jung, B., Paik, I., Lee, H.S., Sun, T.P., Kamiya, Y., and Choi, G. (2007). PIL5, a phytochromeinteracting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19: 1192-1208.
50. Olszewski, N., Sun, T.P., and Gubler, F. (2002). Gibberellin signaling: Biosynthesis, catabolism, and response pathways. Plant Cell 14 (Suppl): S61-S80.
51. Ozga, J.A., and Reinecke, D.M. (2003). Hormonal interactions in fruit development. J. Plant Growth Regul. 22: 73-81.
52. Ozga, J.A., Reinecke, D.M., Ayele, B.T., Ngo, P., Nadeau, C., and Wickramarathna, A.D. (2009). Developmental and hormonal regulation of gibberellin biosynthesis and catabolism in pea fruit. Plant Physiol. 150: 448-462.
53. Ozga, J.A., van Huizen, R., and Reinecke, D.M. (2002). Hormone and seed-specific regulation of pea fruit growth. Plant Physiol. 128: 1379-1389.
54. Penfield, S., Josse, E.M., Kannangara, R., Gilday, A.D., Halliday, K. J., and Graham, I.A. (2005). Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr. Biol. 15: 1998-2006.
55. 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.
56. Peng, J., 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.
57. Phillips, A.L., Ward, D.A., Uknes, S., Appleford, N.E., Lange, T., Huttly, A.K., Gaskin, P., Graebe, J.E., and Hedden, P. (1995). Isolation and expression of three gibberellin 20-oxidase cDNA clones from Arabidopsis. Plant Physiol. 108: 1049-1057.
58. Rieu, I., Eriksson, S., Powers, S.J., Gong, F., Griffiths, J., Woolley, L., Benlloch, R., Nilsson, O., Thomas, S.G., Hedden, P., and Phillips, A.L. (2008). Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20: 2420-2436.
59. Roeder, A.H.K., and Yanofsky, M.F. (2006). Fruit development in Arabidopsis. The Arabidopsis Book 4: e0075, doi/.10.1199/tab.0075
60. Ross, J.J., Reid, J.B., Murfet, I.C., and Weston, D.E. (2008). The slender phenotype of pea is deficient in DELLA proteins. Plant Signal. Behav. 3: 590-592.
61. Rotino, G.L., Perri, E., Zottini, M., Sommer, H., and Spena, A. (1997). Genetic engineering of parthenocarpic plants. Nat. Biotechnol. 15: 1398-1401.
62. Sanchez-Fernandez, R., Ardiles-Diaz, W., Van Montagu, M., Inze, D., and May, M.J. (1998). Cloning of a novel Arabidopsis thaliana RGA-like gene, a putative member of the VHIID-domain transcription factor family. J. Exp. Bot. 49: 1609-1610.
63. Santner, A., and Estelle, M. (2009). Recent advances and emerging trends in plant hormone signalling. Nature 459: 1071-1078.
64. 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.
65. Serrani, J.C., Ruiz-Rivero, O., Fos, M., and García-Martínez, J.L. (2008). Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant J. 56: 922-934.
66. Sidaway-Lee, K., Josse, E.M., Brown, A., Gan, Y., Halliday, K.J., Graham, I.A., and Penfield, S. (2010). SPATULA links daytime temperature and plant growth rate. Curr. Biol. 20: 1493-1497.
67. Silverstone, A.L., Ciampaglio, C.N., and Sun, T. (1998). The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10: 155-169.
68. 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: 1555-1566.
69. Smyth, D.R., Bowman, J.L., and Meyerowitz, E.M. (1990). Early flower development in Arabidopsis. Plant Cell 2: 755-767.
70. Sorefan, K., Girin, T., Liljegren, S.J., Ljung, K., Robles, P., Galván-Ampudia, C.S., Offringa, R., Friml, J., Yanofsky, M.F., and Østergaard, L. (2009). A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459: 583-586.
71. Srinivasan, A., and Morgan, D.G. (1996). Growth and development of the pod wall in spring rape (Brassica napus) as related to the presence of seeds and exogenous phytohormones. J. Agric. Sci. 127: 487-500.
72. Srivastava, L.M., Sawhney, V.K., and Taylor, I.E. (1975). Gibberellicacid-induced cell elongation in lettuce hypocotyls. Proc. Natl. Acad. Sci. USA 72: 1107-1111.
73. Sun, T., Goodman, H.M., and Ausubel, F.M. (1992). Cloning the Arabidopsis GA1 locus by genomic subtraction. Plant Cell 4: 119-128.
74. Sun, T.P. (2011). The molecular mechanism and evolution of the GAGID1-DELLA signaling module in plants. Curr. Biol. 21: R338-R345.
75. Talon, M., Zacarias, L., and Primo-Millo, E. (1990). Hormonal changes associated with fruit set and development in mandarins differing in their parthenocarpic ability. Plant Physiol. 79: 400-406.
76. Thomas, S.G., Phillips, A.L., and Hedden, P. (1999). Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc. Natl. Acad. Sci. USA 96: 4698-4703.
77. Tyler, L., Thomas, S.G., Hu, J., Dill, A., Alonso, J.M., Ecker, J.R., and Sun, T.P. (2004). Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol. 135: 1008-1019.
78. Ubeda-Tomás, S., Federici, F., Casimiro, I., Beemster, G.T., Bhalerao, R., Swarup, R., Doerner, P., Haseloff, J., and Bennett, M.J. (2009). Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr. Biol. 19: 1194-1199.
79. Ubeda-Tomás, S., Swarup, R., Coates, J., Swarup, K., Laplaze, L., Beemster, G.T., Hedden, P., Bhalerao, R., and Bennett, M.J. (2008). Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat. Cell Biol. 10: 625-628.
80. Ueguchi-Tanaka, M., Ashikari, M., Nakajima, M., Itoh, H., Katoh, E., Kobayashi, M., Chow, T.Y., Hsing, Y.I., Kitano, H., Yamaguchi, I., and Matsuoka, M. (2005). GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693-698.
81. Ueguchi-Tanaka, M., Nakajima, M., Katoh, E., Ohmiya, H., Asano, K., Saji, S., Hongyu, X., Ashikari, M., Kitano, H., Yamaguchi, I., and Matsuoka, M. (2007). Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19: 2140-2155.
82. van Huizen, R., Ozga, J.A., Reinecke, D.M., Twitchin, B., and Mander, L.N. (1995). Seed and 4-chloroindole-3-acetic acid regulation of gibberellin metabolism in pea pericarp. Plant Physiol. 109: 1213-1217.
83. Vivian-Smith, A., and Koltunow, A.M. (1999). Genetic analysis of growth-regulator-induced parthenocarpy in Arabidopsis. Plant Physiol. 121: 437-451.
84. Vivian-Smith, A., Luo, M., Chaudhury, A., and Koltunow, A.M. (2001). Fruit development is actively restricted in the absence of fertilization in Arabidopsis. Development 128: 2321-2331.
85. Wen, C.K., and Chang, C. (2002). Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14: 87-100.
86. 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.
87. Wittwer, S.H., Bukovac, M.J., Sell, H.M., and Weller, L.E. (1957). Some effects of gibberellin on flowering and fruit setting. Plant Physiol. 32: 39-41.
88. Xu, Y.L., Li, L., Wu, K., Peeters, A.J., Gage, D.A., and Zeevaart, J.A. (1995). The GA5 locus of Arabidopsis thaliana encodes a multifunctional gibberellin 20-oxidase: Molecular cloning and functional expression. Proc. Natl. Acad. Sci. USA 92: 6640-6644.
89. Zentella, R., Zhang, Z.L., Park, M., Thomas, S.G., Endo, A., Murase, K., Fleet, C.M., Jikumaru, Y., Nambara, E., Kamiya, Y., and Sun, T.P. (2007). Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19: 3037-3057.