Lifting DELLA repression of arabidopsis seed germination by nonproteolytic gibberellin signaling

Plant Physiology

Volumn 162, Issue 4, 2013, Pages 2125-2139

  Steber, Camille M ^a   Ariizumi, Tohru ^a,c   Hauvermale, Amber L ^a   Nelson, Sven K ^a   Hanada, Atsushi ^b   Yamaguchi, Shinjiro ^b  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b TOHOKU UNIVERSITY   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ABSCISIC ACID; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; CELL SURFACE RECEPTOR; GAI PROTEIN, ARABIDOPSIS; GIBBERELLIN; GID1A PROTEIN, ARABIDOPSIS; XERICO PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; DORMANCY; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; METABOLISM; MUTATION; PHYSIOLOGY; PLANT; PLANT SEED; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GERMINATION; GIBBERELLINS; MUTATION; PLANT DORMANCY; PLANT SHOOTS; RECEPTORS, CELL SURFACE; SEEDS; SIGNAL TRANSDUCTION;

EID: 84880992864     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.219451     Document Type: Article

References (64)

1. Ariizumi T, Lawrence PK, Steber CM (2011) The role of two F-box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signaling. Plant Physiol 155: 765-775
2. Ariizumi T, Murase K, Sun T-P, Steber CM (2008) Proteolysis-independent downregulation of DELLA repression in Arabidopsis by the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1. Plant Cell 20: 2447-2459
3. Ariizumi T, Steber CM (2007) Seed germination of GA-insensitive sleepy1 mutants does not require RGL2 protein disappearance in Arabidopsis. Plant Cell 19: 791-804
4. Barrero JM, Talbot MJ, White RG, Jacobsen JV, Gubler F (2009) Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol 150: 1006-1021
5. Bewley DJ, Black M (1994). Seeds: Physiology of Development and Germination. Plenum Press, New York
6. Cao D, Cheng H, Wu W, Soo HM, Peng J (2006) Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol 142: 509-525
7. Cao D, Hussain A, Cheng H, Peng J (2005) Loss of function of four DELLA genes leads to light-and gibberellin-independent seed germination in Arabidopsis. Planta 223: 105-113
8. Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131: 1055-1064
9. de Lucas M, Davière J-M, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480-484
10. Dill A, Sun T-P (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159: 777-785
11. Dill A, Thomas SG, Hu J, Steber CM, Sun T-P (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellininduced degradation. Plant Cell 16: 1392-1405
12. Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S, et al (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475-479
13. Finch-Savage WE, Cadman CSC, Toorop PE, Lynn JR, Hilhorst HWM (2007) Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. Plant J 51: 60-78
14. Finkelstein RR, Reeves W, Ariizumi T, Steber CM (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59: 387-415
15. SLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16: 1406-1418
16. Gallego-Bartolomé J, Alabadí D, Blázquez MA (2011) DELLA-induced early transcriptional changes during etiolated development in Arabidopsis thaliana. PLoS ONE 6: e23918
17. Gallego-Bartolomé J, Minguet EG, Marín JA, Prat S, Blázquez MA, Alabadí D (2010) Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Mol Biol Evol 27: 1247-1256
18. Graeber K, Linkies A, Wood ATA, Leubner-Metzger G (2011) A guideline to family-wide comparative state-of-the-art quantitative RT-PCR analysis exemplified with a Brassicaceae cross-species seed germination case study. Plant Cell 23: 2045-2063
19. Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z-L, Powers SJ, Gong F, Phillips AL, Hedden P, Sun T-P, et al (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399-3414
20. Herzog M, Dorne AM, Grellet F (1995) GASA, a gibberellin-regulated gene family from Arabidopsis thaliana related to the tomato GAST1 gene. Plant Mol Biol 27: 743-752
21. Hirano K, Asano K, Tsuji H, Kawamura M, Mori H, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2010) Characterization of the molecular mechanism underlying gibberellin perception complex formation in rice. Plant Cell 22: 2680-2696
22. Hirano K, Kouketu E, Katoh H, Aya K, Ueguchi-Tanaka M, Matsuoka M (2012) The suppressive function of the rice DELLA protein SLR1 is dependent on its transcriptional activation activity. Plant J 71: 443-453
23. Hussain A, Cao D, Cheng H, Wen Z, Peng J (2005) Identification of the conserved serine/threonine residues important for gibberellinsensitivity of Arabidopsis RGL2 protein. Plant J 44: 88-99
24. Iuchi S, Suzuki H, Kim Y-C, Iuchi A, Kuromori T, Ueguchi-Tanaka M, Asami T, Yamaguchi I, Matsuoka M, Kobayashi M, et al (2007) Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J 50: 958-966
25. Jacobsen JV, PearceDW, Poole AT, Pharis RP, Mander LN(2002) Abscisic acid, phaseic acid and gibberellin contents associated with dormancy and germination in barley. Physiol Plant 115: 428-441
26. Karssen CM, der Brinkhorst-van Swan DLC, Breekland AE, Koornneef M (1983) Induction of dormancy during seed development by endogenous abscisic acid: studies in abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. Planta 157: 158-165
27. Karssen CM, Laçka E (1986). A revision of the hormone balance theory of seed dormancy: studies on gibberellin and/or abscisic acid-deficient mutants of Arabidopsis thaliana. In M Bopp, ed, Plant Growth Substances 1985: Proceedings of the 12th International Conference on Plant Growth Substances. Springer-Verlag, New York, pp 315-323
28. Karssen CM, Zagorski S, Kepczynski J, Groot SPC (1989) Key role for endogenous gibberellins in the control of seed germination. Ann Bot (Lond) 63: 71-80
29. Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47: 343-355
30. Koornneef M, Jorna ML, der Brinkhorst-van Swan DLC, Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 61: 385-393
31. Koornneef M, van der Veen JH (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 58: 257-263
32. Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd NP, 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
33. Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45: 309-319
34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) method. Methods 25: 402-408
35. Martin RC, Liu P-P, Nonogaki H (2005) Simple purification of small RNAs from seeds and efficient detection of multiple microRNAs expressed in Arabidopsis thaliana and tomato (Lycopersicon esculentum) seeds. Seed Sci Res 15: 319-328
36. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun T-P, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15: 1120-1130
37. Murase K, Hirano Y, Sun T-P, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456: 459-463
38. Nakajima M, Shimada A, Takashi Y, Kim Y-C, Park S-H, Ueguchi-Tanaka M, Suzuki H, Katoh E, Iuchi S, Kobayashi M, et al (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46: 880-889
39. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15: 1591-1604
40. Oh E, Yamaguchi S, Hu J, Yusuke J, Jung B, Paik I, Lee H-S, Sun T-P, Kamiya Y, Choi G (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19: 1192-1208
41. Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode abscisic acid 89-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141: 97-107
42. Oñate-Sánchez L, Vicente-Carbajosa J (2008) DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques. BMC Res Notes 1: 93
43. Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, Lopez-Molina L (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20: 2729-2745
44. Piskurewicz U, Lopez-Molina L (2009) The GA-signaling repressor RGL3 represses testa rupture in response to changes in GA and ABA levels. Plant Signal Behav 4: 63-65
45. R Development Core Team (2010). R: A Language and Environment for Statistical Computing. http://www.R-project.org/ (February 3, 2012)
46. Shimada A, Ueguchi-Tanaka M, Nakatsu T, Nakajima M, Naoe Y, Ohmiya H, Kato H, Matsuoka M (2008) Structural basis for gibberellin recognition by its receptor GID1. Nature 456: 520-523
47. Silverstone AL, Jung HS, Dill A, Kawaide H, Kamiya Y, Sun TP (2001) Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13: 1555-1566
48. Steber CM, Cooney SE, McCourt P (1998) Isolation of the GA-response mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana. Genetics 149: 509-521
49. Steber CM, McCourt P (2001) A role for brassinosteroids in germination in Arabidopsis. Plant Physiol 125: 763-769
50. Sun T-P, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55: 197-223
51. Suzuki H, Park S-H, Okubo K, Kitamura J, Ueguchi-Tanaka M, Iuchi S, Katoh E, Kobayashi M, Yamaguchi I, Matsuoka M, et al (2009) Differential expression and affinities of Arabidopsis gibberellin receptors can explain variation in phenotypes of multiple knock-out mutants. Plant J 60: 48-55
52. Talon M, Koornneef M, Zeevaart JAD (1990) Accumulation of C19-gibberellins in the gibberellin-insensitive dwarf mutant gai of Arabidopsis thaliana (L.) Heynh. Planta 182: 501-505
53. Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun T-P (2004) Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135: 1008-1019
54. Ueguchi-Tanaka M, Hirano K, Hasegawa Y, Kitano H, 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
55. Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Hongyu X, Ashikari M, Kitano H, Yamaguchi I, et al (2007) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19: 2140-2155
56. Varbanova M, Yamaguchi S, Yang Y, McKelvey K, Hanada A, Borochov R, Yu F, Jikumaru Y, Ross J, Cortes D, et al (2007) Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell 19: 32-45
57. Voegele A, Linkies A, Müller K, Leubner-Metzger G (2011) Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp Bot 62: 5131-5147
58. Wang F, Zhu D, Huang X, Li S, Gong Y, Yao Q, Fu X, Fan L-M, Deng XW (2009) Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21: 2378-2390
59. Wang X, Kang D, Feng S, Serino G, Schwechheimer C, Wei N (2002) CSN1 N-terminal-dependent activity is required for Arabidopsis development but not for Rub1/Nedd8 deconjugation of cullins: a structurefunction study of CSN1 subunit of COP9 signalosome. Mol Biol Cell 13: 646-655
60. Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EMN, Maier A, Schwechheimer C (2007) The DELLA domain of GA INSENSITIVEmediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19: 1209-1220
61. Yamamoto Y, Hirai T, Yamamoto E, Kawamura M, Sato T, Kitano H, Matsuoka M, Ueguchi-Tanaka M (2010) A rice gid1 suppressor mutant reveals that gibberellin is not always required for interaction between its receptor, GID1, and DELLA proteins. Plant Cell 22: 3589-3602
62. Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16: 367-378
63. Yamauchi Y, Takeda-Kamiya N, Hanada A, Ogawa M, Kuwahara A, Seo M, Kamiya Y, Yamaguchi S (2007) Contribution of gibberellin deactivation by AtGA2ox2 to the suppression of germination of dark-imbibed Arabidopsis thaliana seeds. Plant Cell Physiol 48: 555-561
64. Zentella R, Zhang Z-L, ParkM, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, et al (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19: 3037-3057