Loss-of-function of DELLA protein SLN1 activates GA signaling in barley aleurone

Acta Physiologiae Plantarum

Volumn 32, Issue 4, 2010, Pages 789-800

  Chen, Kegui ^a   Tian, Shulan ^a   Yandell, Brian S ^a   Kaeppler, Shawn M ^a   An, Yong qiang Charles ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Aleurone; DELLA; Gibberellic acid; Hordeum vulgare; SLN1; Transcripts

Indexed keywords

HORDEUM; HORDEUM VULGARE;

EID: 77953870244     PISSN: 01375881     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11738-010-0464-3     Document Type: Article

References (70)

1. Achard P, Baghour M, Chapple A, Hedden P, van Der Straeten D, Genschik P, Moritz T, Harberd NP (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc Natl Acad Sci USA 104: 6484-6489. doi: 10. 1073/pnas. 0610717104.
2. 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. doi: 10. 1105/tpc. 106. 048009.
3. 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. doi: 10. 1105/tpc. 108. 058487.
4. 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: 1453-1472. doi: 10. 1105/tpc. 108. 062935.
5. 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. doi: 10. 1007/s00425-005-0057-3.
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. doi: 10. 1104/pp. 106. 082289.
7. Chandler PM (1988) Hormonal regulation of gene expression in the "slender" mutant of barley (Hordeum vulgare L.). Planta 175: 115-120. doi: 10. 1007/BF00402888.
8. Chandler PM, Robertson M (1999) Gibberellin dose-response curves and the characterization of dwarf mutants of barley. Plant Physiol 120: 623-632. doi: 10. 1104/pp. 120. 2. 623.
9. Chandler PM, Marion-Poll A, Ellis M, Gubler F (2002) Mutants at the slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol 129: 181-190. doi: 10. 1104/pp. 010917.
10. Chen K, An Y-QC (2006) Transcriptional responses to gibberellin and abscisic acid in barley aleurone. J Integr Plant Biol 48: 591-612. doi: 10. 1111/j. 1744-7909. 2006. 00270. x.
11. 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. doi: 10. 1242/dev. 00992.
12. Chrispeels MJ, Varner JE (1967) Gibberellic acid-enhanced synthesis and release of α-amylase and ribonuclease by isolated barley and aleurone layers. Plant Physiol 42: 398-406. doi: 10. 1104/pp. 42. 3. 398.
13. Close TJ, Wanamaker SI, Caldo RA, Turner SM, Ashlock DA, Dickerson JA, Wing RA, Muehlbauer GJ, Kleinhofs A, Wise RP (2004) A new resource for cereal genomics: 22 k barley GeneChip comes of age. Plant Physiol 134: 960-968. doi: 10. 1104/pp. 103. 034462.
14. Dill A, Jung H-S, Sun T-P (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci USA 98: 14162-14167. doi: 10. 1073/pnas. 251534098.
15. Fincher GB (1989) Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu Rev Plant Physiol Plant Molec Biol 40: 305-346. doi: 10. 1146/annurev. pp. 40. 060189. 001513.
16. Foster CA (1977) Slender: an accelerated extension growth mutant of barley. Barley Genet Newslett 7: 24-27.
17. Fu X, Richards DE, Ait-ali T, Hynes LW, Ougham H, Peng J, Harberd NP (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14: 3191-3200. doi: 10. 1105/tpc. 006197.
18. Fu X, Richards DE, Fleck B, Xie D, Burton N, Harberd NP (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. doi: 10. 1105/tpc. 021386.
19. Fukao T, Bailey-Serres J (2008) Submergence tolerance conferred by SUB1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proc Natl Acad Sci USA 105: 16814-16819. doi: 10. 1073/pnas. 0807821105.
20. Gocal GFW, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP, Li SF, Parish RW, Dennis ES, Weigel D, King RW (2001) GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol 127: 1682-1693. doi: 10. 1104/pp. 010442.
21. Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z-L, Powers SJ, Gong F, Phillips AL, Hedden P, Sun T-P, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399-3414. doi: 10. 1105/tpc. 106. 047415.
22. Gubler F, Kalla R, Roberts JK, Jacobsen JV (1995) Gibberellin-regulated expression of a MYB gene in barley aleurone cells: evidence for MYB transactivation of a high-pl α-amylase gene promoter. Plant Cell 7: 1879-1891. doi: 10. 1105/tpc. 7. 11. 1879.
23. Gubler F, Raventos D, Keys M, Watts R, Mundy J, Jacobsen VJ (1999) Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J 17: 1-9. doi: 10. 1046/j. 1365-313X. 1999. 00346. x.
24. Gubler F, Chandler PM, White RG, Llewellyn DJ, Jacobsen JV (2002) Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. Plant Physiol 129: 191-200. doi: 10. 1104/pp. 010918.
25. Hou X, Hu W-W, Shen L, Lee LYC, Tao Z, Han J-H, Yu H (2008) Global identification of DELLA target genes during Arabidopsis flower development. Plant Physiol 147: 1126-1142. doi: 10. 1104/pp. 108. 121301.
26. Huttly AK, Phillips AL (1995) Gibberellin-regulated plant genes. Physiol Plant 95: 310-317. doi: 10. 1111/j. 1399-3054. 1995. tb00843. x.
27. Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, 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. doi: 10. 1105/tpc. 13. 5. 999.
28. Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14: 57-70. doi: 10. 1105/tpc. 010319.
29. Itoh H, Sasaki A, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Hasegawa Y, Minami E, Ashikari M, Matsuoka M (2005) Dissection of the phosphorylation of rice DELLA protein, SLENDER RICE1. Plant Cell Physiol 46: 1392-1399. doi: 10. 1093/pcp/pci152.
30. Iuchi S, Suzuki H, Kim Y-C, Iuchi A, Kuromori T, Ueguchi-Tanaka M, Asami T, Yamaguchi I, Matsuoka M, Kobayashi M, Nakajima M (2007) Multiple loss-of-function of arabidopsis gibberellin receptor atgid1s completely shuts down a gibberellin signal. Plant J 50: 958-966. doi: 10. 1111/j. 1365-313X. 2007. 03098. x.
31. Kaneko M, Itoh H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M (2002) The alpha-amylase induction in endosperm during rice seed germination is caused by gibberellin synthesized in epithelium. Plant Physiol 128: 1264-1270. doi: 10. 1104/pp. 010785.
32. Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Ashikari M, Matsuoka M (2003) Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J 35: 104-115. doi: 10. 1046/j. 1365-313X. 2003. 01780. x.
33. 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: 33-44. doi: 10. 1105/tpc. 017327.
34. King KE, Moritz T, Harberd NP (2001) Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159: 767-776.
35. Koornneef M, Veen JH (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsisthaliana (L.) heynh. Theor Appl Genet 58: 257-263. doi: 10. 1007/BF00265176.
36. 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. doi: 10. 1101/gad. 969002.
37. Liu Y, Bergervoet JHW, Vos CHR, Hilhorst HWM, Kraak HL, Karssen CM, Bino RJ (1994) Nuclear replication activities during imbibition of abscisic acid- and gibberellin-deficient tomato (Lycopersicon esculentum Mill.) seeds. Planta 194: 368-373. doi: 10. 1007/BF00197537.
38. Maymon I, Greenboim-Wainberg Y, Sagiv S, Kieber JJ, Moshelion M, Olszewski N, Weiss D (2009) Cytosolic activity of spindly implies the existence of a della-independent gibberellin-response pathway. Plant J 58: 979-988. doi: 10. 1111/j. 1365-313X. 2009. 03840. x.
39. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun T-P, Steber CM (2003) The ArabidopsisSLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15: 1120-1130. doi: 10. 1105/tpc. 010827.
40. Mena M, Cejudo FJ, Isabel-Lamoneda I, Carbonero P (2002) A role for the DOF transcription factor BPBF in the regulation of gibberellin-responsive genes in barley aleurone. Plant Physiol 130: 111-119. doi: 10. 1104/pp. 005561.
41. Millar AA, Gubler F (2005) The ArabidopsisGAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17: 705-721. doi: 10. 1105/tpc. 104. 027920.
42. Murray F, Kalla R, Jacobsen J, Gubler F (2003) A role for HvGAMYB in anther development. Plant J 33: 481-491. doi: 10. 1046/j. 1365-313X. 2003. 01641. x.
43. Nakajima M, Shimada A, Takashi Y, Kim Y-C, Park S-H, Ueguchi-Tanaka M, Suzuki H, Katoh E, Iuchi S, Kobayashi M, Maeda T, Matsuoka M, Yamaguchi I (2006) Identification and characterization of arabidopsis gibberellin receptors. Plant J 46: 880-889. doi: 10. 1111/j. 1365-313X. 2006. 02748. x.
44. 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. doi: 10. 1105/tpc. 107. 050153.
45. Peng J (1997) The ArabidopsisGAI gene defines a signalling pathway that negatively regulates gibberellin responses. Genes Dev 11: 3194-3205. doi: 10. 1101/gad. 11. 23. 3194.
46. Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400: 256-261. doi: 10. 1038/22307.
47. Radley M (1967) Site of production of gibberellin-like substances in germinating barley embryos. Planta 75: 164-171. doi: 10. 1007/BF00387132.
48. Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong D-H, An G, Kitano H, Ashikari M, Matsuoka M (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299: 1896-1898. doi: 10. 1126/science. 1081077.
49. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsisthaliana development. Nat Genet 37: 501-506. doi: 10. 1038/ng1543.
50. Silverstone AL, Ciampaglio CN, Sun TP (1998) The ArabidopsisRGA gene encodes a transcriptional regulator repressing the gibberellin signal-transduction pathway. Plant Cell 10: 155-169. doi: 10. 1105/tpc. 10. 2. 155.
51. Silverstone AL, Jung H-S, Dill A, Kawaide H, Kamiya Y, Sun T-P (2001) Repressing a repressor: Gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13: 1555-1566. doi: 10. 1105/tpc. 13. 7. 1555.
52. Skadsen RW (1993) Aleurones from a barley with low α-amylase activity become highly responsive to gibberellin when detached from the starchy endosperm. Plant Physiol 102: 195-203. doi: 10. 1104/pp. 102. 1. 195.
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: 427-444. doi: 10. 1111/j. 1365-313X. 2006. 02795. x.
54. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121. doi: 10. 1073/pnas. 091062498.
55. 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. doi: 10. 1104/pp. 104. 039578.
56. Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow T-Y, Hsing Y-Ic, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693-698. doi: 10. 1038/nature04028.
57. Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Hongyu X, Ashikari M, Kitano H, Yamaguchi I, Matsuoka M (2007) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19: 2140-2155. doi: 10. 1105/tpc. 106. 043729.
58. 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. doi: 10. 1105/tpc. 108. 061648.
59. Vierstra RD (2003) The ubiquitin/26s proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci 8: 135-142. doi: 10. 1016/S1360-1385(03)00014-1.
60. Washio K (2003) Functional dissections between GAMYB and Dof transcription factors suggest a role for protein-protein associations in the gibberellin-mediated expression of the RAmy1A gene in the rice aleurone. Plant Physiol 133: 850-863. doi: 10. 1104/pp. 103. 027334.
61. Wattenberg BW, Pitson SM, Raben DM (2006) The sphingosine and diacylglycerol kinase superfamily of signaling kinases: localization as a key to signaling function. J Lipid Res 47: 1128-1139. doi: 10. 1194/jlr. R600003-JLR200.
62. Wen C-K, Chang C (2002) ArabidopsisRGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14: 87-100. doi: 10. 1105/tpc. 010325.
63. Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EMN, Maier A, 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. doi: 10. 1105/tpc. 107. 051441.
64. Woodger FJ, Jacobsen JV, Gubler F (2004) GMPOZ, a BTB/POZ domain nuclear protein, is a regulator of hormone responsive gene expression in barley aleurone. Plant Cell Physiol 45: 945-950. doi: 10. 1093/pcp/pch100.
65. Wu Z, Irizarry RA (2004) Preprocessing of oligonucleotide array data. Nat Biotech 22: 656-658. doi: 10. 1038/nbt0604-656b.
66. Yu H, Ito T, Zhao Y, Peng J, Kumar P, Meyerowitz EM (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci USA 101: 7827-7832. doi: 10. 1073/pnas. 0402377101.
67. Zentella R, Yamauchi D, Ho T-hD (2002) Molecular dissection of the gibberellin/abscisic acid signaling pathways by transiently expressed RNA interference in barley aleurone cells. Plant Cell 14: 2289-2301. doi: 10. 1105/tpc. 003376.
68. Zentella R, Zhang Z-L, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun T-P (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19: 3037-3057. doi: 10. 1105/tpc. 107. 054999.
69. Zhang Z-L, Xie Z, Zou X, Casaretto J, Ho T-hD, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134: 1500-1513. doi: 10. 1104/pp. 103. 034967.
70. Zou X, Neuman D, Shen QJ (2008) Interactions of two transcriptional repressors and two transcriptional activators in modulating gibberellin signaling in aleurone cells. Plant Physiol 148: 176-186. doi: 10. 1104/pp. 108. 123653.