Cytokinin antagonizes abscisic acid-mediated inhibition of cotyledon greening by promoting the degradation of ABSCISIC ACID INSENSITIVE5 protein in Arabidopsis

Plant Physiology

Volumn 164, Issue 3, 2014, Pages 1515-1526

  Guan, Chunmei ^a,b   Wang, Xingchun ^c   Feng, Jian ^a,b   Hong, Sulei ^a,b   Liang, Yan ^a   Ren, Bo ^a   Zuo, Jianru ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c SHANXI AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ABI5 PROTEIN, ARABIDOPSIS; ABSCISIC ACID; ARABIDOPSIS PROTEIN; ARR12 PROTEIN, ARABIDOPSIS; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CYTOKININ; PROTEASOME; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; COTYLEDON; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; COTYLEDON; CYTOKININS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84897602395     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.234740     Document Type: Article

References (68)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
2. Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, Etheridge N, Argyros DA, Mason MG, Kieber JJ, Schaller GE (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20: 2102-2116
3. Barzilai E, Mayer AM (1964) Kinins in germinating lettuoe seed. Aust J Biol Sci 17: 798-800
4. Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82: 259-266
5. Bewley JD (1997) Seed germination and dormancy. Plant Cell 9: 1055-1066
6. Bewley JD, Black M (1994) Seeds: Physiology of Development and Germination. Plenum Press, New York
7. Black M, Bewley JD, Fountain D (1974) Lettuce seed germination and cytokinins: their entry and formation. Planta 117: 145-152
8. Borisjuk L, Rolletschek H, Radchuk R, Weschke W, Wobus U, Weber H (2004) Seed development and differentiation: a role for metabolic regulation. Plant Biol (Stuttg) 6: 375-386
9. Brandstatter I, Kieber JJ (1998) Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell 10: 1009-1019
10. Chory J, Aguilar N, Peto CA (1991) The phenotype of Arabidopsis thaliana det1 mutants suggests a role for cytokinins in greening. Symp Soc Exp Biol 45: 21-29
11. Chory J, Reinecke D, Sim S, Washburn T, Brenner M (1994) A role for cytokinins in de-etiolation in Arabidopsis (det mutants have an altered response to cytokinins). Plant Physiol 104: 339-347
12. Davies PJ (2004) Plant Hormones: Biosynthesis, Signal Transduction, Action! Ed 3. Kluwer Academic Press, Dordrecht, The Netherlands
13. Deng Y, Dong H, Mu J, Ren B, Zheng B, Ji Z, Yang WC, Liang Y, Zuo J (2010) Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell 22: 1232-1248
14. Finkelstein RR (1994) Maternal effects govern variable dominance of two abscisic acid response mutations in Arabidopsis thaliana. Plant Physiol 105: 1203-1208
15. Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell (Suppl) 14: S15-S45
16. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12: 599-609
17. Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10: 1043-1054
18. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4: 1251-1261
19. Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17: 172-179
20. Higuchi M, Pischke MS, Mähönen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, et al (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101: 8821-8826
21. Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, et al (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18: 3073-3087
22. Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63: 353-380
23. Imamura A, Hanaki N, Umeda H, Nakamura A, Suzuki T, Ueguchi C, Mizuno T (1998) Response regulators implicated in His-to-Asp phosphotransfer signaling in Arabidopsis. Proc Natl Acad Sci USA 95: 2691-2696
24. Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409: 1060-1063
25. Ishida K, Yamashino T, Mizuno T (2008) Expression of the cytokinin-induced type-A response regulator gene ARR9 is regulated by the circadian clock in Arabidopsis thaliana. Biosci Biotechnol Biochem 72: 3025-3029
26. Kakimoto T (2003) Perception and signal transduction of cytokinins. Annu Rev Plant Biol 54: 605-627
27. Karssen CM, Brinkhorst-van der Swan DL, Breekland AE, Koornneef M (1983) Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. Planta 157: 158-165
28. Khan AA (1971) Cytokinins: permissive role in seed germination. Science 171: 853-859
29. Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant 61: 377-383
30. Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15: 281-307
31. Lee JH, Yoon HJ, Terzaghi W, Martinez C, Dai M, Li J, Byun MO, Deng XW (2010) DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 22: 1716-1732
32. Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calciummodulated protein phosphatase. Science 264: 1448-1452
33. Liu H, Stone SL (2010) Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell 22: 2630-2641
34. Lopez-Molina L, Chua NH (2000) A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana. Plant Cell Physiol 41: 541-547
35. Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98: 4782-4787
36. Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH (2003) AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 17: 410-418
37. Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32: 317-328
38. Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452-1455
39. Mok MC (1994) Cytokinins and plant development: an overview. In DWS Mok, MC Mok, eds, Cytokinins: Chemistry, Activity, and Function. CRC Press, Boca Raton, FL, pp 155-166
40. Müller B, Sheen J (2007) Arabidopsis cytokinin signaling pathway. Sci STKE 2007: cm5
41. Müller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453: 1094-1097
42. Müller K, Tintelnot S, Leubner-Metzger G (2006) Endosperm-limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant Cell Physiol 47: 864-877
43. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56: 165-185
44. Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16: 1365-1377
45. Nishiyama R, Le DT, Watanabe Y, Matsui A, Tanaka M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Transcriptome analyses of a salttolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS ONE 7: e32124
46. Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, et al (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23: 2169-2183
47. Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell (Suppl) 14: S61-S80
48. Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, Chico JM, Bossche RV, Sewell J, Gil E, et al (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464: 788-791
49. Penfield S, Graham S, Graham IA (2005) Storage reserve mobilization in germinating oilseeds: Arabidopsis as a model system. Biochem Soc Trans 33: 380-383
50. 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
51. Ren B, Liang Y, Deng Y, Chen Q, Zhang J, Yang X, Zuo J (2009) Genomewide comparative analysis of type-A Arabidopsis response regulator genes by overexpression studies reveals their diverse roles and regulatory mechanisms in cytokinin signaling. Cell Res 19: 1178-1190
52. Riefler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18: 40-54
53. Sakai H, Honma T, Aoyama T, Sato S, Kato T, Tabata S, Oka A (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294: 1519-1521
54. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57: 431-449
55. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
56. Shi Y, Tian S, Hou L, Huang X, Zhang X, Guo H, Yang S (2012) Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 24: 2578-2595
57. Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22: 3560-3573
58. Stone SL, Williams LA, Farmer LM, Vierstra RD, Callis J (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18: 3415-3428
59. Sun J, Niu QW, Tarkowski P, Zheng B, Tarkowska D, Sandberg G, Chua NH, Zuo J (2003) The Arabidopsis AtIPT8/PGA22 gene encodes an isopentenyl transferase that is involved in de novo cytokinin biosynthesis. Plant Physiol 131: 167-176
60. Thomas TH, Hare PD, van Staden J (1997) Phytochrome and cytokinin responses. Plant Growth Regul 23: 105-122
61. To JP, Deruère J, Maxwell BB, Morris VF, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2007) Cytokinin regulates type-A Arabidopsis Response Regulator activity and protein stability via two-component phosphorelay. Plant Cell 19: 3901-3914
62. To JP, Kieber JJ (2008) Cytokinin signaling: two-components and more. Trends Plant Sci 13: 85-92
63. Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104: 20623-20628
64. Wang Y, Li L, Ye T, Zhao S, Liu Z, Feng YQ, Wu Y (2011) Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. Plant J 68: 249-261
65. Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12: 527-538
66. Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42: 1017-1023
67. Zheng Y, Schumaker KS, Guo Y (2012) Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana. Proc Natl Acad Sci USA 109: 12822-12827
68. Zuo J, Niu QW, Chua NH (2000) An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24: 265-273