Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis

Plant Physiology

Volumn 164, Issue 1, 2014, Pages 424-439

  Bu, Qingyun ^a,b   Lv, Tianxiao ^a,c   Shen, Hui ^b   Luong, Phi ^b   Wang, Jimmy ^b   Wang, Zhenyu ^a   Huang, Zhigang ^d   Xiao, Langtao ^d   Engineer, Cawas ^e   Kim, Tae Houn ^e,f   Schroeder, Julian I ^e   Huq, Enamul ^b  

^a NORTHEAST INSTITUTE OF GEOGRAPHY AND AGRICULTURAL ECOLOGY   (China)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d HUNAN AGRICULTURAL UNIVERSITY   (China)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; F BOX PROTEIN; MAX2 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; DROUGHT; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT STOMA; SEEDLING; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; DROUGHTS; F-BOX PROTEINS; GENE EXPRESSION REGULATION, PLANT; GERMINATION; MUTATION; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; SEEDLING; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84891764933     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.226837     Document Type: Article

References (71)

1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15: 63-78
2. Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16: 2463-2480
3. Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14: 1232-1238
4. Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8: 443-449
5. Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjärvi J, Ghassemian M, Stephan AB, Hu H, Schroeder JI (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA 109: 10593-10598
6. Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6: 18-28
7. Bu Q, Li H, Zhao Q, Jiang H, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Wang D, et al (2009) The Arabidopsis RING finger E3 ligase RHA2a is a novel positive regulator of abscisic acid signaling during seed germination and early seedling development. Plant Physiol 150: 463-481
8. Carles C, Bies-Etheve N, Aspart L, Léon-Kloosterziel KM, Koornneef M, Echeverria M, Delseny M (2002) Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J 30: 373-383
9. Chen Z, Zhang H, Jablonowski D, Zhou X, Ren X, Hong X, Schaffrath R, Zhu JK, Gong Z (2006) Mutations in ABO1/ELO2, a subunit of holo-Elongator, increase abscisic acid sensitivity and drought tolerance in Arabidopsis thaliana. Mol Cell Biol 26: 6902-6912
10. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61: 651-679
11. Deshaies RJ (1999) SCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 15: 435-467
12. Dill A, Thomas SG, Hu J, Steber CM, Sun TP (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellininduced degradation. Plant Cell 16: 1392-1405
13. Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell (Suppl) 14: S15-S45
14. 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
15. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462: 660-664
16. Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147: 15-27
17. Gagne JM, Downes BP, Shiu SH, Durski AM, Vierstra RD (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
18. Gagne JM, Smalle J, Gingerich DJ, Walker JM, Yoo SD, Yanagisawa S, Vierstra RD (2004) Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc Natl Acad Sci USA 101: 6803-6808
19. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, et al (2008) Strigolactone inhibition of shoot branching. Nature 455: 189-194
20. Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an γ/γhydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22: 2032-2036
21. Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21: R346-R355
22. Islam MA, Du H, Ning J, Ye H, Xiong L (2009) Characterization of Glossy1-homologous genes in rice involved in leaf wax accumulation and drought resistance. Plant Mol Biol 70: 443-456
23. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27: 325-333
24. Koops P, Pelser S, Ignatz M, Klose C, Marrocco-Selden K, Kretsch T (2011) EDL3 is an F-box protein involved in the regulation of abscisic acid signalling in Arabidopsis thaliana. J Exp Bot 62: 5547-5560
25. Kurkela S, Borg-Franck M (1992) Structure and expression of kin2, one of two cold-and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol 19: 689-692
26. Kuromori T, Sugimoto E, Shinozaki K (2011) Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J 67: 885-894
27. Kwak JM, Moon JH, Murata Y, Kuchitsu K, Leonhardt N, DeLong A, Schroeder JI (2002) Disruption of a guard cell-expressed protein phosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in Arabidopsis. Plant Cell 14: 2849-2861
28. Lång V, Palva ET (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 20: 951-962
29. Lee SB, Jung SJ, Go YS, Kim HU, Kim JK, Cho HJ, Park OK, Suh MC (2009) Two Arabidopsis 3-ketoacyl CoA synthase genes, KCS20 and KCS2/DAISY, are functionally redundant in cuticular wax and root suberin biosynthesis, but differentially controlled by osmotic stress. Plant J 60: 462-475
30. Leube MP, Grill E, Amrhein N (1998) ABI1 of Arabidopsis is a protein serine/threonine phosphatase highly regulated by the proton and magnesium ion concentration. FEBS Lett 424: 100-104
31. Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264: 1448-1452
32. Leung J, Merlot S, Gosti F, Bertauche N, Blatt MR, Giraudat J (1998) The role of ABI1 in abscisic acid signal transduction: from gene to cell. Symp Soc Exp Biol 51: 65-71
33. Li H, Jiang H, Bu Q, Zhao Q, Sun J, Xie Q, Li C (2011) The Arabidopsis RING finger E3 ligase RHA2b acts additively with RHA2a in regulating abscisic acid signaling and drought response. Plant Physiol 156: 550-563
34. Lolle SJ, Berlyn GP, Engstrom EM, Krolikowski KA, Reiter WD, Pruitt RE (1997) Developmental regulation of cell interactions in the Arabidopsis fiddlehead-1 mutant: a role for the epidermal cell wall and cuticle. Dev Biol 189: 311-321
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, 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
37. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068
38. Melcher K, Ng LM, Zhou XE, Soon FF, Xu Y, Suino-Powell KM, Park SY, Weiner JJ, Fujii H, Chinnusamy V, et al (2009) A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462: 602-608
39. Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452-1455
40. Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14: 3089-3099
41. Nambara E, Suzuki M, Abrams S, McCarty DR, Kamiya Y, McCourt P (2002) A screen for genes that function in abscisic acid signaling in Arabidopsis thaliana. Genetics 161: 1247-1255
42. Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108: 8897-8902
43. Nishimura N, Hitomi K, Arvai AS, Rambo RP, Hitomi C, Cutler SR, Schroeder JI, Getzoff ED (2009) Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326: 1373-1379
44. Nishimura N, Sarkeshik A, Nito K, Park SY, Wang A, Carvalho PC, Lee S, Caddell DF, Cutler SR, Chory J, et al (2010) PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61: 290-299
45. Owen SJ, Abrams SR (2009) Measurement of plant hormones by liquid chromatography-mass spectrometry. Methods Mol Biol 495: 39-51
46. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071
47. Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15: 395-401
48. Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu JK, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63: 417-429
49. Rodriguez PL, Benning G, Grill E (1998) ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett 421: 185-190
50. Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes Dev 12: 198-207
51. Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, Rodriguez PL (2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J 37: 354-369
52. Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Márquez JA, Cutler SR, Rodriguez PL (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60: 575-588
53. Shen H, Luong P, Huq E (2007) The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol 145: 1471-1483
54. Shen H, Zhu L, Bu QY, Huq E (2012) MAX2 affects multiple hormones to promote photomorphogenesis. Mol Plant 5: 750-762
55. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58: 221-227
56. Siegel RS, Xue S, Murata Y, Yang Y, Nishimura N, Wang A, Schroeder JI (2009) Calcium elevation-dependent and attenuated resting calciumdependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and inward-rectifying K channels in Arabidopsis guard cells. Plant J 59: 207-220
57. Sorefan K, Booker J, Haurogné K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, et al (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17: 1469-1474
58. Stirnberg P, van De Sande K, Leyser HM (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129: 1131-1141
59. Tamura N, Yoshida T, Tanaka A, Sasaki R, Bando A, Toh S, Lepiniec L, Kawakami N (2006) Isolation and characterization of high temperatureresistant germination mutants of Arabidopsis thaliana. Plant Cell Physiol 47: 1081-1094
60. Toh S, Kamiya Y, Kawakami N, Nambara E, McCourt P, Tsuchiya Y (2012) Thermoinhibition uncovers a role for strigolactones in Arabidopsis seed germination. Plant Cell Physiol 53: 107-117
61. Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt P (2010) A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 6: 741-749
62. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200
63. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51: 1821-1839
64. Umezawa T, Okamoto M, Kushiro T, Nambara E, Oono Y, Seki M, Kobayashi M, Koshiba T, Kamiya Y, Shinozaki K (2006) CYP707A3, a major ABA 8-hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana. Plant J 46: 171-182
65. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139: 1285-1295
66. Waters MT, Smith SM (2013) KAI2-and MAX2-mediated responses to karrikins and strigolactones are largely independent of HY5 in Arabidopsis seedlings. Mol Plant 6: 63-75
67. Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13: 1779-1790
68. Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280: 1091-1094
69. Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 1: 771-781
70. Zhang Y, Xu W, Li Z, Deng XW, Wu W, Xue Y (2008) F-box protein DOR functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol 148: 2121-2133
71. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53: 247-273