Crosstalk between GA and JA signaling mediates plant growth and defense

Plant Cell Reports

Volumn 32, Issue 7, 2013, Pages 1067-1074

  Hou, Xingliang ^a   Ding, Lihua ^b   Yu, Hao ^b  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

GA; JA; Phytohormone signaling; Plant defense; Plant growth

Indexed keywords

CYCLOPENTANE DERIVATIVE; GIBBERELLIN; JASMONIC ACID; OXYLIPIN; PHYTOHORMONE;

GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; GIBBERELLINS; OXYLIPINS; PLANT GROWTH REGULATORS; SIGNAL TRANSDUCTION;

EID: 84878990345     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-013-1423-4     Document Type: Review

References (74)

1. Achard P, Vriezen WH, van Der Straeten D, Harberd NP (2003) Ethylene regulates arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15: 2816-2825.
2. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311: 91-94.
3. Achard P, Renou JP, Berthome R, Harberd NP, Genschik P (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 18: 656-660.
4. Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GTS, Genschik P (2009) Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 19: 1188-1193.
5. Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T, Sablowski R, Ostergaard L (2010) Gibberellins control fruit patterning in Arabidopsis thaliana. Gene Dev 24: 2127-2132.
6. Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14: 810-817.
7. Baldwin IT (2010) Plant volatiles. Curr Biol 20: R392-R397.
8. Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218: 683-692.
9. Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape 'green revolution' mutation. Nature 416: 847-850.
10. Browse J, Howe GA (2008) New weapons and a rapid response against insect attack. Plant Physiol 146: 832-838.
11. 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.
12. Chen H, Xue L, Chintamanani S, Germain H, Lin H, Cui H, Cai R, Zuo J, Tang X, Li X, Guo H, Zhou JM (2009) ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21: 2527-2540.
13. 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.
14. Cheng H, Song SS, Xiao LT, Soo HM, Cheng ZW, Xie DX, Peng JR (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 5: e1000440.
15. Cheng Z, Sun L, Qi T, Zhang B, Peng W, Liu Y, Xie D (2011) The bHLH transcription factor MYC3 interacts with the Jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis. Mol Plant 4: 279-288.
16. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671.
17. Cowling RJ, Harberd NP (1999) Gibberellins control Arabidopsis hypocotyl growth via regulation of cellular elongation. J Exp Bot 50: 1351-1357.
18. de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blazquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480-484.
19. Devoto A, Nieto-Rostro M, Xie D, Ellis C, Harmston R, Patrick E, Davis J, Sherratt L, Coleman M, Turner JG (2002) COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J 32: 457-466.
20. Dill A, Sun T (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159: 777-785.
21. Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci USA 98: 14162-14167.
22. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87: 7713-7716.
23. Farmer EE, Almeras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6: 372-378.
24. Feng S, Ma L, Wang X, Xie D, Dinesh kumar SP, Wei N, Deng XW (2003) The COP9 signalosome interacts physically with SCF COI1 and modulates jasmonate responses. Plant Cell 15: 1083-1094.
25. Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S, Schafer E, Fu X, Fan LM, Deng XW (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475-479.
26. Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM, Pauwels L, Witters E, Puga MI, Paz-Ares J, Goossens A, Reymond P, De Jaeger G, Solano R (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23: 701-715.
27. Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-Iso-jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5: 344-350.
28. Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421: 740-743.
29. Goto N, Pharis RP (1999) Role of gibberellins in the development of floral organs of the gibberellin-deficient mutant, ga1-1, of Arabidopsis thaliana. Can J Bot 77: 944-954.
30. Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun TP, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399-3414.
31. Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5: 523-530.
32. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24: 2635-2648.
33. Hou X, Hu WW, Shen L, Lee LY, Tao Z, Han JH, Yu H (2008) Global identification of DELLA target genes during Arabidopsis flower development. Plant Physiol 147: 1126-1142.
34. Hou X, Lee LY, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19: 884-894.
35. 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.
36. Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Ann Rev Plant Biol 59: 365-386.
37. Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105: 7100-7105.
38. Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305: 665-668.
39. Koornneef M, Vanderveen JH (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L) Heynh. Theor Applied Genet 58: 257-263.
40. Koornneef M, Vaneden J, Hanhart CJ, Dejongh AMM (1983) Genetic fine-structure of the GA-1 locus in the higher-plant Arabidopsis thaliana (L) Heynh. Genet Res 41: 57-68.
41. 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. Gene Dev 16: 646-658.
42. Lee LYC, Hou XL, Fang L, Fan SG, Kumar PP, Yu H (2012) STUNTED mediates the control of cell proliferation by GA in Arabidopsis. Development 139: 1568-1576.
43. Mandaokar A, Thines B, Shin B, Lange BM, Choi G, Koo YJ, Yoo YJ, Choi YD, Choi G, Browse J (2006) Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J 46: 984-1008.
44. Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456: 459-463.
45. Navarro L, Bari R, Achard P, Lison P, Nemri A, Harberd NP, Jones JD (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18: 650-655.
46. Niu Y, Figueroa P, Browse J (2011) Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. J Exp Bot 62: 2143-2154.
47. Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14(Suppl): S61-S80.
48. Perazza D, Vachon G, Herzog M (1998) Gibberellins promote trichome formation by up-regulating GLABROUS1 in Arabidopsis. Plant Physiol 117: 375-383.
49. Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18: 111-119.
50. Qi T, Song S, Ren Q, Wu D, Huang H, Chen Y, Fan M, Peng W, Ren C, Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate Jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 23: 1795-1814.
51. Robson F, Okamoto H, Patrick E, Harris SR, Wasternack C, Brearley C, Turner JG (2010) Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell 22: 1143-1160.
52. Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468: 400-405.
53. 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.
54. Silverstone AL, Mak PYA, Martinez EC, Sun TP (1997) The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146: 1087-1099.
55. Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, Xie D (2011) The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23: 1000-1013.
56. Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97: 10625-10630.
57. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448: 661-665.
58. Traw MB, Bergelson J (2003) Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiol 133: 1367-1375.
59. Ubeda-Tomas S, Federici F, Casimiro I, Beemster GTS, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19: 1194-1199.
60. Wagner GJ, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 93: 3-11.
61. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100: 681-697.
62. Wen CK, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14: 87-100.
63. Wild M, Daviere JM, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24: 3307-3319.
64. 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.
65. Xu L, Liu F, Lechner E, Genschik P, Crosby WL, Ma H, Peng W, Huang D, Xie D (2002) The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14: 1919-1935.
66. Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21: 2220-2236.
67. Yang T, Davies PJ, Reid JB (1996) Genetic dissection of the relative roles of auxin and gibberellin in the regulation of stem elongation in intact light-grown peas. Plant Physiol 110: 1029-1034.
68. Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li J, Deng XW, Lee CM, Thomashow MF, Yang Y, He Z, He SY (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci USA 109: E1192-E1200.
69. Yoshida Y, Sano R, Wada T, Takabayashi J, Okada K (2009) Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development 136: 1039-1048.
70. 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.
71. Zhai Q, Li CB, Zheng W, Wu X, Zhao J, Zhou G, Jiang H, Sun J, Lou Y, Li C (2007) Phytochrome chromophore deficiency leads to overproduction of jasmonic acid and elevated expression of jasmonate-responsive genes in Arabidopsis. Plant Cell Physiol 48: 1061-1071.
72. Zhang Y, Turner JG (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS ONE 3: e3699.
73. Zhou Z, An L, Sun L, Zhu S, Xi W, Broun P, Yu H, Gan Y (2011) Zinc finger protein5 is required for the control of trichome initiation by acting upstream of zinc finger protein8 in Arabidopsis. Plant Physiol 157: 673-682.
74. Zhu Z, An F, Feng Y, Li P, Xue L, A M, Jiang Z, Kim JM, To TK, Li W, Zhang X, Yu Q, Dong Z, Chen WQ, Seki M, Zhou JM, Guo H (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108: 12539-12544.