Jasmonate Action and Biotic Stress Response in Plants

doi:10.13560/j.cnki.biotech.bull.1985.2018-0442

Abstract

Abstract: Being sessile,plants are always challenged by a variety of environmental stresses,including herbivorous insect attack and microbial pathogen infection. To defend themselves against these stresses,plants have evolved sophisticated and highly regulated defense system,such as activation of biosynthesis of plant hormones that regulate defense-related gene expression and secondary metabolite production. Intriguingly,many herbivorous insects and microbial pathogens have been found to employ distinct strategies to evade,overcome,or even manipulate plants' defense system to facilitate their exploitation of host plants. Jasmonate,an important class of lipid-derived plant hormone,regulates multiple aspects of plant growth and development and also plays crucial roles in plant responses to diverse biotic and abiotic stresses. In recent years,the biosynthesis,signal transduction and biological functions of jasmonate have been extensively studied,and significant progresses have been achieved. In this review,we provide a overview of jasmonate biosynthesis regulation and signaling transduction pathway. We also discuss the mechanisms of jasmonate action in plant biotic stress responses and summarize the various strategies used by herbivorous insects or microbial pathogens to hijack jasmonate pathway. This review would be helpful for an in-depth understanding of jasmonate-mediated interactions of plants with pathogenic organisms.

Key words: jasmonate, plant, biotic stress, plant-pathogen interaction

WU De-wei, WANG Jiao-jiao, XIE Dao-xin. Jasmonate Action and Biotic Stress Response in Plants[J]. Biotechnology Bulletin, 2018, 34(7): 14-23.

References

[1] Wasternack C, Hause B.Jasmonates:biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany[J]. Ann Bot, 2013, 111(6):1021-1058.
[2] Huang H, Liu B, Liu L, et al.Jasmonate action in plant growth and development[J]. J Exp Bot, 2017, 68(6):1349-1359.
[3] Zhang L, Zhang F, et al.Jasmonate signaling and manipulation by pathogens and insects[J]. J Exp Bot, 2017, 68(6):1371-1385.
[4] Yan C, Xie D.Jasmonate in plant defence:sentinel or double agent?[J]. Plant Biotechnol J, 2015, 13(9):1233-1240.
[5] Browse J, Jasmonate passes muster:A receptor and targets for the defense hormone[J]. Annu Rev Plant Biol, 2009, 60:183-205.
[6] Howe GA, Jander G.Plant immunity to insect herbivores[J]. Annu Rev Plant Biol, 2008, 59:41-66.
[7] Liechti R, Farmer EE.The jasmonate pathway[J]. Science, 2002, 296(5573):1649-1650.
[8] Wasternack C, Song S.Jasmonates:biosynthesis, metabolism, and signaling by proteins activating and repressing transcription[J]. J Exp Bot, 2017, 68(6):1303-1321.
[9] Chini A, Monte I, Zamarreno AM, et al.An OPR3-independent pathway uses 4, 5-didehydrojasmonate for jasmonate synthesis[J]. Nat Chem Biol, 2018, 14(2):171-178.
[10] Fonseca S, Chini A, Hamberg M, et al.(+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate[J]. Nat Chem Biol, 2009, 5(5):344-350.
[11] Staswick PE, Tiryaki I.The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis[J]. Plant Cell, 2004, 16(8):2117-2127.
[12] Yan J, Li S, Gu M, et al.Endogenous bioactive jasmonate is composed of a set of(+)-7-iso-JA-amino acid conjugates[J]. Plant Physiol, 2016, 172(4):2154-2164.
[13] Browse J, Howe GA.New weapons and a rapid response against insect attack[J]. Plant Physiol, 2008, 146(3):832-838.
[14] Mousavi SAR, Chauvin A, Pascaud F, et al.GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling[J]. Nature, 2013, 500(7463):422-426.
[15] Yan C, Fan M, Yang M, et al.Injury activates Ca²+/calmodulin-dependent phosphorylation of JAV1-JAZ8-WRKY51 complex for jasmonate biosynthesis[J]. Mol Cell, 2018, 70(1):136-149.
[16] Hu P, Zhou W, Cheng ZW, et al.JAV1 Controls jasmonate-regulated plant defense[J]. Mol Cell, 2013, 50(4):504-515.
[17] Xie DX, Feys BF, James S, et al.COI1:An Arabidopsis gene required for jasmonate-regulated defense and fertility[J]. Science, 1998, 280(5366):1091-1094.
[18] Song S, Qi T, Wasternack C, et al.Jasmonate signaling and crosstalk with gibberellin and ethylene[J]. Curr Opin Plant Biol, 2014, 21:112-119.
[19] Xu L, Liu F, Lechner E, et al.The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis[J]. Plant Cell, 2002, 14(8):1919-1935.
[20] Yan Y, Stolz S, Chételat A, et al.A downstream mediator in the growth repression limb of the jasmonate pathway[J]. Plant Cell, 2007, 19(8):2470-2483.
[21] Thines B, Katsir L, Melotto M, et al.JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling[J]. Nature, 2007, 448(7154):661-665.
[22] Chini A, Fonseca S, Fernández G, et al.The JAZ family of repressors is the missing link in jasmonate signalling[J]. Nature, 2007, 448(7154):666-671.
[23] Yan JB, Zhang C, Gu M, et al.The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor[J]. Plant Cell, 2009, 21(8):2220-2236.
[24] Sheard LB, Tan X, Mao HB, et al.Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor[J]. Nature, 2010, 468(7322):400-405.
[25] Katsir L, Schilmiller AL, Staswick PE, et al.COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine[J]. Proc Natl Acad Sci USA, 2008, 105(19):7100-7105.
[26] Yan J, Li H, Li S, et al.The Arabidopsis F-box protein CORONATINE INSENSITIVE1 is stabilized by SCFCOI1 and degraded via the 26S proteasome pathway[J]. Plant Cell, 2013, 25(2):486-498.
[27] Qi T, Wang J, et al.Regulation of jasmonate-induced leaf senesc-ence by antagonism between bHLH subgroup IIIe and IIId factors in Arabidopsis[J]. Plant Cell, 2015, 27(6):1634-1649.
[28] Schweizer F, Fernández-Calvo P, Zander M, et al.Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, andMYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior[J]. Plant Cell, 2013, 25(8):3117-3132.
[29] Fernandez-Calvo P, Chini A, Fernandez-Barbero G, et al.The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses[J]. Plant Cell, 2011, 23(2):701-715.
[30] Cheng Z, Sun L, Qi T, et al.The bHLH transcription factor MYC3 interacts with the Jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis[J]. Mol Plant, 2011, 4(2):279-288.
[31] Chen Q, Sun J, Zhai Q, et al.The basic helix-loop-helix transcription factor myc2 directly represses plethora expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis[J]. Plant Cell, 2011, 23(9):3335-3352.
[32] Song S, Qi T, Huang H, et al.The jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect jasmonate-regulated stamen development in Arabidopsis[J]. Plant Cell, 2011, 23(3):1000-1013.
[33] Zhang F, Yao J, Ke J, et al.Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling[J]. Nature, 2015, 525(7568):269-273.
[34] Chen R, Jiang H, Li L, et al.The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors[J]. Plant Cell, 2012, 24(7):2898-2916.
[35] Zhu Z, An F, Feng Y, et al.Derepression of ethylene-stabilized transcription factors(EIN3/EIL1)mediates jasmonate and ethylene signaling synergy in Arabidopsis[J]. Proc Natl Acad Sci USA, 2011, 108(30):12539-12544.
[36] Shyu C, Figueroa P, Depew CL, et al.JAZ8 lacks a canonical degron and has an EAR motif that mediates transcriptional repression of jasmonate responses in Arabidopsis[J]. Plant Cell, 2012, 24(2):536-550.
[37] Pauwels L, Barbero GF, Geerinck J, et al.NINJA connects the co-repressor TOPLESS to jasmonate signalling[J]. Nature, 2010, 464(7289):788-791.
[38] Song S, Huang H, Gao H, et al.Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis[J]. Plant Cell, 2014, 26(1):263-279.
[39] Hong GJ, Xue XY, Mao YB, et al.Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression[J]. Plant Cell, 2012, 24(6):2635-2648.
[40] Ishida T, Kurata T, Okada K, et al.A genetic regulatory network in the development of trichomes and root hairs[J]. Annu Rev Plant Biol, 2008, 59:365-386.
[41] Winkel-Shirley B.Biosynthesis of flavonoids and effects of stress[J]. Curr Opin Plant Biol, 2002, 5(3):218-223.
[42] Broun P.Transcriptional control of flavonoid biosynthesis:a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis[J]. Curr Opin Plant Biol, 2005, 8(3):272-279.
[43] Qi T, Song S, Ren Q, et al.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[J]. Plant Cell, 2011, 23(5):1795-1814.
[44] Boter M, Golz JF, Gimenez-Ibanez S, et al.FILAMENTOUS FLOWER is a direct target of JAZ3 and modulates responses to jasmonate[J]. Plant Cell, 2015, 27(11):3160-3174.
[45] Fonseca S, Fernandez-Calvo P, et al.bHLH003, bHLH013 and bHLH017 are new targets of JAZ repressors negatively regulating JA responses[J]. PLoS One, 2014, 9(1):e86182.
[46] Song SS, Qi TC, Fan M, et al.The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development[J]. PLoS Genetics, 2013, 9(7):e1003653.
[47] Sasaki-Sekimoto Y, Jikumaru Y, Obayashi T, et al.Basic helix-loop-helix transcription factors JASMONATE-ASSOCIATED MYC2-LIKE1(JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis[J]. Plant Physiol, 2013, 163(1):291-304.
[48] Nakata M, Mitsuda N, Herde M, et al.A bHLH-type transcription factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, acts as a repressor to negatively regulate jasmonate signaling in Arabidopsis[J]. Plant Cell, 2013, 25(5):1641-1656.
[49] Ning Y, Liu W, Wang GL.Balancing immunity and yield in crop plants[J]. Trends Plant Sci, 2017, 22(12):1069-1079.
[50] Mao YB, Liu YQ, et al.Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance[J]. Nat Commun, 2017, 8:13925.
[51] Musser RO, Hum-Musser SM, Eichenseer H, et al.Herbivory:caterpillar saliva beats plant defences[J]. Nature, 2002, 416(6881):599-600.
[52] Chung SH, Rosa C, Scully ED, et al.Herbivore exploits orally secreted bacteria to suppress plant defenses[J]. Proc Natl Acad Sci USA, 2013, 110(39):15728-15733.
[53] Verhage A, Vlaardingerbroek I, Raaymakers C, et al.Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory[J]. Front Plant Sci, 2011, 2:47.
[54] Geng X, Cheng J, Gangadharan A, et al.The coronatine toxin of Pseudomonas syringae is a multifunctional suppressor of Arabidopsis defense[J]. Plant Cell, 2012, 24(11):4763-4774.
[55] Zheng XY, Spivey NW, Zeng W, et al.Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation[J]. Cell Host Microbe, 2012, 11(6):587-596.
[56] Melotto M, Underwood W, Koczan J, et al.Plant stomata function in innate immunity against bacterial invasion[J]. Cell, 2006, 126(5):969-980.
[57] Cui H, Wang Y, et al.Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4[J]. Cell Host Microbe, 2010, 7(2):164-175.
[58] Zhou Z, Wu Y, Yang Y, et al.An Arabidopsis plasma membrane proton ATPase modulates JA signaling and is exploited by the Pseudomonas syringae effector protein AvrB for stomatal invasion[J]. Plant Cell, 2015, 27(7):2032-2041.
[59] Jiang S, Yao J, Ma KW, et al.Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors[J]. PLoS Pathog, 2013, 9(10):e1003715.
[60] Gimenez-Ibanez S, Boter M, Fernandez-Barbero G, et al.The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis[J]. PLoS Biology, 2014, 12(2):e1001792.
[61] Yang L, Teixeira PJ, Biswas S, et al.Pseudomonas syringae type III effector HopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses and virulence[J]. Cell Host Microbe, 2017, 21(2):156-168.
[62] El Oirdi M, El Rahman TA, Rigano L, et al.Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato[J]. Plant Cell, 2011, 23(6):2405-2421.
[63] Zhu W, Wei W, Fu Y, et al.A secretory protein of necrotrophic fungus Sclerotinia sclerotiorum that suppresses host resistance[J]. PLoS One, 2013, 8(1):e53901.
[64] Plett JM, Daguerre Y, Wittulsky S, et al.Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid(JA)responsive genes[J]. Proc Natl Acad Sci USA, 2014, 111(22):8299-8304.
[65] Gimenez-Ibanez S, Chini A, Solano R.How microbes twist jasmonate signaling around their little fingers[J]. Plants(Basel), 2016, 5(1):9.
[66] Thatcher LF, Gardiner DM, Kazan K, et al.A highly conserved effector in Fusarium oxysporum is required for full virulence on Arabidopsis[J]. Mol Plant Microbe In, 2012, 25(2):180-190.
[67] Thatcher LF, Manners JM, Kazan K.Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis[J]. Plant J, 2009, 58(6):927-939.
[68] Sugio A, Kingdom HN, MacLean AM, et al. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis[J]. Proc Natl Acad Sci USA, 2011, 108(48):E1254-E1263.
[69] Ziebell H, Murphy AM, Groen SC, et al.Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco[J]. Sci Rep, 2011, 1:187.
[70] Lewsey MG, Murphy AM, MacLean D, et al. Disruption of two defensive signaling pathways by a viral RNA silencing suppressor[J]. Mol Plant Microbe Intrant, 2010, 23(7):835-845.
[71] Wu D, Qi T, Li WX, et al.Viral effector protein manipulates host hormone signaling to attract insect vectors[J]. Cell Res, 2017, 27(3):402-415.
[72] Li R, Weldegergis BT, Li J, et al.Virulence factors of geminivirus interact with MYC2 to subvert plant resistance and promote vector performance[J]. Plant Cell, 2014, 26(12):4991-5008.
[73] Yang JY, Iwasaki M, Machida C, et al.betaC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses[J]. Gene Dev, 2008, 22(18):2564-2577.
[74] Zhang T, Luan JB, Qi JF, et al.Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor[J]. Mol Ecol, 2012, 21(5):1294-1304.
[75] Zhang C, Ding Z, Wu K, et al.Suppression of jasmonic acid-mediated defense by viral-inducible microRNA319 facilitates virus infection in rice[J]. Mol Plant, 2016, 9(9):1302-1314.
[76] Lozano-Duran R, Rosas-Diaz T, Gusmaroli G, et al.Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana[J]. Plant Cell, 2011, 23(3):1014-1032.
[77] Jia Q, Liu N, et al.CLCuMuB betaC1 subverts ubiquitination by interacting with NbSKP1s to enhance geminivirus infection in Nicotiana benthamiana[J]. PLoS Pathog, 2016, 12(6):e1005668.
[78] Westwood JH, Lewsey MG, Murphy AM, et al.Interference with jasmonic acid-regulated gene expression is a general property of viral suppressors of RNA silencing but only partly explains virus-induced changes in plant-aphid interactions[J]. J Gen Virol, 2014, 95:733-739.
[79] Rojas MR, Hagen C, Lucas WJ, et al.Exploiting chinks in the plant’s armor:evolution and emergence of geminiviruses[J]. Annu Rev Phytopathol, 2005, 43:361-394.
[80] Cui X, Li G, et al.A begomovirus DNAbeta-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus[J]. J Virol, 2005, 79(16):10764-10775.
[81] Li HW, Lucy AP, Guo HS, et al.Strong host resistance targeted against a viral suppressor of the plant gene silencing defence mechanism[J]. EMBO J, 1999, 18(10):2683-2691.
[82] Oka K, Kobayashi M, Mitsuhara I, et al.Jasmonic acid negatively regulates resistance to tobacco mosaic virus in tobacco[J]. Plant Cell Physiol, 2013, 54(12):1999-2010.