Abstract
Jasmonic acid (JA) is a natural hormone regulator involved in development, responses against wounding and pathogen attack. Upon perception of pathogens, JA is synthesized and mediates a signaling cascade initiating various defense responses. Traditionally, necrotrophic fungi have been shown to be the primary activators of JAdependent defenses through the JA-receptor, COI1. Conversely, plants infected with biotrophic fungi have classically been associated with suppressing JA-mediated responses. However, recent evidence has shown that certain biotrophic fungal species also trigger activation of JA-mediated responses and mutants deficient in JA signaling show an increase in susceptibility to certain biotrophic fungal pathogens. These findings suggest a new role for JA in defense against fungal biotrophs. This review will focus on recent research advancing our knowledge of JA-dependant responses involved in defense against both biotrophic and necrotrophic fungi.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
AbuQamar S, Chai M F, Luo H, Song F, Mengiste T (2008). Tomato protein kinase 1b mediates signaling of plant responses to necrotrophic fungi and insect herbivory. Plant Cell, 20(7): 1964–1983
Avdiushko S, Croft K P, Brown G C, Jackson D M, Hamilton-Kemp T R, Hildebrand D (1995). Effect of volatile methyl jasmonate on the oxylipin pathway in tobacco, cucumber, and arabidopsis. Plant Physiol, 109(4): 1227–1230
Berrocal-Lobo M, Molina A, Solano R (2002). Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J, 29(1): 23–32
Berrocal-Lobo M, Stone S, Yang X, Antico J, Callis J, Ramonell K M, Somerville S (2010). ATL9, a RING zinc finger protein with E3 ubiquitin ligase activity implicated in chitin- and NADPH oxidasemediated defense responses. PLoS ONE, 5(12): e14426
Brodersen P, Petersen M, Bjørn Nielsen H, Zhu S, Newman M A, Shokat K M, Rietz S, Parker J, Mundy J (2006). Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J, 47(4): 532–546
Chehab E W, Kim S, Savchenko T, Kliebenstein D, Dehesh K, Braam J (2011). Intronic T-DNA insertion renders Arabidopsis opr3 a conditional jasmonic acid-producing mutant. Plant Physiol, 156(2): 770–778
Chini A, Fonseca S, Fernández G, Adie B, Chico J M, Lorenzo O, García-Casado G, López-Vidriero I, Lozano F M, Ponce M R, Micol J L, Solano R (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature, 448(7154): 666–671
Cui H, Wang Y, Xue L, Chu J, Yan C, Fu J, Chen M, Innes RW, Zhou J M (2010). Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe, 7(2): 164–175
Desmond O J, Edgar C I, Manners J M, Maclean D J, Schenk P M, Kazan K (2005). Methyl jasmonate induced gene expression in wheat delays symptom development by the crown rot pathogen Fusarium pseudograminearum. Physiol Mol Plant Pathol, 67(3–5): 171–179
Dombrecht B, Xue G P, Sprague S J, Kirkegaard J A, Ross J J, Reid J B, Fitt G P, Sewelam N, Schenk P M, Manners J M, Kazan K (2007). MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell, 19(7): 2225–2245
Egusa M, Ozawa R, Takabayashi J, Otani H, Kodama M (2009). The jasmonate signaling pathway in tomato regulates susceptibility to a toxin-dependent necrotrophic pathogen. Planta, 229(4): 965–976
El-Wakeil N E, Volkmar C, Sallam A A (2010). Jasmonic acid induces resistance to economically important insect pests in winter wheat. Pest Manag Sci, 66(5): 549–554
Ellis C, Karafyllidis I, Turner J G (2002). Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol Plant Microbe Interact, 15(10): 1025–1030
Ellis C, Turner J G (2001). The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell, 13(5): 1025–1033
Fabro G, Di Rienzo J A, Voigt C A, Savchenko T, Dehesh K, Somerville S, Alvarez M E (2008). Genome-wide expression profiling Arabidopsis at the stage of Golovinomyces cichoracearum haustorium formation. Plant Physiol, 146(3): 1421–1439
Farmer E E, Alméras E, Krishnamurthy V (2003). Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol, 6(4): 372–378
Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel F M, Dewdney J (2007). Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol, 144(1): 367–379
Frenkel M, Kulheim C, Jankanpaaa H J, Skogstrom O, Dall’Osto L, Agren J, Bassi R, Moritz T, Moen J, Jansson S (2009). Improper excess light energy dissipation in Arabidopsis results in a metabolic reprogramming. BMC Plant Biol, 9:12
Frye C A, Tang D Z, Innes R W (2001). Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA, 98(1): 373–378
Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, Zhang Y (2008). MEKK1, MKK1/MKK2 and MPK4 function together in a mitogenactivated protein kinase cascade to regulate innate immunity in plants. Cell Res, 18(12): 1190–1198
Gfeller A, Liechti R, Farmer E E (2010). Arabidopsis jasmonate signaling pathway. Sci Signal, 3(109): cm4
Glazebrook J (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol, 43(1): 205–227
Glazebrook J, Chen W, Estes B, Chang H S, Nawrath C, Métraux J P, Zhu T, Katagiri F (2003). Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J, 34(2): 217–228
Guo H, Ecker J R (2004). The ethylene signaling pathway: new insights. Curr Opin Plant Biol, 7(1): 40–49
Gupta V, Willits M G, Glazebrook J (2000). Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. Mol Plant Microbe Interact, 13(5): 503–511
Hilpert B, Bohlmann H, op den Camp R O, Przybyla D, Miersch O, Buchala A, Apel K (2001). Isolation and characterization of signal transduction mutants of Arabidopsis thaliana that constitutively activate the octadecanoid pathway and form necrotic microlesions. Plant J, 26(4): 435–446
Jayaraj J, Muthukrishnan S, Liang G H, Velazhahan R (2004). Jasmonic acid and salicylic acid induce accumulation of β-1,3-glucanase and thaumatin-like proteins in wheat and enhance resistance against Stagonospora nodorum. Biol Plant, 48(3): 425–430
Kachroo A, Kachroo P (2009). Fatty Acid-derived signals in plant defense. Annu Rev Phytopathol, 47(1): 153–176
Kazan K, Manners J M (2008). Jasmonate signaling: toward an integrated view. Plant Physiol, 146(4): 1459–1468
Kidd B N, Edgar C I, Kumar K K, Aitken E A, Schenk P M, Manners J M, Kazan K (2009). The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell, 21(8): 2237–2252
Kloek A P, Verbsky M L, Sharma S B, Schoelz J E, Vogel J, Klessig D F, Kunkel B N (2001). Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J, 26(5): 509–522
Kunkel B N, Brooks D M (2002). Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol, 5(4): 325–331
Li J, Brader G, Kariola T, Palva E T (2006). WRKY70 modulates the selection of signaling pathways in plant defense. Plant J, 46(3): 477–491
Li J, Brader G, Palva E T (2004). The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell, 16(2): 319–331
Lorenzo O, Chico J M, Sánchez-Serrano J J, Solano R (2004). JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell, 16(7): 1938–1950
Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks A A, Shah J (2010). Involvement of salicylate and jasmonate signaling pathways in Arabidopsis interaction with Fusarium graminearum. Mol Plant Microbe Interact, 23(7): 861–870
McConn M, Browse J (1996). The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell, 8(3): 403–416
Miersch O, Schneider G, Sembdner G (1991). Hydroxylated jasmonic acid and related compounds from Botryodiplodia theobromae. Phytochemistry, 30(12): 4049–4051
Murray S L, Ingle R A, Petersen L N, Denby K J (2007). Basal resistance against Pseudomonas syringae in Arabidopsis involves WRKY53 and a protein with homology to a nematode resistance protein. Mol Plant Microbe Interact, 20(11): 1431–1438
Pena-Cortes H, Barrios P, Dorta F, Polanco V, Sanchez C, Sanchez E, Ramirez I (2004). Involvement of jasmonic acid and derivatives in plant responses to pathogens and insects and in fruit ripening. J Plant Growth Regul, 23: 246–260
Penninckx I A, Eggermont K, Terras F R, Thomma B P, De Samblanx G W, Buchala A, Métraux J P, Manners J M, Broekaert W F (1996). Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell, 8(12): 2309–2323
Penninckx I A, Thomma B P, Buchala A, Métraux J P, Broekaert W F (1998). Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell, 10(12): 2103–2113
Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen H B, Lacy M, Austin M J, Parker J E, Sharma S B, Klessig D F, Martienssen R, Mattsson O, Jensen A B, Mundy J (2000). Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell, 103(7): 1111–1120
Qiu J L, Zhou L, Yun B W, Nielsen H B, Fiil B K, Petersen K, Mackinlay J, Loake G J, Mundy J, Morris P C (2008). Arabidopsis mitogenactivated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol, 148(1): 212–222
Ramonell K, Berrocal-Lobo M, Koh S, Wan J, Edwards H, Stacey G, Somerville S (2005). Loss-of-function mutations in chitin responsive genes show increased susceptibility to the powdery mildew pathogen Erysiphe cichoracearum. Plant Physiol, 138(2): 1027–1036
Schmelz E A, Kaplan F, Huffaker A, Dafoe N J, Vaughan M M, Ni X, Rocca J R, Alborn H T, Teal P E (2011). Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize. Proc Natl Acad Sci USA, 108(13): 5455–5460
Spoel S H, Johnson J S, Dong X (2007). Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA, 104(47): 18842–18847
Staswick P E, Tiryaki I (2004). The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell, 16(8): 2117–2127
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(19): 10625–10630
Stintzi A, Weber H, Reymond P, Browse J, Farmer E E (2001). Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci USA, 98(22): 12837–12842
Takahashi H, Kanayama Y, Zheng M S, Kusano T, Hase S, Ikegami M, Shah J (2004). Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiol, 45(6): 803–809
Thaler J S, Owen B, Higgins V J (2004). The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol, 135(1): 530–538
Thatcher L F, Manners J M, Kazan K (2009). Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis. Plant J, 58(6): 927–939
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He S Y, Howe G A, Browse J (2007). JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature, 448(7154): 661–665
Thomma B P, Eggermont K, Penninckx I A, Mauch-Mani B, Vogelsang R, Cammue B P, Broekaert W F (1998). Separate jasmonatedependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA, 95(25): 15107–15111
Thomma B P, Nelissen I, Eggermont K, Broekaert W F (1999). Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J, 19(2): 163–171
vanWees S C, Chang H S, Zhu T, Glazebrook J (2003). Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol, 132(2): 606–617
Vick B A, Zimmerman D C (1984). Biosynthesis of jasmonic acid by several plant species. Plant Physiol, 75(2): 458–461
Vijayan P, Shockey J, Lévesque C A, Cook R J, Browse J (1998). A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci USA, 95(12): 7209–7214
Walters D, Cowley T, Mitchell A (2002). Methyl jasmonate alters polyamine metabolism and induces systemic protection against powdery mildew infection in barley seedlings. J Exp Bot, 53(369): 747–756
Wan J, Zhang X C, Neece D, Ramonell KM, Clough S, Kim S Y, Stacey M G, Stacey G (2008). A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell, 20(2): 471–481
Wang Z, Mao H, Dong C, Ji R, Cai L, Fu H, Liu S (2009). Overexpression of Brassica napus MPK4 enhances resistance to Sclerotinia sclerotiorum in oilseed rape. Mol Plant Microbe Interact, 22(3): 235–244
Wasternack C (2007). Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot (Lond), 100(4): 681–697
Wasternack C, Kombrink E (2010). Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol, 5(1): 63–77
Xiao, S., Ellwood, S., Findlay, K., Oliver, R.P., and Turner, J.G. (1997). Characterization of three loci controlling resistance of Arabidopsis thaliana accession Ms-0 to two powdery mildew diseases. Plant J, 12: 757–768
Xie D X, Feys B F, James S, Nieto-Rostro M, Turner J G (1998). COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science, 280(5366): 1091–1094
Xu L, Liu F, Lechner E, Genschik P, Crosby W L, 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(8): 1919–1935
Yalpani N, Silverman P, Wilson T M, Kleier D A, Raskin I (1991). Salicylic acid is a systemic signal and an inducer of pathogenesisrelated proteins in virus-infected tobacco. Plant Cell, 3(8): 809–818
Zhou N, Tootle T L, Glazebrook J (1999). Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell, 11(12): 2419–2428
Zimmerli L, Stein M, Lipka V, Schulze-Lefert P, Somerville S (2004). Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J, 40(5): 633–646
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Antico, C.J., Colon, C., Banks, T. et al. Insights into the role of jasmonic acid-mediated defenses against necrotrophic and biotrophic fungal pathogens. Front. Biol. 7, 48–56 (2012). https://doi.org/10.1007/s11515-011-1171-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11515-011-1171-1