Insights into the role of jasmonic acid-mediated defenses against necrotrophic and biotrophic fungal pathogens

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 JA-dependent 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.

Keywords

jasmonic acid (JA) / methyl jasmonate (MeJA) / biotrophic fungi / necrotrophic fungi / COI1

References

[1] 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

[2] 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

[3] 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

[4] 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 oxidase-mediated defense responses. PLoS ONE, 5(12): e14426

[5] 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

[6] 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

[7] 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

[8] Cui H, Wang Y, Xue L, Chu J, Yan C, Fu J, Chen M, Innes R W, 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

[9] 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

[10] 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

[11] 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

[12] 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

[13] 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

[14] 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

[15] 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

[16] 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

[17] 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

[18] 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

[19] 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

[20] Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, Zhang Y (2008). MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res, 18(12): 1190–1198

[21] Gfeller A, Liechti R, Farmer E E (2010). Arabidopsis jasmonate signaling pathway.Sci Signal, 3(109): cm4

[22] Glazebrook J (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol, 43(1): 205–227

[23] 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

[24] Guo H, Ecker J R (2004). The ethylene signaling pathway: new insights. Curr Opin Plant Biol, 7(1): 40–49

[25] 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

[26] 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

[27] 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

[28] Kachroo A, Kachroo P (2009). Fatty Acid-derived signals in plant defense. Annu Rev Phytopathol, 47(1): 153–176

[29] Kazan K, Manners J M (2008). Jasmonate signaling: toward an integrated view. Plant Physiol, 146(4): 1459–1468

[30] 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

[31] 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

[32] Kunkel B N, Brooks D M (2002). Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol, 5(4): 325–331

[33] 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

[34] 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

[35] 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

[36] 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

[37] 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

[38] Miersch O, Schneider G, Sembdner G (1991). Hydroxylated jasmonic acid and related compounds from Botryodiplodia theobromae. Phytochemistry, 30(12): 4049–4051

[39] 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

[40] 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

[41] 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

[42] 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

[43] 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

[44] 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 mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol, 148(1): 212–222

[45] 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

[46] 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

[47] 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

[48] 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

[49] 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

[50] 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

[51] 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

[52] 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

[53] 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

[54] 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

[55] Thomma B P, Eggermont K, Penninckx I A, Mauch-Mani B, Vogelsang R, Cammue B P, Broekaert W F (1998). Separate jasmonate-dependent 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

[56] 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

[57] van Wees 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

[58] Vick B A, Zimmerman D C (1984). Biosynthesis of jasmonic acid by several plant species. Plant Physiol, 75(2): 458–461

[59] 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

[60] 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

[61] Wan J, Zhang X C, Neece D, Ramonell K M, 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

[62] 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

[63] 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

[64] 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

[65] 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

[66] 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

[67] 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

[68] Yalpani N, Silverman P, Wilson T M, Kleier D A, Raskin I (1991). Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell, 3(8): 809–818

[69] 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

[70] 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

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag Berlin Heidelberg