Please wait a minute...

Frontiers in Biology

Front Biol    2012, Vol. 7 Issue (1) : 48-56
Insights into the role of jasmonic acid-mediated defenses against necrotrophic and biotrophic fungal pathogens
Christopher J. ANTICO, Chad COLON, Taylor BANKS, Katrina M. RAMONELL()
Department of Biological Sciences, University of Alabama, Tuscaloosa, AL 35487, USA
Download: PDF(298 KB)   HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

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     
Corresponding Author(s): RAMONELL Katrina M.,   
Issue Date: 01 February 2012
 Cite this article:   
Christopher J. ANTICO,Chad COLON,Taylor BANKS, et al. Insights into the role of jasmonic acid-mediated defenses against necrotrophic and biotrophic fungal pathogens[J]. Front Biol, 2012, 7(1): 48-56.
E-mail this article
E-mail Alert
Articles by authors
Christopher J. ANTICO
Taylor BANKS
Fig.1  Schematic Diagram of the JA signaling pathway. JA biosynthesis is initiated by necrotrophic fungal infection, wounding, and herbivory. Once synthesized, derivatives of JA can be modified by JMT making methyl jasmonate and JAR1 with the addition of isoleucine. JA and its derivatives migrate across the nuclear envelope where they are bound by the JA-receptor, COI1. SCF-COI1 complex is activated by JA and specifically targets JAZ proteins (JAZ3 and JAZ1) for protein ubiquitination and subsequent degradation by the proteasome. JAZ proteins are negative regulators of JA-responsive genes. However, once degraded, (also known as ) transcription factor can transcribe JA-responsive genes, which can activate or repress several different functions. The SA-mediated pathway acts antagonistically to repress JA signaling. SA can directly inhibit JA, and activate , which also inhibits JA. Conversely, JA can inhibit SA-mediated responses by suppressing expression through the SCF-COI1 complex. JA signaling can be activated and repressed through other proteins in various pathways. In the MAP kinase cascade, , bound to , can activate JA signaling, but the complex of and can suppress JA-responsive gene, . Red arrows indicate activation. Blue bars indicate suppression. Red dotted arrows indicate binding. Blue dotted arrows indicate degradation. Modified from Kazan and Manners, 2008.
A. thalianaA. brassicicolacoi1SusceptibleThomma et al., 1998
A. thalianaB. cinereacoi1SusceptibleThomma et al., 1998
A. thalianaP. cucumerinacoi1SusceptibleThomma et al., 1998
A. thalianaF. oxysporumcoi1SusceptibleThatcher et al., 2009
A. thalianaB. cinereajar1SusceptibleKachroo and Kachroo, 2009
A. thalianaA. brasscicolapad3SusceptibleFerrari et al., 2007
A. thalianaB. cinereapad3SusceptibleFerrari et al., 2007
A. thalianaA. brasscicolafad3 fad7 fad8SusceptibleStintzi et al., 2001
A. thalianaA. brasscicolaopr3ResistantStintzi et al., 2001
A. thalianaB. cinereaopr3ResistantChehab et., 2011
A. thalianaB. cinereajin1ResistantKachroo and Kachroo, 2009
A. thalianaP. cucumerinajin1ResistantKachroo and Kachroo, 2009
A. thalianaF. graminearumopr3ResistantMakandar et al., 2010
A. thalianaF. graminearumcoi1ResistantMakandar et al., 2010
A. thalianaF. graminearumjar1ResistantMakandar et al., 2010
L. esculentum (Tomato)F. oxysporumdef1SusceptibleThaler et al., 2004
L. esculentum (Tomato)V. dahliadef1SusceptibleThaler et al., 2004
L. esculentum (Tomato)B. cinereadef1SusceptibleThaler et al., 2004
L. esculentum (Tomato)Fusarium speciesjai1SusceptibleThaler et al., 2004
L. esculentum (Tomato)B. cinereajai1SusceptibleAbuQamar et al., 2008
L. esculentum (Tomato)B. cinereaspr2SusceptibleLi et al., 2004;AbuQamar et al., 2008
L. esculentum (Tomato)B. cinereaacx1SusceptibleLi et al., 2006
L. esculentum (Tomato)A. alternatedef1ResistantEgusa et al., 2009
T. aestivum (Wheat)F. oxysporumpft1SusceptibleKidd et al., 2009
Tab.1  The phenotypes of JA-related mutants when challenged with necrotrophic fungi
A. thalianaG. cichoracearumcoi1SusceptibleKloek et al., 2001; Ellis et al., 2002
A. thalianaG. cichoracearumcev1ResistantXiao et al., 1997; Ellis et al., 2002
A. thalianaG. cichoracearumjar1SusceptibleFabro et al., 2008
A. thalianaE. orontiicev1ResistantEllis and Turner, 2001
L. esculentum (Tomato)C. fulvumdef1NeutralThaler et al., 2004
L. esculentum (Tomato)O. neolycopersicidef1NeutralThaler et al., 2004
Tab.2  The phenotypes of JA-related mutants when challenged with biotrophic fungi
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
doi: 10.1105/tpc.108.059477 pmid:18599583
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
doi: 10.1104/pp.109.4.1227 pmid:8539290
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
doi: 10.1046/j.1365-313x.2002.01191.x pmid:12060224
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
doi: 10.1371/journal.pone.0014426 pmid:21203445
5 Brodersen P, Petersen M, Bj?rn 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
doi: 10.1111/j.1365-313X.2006.02806.x pmid:16813576
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
doi: 10.1104/pp.111.174169 pmid:21487047
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
doi: 10.1038/nature06006 pmid:17637675
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
doi: 10.1016/j.chom.2010.01.009 pmid:20159621
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
doi: 10.1016/j.pmpp.2005.12.007
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
doi: 10.1105/tpc.106.048017 pmid:17616737
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
doi: 10.1007/s00425-009-0890-x pmid:19148670
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
doi: 10.1002/ps.1906 pmid:20127756
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
doi: 10.1094/MPMI.2002.15.10.1025 pmid:12437300
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
doi: 10.1104/pp.107.111286 pmid:18218973
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
doi: 10.1016/S1369-5266(03)00045-1 pmid:12873533
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
doi: 10.1104/pp.107.095596 pmid:17384165
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
doi: 10.1073/pnas.011405198 pmid:11114160
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
doi: 10.1038/cr.2008.300 pmid:18982020
21 Gfeller A, Liechti R, Farmer E E (2010). Arabidopsis jasmonate signaling pathway.Sci Signal , 3(109): cm4
doi: 10.1126/scisignal.3109cm4 pmid:20159850
22 Glazebrook J (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol , 43(1): 205–227
doi: 10.1146/annurev.phyto.43.040204.135923 pmid:16078883
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
doi: 10.1046/j.1365-313X.2003.01717.x pmid:12694596
24 Guo H, Ecker J R (2004). The ethylene signaling pathway: new insights. Curr Opin Plant Biol , 7(1): 40–49
doi: 10.1016/j.pbi.2003.11.011 pmid:14732440
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
doi: 10.1094/MPMI.2000.13.5.503 pmid:10796016
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
doi: 10.1046/j.1365-313X.2001.2641036.x pmid:11439130
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
doi: 10.1023/B:BIOP.0000041097.03177.2d
28 Kachroo A, Kachroo P (2009). Fatty Acid-derived signals in plant defense. Annu Rev Phytopathol , 47(1): 153–176
doi: 10.1146/annurev-phyto-080508-081820 pmid:19400642
29 Kazan K, Manners J M (2008). Jasmonate signaling: toward an integrated view. Plant Physiol , 146(4): 1459–1468
doi: 10.1104/pp.107.115717 pmid:18390489
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
doi: 10.1105/tpc.109.066910 pmid:19671879
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
doi: 10.1046/j.1365-313x.2001.01050.x pmid:11439137
32 Kunkel B N, Brooks D M (2002). Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol , 5(4): 325–331
doi: 10.1016/S1369-5266(02)00275-3 pmid:12179966
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
doi: 10.1111/j.1365-313X.2006.02712.x pmid:16623907
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
doi: 10.1105/tpc.016980 pmid:14742872
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
doi: 10.1105/tpc.022319 pmid:15208388
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
doi: 10.1094/MPMI-23-7-0861 pmid:20521949
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
doi: 10.1105/tpc.8.3.403 pmid:12239389
38 Miersch O, Schneider G, Sembdner G (1991). Hydroxylated jasmonic acid and related compounds from Botryodiplodia theobromae. Phytochemistry , 30(12): 4049–4051
doi: 10.1016/0031-9422(91)83464-V
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
doi: 10.1094/MPMI-20-11-1431 pmid:17977154
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
doi: 10.1016/S0092-8674(00)00213-0 pmid:11163186
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
doi: 10.1104/pp.108.120006 pmid:18599650
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
doi: 10.1104/pp.105.060947 pmid:15923325
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
doi: 10.1073/pnas.1014714108 pmid:21402917
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
doi: 10.1073/pnas.0708139104 pmid:17998535
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
doi: 10.1105/tpc.104.023549 pmid:15258265
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
doi: 10.1073/pnas.190264497 pmid:10973494
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
doi: 10.1073/pnas.211311098 pmid:11592974
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
doi: 10.1093/pcp/pch085 pmid:15215516
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
doi: 10.1104/pp.104.041566 pmid:15133157
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
doi: 10.1111/j.1365-313X.2009.03831.x pmid:19220788
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
doi: 10.1038/nature05960 pmid:17637677
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
doi: 10.1073/pnas.95.25.15107 pmid:9844023
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
doi: 10.1046/j.1365-313X.1999.00513.x pmid:10476063
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
doi: 10.1104/pp.103.022186 pmid:12805591
58 Vick B A, Zimmerman D C (1984). Biosynthesis of jasmonic acid by several plant species. Plant Physiol , 75(2): 458–461
doi: 10.1104/pp.75.2.458 pmid:16663643
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
doi: 10.1073/pnas.95.12.7209 pmid:9618564
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
doi: 10.1093/jexbot/53.369.747 pmid:11886895
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
doi: 10.1105/tpc.107.056754 pmid:18263776
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
doi: 10.1094/MPMI-22-3-0235 pmid:19245318
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
doi: 10.1093/aob/mcm079 pmid:17513307
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
doi: 10.1021/cb900269u pmid:20025249
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
doi: 10.1126/science.280.5366.1091 pmid:9582125
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
doi: 10.1105/tpc.003368 pmid:12172031
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
doi: 10.1111/j.1365-313X.2004.02236.x pmid:15546348
Related articles from Frontiers Journals
[1] Xin YANG, Fengyang DENG, Katrina M. RAMONELL. Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity[J]. Front Biol, 2012, 7(2): 155-166.
Full text