Leptosphaeria maculans effector AvrLm4-7 affects salicylic acid (SA) and ethylene (ET) signalling and hydrogen peroxide (H2 O2 ) accumulation in Brassica napus
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
26575525
PubMed Central
PMC6638468
DOI
10.1111/mpp.12332
Knihovny.cz E-zdroje
- Klíčová slova
- AvrLm4-7, Brassica napus, Leptosphaeria, ROS, effector, ethylene, salicylic acid,
- MeSH
- alely MeSH
- antioxidancia farmakologie MeSH
- Ascomycota účinky léků izolace a purifikace metabolismus MeSH
- Brassica napus účinky léků růst a vývoj metabolismus mikrobiologie MeSH
- chromatografie kapalinová MeSH
- cyklopentany metabolismus MeSH
- ethyleny metabolismus MeSH
- fungální proteiny metabolismus MeSH
- hmotnostní spektrometrie MeSH
- interakce hostitele a patogenu účinky léků MeSH
- kotyledon účinky léků metabolismus mikrobiologie MeSH
- kyselina abscisová metabolismus MeSH
- kyselina askorbová farmakologie MeSH
- kyselina salicylová metabolismus MeSH
- oxylipiny metabolismus MeSH
- peroxid vodíku metabolismus MeSH
- polymerázová řetězová reakce s reverzní transkripcí MeSH
- regulátory růstu rostlin metabolismus MeSH
- signální transdukce * účinky léků MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- antioxidancia MeSH
- cyklopentany MeSH
- ethyleny MeSH
- fungální proteiny MeSH
- jasmonic acid MeSH Prohlížeč
- kyselina abscisová MeSH
- kyselina askorbová MeSH
- kyselina salicylová MeSH
- oxylipiny MeSH
- peroxid vodíku MeSH
- regulátory růstu rostlin MeSH
To achieve host colonization, successful pathogens need to overcome plant basal defences. For this, (hemi)biotrophic pathogens secrete effectors that interfere with a range of physiological processes of the host plant. AvrLm4-7 is one of the cloned effectors from the hemibiotrophic fungus Leptosphaeria maculans 'brassicaceae' infecting mainly oilseed rape (Brassica napus). Although its mode of action is still unknown, AvrLm4-7 is strongly involved in L. maculans virulence. Here, we investigated the effect of AvrLm4-7 on plant defence responses in a susceptible cultivar of B. napus. Using two isogenic L. maculans isolates differing in the presence of a functional AvrLm4-7 allele [absence ('a4a7') and presence ('A4A7') of the allele], the plant hormone concentrations, defence-related gene transcription and reactive oxygen species (ROS) accumulation were analysed in infected B. napus cotyledons. Various components of the plant immune system were affected. Infection with the 'A4A7' isolate caused suppression of salicylic acid- and ethylene-dependent signalling, the pathways regulating an effective defence against L. maculans infection. Furthermore, ROS accumulation was decreased in cotyledons infected with the 'A4A7' isolate. Treatment with an antioxidant agent, ascorbic acid, increased the aggressiveness of the 'a4a7' L. maculans isolate, but not that of the 'A4A7' isolate. Together, our results suggest that the increased aggressiveness of the 'A4A7' L. maculans isolate could be caused by defects in ROS-dependent defence and/or linked to suppressed SA and ET signalling. This is the first study to provide insights into the manipulation of B. napus defence responses by an effector of L. maculans.
Faculty of Science Charles University Prague Prague Czech Republic
INRA UMR INRA AgroParisTech 1290 Bioger Avenue Lucien Brétignières Thiverval Grignon France
Institute of Experimental Botany Academy of Sciences of the Czech Republic Prague Czech Republic
Zobrazit více v PubMed
Ansan‐Melayah, D. , Balesdent, M. , Buée, M. and Rouxel, T. (1995) Genetic characterization of AvrLm1, the first avirulence gene of Leptosphaeria maculans . Phytopathology, 85, 1525–1529.
Apel, K. and Hirt, H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399. PubMed
Balesdent, M. , Attard, A. , Kühn, M. and Rouxel, T. (2002) New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans . Phytopathology, 92, 1122–1133. PubMed
Balesdent, M. , Barbetti, M. , Li, H. , Sivasithamparam, K. , Gout, L. and Rouxel, T. (2005) Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology, 95, 1061–1071. PubMed
Balesdent, M.H. , Fudal, I. , Ollivier, B. , Bally, P. , Grandaubert, J. , Eber, F. , Chèvre, A.M. , Leflon, M. and Rouxel, T. (2013) The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa . New Phytol. 198, 887–898. PubMed
Balesdent, M.‐H. , Louvard, K. , Pinochet, X. and Rouxel, T. (2006) A large‐scale survey of races of Leptosphaeria maculans occurring on oilseed rape in France. Eur. J. Plant Pathol. 114, 53–65.
Bell, E. , Creelman, R.A. and Mullet, J.E. (1995) A chloroplast lipoxygenase is required for wound‐induced jasmonic acid accumulation in Arabidopsis . Proc. Natl. Acad. Sci. USA, 92, 8675–8679. PubMed PMC
Block, A. and Alfano, J.R. (2011) Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr. Opin. Microbiol. 14, 39–46. PubMed PMC
Blondeau, K. , Blaise, F. , Graille, M. , Kale, S.D. , Linglin, J. , Ollivier, B. , Labarde, A. , Lazar, N. , Daverdin, G. , Balesdent, M.H. Choi, D.H.Y. , Tyler, B.M. , Rouxel, T. , van Tilbeurgh, H. and Fudal, I. (2015) Crystal structure of the effector AvrLm4–7 of Leptosphaeria maculans reveals insights into its translocation into plant cells and recognition by resistance proteins. Plant J. 83, 610–624. doi: 10.1111/tpj.12913. PubMed DOI
Buscaill, P. and Rivas, S. (2014) Transcriptional control of plant defence responses. Curr. Opin. Plant Biol. 20, 35–46. PubMed
Chisholm, S.T. , Coaker, G. , Day, B. and Staskawicz, B.J. (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell, 124, 803–814. PubMed
Denancé, N. , Sánchez‐Vallet, A. , Goffner, D. and Molina, A. (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front. Plant Sci. 4, 155. PubMed PMC
Deslandes, L. and Rivas, S. (2012) Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17, 644–655. PubMed
Dobrev, P.I. and Kamínek, M. (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed‐mode solid‐phase extraction. J. Chromatogr. A, 950, 21–29. PubMed
Dobrev, P.I. and Vankova, R. (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt‐stressed plant tissues In: Plant Salt Tolerance, pp. 251–261. Springer. PubMed
Dodds, P.N. and Rathjen, J.P. (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11, 539–548. PubMed
Doehlemann, G. and Hemetsberger, C. (2013) Apoplastic immunity and its suppression by filamentous plant pathogens. New Phytol. 198, 1001–1016. PubMed
Dou, D. and Zhou, J.‐M. (2012) Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe, 12, 484–495. PubMed
Draper, J. (1997) Salicylate, superoxide synthesis and cell suicide in plant defence. Trends Plant Sci. 2, 162–165.
Foyer, C.H. and Noctor, G. (2013) Redox signaling in plants. Antioxid. Redox. Signal. 18, 2087–2090. PubMed
Fudal, I. , Ross, S. , Gout, L. , Blaise, F. , Kuhn, M. , Eckert, M. , Cattolico, L. , Bernard‐Samain, S. , Balesdent, M.H. and Rouxel, T. (2007) Heterochromatin‐like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map‐based cloning of AvrLm6 . Mol. Plant–Microbe Interact. 20, 459–470. PubMed
Gan, P. , Ikeda, K. , Irieda, H. , Narusaka, M. , O'Connell, R.J. , Narusaka, Y. , Takano, Y. , Kubo, Y. and Shirasu, K. (2013) Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol. 197, 1236–1249. PubMed
Gardiner, D.M. and Howlett, B.J. (2004) Negative selection using thymidine kinase increases the efficiency of recovery of transformants with targeted genes in the filamentous fungus Leptosphaeria maculans . Curr. Genet. 45, 249–255. PubMed
Ghanbarnia, K. , Fudal, I. , Larkan, N.J. , Links, M.G. , Balesdent, M.H. , Profotova, B. , Fernando, W. , Rouxel, T. and Borhan, M.H. (2015) Rapid identification of the Leptosphaeria maculans avirulence gene AvrLm2, using an intraspecific comparative genomics approach. Mol. Plant Pathol. 16, 699–709. PubMed PMC
Ghanbarnia, K. , Lydiate, D.J. , Rimmer, S.R. , Li, G. , Kutcher, H.R. , Larkan, N.J. , McVetty, P.B. and Fernando, W.D. (2012) Genetic mapping of the Leptosphaeria maculans avirulence gene corresponding to the LepR1 resistance gene of Brassica napus . Theor. Appl. Genet. 124, 505–513. PubMed
Giraldo, M.C. and Valent, B. (2013) Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11, 800–814. PubMed
Glazebrook, J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205–227. PubMed
Gout, L. , Fudal, I. , Kuhn, M.L. , Blaise, F. , Eckert, M. , Cattolico, L. , Balesdent, M.H. and Rouxel, T. (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans . Mol. Microbiol. 60, 67–80. PubMed
Hammond, K.E. and Lewis, B. (1987) The establishment of systemic infection in leaves of oilseed rape by Leptosphaeria maculans . Plant Pathol. 36, 135–147.
Hemetsberger, C. , Herrberger, C. , Zechmann, B. , Hillmer, M. and Doehlemann, G. (2012) The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog. 8, e1002684. PubMed PMC
Herrera‐Vásquez, A. , Salinas, P. and Holuigue, L. (2015) Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front. Plant Sci. 6, 1–9. PubMed PMC
Hogenhout, S.A. , Van der Hoorn, R.A. , Terauchi, R. and Kamoun, S. (2009) Emerging concepts in effector biology of plant‐associated organisms. Mol. Plant–Microbe Interact. 22, 115–122. PubMed
Howlett, B.J. (2004) Current knowledge of the interaction between Brassica napus and Leptosphaeria maculans . Can. J. Plant Pathol. 26, 245–252.
Huang, Y.‐J. , Balesdent, M.‐H. , Li, Z.‐Q. , Evans, N. , Rouxel, T. and Fitt, B.D. (2010) Fitness cost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur. J. Plant Pathol. 126, 279–291.
Huang, Y.‐J. , Li, Z.‐Q. , Evans, N. , Rouxel, T. , Fitt, B.D. and Balesdent, M.‐H. (2006) Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur. J. Plant Pathol. 114, 77–89.
Janda, M. , Šašek, V. , Chmelařová, H. , Andrejch, J. , Nováková, M. , Hajšlová, J. , Burketová, L. and Valentová, O. (2015) Phospholipase D affects translocation of NPR1 to the nucleus in Arabidopsis thaliana . Front. Plant Sci. 6, 59. PubMed PMC
Jefferson, R.A. , Kavanagh, T.A. and Bevan, M.W. (1987) GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907. PubMed PMC
Jindřichová, B. , Fodor, J. , Šindelářová, M. , Burketová, L. and Valentová, O. (2011) Role of hydrogen peroxide and antioxidant enzymes in the interaction between a hemibiotrophic fungal pathogen, Leptosphaeria maculans, and oilseed rape. Environ. Exp. Bot. 72, 149–156.
Jones, J.D. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323–329. PubMed
de Jong, A.J. , Yakimova, E.T. , Kapchina, V.M. and Woltering, E.J. (2002) A critical role for ethylene in hydrogen peroxide release during programmed cell death in tomato suspension cells. Planta, 214, 537–545. PubMed
Kazan, K. and Lyons, R. (2014) Intervention of phytohormone pathways by pathogen effectors. Plant Cell, 26, 2285–2309. PubMed PMC
Kim, J.‐G. , Stork, W. and Mudgett, M.B. (2013) Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth. Cell Host Microbe, 13, 143–154. PubMed PMC
Kim, J.‐G. , Taylor, K.W. , Hotson, A. , Keegan, M. , Schmelz, E.A. and Mudgett, M.B. (2008) XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas‐infected tomato leaves. Plant Cell, 20, 1915–1929. PubMed PMC
Larkan, N. , Lydiate, D. , Parkin, I. , Nelson, M. , Epp, D. , Cowling, W. , Rimmer, S. and Borhan, M. (2013) The Brassica napus blackleg resistance gene LepR3 encodes a receptor‐like protein triggered by the Leptosphaeria maculans effector AVRLM1 . New Phytol. 197, 595–605. PubMed
Lee, S.‐J. and Rose, J.K. (2010) Mediation of the transition from biotrophy to necrotrophy in hemibiotrophic plant pathogens by secreted effector proteins. Plant Signal. Behav. 5, 769–772. PubMed PMC
Parlange, F. , Daverdin, G. , Fudal, I. , Kuhn, M.L. , Balesdent, M.H. , Blaise, F. , Grezes‐Besset, B. and Rouxel, T. (2009) Leptosphaeria maculans avirulence gene AvrLm4‐7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4‐mediated recognition through a single amino acid change. Mol. Microbiol. 71, 851–863. PubMed
Persson, M. , Staal, J. , Oide, S. and Dixelius, C. (2009) Layers of defense responses to Leptosphaeria maculans below the RLM1‐ and camalexin‐dependent resistances. New Phytol. 182, 470–482. PubMed
Pieterse, C.M. , Leon‐Reyes, A. , Van der Ent, S. and Van Wees, S.C. (2009) Networking by small‐molecule hormones in plant immunity. Nat. Chem. Biol. 5, 308–316. PubMed
Pieterse, C.M. , Van der Does, D. , Zamioudis, C. , Leon‐Reyes, A. and Van Wees, S.C. (2012) Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489–521. PubMed
Rafiqi, M. , Ellis, J.G. , Ludowici, V.A. , Hardham, A.R. and Dodds, P.N. (2012) Challenges and progress towards understanding the role of effectors in plant–fungal interactions. Curr. Opin. Plant Biol. 15, 477–482. PubMed
Robert‐Seilaniantz, A. , Grant, M. and Jones, J.D. (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate–salicylate antagonism. Annu. Rev. Phytopathol. 49, 317–343. PubMed
Rouxel, T. and Balesdent, M.H. (2013) From model to crop plant–pathogen interactions: cloning of the first resistance gene to Leptosphaeria maculans in Brassica napus . New Phytol. 197, 356–358. PubMed
Rouxel, T. and de Wit, P.J. (2012) Dothideomycete effectors facilitating biotrophic and necrotrophic lifestyles In: Effectors in Plant–Microbe Interactions (Francis M. and Sophien K., eds). John Wiley & Sons.
Rudd, J. , Kanyuka, K. , Hassani‐Pak, K. , Derbyshire, M. , Devonshire, J. , Saqi, M. , Desai, N. , Powers, S. , Hooper, J. , Ambroso, L. , Bharti, A. , Farmer, A. , Hammond‐Kosack, K. , Dietrich, R. and Courbot, M. (2015) Transcriptome and metabolite profiling the infection cycle of Zymoseptoria tritici on wheat (Triticum aestivum) reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions, and a variation on the hemibiotrophic lifestyle definition. Plant Physiol. 167, 1158–1185. DOI:10.1104/pp.114.255927. PubMed DOI PMC
Šašek, V. , Janda, M. , Delage, E. , Puyaubert, J. , Guivarc'h, A. , López Maseda, E. , Dobrev, P.I. , Caius, J. , Bóka, K. and Valentová, O. (2014) Constitutive salicylic acid accumulation in pi4kIIIβ1β2 Arabidopsis plants stunts rosette but not root growth. New Phytol. 203, 805–816. PubMed
Šašek, V. , Nováková, M. , Jindrichová, B. , Bóka, K. , Valentová, O. and Burketová, L. (2012) Recognition of avirulence gene AvrLm1 from hemibiotrophic ascomycete Leptosphaeria maculans triggers salicylic acid and ethylene signaling in Brassica napus . Mol. Plant–Microbe Interact. 25, 1238–1250. PubMed
Schmidt, S.M. and Panstruga, R. (2011) Pathogenomics of fungal plant parasites: what have we learnt about pathogenesis? Curr. Opin. Plant Biol. 14, 392–399. PubMed
Soyer, J.L. , El Ghalid, M. , Glaser, N. , Ollivier, B. , Linglin, J. , Grandaubert, J. , Balesdent, M.‐H. , Connolly, L.R. , Freitag, M. , Rouxel, T. and Fudal, I. (2014) Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans . PLoS Genet. 10, e1004227. PubMed PMC
Thatcher, L.F. , Manners, J.M. and Kazan, K. (2009) Fusarium oxysporum hijacks COI1‐mediated jasmonate signaling to promote disease development in Arabidopsis . Plant J. 58, 927–939. PubMed
Tsuda, K. and Katagiri, F. (2010) Comparing signaling mechanisms engaged in pattern‐triggered and effector‐triggered immunity. Curr. Opin. Plant Biol. 13, 459–465. PubMed
Van de Wouw, A.P. , Lowe, R.G. , Elliott, C.E. , Dubois, D.J. and Howlett, B.J. (2014) An avirulence gene, AvrLmJ1, from the blackleg fungus, Leptosphaeria maculans, confers avirulence to Brassica juncea cultivars. Mol. Plant Pathol. 15, 523–530. PubMed PMC
West, J. , Kharbanda, P. , Barbetti, M. and Fitt, B.D. (2001) Epidemiology and management of Leptosphaeria maculans (phoma stem canker) on oilseed rape in Australia, Canada and Europe. Plant Pathol. 50, 10–27.
Dual Mode of the Saponin Aescin in Plant Protection: Antifungal Agent and Plant Defense Elicitor
Hydrogen Peroxide: Its Role in Plant Biology and Crosstalk with Signalling Networks