Proteinaceous necrotrophic effectors in fungal virulence
Kar-Chun Tan A B D , Richard P. Oliver B , Peter S. Solomon C and Caroline S. Moffat AA Australian Centre for Necrotrophic Fungal Pathogens, Murdoch University, SABC, Murdoch, WA 6150, Australia.
B Australian Centre for Necrotrophic Fungal Pathogens, Curtin University, Bentley, WA 6845, Australia.
C Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.
D Corresponding author. Email: kar-chun.tan@curtin.edu.au
Functional Plant Biology 37(10) 907-912 https://doi.org/10.1071/FP10067
Submitted: 29 March 2010 Accepted: 10 August 2010 Published: 23 September 2010
Abstract
The host–pathogen interface can be considered as a biological battlefront. Molecules produced by both the pathogen and the host are critical factors determining the outcome of the interaction. Recent studies have revealed that an increasing number of necrotrophic fungal pathogens produce small proteinaceous effectors that are able to function as virulence factors. These molecules can cause tissue death in host plants that possess dominant sensitivity genes, leading to subsequent pathogen colonisation. Such effectors are only found in necrotrophic fungi, yet their roles in virulence are poorly understood. However, several recent key studies of necrotrophic effectors from two wheat (Triticum aestivum L.) pathogens, Pyrenophora tritici-repentis (Died.) Drechs. and Stagonospora nodorum (Berk.) Castell. & Germano, have shed light upon how these effector proteins serve to disable the host from the inside out.
Additional keywords: host-selective toxin, net blotch, Pyrenophora, septoria, Stagonospora, tan spot.
Abeysekara NS,
Friesen TL,
Keller B, Faris JD
(2009) Identification and characterization of a novel host-toxin interaction in the wheat–Stagonospora nodorum pathosystem. Theoretical and Applied Genetics 120, 117–126.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Adhikari TB,
Bai J,
Meinhardt SW,
Gurung S,
Myrfield M,
Patel J,
Ali S,
Gudmestad NC, Rasmussen JB
(2009)
Tsn1-mediated host responses to ToxA from Pyrenophora tritici-repentis. Molecular Plant—Microbe Interactions 22, 1056–1068.
| Crossref | GoogleScholarGoogle Scholar |
Ali S, Francl LJ
(2003) Population race structure of Pyrenophora tritici-repentis prevalent on wheat and noncereal grasses in the Great Plains. Plant Disease 87, 418–422.
| Crossref | GoogleScholarGoogle Scholar |
Anderson JA,
Effertz RJ,
Faris JD,
Francl LJ,
Meinhardt SW, Gill BS
(1999) Genetic analysis of sensitivity to a Pyrenophora tritici-repentis necrosis-inducing toxin in durum and common wheat. Phytopathology 89, 293–297.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Andrie RM,
Schoch CL,
Hedges R,
Spatafora JW, Ciuffetti LM
(2008) Homologs of ToxB, a host-selective toxin gene from Pyrenophora tritici-repentis, are present in the genome of sister-species Pyrenophora bromi and other members of the Ascomycota. Fungal Genetics and Biology 45, 363–377.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ballance GM,
Lamari L, Bernier CC
(1989) Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis. Physiological and Molecular Plant Pathology 35, 203–213.
| Crossref | GoogleScholarGoogle Scholar |
Baluska F,
Samaj J,
Wojtaszek P,
Volkmann D, Menzel D
(2003) Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiology 133, 482–491.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Barthe P,
Pujade-Renaud V,
Breton F,
Gargani D,
Thai R,
Roumestand C, de Lamotte F
(2007) Structural analysis of cassiicolin, a host-selective protein toxin from Corynespora cassiicola. Journal of Molecular Biology 367, 89–101.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Catanzariti AM,
Dodds PN,
Lawrence GJ,
Ayliffe MA, Ellis JG
(2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. The Plant Cell 18, 243–256.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ciuffetti LM,
Tuori RP, Gaventa JM
(1997) A single gene encodes a selective toxin causal to the development of tan spot of wheat. The Plant Cell 9, 135–144.
| Crossref |
PubMed |
D’Souza SE,
Ginsberg MH, Plow EF
(1991) Arginyl-glycyl-aspartic acid (RGD): a cell adhesion motif. Trends in Biochemical Sciences 16, 246–250.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
de Lamotte F,
Duviau MP,
Sanier C,
Thai R,
Poncet J,
Bieysse D,
Breton F, Pujade-Renaud V
(2007) Purification and characterization of cassiicolin, the toxin produced by Corynespora cassiicola, causal agent of the leaf fall disease of rubber tree. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences 849, 357–362.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Faik A,
Laboure AM,
Gulino D,
Mandaron P, Falconet D
(1998) A plant surface protein sharing structural properties with animal integrins. European Journal of Biochemistry 253, 552–559.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Faris JD,
Anderson JA,
Francl LJ, Jordahl JG
(1996) Chromosomal location of a gene conditioning insensitivity in wheat to a necrosis-inducing culture filtrate from Pyrenophora tritici-repentis. Phytopathology 86, 459–463.
| Crossref | GoogleScholarGoogle Scholar |
Faris JD,
Zhang Z,
Lu H,
Lu S, Reddy L ,
et al
.
(2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proceedings of the National Academy of Sciences of the United States of America 107, 13544–13549.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Friesen TL, Faris JD
(2004) Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theoretical and Applied Genetics 109, 464–471.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Friesen TL,
Ali S,
Klein KK, Rasmussen JB
(2005) Population genetic analysis of a global collection of Pyrenophora tritici-repentis, a causal agent of tan spot of wheat. Phytopathology 95, 1144–1150.
| Crossref |
PubMed |
Friesen TL,
Stukenbrock EH,
Liu ZH,
Meinhardt S, Ling H ,
et al
.
(2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genetics 38, 953–956.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Friesen TL,
Meinhardt SW, Faris JD
(2007) The Stagonospora nodorum–wheat pathosystem involves multiple proteinaceous host-selective toxins and corresponding host sensitivity genes that interact in an inverse gene-for-gene manner. The Plant Journal 51, 681–692.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Friesen TL,
Faris JD,
Solomon PS, Oliver RP
(2008a) Host-specific toxins: effectors of necrotrophic pathogenicity. Cellular Microbiology 10, 1421–1428.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Friesen TL,
Zhang Z,
Solomon PS,
Oliver RP, Faris JD
(2008b) Characterization of the interaction of a novel Stagonospora nodorum host-selective toxin with a wheat susceptibility gene. Plant Physiology 146, 682–693.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hammond-Kosack KE, Rudd JJ
(2008) Plant resistance signalling hijacked by a necrotrophic fungal pathogen. Plant Signaling & Behavior 3, 993–995.
| PubMed |
Hane JK,
Lowe RG,
Solomon PS,
Tan KC, Schoch CL ,
et al
.
(2007) Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. The Plant Cell 19, 3347–3368.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Isberg RR, Tran Van Nhieu G
(1994) Binding and internalisation of micro-organisms by integrin receptors. Trends in Microbiology 2, 10–14.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Keller B,
Winzeler H,
Winzeler M, Fried PM
(1994) Differential sensitivity of wheat embryos against extracts containing toxins of Septoria nodorum: first steps towards in vitro selection. Journal of Phytopathology 141, 233–240.
| Crossref | GoogleScholarGoogle Scholar |
Keren N,
Ohkawa H,
Welsh EA,
Liberton M, Pakrasi HB
(2005) Psb29, a conserved 22-kD protein, functions in the biogenesis of Photosystem II complexes in Synechocystis and Arabidopsis. The Plant Cell 17, 2768–2781.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Labouré AM,
Faik A,
Mandaron P, Falconet D
(1999) RGD-dependent growth of maize calluses and immunodetection of an integrin-like protein. FEBS Letters 442, 123–128.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lamari L,
Strelkov SE,
Yahyaoui A,
Amedov M,
Saidov M,
Djunusova M, Koichibayev M
(2005) Virulence of Pyrenophora tritici-repentis in the countries of the Silk Road. Canadian Journal of Plant Pathology 27, 383–388.
| Crossref |
Liu ZH,
Faris JD,
Meinhardt SW,
Ali S,
Rasmussen JB, Friesen TL
(2004) Genetic and physical mapping of a gene conditioning sensitivity in wheat to a partially purified host-selective toxin produced by Stagonospora nodorum. Phytopathology 94, 1056–1060.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liu Z,
Faris JD,
Oliver RP,
Tan KC, Solomon PS ,
et al
.
(2009) SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLoS Pathogens 5, e1000581.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lorang JM,
Sweat TA, Wolpert TJ
(2007) Plant disease susceptibility conferred by a “resistance” gene. Proceedings of the National Academy of Sciences of the United States of America 104, 14861–14866.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Manning VA, Ciuffetti LM
(2005) Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. The Plant Cell 17, 3203–3212.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Manning VA,
Hardison LK, Ciuffetti LM
(2007) Ptr ToxA interacts with a chloroplast-localized protein. Molecular Plant—Microbe Interactions 20, 168–177.
| Crossref | GoogleScholarGoogle Scholar |
Manning VA,
Hamilton SM,
Karplus PA, Ciuffetti LM
(2008) The Arg-Gly-Asp-containing, solvent-exposed loop of Ptr ToxA is required for internalization. Molecular Plant—Microbe Interactions 21, 315–325.
| Crossref | GoogleScholarGoogle Scholar |
Manning VA,
Chu AL,
Steeves JE,
Wolpert TJ, Ciuffetti LM
(2009) A host-selective toxin of Pyrenophora tritici-repentis, Ptr ToxA, induces photosystem changes and reactive oxygen species accumulation in sensitive wheat. Molecular Plant—Microbe Interactions 22, 665–676.
| Crossref | GoogleScholarGoogle Scholar |
Martin GB,
Bogdanove AJ, Sessa G
(2003) Understanding the functions of plant disease resistance proteins. Annual Review of Plant Biology 54, 23–61.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Martinez JP,
Ottum SA,
Ali S,
Franci LJ, Ciuffetti LM
(2001) Characterization of the ToxB gene from Pyrenophora tritici-repentis. Molecular Plant—Microbe Interactions 14, 675–677.
| Crossref | GoogleScholarGoogle Scholar |
Meehan F, Murphy HC
(1946) A new Helminthosporium blight of oats. Science 104, 413–414.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nagpal P, Quatrano RS
(1999) Isolation and characterization of a cDNA clone from Arabidopsis thaliana with partial sequence similarity to integrins. Gene 230, 33–40.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Orolaza NP,
Lamari L, Ballance GM
(1995) Evidence of a host-specific chlorosis toxin from Pyrenophora tritici-repentis, the causal agent of tan spot of wheat. Phytopathology 85, 1282–1287.
| Crossref | GoogleScholarGoogle Scholar |
Pandelova I,
Betts MF,
Manning VA,
Wilhelm LJ,
Mockler TC, Ciuffetti LM
(2009) Analysis of transcriptome changes induced by Ptr ToxA in wheat provides insights into the mechanisms of plant susceptibility. Molecular Plant 2, 1067–1083.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Parada RY,
Sakuno E,
Mori N,
Oka K,
Egusa M,
Kodama M, Otani H
(2008)
Alternaria brassicae produces a host-specific protein toxin from germinating spores on host leaves. Phytopathology 98, 458–463.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Reddy L,
Friesen TL,
Meinhardt SW,
Chao S, Faris JD
(2008) Genomic analysis of the Snn1 locus on wheat chromosome arm 1BS and the identification of candidate genes. The Plant Genome 1, 55–66.
| Crossref | GoogleScholarGoogle Scholar |
Rohe M,
Gierlich A,
Hermann H,
Hahn M,
Schmidt B,
Rosahl S, Knogge W
(1995) The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. The EMBO Journal 14, 4168–4177.
| PubMed |
Ruoslahti E, Pierschbacher MD
(1986) Arg-gly-asp: a versatile cell recognition signal. Cell 44, 517–518.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sarma GN,
Manning VA,
Ciuffetti LM, Karplus PA
(2005a) Structure of Ptr ToxA: an RGD-containing host-selective toxin from Pyrenophora tritici-repentis. The Plant Cell 17, 3190–3202.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sarma GN,
Manning VA,
Ciuffetti LM, Karplus PA
(2005b) Structure of Ptr ToxA: an RGD-containing host-selective toxin from Pyrenophora tritici-repentis. The Plant Cell 17, 3190–3202.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sarpeleh A,
Wallwork H,
Catcheside DE,
Tate ME, Able AJ
(2007) Proteinaceous metabolites from Pyrenophora teres contribute to symptom development of barley net blotch. Phytopathology 97, 907–915.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sarpeleh A,
Wallwork H,
Tate ME,
Catcheside DEA, Able AJ
(2008) Initial characterization of phytotoxic proteins isolated from Pyrenophora teres. Physiological and Molecular Plant Pathology 72, 73–79.
| Crossref | GoogleScholarGoogle Scholar |
Schürch S,
Linde CC,
Knogge W,
Jackson LF, McDonald BA
(2004) Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Molecular Plant—Microbe Interactions 17, 1114–1125.
| Crossref | GoogleScholarGoogle Scholar |
Solomon PS,
Tan K-C, Oliver RP
(2003) The nutrient supply of pathogenic fungi; a fertile field for study. Molecular Plant Pathology 4, 203–210.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Solomon PS,
Lowe RGT,
Tan K-C,
Waters ODC, Oliver RP
(2006)
Stagonospora nodorum: cause of stagonospora nodorum blotch of wheat. Molecular Plant Pathology 7, 147–156.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Strelkov SE,
Lamari L, Ballance GM
(1999) Characterization of a host-specific protein toxin (Ptr ToxB) from Pyrenophora tritici-repentis. Molecular Plant—Microbe Interactions 12, 728–732.
| Crossref | GoogleScholarGoogle Scholar |
Stukenbrock EH, McDonald BA
(2007) Geographical variation and positive diversifying selection in the host specific toxin SnToxA. Molecular Plant Pathology 8, 321–332.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sun Y,
Qian H,
Xu XD,
Han Y,
Yen LF, Sun DY
(2000) Integrin-like proteins in the pollen tube: detection, localization and function. Plant & Cell Physiology 41, 1136–1142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Swatzell LJ,
Edelmann RE,
Makaroff CA, Kiss JZ
(1999) Integrin-like proteins are localized to plasma membrane fractions, not plastids, in Arabidopsis. Plant & Cell Physiology 40, 173–183.
| PubMed |
Tomas A,
Feng GH,
Reeck GR,
Bockus WW, Leach JE
(1990) Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Molecular Plant—Microbe Interactions 3, 221–224.
Tuori RP,
Wolpert TJ, Ciuffetti LM
(1995) Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis. Molecular Plant—Microbe Interactions 8, 41–48.
Van den Ackerveken GF,
Van Kan JA,
Joosten MH,
Muisers JM,
Verbakel HM, De Wit PJ
(1993) Characterization of two putative pathogenicity genes of the fungal tomato pathogen Cladosporium fulvum. Molecular Plant—Microbe Interactions 6, 210–215.
van’t Slot KA,
Gierlich A, Knogge W
(2007) A single binding site mediates resistance- and disease-associated activities of the effector protein NIP1 from the barley pathogen Rhynchosporium secalis. Plant Physiology 144, 1654–1666.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walton JD
(1996) Host-selective toxins: agents of compatibility. The Plant Cell 8, 1723–1733.
| Crossref |
PubMed |
Wang Q,
Sullivan RW,
Kight A,
Henry RL,
Huang J,
Jones AM, Korth KL
(2004) Deletion of the chloroplast-localized Thylakoid formation1 gene product in Arabidopsis leads to deficient thylakoid formation and variegated leaves. Plant Physiology 136, 3594–3604.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wevelsiep L,
Kogel KH, Knogge W
(1991) Purification and characterization of peptides from Rhynchosporium secalis inducing necrosis in barley. Physiological and Molecular Plant Pathology 39, 471–482.
| Crossref | GoogleScholarGoogle Scholar |
Wevelsiep L,
Rupping E, Knogge W
(1993) Stimulation of barley plasmalemma H+-ATPase by phytotoxic peptides from the fungal pathogen Rhynchosporium secalis. Plant Physiology 101, 297–301.
| PubMed |
Wolpert TJ,
Dunkle LD, Ciuffetti LM
(2002) Host-selective toxins and avirulence determinants: what’s in a name? Annual Review of Phytopathology 40, 251–285.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhang HF,
Francl LJ,
Jordahl JG, Meinhardt SW
(1997) Structural and physical properties of a necrosis-inducing toxin from Pyrenophora tritici-repentis. Phytopathology 87, 154–160.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
