1932

Abstract

Great strides have been made in defining the details of the plant defense response involving biotrophic fungal and bacterial pathogens. The groundwork for the current model was laid by H.H. Flor and others who defined the gene-for-gene hypothesis, which is now known to involve effector-triggered immunity (ETI). PAMP-triggered immunity (PTI) is also a highly effective response to most pathogens because of the recognition of common pathogen molecules by pattern recognition receptors. In this article, we consider the three pathogens that make up the foliar disease complex of wheat, , , and , to review the means by which necrotrophic pathogens circumvent, or outright hijack, the ETI and PTI pathways to cause disease.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-120320-012807
2021-08-25
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/phyto/59/1/annurev-phyto-120320-012807.html?itemId=/content/journals/10.1146/annurev-phyto-120320-012807&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abeysekara NS, Friesen TL, Keller B, Faris JD. 2009. Identification and characterization of a novel host-toxin interaction in the wheat–Stagonospora nodorum pathosystem. Theor. Appl. Genet 120:117–26
    [Google Scholar]
  2. 2. 
    Adhikari TB, Bai J, Meinhardt SW, Gurung S, Myrfield M et al. 2009. Tsn1-mediated host responses to ToxA from Pyrenophora tritici-repentis. Mol. Plant-Microbe Interact. 22:1056–68
    [Google Scholar]
  3. 3. 
    Baker EA, Smith IM. 1978. Development of resistant and susceptible reactions in wheat on inoculation with Septoria nodorum. Trans. Br. Mycol. Soc. 71:475–82
    [Google Scholar]
  4. 4. 
    Ballance GM, Lamari L, Bernier CC. 1989. Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis. Physiol. Mol. Plant Pathol. 35:203–13
    [Google Scholar]
  5. 5. 
    Ballance GM, Lamari L, Kowatsch R, Bernier CC. 1996. Cloning, expression and occurrence of the gene encoding the Ptr necrosis toxin from Pyrenophora tritici-repentis. Mol. Plant Pathol. Online 1996.1209
    [Google Scholar]
  6. 6. 
    Ben MBarek S, Cordewener JHG, Ghaffary SMT, van der Lee TAJ, Liu Z et al. 2015. FPLC and liquid-chromatography mass spectrometry identify candidate necrosis-inducing proteins from culture filtrates of the fungal wheat pathogen Zymoseptoria tritici. Fungal Genet. Biol. 79:54–62
    [Google Scholar]
  7. 7. 
    Bird PM, Ride JP. 1981. The resistance of wheat to Septoria nodorum: fungal development in relation to host lignification. Physiol. Plant Pathol. 19:289–99
    [Google Scholar]
  8. 8. 
    Brading PA, Verstappen ECP, Kema GHJ, Brown JKM. 2002. A gene-for-gene relationship between wheat and Mycosphaerella graminicola, the Septoria tritici blotch pathogen. Phytopathology 92:439–45
    [Google Scholar]
  9. 9. 
    Breen S, Williams SJ, Winterberg B, Kobe B, Solomon PS. 2016. Wheat PR-1 proteins are targeted by necrotrophic pathogen effector proteins. Plant J 88:13–25
    [Google Scholar]
  10. 10. 
    Brown JK, Chartrain L, Lasserre-Zuber P, Saintenac C. 2015. Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genet. Biol. 79:33–41
    [Google Scholar]
  11. 11. 
    Chartrain L, Brading PA, Brown JKM. 2005. Presence of the Stb6 gene for resistance to Septoria tritici blotch (Mycosphaerella graminicola) in cultivars used in wheat-breeding programmes worldwide. Plant Pathol 54:134–43
    [Google Scholar]
  12. 12. 
    Ciuffetti LM, Manning VA, Pandelova I, Figueroa Betts M, Martinez JP 2010. Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol 187:911–19
    [Google Scholar]
  13. 13. 
    Ciuffetti LM, Tuori RP, Gaventa JM. 1997. A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell 9:135–44
    [Google Scholar]
  14. 14. 
    de Guillen K, Ortiz-Vallejo D, Gracy J, Fournier E, Kroj T, Padilla A. 2015. Structure analysis uncovers a highly diverse but structurally conserved effector family in phytopathogenic fungi. PLOS Pathog 11:e1005228
    [Google Scholar]
  15. 15. 
    Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev. Genet. 11:239–48
    [Google Scholar]
  16. 16. 
    Effertz RJ, Anderson JA, Francl LJ. 2001. Restriction fragment length polymorphism mapping of resistance to two races of Pyrenophora tritici-repentis in adult and seedling wheat. Phytopathology 91:572–78
    [Google Scholar]
  17. 17. 
    Effertz RJ, Meinhardt SW, Anderson JA, Jordahl JG, Francl LJ. 2002. Identification of a chlorosis-inducing toxin from Pyrenophora tritici-repentis and the chromosomal location of an insensitivity locus in wheat. Phytopathology 92:527–33
    [Google Scholar]
  18. 18. 
    Faris JD, Anderson JA, Francl LJ, Jordahl JG. 1996. Chromosomal location of a gene conditioning insensitivity in wheat to a necrosis-inducing culture filtrate of Pyrenophora tritici-repentis. Phytopathology 86:459–63
    [Google Scholar]
  19. 19. 
    Faris JD, Anderson JA, Francl LJ, Jordahl JG. 1997. RFLP mapping of resistance to chlorosis induction by Pyrenophora tritici-repentis in wheat. Theor. Appl. Genet. 94:98–103
    [Google Scholar]
  20. 20. 
    Faris JD, Friesen TL. 2009. Reevaluation of a tetraploid wheat population indicates that the Tsn1-ToxA interaction is the only factor governing Stagonospora nodorum blotch susceptibility. Phytopathology 99:906–12
    [Google Scholar]
  21. 21. 
    Faris JD, Friesen TL. 2020. Plant genes hijacked by necrotrophic fungal pathogens. Curr. Opin. Plant Biol. 56:74–80
    [Google Scholar]
  22. 22. 
    Faris JD, Liu Z, Xu SS. 2013. Genetics of tan spot resistance in wheat. Theor. Appl. Genet. 126:2197–217
    [Google Scholar]
  23. 23. 
    Faris JD, Zhang Z, Lu H, Lu Z, Reddy L et al. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. PNAS 107:13544–49
    [Google Scholar]
  24. 24. 
    Figueroa M, Manning VA, Pandelova I, Ciuffetti LM. 2015. Persistence of the host-selective toxin Ptr ToxB in the apoplast. Mol. Plant-Microbe Interact. 28:1082–90
    [Google Scholar]
  25. 25. 
    Flor HH. 1942. Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:653–69
    [Google Scholar]
  26. 26. 
    Flor HH. 1955. Host-parasite interaction in flax rust—its genetics and other implications. Phytopathology 45:680–85
    [Google Scholar]
  27. 27. 
    Flor HH. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275–96
    [Google Scholar]
  28. 28. 
    Friesen TL, Chu CG, Liu ZH, Xu SS, Halley S, Faris JD. 2009. Host-selective toxins produced by Stagonospora nodorum confer disease susceptibility in adult wheat plants under field conditions. Theor. Appl. Genet. 118:1489–97
    [Google Scholar]
  29. 29. 
    Friesen TL, Chu CG, Xu SS, Faris JD. 2012. SnTox5-Snn5: a novel Stagonospora nodorum effector-wheat gene interaction and its relationship with the SnToxA-Tsn1 and SnTox3-Snn3-B1 interactions. Mol. Plant Pathol. 13:91101–9
    [Google Scholar]
  30. 30. 
    Friesen TL, Faris JD. 2004. Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theor. Appl. Genet. 109:464–71
    [Google Scholar]
  31. 31. 
    Friesen TL, Faris JD. 2010. Characterization of the wheat-Stagonospora nodorum disease system: What is the molecular basis of this quantitative necrotrophic disease interaction?. Can. J. Plant Pathol 32:20–28
    [Google Scholar]
  32. 32. 
    Friesen TL, Faris JD, Solomon PS, Oliver RP. 2008. Host specific toxins: effectors of necrotrophic pathogenicity. Cell. Microbiol. 10:1421–28
    [Google Scholar]
  33. 33. 
    Friesen TL, Holmes DJ, Bowden RL, Faris JD. 2018. ToxA is present in the US Bipolaris sorokiniana population and is a significant virulence factor on wheat harboring Tsn1. Plant Dis 102:2446–52
    [Google Scholar]
  34. 34. 
    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. Plant J 51:681–92
    [Google Scholar]
  35. 35. 
    Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H et al. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38:953–56
    [Google Scholar]
  36. 36. 
    Friesen TL, Zhang Z, Solomon PS, Oliver RP, Faris JD. 2008. Characterization of the interaction of a novel Stagonospora nodorum host-selective toxin with a wheat susceptibility gene. Plant Physiol 146:682–93
    [Google Scholar]
  37. 37. 
    Gao Y, Faris JD, Liu ZH, Xu SS, Friesen TL. 2015. Identification and characterization of the SnTox6-Snn6 interaction in the wheat-Parastagonospora nodorum pathosystem. Mol. Plant-Microbe Interact. 28:615–25
    [Google Scholar]
  38. 38. 
    Hane JK, Lowe RGT, Solomon PS, Tan K-C, Schoch CL et al. 2007. Dothideomycete-plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19:3347–68
    [Google Scholar]
  39. 39. 
    Haueisen J, Möller M, Eschenbrenner CJ, Grandaubert J, Seybold H et al. 2019. Highly flexible infection programs in a specialized wheat pathogen. Ecol. Evol. 9:275–94
    [Google Scholar]
  40. 40. 
    Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323–29
    [Google Scholar]
  41. 41. 
    Kariyawasam GK, Richards JK, Wyatt NA, Running K, Xu SS et al. 2021. The Parastagonospora nodorum necrotrophic effector SnTox5 targets the wheat gene Snn5 and facilitates entry into the leaf mesophyll. New Phytol https://doi.org/10.1111/nph.17602
    [Crossref] [Google Scholar]
  42. 42. 
    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. J. Phytopathol. 141:233–40
    [Google Scholar]
  43. 43. 
    Kema GHJ, Mirzadi Gohari A, Aouini L, Gibriel HAY, Ware SB et al. 2018. Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance. Nat. Genet. 50:375–80
    [Google Scholar]
  44. 44. 
    Kema GHJ, Verstappen ECP, Waalwijk C. 2000. Avirulence in the wheat Septoria tritici leaf blotch fungus Mycosphaerella graminicola is controlled by a single locus. Mol. Plant-Microbe Interact. 13:1375–79
    [Google Scholar]
  45. 45. 
    Kema GHJ, Yu DZ, Rijkenberg FHJ, Shaw MW, Baayen RP. 1996. Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86:777–86
    [Google Scholar]
  46. 46. 
    Keon J, Antoniw J, Carzaniga R, Deller S, Ward JL et al. 2007. Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Mol. Plant-Microbe Interact. 20:178–93
    [Google Scholar]
  47. 47. 
    Kwon CY, Rasmussen JB, Meinhardt SW. 1998. Activity of Ptr ToxA from Pyrenophora tritici-repentis requires host metabolism. Physiol. Mol. Plant Pathol. 52:201–12
    [Google Scholar]
  48. 48. 
    Lamari L, Bernier CC. 1989. Toxin of Pyrenophora tritici-repentis: host-specificity, significance in disease, and inheritance of host-reaction. Phytopathology 79:740–44
    [Google Scholar]
  49. 49. 
    Lamari L, Bernier CC. 1989. Virulence of isolates of Pyrenophora tritici-repentis on 11 wheat cultivars and cytology of the differential host reactions. Can. J. Plant Pathol. 11:284–90
    [Google Scholar]
  50. 50. 
    Lamari L, Sayoud R, Boulif M, Bernier CC. 1995. Identification of a new race in Pyrenophora tritici-repentis: implications for the current pathotype classification system. Can. J. Plant Pathol. 17:312–18
    [Google Scholar]
  51. 51. 
    Lamari L, Strelkov SE. 2010. The wheat/Pyrenophora tritici-repentis interaction: progress towards an understanding of tan spot disease Can. . J. Plant Pathol. 32:4–10
    [Google Scholar]
  52. 52. 
    Lamari L, Strelkov SE, Yahyaoui A, Orabi J, Smith RB. 2003. The identification of two new races of Pyrenophora tritici-repentis from the host center of diversity confirms a one-to-one relationship in tan spot of wheat. Phytopathology 93:391–96
    [Google Scholar]
  53. 53. 
    Larez CR, Hosford RM Jr., Freeman TP. 1986. Infection of wheat and oats by Pyrenophora tritici-repentis and initial characterization of resistance. Phytopathology 76:931–38
    [Google Scholar]
  54. 54. 
    Lee WS, Rudd JJ, Hammond-Kosack KE, Kanyuka K 2014. Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Mol. Plant-Microbe Interact. 27:236–43
    [Google Scholar]
  55. 55. 
    Lehtinen U. 1993. Plant cell wall degrading enzymes of Septoria nodorum. . Physiol. Mol. Plant Pathol. 43:121–34
    [Google Scholar]
  56. 56. 
    Li W, Wang B, Wu J, Lu G, Hu Y et al. 2009. The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol. Plant-Microbe Interact. 22:411–20
    [Google Scholar]
  57. 57. 
    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 94:1056–60
    [Google Scholar]
  58. 58. 
    Liu ZH, Faris JD, Oliver RP, Tan K-C, Solomon PS et al. 2009. SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLOS Pathog 5:e1000581
    [Google Scholar]
  59. 59. 
    Liu ZH, Friesen TL, Rasmussen JB, Ali S, Meinhardt SW, Faris JD. 2004. Quantitative trait loci analysis and mapping of seedling resistance to Stagonospora nodorum leaf blotch in wheat. Phytopathology 94:1061–67
    [Google Scholar]
  60. 60. 
    Liu Z, Gao Y, Kim YM, Faris JD, Shelver WL et al. 2016. SnTox1, a Parastagonospora nodorum necrotrophic effector, is a dual-function protein that facilitates infection while protecting from wheat-produced chitinases. New Phytol 211:1052–64
    [Google Scholar]
  61. 61. 
    Liu Z, Zhang Z, Faris JD, Oliver RP, Syme R et al. 2012. The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLOS Pathog 8:e1002467
    [Google Scholar]
  62. 62. 
    Loughman R, Deverall BJ. 1986. Infection of resistant and susceptible cultivars of wheat by Pyrenophora tritici-repentis. Plant Pathol 35:443–50
    [Google Scholar]
  63. 63. 
    Lu S, Faris JD, Sherwood R, Friesen TL, Edwards MC. 2014. A dimeric PR-1-type pathogenesis-related protein interacts with ToxA and potentially mediates ToxA-induced necrosis in sensitive wheat. Mol. Plant Pathol. 15:650–63
    [Google Scholar]
  64. 64. 
    Magro P. 1984. Production of polysaccharide-degrading enzymes by Septoria nodorum in culture and during pathogenesis. Plant Sci. Lett. 37:63–68
    [Google Scholar]
  65. 65. 
    Manning VA, Andrie RM, Trippe AF, Ciuffetti LM. 2004. Ptr ToxA requires multiple motifs for complete activity. Mol. Plant-Microbe Interact. 17:491–501
    [Google Scholar]
  66. 66. 
    Manning VA, Chu AL, Scofield SR, Ciuffetti LM. 2010. Intracellular expression of a host-selective toxin, ToxA, in diverse plants phenocopies silencing of a ToxA-interacting protein, ToxABP1. New Phytol 187:1034–47
    [Google Scholar]
  67. 67. 
    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. Mol. Plant-Microbe Interact. 22:665–76
    [Google Scholar]
  68. 68. 
    Manning VA, Ciuffetti LM. 2005. Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell 17:3203–12
    [Google Scholar]
  69. 69. 
    Manning VA, Hamilton SM, Karplus PA, Ciuffetti LM. 2008. The Arg-Gly-Asp-containing, solvent-exposed loop of Ptr ToxA is required for internalization. Mol. Plant-Microbe Interact. 21:315–25
    [Google Scholar]
  70. 70. 
    Manning VA, Hardison LK, Ciuffetti LM. 2007. Ptr ToxA interacts with a chloroplast localized protein. Mol. Plant-Microbe Interact. 20:168–77
    [Google Scholar]
  71. 71. 
    Marshall R, Kombrink A, Motteram J, Loza-Reyes E, Lucas J et al. 2011. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol 156:756–69
    [Google Scholar]
  72. 72. 
    Martinez JP, Oesch NW, Ciuffetti LM. 2004. Characterization of the multiple copy host-selective toxin gene, ToxB, in pathogenic and nonpathogenic isolates of Pyrenophora tritici-repentis. Mol. Plant-Microbe Interact. 22:665–76
    [Google Scholar]
  73. 73. 
    Martinez JP, Ottum SA, Ali S, Francl LJ, Ciuffetti LM. 2001. Characterization of the ToxB gene from Pyrenophora tritici-repentis. Mol. Plant-Microbe Interact. 14:675–77
    [Google Scholar]
  74. 74. 
    McDonald MC, Ahren D, Simpfendorfer S, Milgate A, Solomon PS. 2018. The discovery of the virulence gene ToxA in the wheat and barley pathogen Bipolaris sorokiniana. Mol. Plant Pathol. 19:432–39
    [Google Scholar]
  75. 75. 
    McDonald MC, Oliver RP, Friesen TL, Brunner PC, McDonald BA. 2013. Global diversity and distribution of three necrotrophic effectors in Phaeosphaeria nodorum and related species. New Phytol 199:241–51
    [Google Scholar]
  76. 76. 
    Mehra LK, Adhikari U, Ojiambo PS, Cowger C. 2019. Septoria nodorum blotch of wheat. Plant Health Instr https://doi.org/10.1094/PHI-I-2019-0514-01
    [Crossref] [Google Scholar]
  77. 77. 
    Meile L, Croll D, Brunner PC, Plissonneau C, Hartmann FE et al. 2018. A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to Septoria tritici blotch. New Phytol 219:1048–61
    [Google Scholar]
  78. 78. 
    Meinhardt SW, Cheng W, Kwon CY, Donohue CM, Rasmussen JB. 2002. Role of the Arginyl-glycyl-aspartic motif in the action of PtrToxA produced by Pyrenophora tritici-repentis. Plant Physiol 130:1545–51
    [Google Scholar]
  79. 79. 
    Murray GM, Brennan JP. 2009. Estimating disease losses to the Australian wheat industry. Australas. Plant Pathol. 38:558–70
    [Google Scholar]
  80. 80. 
    Nyarko A, Singarapu KK, Figueroa M, Manning VA, Pandelova I et al. 2014. Solution NMR structures of Pyrenophora tritici-repentis ToxB and its inactive homolog reveal potential determinants of toxin activity. J. Biol. Chem. 289:25946–56
    [Google Scholar]
  81. 81. 
    Oliver RP, Friesen TL, Faris JD, Solomon PS. 2012. Stagonospora nodorum: from pathology to genomics and host resistance. Annu. Rev. Phytopathol. 50:23–43
    [Google Scholar]
  82. 82. 
    O'Reilly P, Downes MJ 1986. Form of survival of Septoria nodorum on symptomless winter wheat. Trans. Br. Mycol. Soc. 86:381–85
    [Google Scholar]
  83. 83. 
    Orton ES, Deller S, Brown JKM. 2011. Mycosphaerella graminicola: from genomics to disease control. Mol. Plant Pathol. 12:413–24
    [Google Scholar]
  84. 84. 
    Outram MA, Sung Y-C, Yu D, Dagvadorj B, Rima SA et al. 2020. The crystal structure of SnTox3 from the necrotrophic fungus Parastagonospora nodorum reveals a unique effector fold and insights into Kex2 protease processing of fungal effectors. New Phytol https://doi.org/10.1111/nph.17516
    [Crossref] [Google Scholar]
  85. 85. 
    Palma-Guerrero J, Ma X, Torriani SFF, Zala M, Francisco CS et al. 2017. Comparative transcriptome analyses in Zymoseptoria tritici reveal significant differences in gene expression among strains during plant infection. Mol. Plant-Microbe Interact. 30:231–44
    [Google Scholar]
  86. 86. 
    Pandelova I, Betts MF, Manning VA, Wilhelm LJ, Mockler TC, Ciuffetti LM. 2009. Transcriptional reprogramming induced by Ptr ToxA in wheat provides insights into the mechanisms of plant susceptibility. Mol. Plant 2:1067–83
    [Google Scholar]
  87. 87. 
    Pandelova I, Figueroa M, Wilhelm LJ, Manning VA, Mankaney AN et al. 2012. Host-selective toxins of Pyrenophora tritici-repentis induce common responses associated with host susceptibility. PLOS ONE 7:e40240
    [Google Scholar]
  88. 88. 
    Park C-H, Chen S, Shirsekar G, Zhou B, Khang CH et al. 2012. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell 24:4748–62
    [Google Scholar]
  89. 89. 
    Rasmussen JB, Kwon CY, Meinhardt SW. 2004. Requirement of host signaling mechanisms for the action of Ptr ToxA in wheat. Eur. J. Plant Pathol. 110:333–35
    [Google Scholar]
  90. 90. 
    Richards JK, Kariyawasam GK, Seneviratne S, Wyatt NA, Xu SS et al. 2021. A triple threat: the Parastagonospora nodorum SnTox267 effector exploits three distinct host genetic factors to cause disease in wheat. New Phytol https://doi.org/10.1111/nph.17601
    [Crossref] [Google Scholar]
  91. 91. 
    Richards JK, Stukenbrock EH, Carpenter J, Liu Z, Cowger C et al. 2019. Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States. PLOS Genet 15:e1008223
    [Google Scholar]
  92. 92. 
    Rudd JJ, Kanyuka K, Hassani-Pak K, Derbyshire M, Andongabo A et al. 2015. Transcriptome and metabolite profiling of 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 hemi-biotrophic lifestyle definition. Plant Physiol 167:1158–85
    [Google Scholar]
  93. 93. 
    Ruud AK, Windju S, Belova T, Friesen TL, Lillemo M. 2017. Mapping of SnTox3-Snn3 as a major determinant of field susceptibility to Septoria nodorum leaf blotch in the SHA3/CBRD x Naxos population. Theor. Appl. Genet. 130:1361–74
    [Google Scholar]
  94. 94. 
    Saintenac C, Lee W, Cambon F, Lee W-S, Cambon F et al. 2018. Wheat receptor-kinase-like protein Stb6 controls gene-for-gene resistance to fungal pathogen Zymoseptoria tritici. Nat. Genet. 50:368–74
    [Google Scholar]
  95. 95. 
    Sánchez-Vallet A, McDonald MC, Solomon PS, McDonald BA. 2015. Is Zymoseptoria tritici a hemibiotroph?. Fungal Genet. Biol. 79:29–32
    [Google Scholar]
  96. 96. 
    Sarma GN, Manning VA, Ciuffetti LM, Karplus PA. 2005. Structure of Ptr ToxA: an RGD-containing host-selective toxin from Pyrenophora tritici-repentis. Plant Cell 17:3190–202
    [Google Scholar]
  97. 97. 
    Shi GJ, Friesen TL, Saini J, Xu SS, Rasmussen JB, Faris JD. 2015. The wheat Snn7 gene confers susceptibility upon recognition of the Parastagonospora nodorum necrotrophic effector SnTox7. Plant Genome https://doi.org/10.3835/plantgenome2015.02.0007
    [Crossref] [Google Scholar]
  98. 98. 
    Shi GJ, Zhang ZC, Friesen TL, Bansal U, Cloutier S et al. 2016. Marker development, saturation mapping, and high-resolution mapping of the Septoria nodorum blotch susceptibility gene Snn3-B1 in wheat. Mol. Genet. Genom. 291:107–19
    [Google Scholar]
  99. 99. 
    Shi G, Zhang Z, Friesen TL, Raats D, Fahima T et al. 2016. The hijacking of a receptor kinase-driven pathway by a wheat fungal pathogen leads to disease. Sci. Adv. 10:e1600822
    [Google Scholar]
  100. 100. 
    Singh RP, Singh PK, Rutkoski J, Hodson DP, He X et al. 2016. Disease impact on wheat yield potential and prospects of genetic control. Annu. Rev. Phytopathol. 54:303–22
    [Google Scholar]
  101. 101. 
    Solomon PS, Lowe RGT, Tan K-C, Waters ODC, Oliver RP. 2006. Stagonospora nodorum: cause of Stagonospora nodorum blotch of wheat. Mol. Plant Pathol. 7:147–56
    [Google Scholar]
  102. 102. 
    Stewart EL, Croll D, Lendenmann MH, Sánchez-Vallet A, Hartmann FE et al. 2018. Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici. Mol. Plant Pathol. 19:201–16
    [Google Scholar]
  103. 103. 
    Strelkov SE, Kowatsch RF, Ballance GM, Lamari L. 2006. Characterization of the ToxB gene from North African and Canadian isolates of Pyrenophora tritici-repentis. Physiol. Mol. Plant Pathol. 67:164–70
    [Google Scholar]
  104. 104. 
    Strelkov SE, Lamari L. 2003. Host-parasite interaction in tan spot [Pyrenophora tritici-repentis] of wheat. Can. J. Plant Pathol. 25:339–49
    [Google Scholar]
  105. 105. 
    Strelkov SE, Lamari L, Ballance GM. 1998. Induced chlorophyll degradation by a chlorosis toxin from Pyrenophora tritici-repentis. Can. J. Plant Pathol. 20:428–35
    [Google Scholar]
  106. 106. 
    Strelkov SE, Lamari L, Ballance GM. 1999. Characterization of a host specific protein toxin (Ptr ToxB) from Pyrenophora tritici-repentis. Mol. Plant-Microbe Interact. 12:728–32
    [Google Scholar]
  107. 107. 
    Strelkov SE, Lamari L, Sayoud R, Smith RB. 2002. Comparative virulence of chlorosis-inducing races of Pyrenophora tritici-repentis. Can. J. Plant Pathol. 24:29–35
    [Google Scholar]
  108. 108. 
    Sung YC, Outram MA, Breen S, Wang C, Dagvadorj B et al. 2021. PR1-mediated defence via C-terminal peptide release is targeted by a fungal pathogen effector. New Phytol 229:3467–80
    [Google Scholar]
  109. 109. 
    Tai Y-S, Bragg J, Meinhardt SW. 2007. Functional characterization of ToxA and molecular identification of its intracellular targeting protein in wheat. Am. J. Plant Physiol. 2:76–89
    [Google Scholar]
  110. 110. 
    Thomma BPHJ, Nurnberger T, Joosten MHAJ. 2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15
    [Google Scholar]
  111. 111. 
    Tomás A, Bockus WW. 1987. Cultivar-specific toxicity of culture filtrates of Pyrenophora tritici-repentis. Phytopathology 77:1337–40
    [Google Scholar]
  112. 112. 
    Tomás 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. Mol. Plant-Microbe Interact. 8:41–48
    [Google Scholar]
  113. 113. 
    Toruno TY, Stergiopoulos I, Coaker G. 2016. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54:419–41
    [Google Scholar]
  114. 114. 
    Tuori RP, Wolpert TJ, Ciuffetti LM. 1995. Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis. Mol. Plant-Microbe Interact. 8:41–48
    [Google Scholar]
  115. 115. 
    Wicki W, Messmer M, Winzeler M, Stamp P, Schmid JE. 1999. In vitro screening for resistance against Septoria nodorum blotch in wheat. Theor. Appl. Genet. 99:1273–80
    [Google Scholar]
  116. 116. 
    Winterberg B, Du Fall LA, Song X, Pascovici D, Care N et al. 2014. The necrotrophic effector protein SnTox3 re-programs metabolism and elicits a strong defence response in susceptible wheat leaves. BMC Plant Biol 14:215–29
    [Google Scholar]
  117. 117. 
    Xu SS, Friesen TL, Cai X. 2004. Sources and genetic control of resistance to Stagonospora nodorum blotch in wheat. Recent Research Development in Genetics and Breeding, Vol. 1 SG Pandalai 449–69 Kerala, India: Research Signpost
    [Google Scholar]
  118. 118. 
    Yang F, Li W, Derbyshire M, Larsen MR, Rudd JJ, Palmisano G. 2015. Unraveling incompatibility between wheat and the fungal pathogen Zymoseptoria tritici through apoplastic proteomics. BMC Genom 16:362
    [Google Scholar]
  119. 119. 
    Yang F, Li W, Jørgensen HJL. 2013. Transcriptional reprogramming of wheat and the hemibiotrophic pathogen Septoria tritici during two phases of the compatible interaction. PLOS ONE 8:e81606
    [Google Scholar]
  120. 120. 
    Zhang H-F, Francl LJ, Jordahl JG, Meinhardt SW. 1997. Structural and physical properties of a necrosis-inducing toxin from Pyrenophora tritici-repentis. Phytopathology 87:154–60
    [Google Scholar]
  121. 121. 
    Zhang Z, Friesen TL, Xu SS, Shi G, Liu Z-H et al. 2011. Homoeologous wheat genes mediate recognition of SnTox3 to confer effector-triggered susceptibility to Stagonospora nodorum. Plant J 65:27–38
    [Google Scholar]
  122. 122. 
    Zhang Z, Running KLD, Seneviratne S, Peters-Haugrud AR, Szabo-Hever A et al. 2021. A protein kinase-major sperm protein gene hijacked by a necrotrophic fungal pathogen triggers disease susceptibility in wheat. Plant J https://doi.org/10.1111/tpj.15194
    [Crossref] [Google Scholar]
  123. 123. 
    Zhong Z, Marcel TC, Hartmann FE, Ma X, Plissonneau C et al. 2017. A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytol 214:619–31
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-120320-012807
Loading
/content/journals/10.1146/annurev-phyto-120320-012807
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error