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Abstract

The HOG1 mitogen-activated protein kinase (MAPK) pathway is activated through two-component histidine kinase (HK) signalling. This pathway was first characterized in the budding yeast as a regulator of osmotolerance. The fungus is the causal agent of septoria nodorum blotch of wheat. This pathogen uses host-specific effectors in tandem with general pathogenicity mechanisms to carry out its infection process. Genes showing strong sequence homology to HOG1 signalling pathway genes have been identified in the genome of . In this study, we examined the role of the pathway in the virulence of on wheat by disrupting putative pathway component genes: HOG1 (SNOG_13296) MAPK and NIK1 (SNOG_11631) hybrid HK. Mutants deleted in NIK1 and HOG1 were insensitive to dicarboximide and phenylpyrrole fungicides, but not a fungicide that targets ergosterol biosynthesis. Furthermore, both Δnik1 and Δhog1 mutants showed increased sensitivity to hyperosmotic stress. However, HOG1, but not NIK1, is required for tolerance to elevated temperatures. HOG1 deletion conferred increased tolerance to 6-methoxy-2-benzoxazolinone, a cereal phytoalexin. This suggests that the HOG1 signalling pathway is not exclusively associated with NIK1. Both Δnik1 and Δhog1 mutants retained the ability to infect and cause necrotic lesions on wheat. However, we observed that the Δhog1 mutation resulted in reduced production of pycnidia, asexual fruiting bodies that facilitate spore dispersal during late infection. Our study demonstrated the overlapping and distinct roles of a HOG1 MAPK and two-component HK signalling in growth and pathogenicity.

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2016-06-01
2021-08-02
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References

  1. Adam A., Kohut G., Hornok L. 2008a; Cloning and characterization of a HOG-type MAP kinase encoding gene from Fusarium proliferatum . Acta Phytopathol Entomol Hung 43:1–13 [CrossRef]
    [Google Scholar]
  2. Adam A. L., Kohut G., Hornok L. 2008b; Fphog1, a HOG-type MAP kinase gene, is involved in multistress response in Fusarium proliferatum . J Basic Microbiol 48:151–159 [CrossRef]
    [Google Scholar]
  3. Avenot H., Simoneau P., Iacomi-Vasilescu B., Bataillé-Simoneau N. 2005; Characterization of mutations in the two-component histidine kinase gene AbNIK1 from Alternaria brassicicola that confer high dicarboximide and phenylpyrrole resistance. Curr Genet 47:234–243 [View Article][PubMed]
    [Google Scholar]
  4. Bahn Y. S., Xue C., Idnurm A., Rutherford J. C., Heitman J., Cardenas M. E. 2007; Sensing the environment: lessons from fungi. Nat Rev Microbiol 5:57–69 [View Article][PubMed]
    [Google Scholar]
  5. Brewster J. L., de Valoir T., Dwyer N. D., Winter E., Gustin M. C. 1993; An osmosensing signal transduction pathway in yeast. Science 259:1760–1763 [View Article][PubMed]
    [Google Scholar]
  6. Casey T., Solomon P. S., Bringans S., Tan K.-C., Oliver R. P., Lipscombe R. 2010; Quantitative proteomic analysis of G-protein signalling in Stagonospora nodorum using isobaric tags for relative and absolute quantification. Proteomics 10:38–47 [View Article][PubMed]
    [Google Scholar]
  7. Catlett N. L., Yoder O. C., Turgeon B. G. 2003; Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot Cell 2:1151–1161 [View Article][PubMed]
    [Google Scholar]
  8. Cho Y., Kim K. H., La Rota M., Scott D., Santopietro G., Callihan M., Mitchell T. K., Lawrence C. B. 2009; Identification of novel virulence factors associated with signal transduction pathways in Alternaria brassicicola. Mol Microbiol 72:1316–1333 [View Article][PubMed]
    [Google Scholar]
  9. Chooi Y. H., Muria-Gonzalez M. J., Solomon P. S. 2014; A genome-wide survey of the secondary metabolite biosynthesis genes in the wheat pathogen Parastagonospora nodorum . Mycology 5:192–206 [View Article][PubMed]
    [Google Scholar]
  10. Chooi Y. H., Krill C., Barrow R. A., Chen S., Trengove R., Oliver R. P., Solomon P. S. 2015a; An in planta-expressed polyketide synthase produces (R)-mellein in the wheat pathogen Parastagonospora nodorum . Appl Environ Microb 81:177–186 [CrossRef]
    [Google Scholar]
  11. Chooi Y. H., Muria-Gonzalez M. J., Mead O. L., Solomon P. S. 2015b; SnPKS19 encodes the polyketide synthase for alternariol mycotoxin biosynthesis in the wheat pathogen Parastagonospora nodorum . Appl Environ Microb 81:5309–5317 [CrossRef]
    [Google Scholar]
  12. Detweiler A. R., Vargas J. M. J., Danneberger T. K. 1983; Resistance of Sclerotinia homoeocarpa to iprodione and benomyl. Plant Journal 67:627–630
    [Google Scholar]
  13. Dixon K. P., Xu J. R., Smirnoff N., Talbot N. J. 1999; Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea . Plant Cell 11:2045–2058[PubMed] [CrossRef]
    [Google Scholar]
  14. Du Fall L. A., Solomon P. S. 2013; The necrotrophic effector SnToxA induces the synthesis of a novel phytoalexin in wheat. New Phytol 200:185–200 [View Article][PubMed]
    [Google Scholar]
  15. Duan Y., Ge C., Liu S., Wang J., Zhou M. 2013; A two-component histidine kinase Shk1 controls stress response, sclerotial formation and fungicide resistance in Sclerotinia sclerotiorum . Physiol Mol Plant Pathol 14:708–718 [View Article][PubMed]
    [Google Scholar]
  16. Eyal Z., Scharen A. L., Prescott J. M., van Ginkel M. 1987 The Septoria Diseases of Wheat: Concepts and Methods of Disease Management Texcoco: CIMMYT;
    [Google Scholar]
  17. Eyal Z. 1999; The septoria tritici and Stagonospora nodorum blotch diseases of wheat. Eur J Plant Pathol 105:629–641 [CrossRef]
    [Google Scholar]
  18. Friesen T. L., Faris J. D., Solomon P. S., Oliver R. P. 2008; Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10:1421–1428 [View Article][PubMed]
    [Google Scholar]
  19. Fujimura M., Banna S., Ichiishi A., Fukumori F. 2015; Histidine kinase inhibitors. In Fungicide Resistance in Plant Pathogens pp 181–197 . Edited by Ishii H., Hollomon D. W. Tokyo: Springer; [CrossRef]
    [Google Scholar]
  20. Gardiner D. M., McDonald M. C., Covarelli L., Solomon P. S., Rusu A. G., Marshall M., Kazan K., Chakraborty S., McDonald B. A., Manners J. M. 2012; Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLoS Pathog 8:e1002952 [View Article][PubMed]
    [Google Scholar]
  21. Grabke A., Fernández-Ortuño D., Amiri A., Li X., Peres N. A., Smith P., Schnabel G. 2014; Characterization of iprodione resistance in Botrytis cinerea from strawberry and blackberry. Phytopathology 104:396–402 [View Article][PubMed]
    [Google Scholar]
  22. Grebe T. W., Stock J. B. 1999; The histidine protein kinase superfamily. Adv Microb Physiol 41:139–227[PubMed] [CrossRef]
    [Google Scholar]
  23. Gummer J. P., Trengove R. D., Oliver R. P., Solomon P. S. 2012; A comparative analysis of the heterotrimeric G-protein Gα, Gβ and Gγ subunits in the wheat pathogen Stagonospora nodorum . BMC Microbiol 12:131 [View Article][PubMed]
    [Google Scholar]
  24. Gummer J. P., Trengove R. D., Oliver R. P., Solomon P. S. 2013; Dissecting the role of G-protein signalling in primary metabolism in the wheat pathogen Stagonospora nodorum . Microbiology 159:1972–1985 [View Article][PubMed]
    [Google Scholar]
  25. Gustin M. C., Albertyn J., Alexander M., Davenport K. 1998; MAP kinase pathways in the yeast Saccharomyces cerevisiae . Microbiol Mol Biol Rev 62:1264–1300[PubMed]
    [Google Scholar]
  26. Hahn M., Leroch M. 2015; Multidrug efflux transporters. In Fungicide Resistance in Plant Pathogens: Principles and Guides to Practical Management pp 233–248 . Edited by Ishii H., Hollomon D. W. Japan: Springer;
    [Google Scholar]
  27. Hane J. K., Lowe R. G., Solomon P. S., Tan K.-C., Schoch C. L., Spatafora J. W., Crous P. W., Kodira C., Birren B. W. et al. 2007; Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum . Plant Cell 19:3347–3368 [View Article][PubMed]
    [Google Scholar]
  28. Heller J., Ruhnke N., Espino J. J., Massaroli M., Collado I. G., Tudzynski P. 2012; The mitogen-activated protein kinase BcSak1 of Botrytis cinerea is required for pathogenic development and has broad regulatory functions beyond stress response. Mol Plant Microbe Interact 25:802–816 [View Article][PubMed]
    [Google Scholar]
  29. Igbaria A., Lev S., Rose M. S., Lee B. N., Hadar R., Degani O., Horwitz B. A. 2008; Distinct and combined roles of the MAP kinases of Cochliobolus heterostrophus in virulence and stress responses. Mol Plant Microbe Interact 21:769–780 [View Article][PubMed]
    [Google Scholar]
  30. IpCho S. V. S., Tan K.-C., Koh G., Gummer J., Oliver R. P., Trengove R. D., Solomon P. S. 2010; The transcription factor StuA regulates central carbon metabolism, mycotoxin production, and effector gene expression in the wheat pathogen Stagonospora nodorum . Eukaryot Cell 9:1100–1108 [View Article][PubMed]
    [Google Scholar]
  31. Izumitsu K., Yoshimi A., Tanaka C. 2007; Two-component response regulators Ssk1p and Skn7p additively regulate high-osmolarity adaptation and fungicide sensitivity in Cochliobolus heterostrophus . Eukaryot Cell 6:171–181 [View Article][PubMed]
    [Google Scholar]
  32. Jacob S., Foster A. J., Yemelin A., Thines E. 2014; Histidine kinases mediate differentiation, stress response, and pathogenicity in Magnaporthe oryzae . Microbiologyopen 3:668–687 [View Article][PubMed]
    [Google Scholar]
  33. Kettle A. J., Batley J., Benfield A. H., Manners J. M., Kazan K., Gardiner D. M. 2015; Degradation of the benzoxazolinone class of phytoalexins is important for virulence of Fusarium pseudograminearum towards wheat. Mol Plant Pathol 16:946962 [View Article][PubMed]
    [Google Scholar]
  34. Kojima K., Takano Y., Yoshimi A., Tanaka C., Kikuchi T., Okuno T. 2004; Fungicide activity through activation of a fungal signalling pathway. Mol Microbiol 53:1785–1796 [View Article][PubMed]
    [Google Scholar]
  35. Li W., Csukai M., Corran A., Crowley P., Solomon P. S., Oliver R. P. 2008; Malayamycin, a new streptomycete antifungal compound, specifically inhibits sporulation of Stagonospora nodorum (Berk) Castell and Germano, the cause of wheat glume blotch disease. Pest Manag Sci 64:1294–1302 [View Article][PubMed]
    [Google Scholar]
  36. Lin C. H., Chung K. R. 2010; Specialized and shared functions of the histidine kinase- and HOG1 MAP kinase-mediated signaling pathways in Alternaria alternata, a filamentous fungal pathogen of citrus. Fungal Genet Biol 47:818–827 [View Article][PubMed]
    [Google Scholar]
  37. Liu W., Leroux P., Fillinger S. 2008; The HOG1-like MAP kinase Sak1 of Botrytis cinerea is negatively regulated by the upstream histidine kinase Bos1 and is not involved in dicarboximide- and phenylpyrrole-resistance. Fungal Genet Biol 45:1062–1074 [View Article][PubMed]
    [Google Scholar]
  38. Lowe R. G., Lord M., Rybak K., Trengove R. D., Oliver R. P., Solomon P. S. 2008; A metabolomic approach to dissecting osmotic stress in the wheat pathogen Stagonospora nodorum . Fungal Genet Biol 45:1479–1486 [View Article][PubMed]
    [Google Scholar]
  39. Lowe R. G., Lord M., Rybak K., Trengove R. D., Oliver R. P., Solomon P. S. 2009; Trehalose biosynthesis is involved in sporulation of Stagonospora nodorum . Fungal Genet Biol 46:381–389 [View Article][PubMed]
    [Google Scholar]
  40. Luo Y. Y., Yang J. K., Zhu M. L., Liu C. J., Li H. Y., Lu Z. B., Pan W. Z., Zhang Z. H., Bi W., Zhang K. Q. 2012; The group III two-component histidine kinase AlHK1 is involved in fungicides resistance, osmosensitivity, spore production and impacts negatively pathogenicity in Alternaria longipes. Curr Microbiol 64:449–456 [View Article][PubMed]
    [Google Scholar]
  41. Madhani H. D., Fink G. R. 1998; The riddle of MAP kinase signaling specificity. Trends Genet 14:151–155[PubMed] [CrossRef]
    [Google Scholar]
  42. Maeda T., Wurgler-Murphy S. M., Saito H. 1994; A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369:242–245 [View Article][PubMed]
    [Google Scholar]
  43. Maeda T., Takekawa M., Saito H. 1995; Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269:554–558[PubMed] [CrossRef]
    [Google Scholar]
  44. Mead O., Thynne E., Winterberg B., Solomon P. S. 2013; Characterising the role of GABA and its metabolism in the wheat pathogen Stagonospora nodorum . PLoS One 8:e78368 [View Article][PubMed]
    [Google Scholar]
  45. Mehrabi R., Zwiers L. H., de Waard M. A., Kema G. H. 2006; MgHog1 regulates dimorphism and pathogenicity in the fungal wheat pathogen Mycosphaerella graminicola . Mol Plant Microbe Interact 19:1262–1269 [View Article][PubMed]
    [Google Scholar]
  46. Moriwaki A., Kubo E., Arase S., Kihara J. 2006; Disruption of SRM1, a mitogen-activated protein kinase gene, affects sensitivity to osmotic and ultraviolet stressors in the phytopathogenic fungus Bipolaris oryzae . FEMS Microbiol Lett 257:253–261 [View Article][PubMed]
    [Google Scholar]
  47. Motoyama T., Kadokura K., Ohira T., Ichiishi A., Fujimura M., Yamaguchi I., Kudo T. 2005; A two-component histidine kinase of the rice blast fungus is involved in osmotic stress response and fungicide action. Fungal Genet Biol 42:200–212 [View Article][PubMed]
    [Google Scholar]
  48. Motoyama T., Ochiai N., Morita M., Iida Y., Usami R., Kudo T. 2008; Involvement of putative response regulator genes of the rice blast fungus Magnaporthe oryzae in osmotic stress response, fungicide action, and pathogenicity. Curr Genet 54:185–195 [View Article][PubMed]
    [Google Scholar]
  49. Nyugen V. T., Schäfer W., Bormann J. 2012; The stress-activated protein kinase FgOS-2 is a key regulator in the life cycle of the cereal pathogen Fusarium graminearum . Mol Plant Microbe Interact 25:1142–1156 [View Article][PubMed]
    [Google Scholar]
  50. Oide S., Liu J., Yun S. H., Wu D., Michev A., Choi M. Y., Horwitz B. A., Turgeon B. G. 2010; Histidine kinase two-component response regulator proteins regulate reproductive development, virulence, and stress responses of the fungal cereal pathogens Cochliobolus heterostrophus and Gibberella zeae . Eukaryot Cell 9:1867–1880 [View Article][PubMed]
    [Google Scholar]
  51. Oliver R. P., Friesen T. L., Faris J. D., Solomon P. S. 2012; Stagonospora nodorum: from pathology to genomics and host resistance. Annu Rev Phytopathol 50:23–43 [View Article][PubMed]
    [Google Scholar]
  52. Park S. M., Choi E. S., Kim M. J., Cha B. J., Yang M. S., Kim D. H. 2004; Characterization of HOG1 homologue, CpMK1, from Cryphonectria parasitica and evidence for hypovirus-mediated perturbation of its phosphorylation in response to hypertonic stress. Mol Microbiol 51:1267–1277 [View Article][PubMed]
    [Google Scholar]
  53. Posas F., Wurgler-Murphy S. M., Maeda T., Witten E. A., Thai T. C., Saito H. 1996; Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell 86:865–875[PubMed] [CrossRef]
    [Google Scholar]
  54. Quaedvlieg W., Verkley G. J., Shin H. D., Barreto R. W., Alfenas A. C., Swart W. J., Groenewald J. Z., Crous P. W. 2013; Sizing up Septoria . Stud Mycol 75:307–390 [View Article][PubMed]
    [Google Scholar]
  55. Rispail N., Di Pietro A. 2010; The two-component histidine kinase Fhk1 controls stress adaptation and virulence of Fusarium oxysporum . Physiol Mol Plant Pathol 11:395–407 [View Article][PubMed]
    [Google Scholar]
  56. Segmüller N., Ellendorf U., Tudzynski B., Tudzynski P. 2007; BcSAK1, a stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea . Eukaryot Cell 6:211–221 [View Article][PubMed]
    [Google Scholar]
  57. Solomon P. S., Thomas S. W., Spanu P., Oliver R. P. 2003; The utilisation of di/tripeptides by Stagonospora nodorum is dispensable for wheat infection. Physiol Mol Plant P 63:191–199 [CrossRef]
    [Google Scholar]
  58. Solomon P. S., Tan K.-C., Sanchez P., Cooper R. M., Oliver R. P. 2004; The disruption of a Gα subunit sheds new light on the pathogenicity of Stagonospora nodorum on wheat. Mol Plant-Microbe Interact 17:456–466 [CrossRef]
    [Google Scholar]
  59. Solomon P. S., Tan K.-C., Oliver R. P. 2005a; Mannitol 1-phosphate metabolism is required for sporulation in planta of the wheat pathogen Stagonospora nodorum . Mol Plant-Microbe Interact 18:110–115 [CrossRef]
    [Google Scholar]
  60. Solomon P. S., Waters O. D., Simmonds J., Cooper R. M., Oliver R. P. 2005b; The Mak2 MAP kinase signal transduction pathway is required for pathogenicity in Stagonospora nodorum . Curr Genet 48:60–68 [CrossRef]
    [Google Scholar]
  61. Solomon P. S., Lowe R. G., Tan K.-C., Waters O. D., Oliver R. P. 2006a; Stagonospora nodorum: cause of Stagonospora nodorum blotch of wheat. Mol Plant Pathol 7:147–156 [CrossRef]
    [Google Scholar]
  62. Solomon P. S., Rybak K., Trengove R. D., Oliver R. P. 2006b; Investigating the role of calcium/calmodulin-dependent protein kinases in Stagonospora nodorum . Mol Microbiol 62:367–381 [CrossRef]
    [Google Scholar]
  63. Solomon P. S., IpCho S. V. S., Hane J. K., Tan K.-C., Oliver R. P. 2008; A quantitative PCR approach to determine gene copy number. Fungal Genetics Report 55:5–8
    [Google Scholar]
  64. Tan K.-C. 2007; The role of signal transduction in the pathogenicity of Stagonospora nodorum on wheat. PhD thesis Department of Veterinary and Biomedical Sciences, Murdoch University; Perth, Australia:
  65. Tan K.-C., Heazlewood J. L., Millar A. H., Thomson G., Oliver R. P., Solomon P. S. 2008; A signaling-regulated, short-chain dehydrogenase of Stagonospora nodorum regulates asexual development. Eukaryot Cell 7:1916–1929 [View Article][PubMed]
    [Google Scholar]
  66. Tan K.-C., Heazlewood J. L., Millar A. H., Oliver R. P., Solomon P. S. 2009a; Proteomic identification of extracellular proteins regulated by the Gna1 Gα subunit in Stagonospora nodorum . Mycol Res 113:523–531 [CrossRef]
    [Google Scholar]
  67. Tan K.-C., Ipcho S. V., Trengove R. D., Oliver R. P., Solomon P. S. 2009b; Assessing the impact of transcriptomics, proteomics and metabolomics on fungal phytopathology. Mol Plant Pathol 10:703–715 [CrossRef]
    [Google Scholar]
  68. Tan K.-C., Trengove R. D., Maker G. L., Oliver R. P., Solomon P. S. 2009c; Metabolite profiling identifies the mycotoxin alternariol in the pathogen Stagonospora nodorum . Metabolomics 5:330–335 [CrossRef]
    [Google Scholar]
  69. Tan K.-C., Oliver R. P., Solomon P. S., Moffat C. S. 2010; Proteinaceous necrotrophic effectors in fungal virulence. Funct Plant Biol 37:907–912 [CrossRef]
    [Google Scholar]
  70. Tan K. C., Phan H. T., Rybak K., John E., Chooi Y. H., Solomon P. S., Oliver R. P. 2015; Functional redundancy of necrotrophic effectors - consequences for exploitation for breeding. Front Plant Sci 6:501 [View Article][PubMed]
    [Google Scholar]
  71. Thind T. S. 2011 Fungicide Resistance in Crop Protection: Risk and Management Wallingford: CABI;
    [Google Scholar]
  72. Viaud M., Fillinger S., Liu W., Polepalli J. S., Le Pêcheur P., Kunduru A. R., Leroux P., Legendre L. 2006; A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea . Mol Plant Microbe Interact 19:1042–1050 [View Article][PubMed]
    [Google Scholar]
  73. Weber R. W. S., Hahn M. 2011; A rapid and simple method for determining fungicide resistance in Botrytis . J Plant Diseases Protect 118:17–25 [View Article]
    [Google Scholar]
  74. Winkler A., Arkind C., Mattison C. P., Burkholder A., Knoche K., Ota I. 2002; Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway, and protein tyrosine phosphatases are essential under heat stress. Eukaryot Cell 1:163–173[PubMed] [CrossRef]
    [Google Scholar]
  75. Xu J. R. 2000; Map kinases in fungal pathogens. Fungal Genet Biol 31:137–152 [View Article][PubMed]
    [Google Scholar]
  76. Yang Q., Yan L., Gu Q., Ma Z. 2012; The mitogen-activated protein kinase kinase kinase BcOs4 is required for vegetative differentiation and pathogenicity in Botrytis cinerea . Appl Microbiol Biotechnol 96:481–492 [View Article][PubMed]
    [Google Scholar]
  77. Yoshimi A., Tsuda M., Tanaka C. 2004; Cloning and characterization of the histidine kinase gene Dic1 from Cochliobolus heterostrophus that confers dicarboximide resistance and osmotic adaptation. Mol Genet Genomics 271:228–236 [View Article][PubMed]
    [Google Scholar]
  78. Yoshimi A., Kojima K., Takano Y., Tanaka C. 2005; Group III histidine kinase is a positive regulator of Hog1-type mitogen-activated protein kinase in filamentous fungi. Eukaryot Cell 4:1820–1828 [View Article][PubMed]
    [Google Scholar]
  79. Yoshimura M. A., Luo Y., Ma Z., Michailides T. J. 2004; Sensitivity of Monilinia fructicola from stone fruit to thiophanate-methyl, iprodione, and tebuconazole. Plant Disease 88:373–378 [CrossRef]
    [Google Scholar]
  80. Zhang H., Liu K., Zhang X., Song W., Zhao Q., Dong Y., Guo M., Zheng X., Zhang Z. 2010; A two-component histidine kinase, MoSLN1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae . Curr Genet 56:517–528 [View Article][PubMed]
    [Google Scholar]
  81. Zhao X., Mehrabi R., Xu J. R. 2007; Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6:1701–1714 [View Article][PubMed]
    [Google Scholar]
  82. Zheng D., Zhang S., Zhou X., Wang C., Xiang P., Zheng Q., Xu J. R. 2012; The FgHOG1 pathway regulates hyphal growth, stress responses, and plant infection in Fusarium graminearum . PLoS One 7:e49495 [View Article][PubMed]
    [Google Scholar]
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