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Current Genetics

, Volume 55, Issue 4, pp 439–448 | Cite as

The MAPKK kinase ChSte11 regulates sexual/asexual development, melanization, pathogenicity, and adaptation to oxidative stress in Cochliobolus heterostrophus

  • Kosuke Izumitsu
  • Akira Yoshimi
  • Daisuke Kubo
  • Atsushi Morita
  • Yoshimoto Saitoh
  • Chihiro Tanaka
Research Article

Abstract

All fungi use multiple mitogen-activated protein kinase (MAPK) cascades to respond to external signals to regulate specialized responses. In this study, we cloned and characterized a putative MAPKKK gene ChSte11, orthologous to yeast STE11, of Cochliobolus heterostrophus. ΔChste11 strains showed defects in conidiation, sexual development, melanization and the formation of appressoria. These mutants were significantly less virulent on corn plants than the wild type. Similar phenotypes were observed in mutants of Chk1-MAPK, a putative downstream protein kinase of ChSte11. These results suggested that ChSte11 regulates various morphological changes and pathogenicity via Chk1 MAPK. Both ΔChste11 and Δchk1 strains showed severe sensitivity to oxidative stress, hydrogen peroxide, and heavy metals, cupric or ferric cations. ΔBmhog1 strains, mutants of the HOG1-type MAPK, did not show sensitivity to these forms of stress. Our results strongly suggested that the Ste11-type MAPKKK regulates not only various morphological changes and pathogenicity, but also adaptations to stress via Chk1-type MAPK in filamentous fungi.

Keywords

STE11 KSS1 FUS3 HOG1 P42/44 

Supplementary material

294_2009_257_MOESM1_ESM.pdf (1.2 mb)
Supplementary Figs 1, 2 (PDF 1222 kb)

References

  1. Albertyn J, Hohmann S, Thevelein JM, Prior BA (1994) GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14:4135–4144PubMedGoogle Scholar
  2. Atoui A, Bao D, Kaur N, Grayburn WS, Calvo AM (2008) Aspergillus nidulans natural product biosynthesis is regulated by MpkB, a putative pheromone response mitogen-activated protein kinase. Appl Env Microbiol 74:3596–3600CrossRefGoogle Scholar
  3. Bardwell L, Cook JG, Chang EC, Cairns BR, Thorner J (1996) Signaling in the yeast pheromone response pathway: specific and high-affinity interaction of the mitogen-activated protein (MAP) kinases Kss1 and Fus3 with the upstream MAP kinase kinase Ste7. Mol Cell Biol 16:3637–3650PubMedGoogle Scholar
  4. Carroll AM, Sweigard JA, Valent B (1994) Improved vectors for selecting resistance to hygromycin. Fungal Genet Newsl 41:22Google Scholar
  5. Dixon KP, Xu JR, Smirnoff N, Talbot NJ (1999) Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11:2045–20586PubMedCrossRefGoogle Scholar
  6. Erdman S, Lin L, Malczynski M, Snyder M (1998) Pheromone-regulated genes required for yeast mating differentiation. J Cell Biol 140:461–483PubMedCrossRefGoogle Scholar
  7. Errede B, Gartner A, Zhou Z, Nasmyth K, Ammerer G (1993) MAP kinase-related FUS3 from S. cerevisiae is activated by STE7 in vitro. Nature 362:261–264PubMedCrossRefGoogle Scholar
  8. Furukawa K, Hoshi Y, Maeda T, Nakajima T, Abe K (2005) Aspergillus nidulans HOG pathway is activated only by two-component signalling pathway in response to osmotic stress. Mol Microbiol 56:1246–1261PubMedCrossRefGoogle Scholar
  9. Gafur A, Tanaka C, Ouchi S, Tsuda M (1997) A PCR-based method for mating type determination in Cochliobolus heterostrophus. Mycoscience 38:455–458CrossRefGoogle Scholar
  10. Gustin MC, Albertyn J, Alexander M, Davenport K (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62:1264–1300PubMedGoogle Scholar
  11. Hirayama T, Maeda T, Saito H, Shinozaki K (1995) Cloning and characterization of seven cDNAs for hyperosmolarity-responsive (HOR) genes of Saccharomyces cerevisiae. Mol Gen Genet 249:127–138PubMedCrossRefGoogle Scholar
  12. Ip YT, Davis RJ (1998) Signal transduction by the c-Jun N-terminal kinase (JNK)—from inflammation to development. Curr Opin Cell Biol 10:205–219PubMedCrossRefGoogle Scholar
  13. 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 6:171–181PubMedCrossRefGoogle Scholar
  14. Jenczmionka NJ, Schäfer W (2005) The Gpmk1 MAP kinase of Fusarium graminearum regulates the induction of specific secreted enzymes. Curr Genet 47:29–36PubMedCrossRefGoogle Scholar
  15. Kawasaki L, Sánchez O, Shiozaki K, Aguirre J (2002) SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol Microbiol 45:1153–1163PubMedCrossRefGoogle Scholar
  16. Kim YK, Kawano T, Li DX, Kolattukudy PE (2000) A mitogen-activated protein kinase kinase required for induction of cytokinesis and appressorium formation by host signals in the conidia of Colletotrichum gloeosporioides. Plant Cell 12:1331–1343PubMedCrossRefGoogle Scholar
  17. Krantz M, Becit E, Hohmann S (2006) Comparative analysis of HOG pathway proteins to generate hypotheses for functional analysis. Curr Genet 49:152–165PubMedCrossRefGoogle Scholar
  18. Lamarre C, Ibrahim-Granet O, Du C, Calderone R, Latgé JP (2007) Characterization of the SKN7 ortholog of Aspergillus fumigatus. Fungal Genet Biol 44:682–690PubMedCrossRefGoogle Scholar
  19. Lev S, Horwitz BA (2003) A mitogen-activated protein kinase pathway modulates the expression of two cellulase genes in Cochliobolus heterostrophus during plant infection. Plant Cell 15:835–844PubMedCrossRefGoogle Scholar
  20. Lev S, Sharon A, Hadar R, Ma H, Horwitz BA (1999) A mitogen-activated protein kinase of the corn-leaf pathogen Cochliobolus heterostrophus is involved in conidiation, appressorium formation, and pathogenicity: diverse roles for mitogen-activated protein kinase homologs in foliar pathogens. Proc Natl Acad Sci USA 96:13542–13547PubMedCrossRefGoogle Scholar
  21. Li D, Bobrowicz P, Wilkinson HH, Ebbole DJ (2005) A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa. Genetics 170:1091–1104PubMedCrossRefGoogle Scholar
  22. Maeda T, Takekawa M, Saito H (1995) Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269:554–558PubMedCrossRefGoogle Scholar
  23. Mey G, Oeser B, Lebrun MH, Tudzynski P (2002) The biotrophic, non-appressoria forming grass pathogen Claviceps purpurea needs a Fus3/Pmk1 homologous MAP kinase for colonization of rye ovarian tissue. Mol Plant Microb Interact 15:303–312CrossRefGoogle Scholar
  24. Neiman AM, Herskowitz I (1999) Reconstitution of a yeast protein kinase cascade in vitro: activation of the yeast MEK homologue STE7 by STE11. Proc Natl Acad Sci USA 91:3398–3402CrossRefGoogle Scholar
  25. Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750PubMedCrossRefGoogle Scholar
  26. Norbeck J, Påhlman AK, Akhtar N, Blomberg A, Adler L (1996) Purification and characterization of two isoenzymes of dl-glycerol-3-phosphatase from Saccharomyces cerevisiae. J Biol Chem 271:13875–13881PubMedCrossRefGoogle Scholar
  27. Oide S, Moeder W, Krasnoff S, Gibson D, Haas H, Yoshioka K, Turgeon BG (2006) NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18:2836–2853PubMedCrossRefGoogle Scholar
  28. Paoletti M, Seymour FA, Alcocer MJC, Kaur N, Calvo AM, Archer DB, Paul S (2007) Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Cur Biol 17:1384–1389CrossRefGoogle Scholar
  29. Posas F, Saito H (1997) Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276:1702–1705PubMedCrossRefGoogle Scholar
  30. Ramamoorthy V, Zhao X, Snyder AK, Xu JR, Shah DM (2007) Two mitogen-activated protein kinase signalling cascades mediate basal resistance to antifungal plant defensins in Fusarium graminearum. Cell Microbiol 9:1491–1506PubMedCrossRefGoogle Scholar
  31. Ruiz-Roldan MC, Maier FJ, Schafer W (2001) PTK1, a mitogen-activated-protein kinase gene, is required for conidiation, appressorium formation, and pathogenicity of Pyrenophora teres on barley. Mol Plant Microb Interact 14:116–125CrossRefGoogle Scholar
  32. Schaeffer HJ, Weber MJ (1999) Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol Cell Biol 19:2435–2444PubMedGoogle Scholar
  33. Taga M, Nagakubo H, Tsuda M, Ueyama A (1978) Ascospore analysis of kasugamycin resistance in the perfect stage of Pyricularia oryzae. Phytopathology 68:815–817CrossRefGoogle Scholar
  34. Takano Y, Kikuchi T, Kubo Y, Hamer JE, Mise K, Furusawa I (2000) The Colletotrichum lagenarium MAP kinase gene CMK1 regulates diverse aspects of fungal pathogenesis. Mol Plant Microb Interact 13:374–383CrossRefGoogle Scholar
  35. Tanaka C, Kubo Y, Tsuda M (1991) Genetic analysis and characterization of Cochliobolus heterostrophus colour mutants. Mycol Res 95:49–56CrossRefGoogle Scholar
  36. Urban M, Mott E, Farley T, Hammond-Kosack K (2003) The Fusarium graminearum MAP1 gene is essential for pathogenicity and development of perithecia. Mol Plant Pathol 4:347–359CrossRefGoogle Scholar
  37. Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143–180PubMedGoogle Scholar
  38. Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defence response. Acta Physiol Plant 19:581–589CrossRefGoogle Scholar
  39. Xu JR, Hamer JE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10:2696–2706PubMedCrossRefGoogle Scholar
  40. Xu JR, Staiger CJ, Hamer JE (1998) Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc Natl Acad Sci USA 95:12713–12718PubMedCrossRefGoogle Scholar
  41. 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 4:1820–1828PubMedCrossRefGoogle Scholar
  42. Zhao X, Kim Y, Park G, Xu JR (2005) A mitogen activated protein kinase cascade regulating infection related morphogenesis in Magnaporthe grisea. Plant Cell 17:1317–1329PubMedCrossRefGoogle Scholar
  43. Zheng L, Campbell M, Murray J, Lam S, Xu JR (2000) The BMP1 gene is essential for pathogenicity in the gray mold fungus Botrytis cinerea. Mol Plant Microb Interact 13:724–732CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Kosuke Izumitsu
    • 1
  • Akira Yoshimi
    • 1
    • 2
  • Daisuke Kubo
    • 1
  • Atsushi Morita
    • 1
  • Yoshimoto Saitoh
    • 1
  • Chihiro Tanaka
    • 1
  1. 1.Laboratory of Environmental Mycoscience, Graduate School of AgricultureKyoto UniversityKyotoJapan
  2. 2.New Industry Creation Hatchery Center (NICHe)Tohoku UniversitySendaiJapan

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