1887

Abstract

is a widespread mycoparasitic fungus, able to successfully colonize a wide range of substrates under different environmental conditions. Transcript profiling revealed a subset of genes induced in under hyperosmotic shock. The gene, a homologue of the MAPK gene that controls the hyperosmotic stress response in , was characterized. complemented the Δ mutation in , but showed different features to yeast alleles: improved osmoresistance by expression of the allele and a lack of lethality when the allele was overexpressed. ThHog1 protein was phosphorylated in under different stress conditions such as hyperosmotic or oxidative stress, among others. By using a ThHog1-GFP fusion, the protein was shown to be localized in nuclei under these stress conditions. Two mutant strains of were constructed: one carrying the allele, and a knockdown -silenced strain. The silenced strain was highly sensitive to osmotic stress, and showed intermediate levels of resistance against oxidative stress, indicating that the main role of ThHog1 protein is in the hyperosmotic stress response. Stress cross-resistance experiments showed evidences of a secondary role of ThHog1 in oxidative stress. The strain carrying the allele was highly resistant to the calcineurin inhibitor cyclosporin A, which suggests the existence of links between the two pathways. The two mutant strains showed a strongly reduced antagonistic activity against the plant pathogens and , which points to a role of ThHog1 protein in fungus–fungus interactions.

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2006-06-01
2024-03-28
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References

  1. Alonso-Monge R, Navarro-Garcia F, Roman E, Negredo A. I, Eisman B, Nombela C, Pla J. 2003; The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans . Eukaryot Cell 2:351–361 [CrossRef]
    [Google Scholar]
  2. Altschul S. F, Madden T. L, Schaffer A. A, Zhang J, Zhang Z, Miller W, Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
    [Google Scholar]
  3. Bahn Y. S, Kojima K, Cox G. M, Heitman J. 2005; Specialization of the HOG pathway and its impact on differentiation and virulence of Cryptococcus neoformans . Mol Biol Cell 16:2285–2300 [CrossRef]
    [Google Scholar]
  4. Ballance D. J. 1986; Sequences important for gene expression in filamentous fungi. Yeast 2:229–236 [CrossRef]
    [Google Scholar]
  5. Bell M, Capone R, Pashtan I, Levitzki A, Engelberg D. 2001; Isolation of hyperactive mutants of the MAPK p38/Hog1 that are independent of MAPK kinase activation. J Biol Chem 276:25351–25358 [CrossRef]
    [Google Scholar]
  6. Bilsland E, Molin C, Swaminathan S, Ramne A, Sunnerhagen P. 2004; Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol Microbiol 53:1743–1756 [CrossRef]
    [Google Scholar]
  7. Brewster J. L, Dwyer N. D, Winter E, Gustin M. C, de Valoir T. 1993; An osmosensing signal transduction pathway in yeast. Science 259:1760–1763 [CrossRef]
    [Google Scholar]
  8. Causton H. C, Ren B, Koh S. S. 7 other authors 2001; Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12:323–337 [CrossRef]
    [Google Scholar]
  9. Chen D, Toone W. M, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bahler J. 2003; Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14:214–229 [CrossRef]
    [Google Scholar]
  10. Degols G, Russell P. 1997; Discrete roles of the Spc1 kinase and the Atf1 transcription factor in the UV response of Schizosaccharomyces pombe . Mol Cell Biol 17:3356–3363
    [Google Scholar]
  11. Degols G, Shiozaki K, Russell P. 1996; Activation and regulation of the Spc1 stress-activated protein kinase in Schizosaccharomyces pombe . Mol Cell Biol 16:2870–2877
    [Google Scholar]
  12. Delgado-Jarana J, Martinez-Rocha A. L, Roldan-Rodriguez R, Roncero M. I, Di Pietro A. 2005; Fusarium oxysporum G-protein beta subunit Fgb1 regulates hyphal growth, development, and virulence through multiple signalling pathways. Fungal Genet Biol 42:61–72 [CrossRef]
    [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 [CrossRef]
    [Google Scholar]
  14. Dumont F. J. 2000; FK506, an immunosuppressant targeting calcineurin function. Curr Med Chem 7:731–748 [CrossRef]
    [Google Scholar]
  15. Fox D. S, Cruz M. C, Sia R. A, Ke H, Cox G. M, Cardenas M. E, Heitman J. 2001; Calcineurin regulatory subunit is essential for virulence and mediates interactions with FKBP12-FK506 in Cryptococcus neoformans . Mol Microbiol 39:835–849 [CrossRef]
    [Google Scholar]
  16. Gasch A. P, Spellman P. T, Kao C. M, Carmel-Harel O, Eisen M. B, Storz G, Botstein D, Brown P. O. 2000; Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257 [CrossRef]
    [Google Scholar]
  17. Goldman G. H, Pellizzon C. H, Marins M, McInerney J. O, Goldman M. H. S. 1998; Trichoderma spp. genome and gene structure. In Trichoderma and Gliocladium pp  209–224 Edited by Harman G. E., Kubicek C. P. London: Taylor & Francis;
    [Google Scholar]
  18. 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
    [Google Scholar]
  19. Han K. H, Prade R. A. 2002; Osmotic stress-coupled maintenance of polar growth in Aspergillus nidulans . Mol Microbiol 43:1065–1078 [CrossRef]
    [Google Scholar]
  20. Harman G. E, Howell C. R, Viterbo A, Chet I, Lorito M. 2004; Trichoderma species – opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56 [CrossRef]
    [Google Scholar]
  21. Hohmann S. 2002; Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66:300–372 [CrossRef]
    [Google Scholar]
  22. Hohmann S, Mager W. H. 1997 Yeast Stress Responses New York: Chapman & Hall;
    [Google Scholar]
  23. Kawasaki L, Sanchez 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 45:1153–1163 [CrossRef]
    [Google Scholar]
  24. 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 [CrossRef]
    [Google Scholar]
  25. Kothe G. O, Free S. J. 1998; The isolation and characterization of nrc-1 and nrc-2 , two genes encoding protein kinases that control growth and development in Neurospora crassa . Genetics 149:117–130
    [Google Scholar]
  26. Kraus P. R, Heitman J. 2003; Coping with stress: calmodulin and calcineurin in model and pathogenic fungi. Biochem Biophys Res Commun 311:1151–1157 [CrossRef]
    [Google Scholar]
  27. Kubicek G. E, Penttila M. E. 1998; Regulation of production of plant polysaccharide degrading enzymes by Trichoderma. In Trichoderma and Gliocladium pp  49–71 Edited by Harman G. E., Kubicek C. P. London: Taylor & Francis;
    [Google Scholar]
  28. Kyriakis J. M, Avruch J. 2001; Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807–869
    [Google Scholar]
  29. Lawrence C. L, Botting C. H, Antrobus R, Coote P. J. 2004; Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress. Mol Cell Biol 24:3307–3323 [CrossRef]
    [Google Scholar]
  30. Lengeler K. B, Davidson R. C, D'Souza C, Harashima T, Shen W. C, Wang P, Pan X, Waugh M, Heitman J. 2000; Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64:746–785 [CrossRef]
    [Google Scholar]
  31. Lev S, Hadar R, Amedeo P, Baker S. E, Yoder O. C, Horwitz B. A. 2005; Activation of an AP1-like transcription factor of the maize pathogen Cochliobolus heterostrophus in response to oxidative stress and plant signals. Eukaryot Cell 4:443–454 [CrossRef]
    [Google Scholar]
  32. Lewis J. G, Learmonth R. P, Watson K. 1995; Induction of heat, freezing and salt tolerance by heat and salt shock in Saccharomyces cerevisiae . Microbiology 141:687–694 [CrossRef]
    [Google Scholar]
  33. Lu Z, Tombolini R, Woo S, Zeilinger S, Lorito M, Jansson J. K. 2004; In vivo study of Trichoderma -pathogen-plant interactions, using constitutive and inducible green fluorescent protein reporter systems. Appl Environ Microbiol 70:3073–3081 [CrossRef]
    [Google Scholar]
  34. Mach R. L, Schindler M, Kubicek C. P. 1994; Transformation of Trichoderma reesei based on hygromycin B resistance using homologous expression signals. Curr Genet 25:567–570 [CrossRef]
    [Google Scholar]
  35. Maeta K, Izawa S, Inoue Y. 2005; Methylglyoxal, a metabolite derived from glycolysis, functions as a signal initiator of the high osmolarity glycerol-mitogen-activated protein kinase cascade and calcineurin/Crz1-mediated pathway in Saccharomyces cerevisiae . J Biol Chem 280:253–260 [CrossRef]
    [Google Scholar]
  36. Mendoza-Mendoza A, Pozo M. J, Grzegorski D, Martinez P, Garcia J. M, Olmedo-Monfil V, Cortes C, Kenerley C, Herrera-Estrella A. 2003; Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen-activated protein kinase. Proc Natl Acad Sci U S A 100:15965–15970 [CrossRef]
    [Google Scholar]
  37. Motoyama T, Ohira T, Kadokura K, Ichiishi A, Fujimura M, Yamaguchi I, Kudo T. 2005; An Os-1 family histidine kinase from a filamentous fungus confers fungicide-sensitivity to yeast. Curr Genet 47:298–306 [CrossRef]
    [Google Scholar]
  38. Mukherjee P. K, Latha J, Hadar R, Horwitz B. A. 2003; TmkA, a mitogen-activated protein kinase of Trichoderma virens , is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot Cell 2:446–455 [CrossRef]
    [Google Scholar]
  39. 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 [CrossRef]
    [Google Scholar]
  40. Penttila M. 1998; Heterologous protein production in Trichoderma. In Trichoderma and Gliocladium pp  365–382 Edited by Harman G. E., Kubicek C. P. London: Taylor & Francis;
    [Google Scholar]
  41. Penttila M, Nevalainen H, Ratto M, Salminen E, Knowles J. 1987; A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei . Gene 61:155–164 [CrossRef]
    [Google Scholar]
  42. Raeder U, Broda P. 1985; Rapid preparation of DNA from filamentous fungi. Lett Appl Microbiol 1:17–20 [CrossRef]
    [Google Scholar]
  43. Reiser V, Ruis H, Ammerer G. 1999; Kinase activity-dependent nuclear export opposes stress-induced nuclear accumulation and retention of Hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae . Mol Biol Cell 10:1147–1161 [CrossRef]
    [Google Scholar]
  44. Rep M, Krantz M, Thevelein J. M, Hohmann S. 2000; The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J Biol Chem 275:8290–8300 [CrossRef]
    [Google Scholar]
  45. Rey M, Llobell A, Monte E, Scala F, Lorito M. 2004; Genomics of Trichoderma. In Fungal Genomics: Applied Mycology & Biotechnology pp  225–248 Edited by Khachatourians G. G. Amsterdam: Elsevier;
    [Google Scholar]
  46. Rodriguez-Hernandez C. J, Sanchez-Perez I, Gil-Mascarell R, Rodriguez-Afonso A, Torres A, Perona R, Murguia J. R. 2003; The immunosuppressant FK506 uncovers a positive regulatory cross-talk between the Hog1p and Gcn2p pathways. J Biol Chem 278:33887–33895 [CrossRef]
    [Google Scholar]
  47. Roux P. P, Blenis J. 2004; ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68:320–344 [CrossRef]
    [Google Scholar]
  48. Sambrook J, Russell D. W. 2001 Molecular Cloning: a Laboratory Manual Cold Spring Harbor; New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  49. Sanchez-Perez I, Rodriguez-Hernandez C. J, Manguan-Garcia C, Torres A, Perona R, Murguia J. R. 2004; FK506 sensitizes mammalian cells to high osmolarity by modulating p38 MAP kinase activation. Cell Mol Life Sci 61:700–708 [CrossRef]
    [Google Scholar]
  50. Shieh J. C, Wilkinson M. G, Buck V, Morgan B. A, Makino K, Millar J. B. 1997; The Mcs4 response regulator coordinately controls the stress-activated Wak1-Wis1-Sty1 MAP kinase pathway and fission yeast cell cycle. Genes Dev 11:1008–1022 [CrossRef]
    [Google Scholar]
  51. Shiozaki K, Russell P. 1997; Stress-activated protein kinase pathway in cell cycle control of fission yeast. Methods Enzymol 283:506–520
    [Google Scholar]
  52. Shitamukai A, Hirata D, Sonobe S, Miyakawa T. 2004; Evidence for antagonistic regulation of cell growth by the calcineurin and high osmolarity glycerol pathways in Saccharomyces cerevisiae . J Biol Chem 279:3651–3661
    [Google Scholar]
  53. Smith D. A, Nicholls S, Morgan B. A, Brown A. J, Quinn J. 2004; A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans . Mol Biol Cell 15:4179–4190 [CrossRef]
    [Google Scholar]
  54. Sousa S. 2004; Improvement of the Trichoderma harzianum CECT 2413 expression system for the production of proteins with biotechnological value. In Bioquímica Vegetal y Fotosíntesis PhD thesis University of Sevilla;
    [Google Scholar]
  55. Widmann C, Gibson S, Jarpe M. B, Johnson G. L. 1999; Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143–180
    [Google Scholar]
  56. 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 [CrossRef]
    [Google Scholar]
  57. Yu V. P, Reed S. I. 2004; Cks1 is dispensable for survival in Saccharomyces cerevisiae . Cell Cycle 3:1402–1404 [CrossRef]
    [Google Scholar]
  58. Zeilinger S, Schmoll M, Pail M, Mach R. L, Kubicek C. P. 2003; Nucleosome transactions on the Hypocrea jecorina (Trichoderma reesei) cellulase promoter cbh2 associated with cellulase induction. Mol Genet Genomics 270:46–55 [CrossRef]
    [Google Scholar]
  59. Zhang Y, Lamm R, Pillonel C, Lam S, Xu J. R. 2002; Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl Environ Microbiol 68:532–538 [CrossRef]
    [Google Scholar]
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