Table of Contents
Journal of Signal Transduction
Volume 2010 (2010), Article ID 123126, 8 pages
http://dx.doi.org/10.1155/2010/123126
Review Article

How a Mycoparasite Employs G-Protein Signaling: Using the Example of Trichoderma

Research Area of Gene Technology and Applied Biochemistry, Working Group Molecular Biochemistry of Fungi, Institute for Chemical Engineering, Vienna University of Technology, Getreidemarkt 9, 1060 Vienna, Austria

Received 20 May 2010; Revised 6 July 2010; Accepted 20 July 2010

Academic Editor: Terry Hebert

Copyright © 2010 Markus Omann and Susanne Zeilinger. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Bölker, “Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis,” Fungal Genetics and Biology, vol. 25, no. 3, pp. 143–156, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. T. Benítez, A. M. Rincón, M. C. Limón, and A. C. Codón, “Biocontrol mechanisms of Trichoderma strains,” International Microbiology, vol. 7, no. 4, pp. 249–260, 2004. View at Google Scholar · View at Scopus
  3. R. Weindling, “Trichoderma lignorum as a parasite of other soil fungi,” Journal of Phytopathology, vol. 22, pp. 837–845, 1932. View at Google Scholar
  4. R. Barak and I. Chet, “Determination, by fluorescein diacetate staining, of fungal viability during mycoparasitism,” Soil Biology and Biochemistry, vol. 18, no. 3, pp. 315–319, 1986. View at Google Scholar · View at Scopus
  5. I. Chet, “Trichoderma-application, mode of action, and potential as a biocontrol agent of soilborne plant pathogenic fungi,” in Innovative Approaches to Plant Disease Control, pp. 137–160, John Wiley & Sons, New York, NY, USA, 1987. View at Google Scholar
  6. L. Hjeljord and A. Tronsmo, “Trichoderma and Gliocladium in biological control: an overview,” in Trichoderma and Gliocladium, G. E. Harman and C. P. Kubicek, Eds., vol. 2, pp. 131–152, Taylor and Francis, London, UK, 1998. View at Google Scholar
  7. C. R. Howell, “Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts,” Plant Disease, vol. 87, no. 1, pp. 4–10, 2003. View at Google Scholar · View at Scopus
  8. D. Klein and D. E. Eveleigh, “Ecology of Trichoderma,” in Trichoderma and Gliocladium, C. P. Kubicek and G. E. Harman, Eds., vol. 1, pp. 57–74, Taylor and Francis, London, UK, 1998. View at Google Scholar
  9. I. Chet and J. Inbar, “Biological control of fungal pathogens,” Applied Biochemistry and Biotechnology, vol. 48, no. 1, pp. 37–43, 1994. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Eisendle, H. Oberegger, R. Buttinger, P. Illmer, and H. Haas, “Biosynthesis and uptake of siderophores is controlled by the PacC-mediated ambient-pH regulatory system in Aspergillus nidulans,” Eukaryotic Cell, vol. 3, no. 2, pp. 561–563, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. G. E. Harman, C. R. Howell, A. Viterbo, I. Chet, and M. Lorito, “Trichoderma species—opportunistic, avirulent plant symbionts,” Nature Reviews Microbiology, vol. 2, no. 1, pp. 43–56, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. Y. Elad, R. Barak, and I. Chet, “Possible role of lectins in mycoparasitism,” Journal of Bacteriology, vol. 154, no. 3, pp. 1431–1435, 1983. View at Google Scholar · View at Scopus
  13. Z. Lu, R. Tombolini, S. Woo, S. Zeilinger, M. Lorito, and J. K. Jansson, “In vivo study of Trichoderma-pathogen-plant interactions, using constitutive and inducible green fluorescent protein reporter systems,” Applied and Environmental Microbiology, vol. 70, no. 5, pp. 3073–3081, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Elad, I. Chet, and Y. Henis, “Degradation of plant pathogenic fungi by Trichoderma harzianum,” Canadian Journal of Microbiology, vol. 28, pp. 719–725, 1982. View at Google Scholar
  15. C. Cortes, A. Gutierrez, V. Olmedo, J. Inbar, I. Chet, and A. Herrera-Estrella, “The expression of genes involved in parasitism by Trichoderma harzianum is triggered by a diffusible factor,” Molecular and General Genetics, vol. 260, no. 2-3, pp. 218–225, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Zeilinger, C. Galhaup, K. Payer et al., “Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host,” Fungal Genetics and Biology, vol. 26, no. 2, pp. 131–140, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. S. H. Barondes, “Lectins: their multiple endogenous cellular functions,” Annual Review of Biochemistry, vol. 50, pp. 207–231, 1981. View at Google Scholar · View at Scopus
  18. J. Inbar and L. Chet, “A newly isolated lectin from the plant pathogenic fungus Sclerotium rolfsii: purification, characterization and role in mycoparasitism,” Microbiology, vol. 140, no. 3, pp. 651–657, 1994. View at Google Scholar · View at Scopus
  19. V. Rocha-Ramírez, C. Omero, I. Chet, B. A. Horwitz, and A. Herrera-Estrella, “Trichoderma atroviride G-protein α-subunit gene tga1 is involved in mycoparasitic coiling and conidiation,” Eukaryotic Cell, vol. 1, no. 4, pp. 594–605, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. P. K. Mukherjee, J. Latha, R. Hadar, and B. A. Horwitz, “Role of two G-protein alpha subunits, TgaA and TgaB, in the antagonism of plant pathogens by Trichoderma virens,” Applied and Environmental Microbiology, vol. 70, no. 1, pp. 542–549, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Reithner, K. Brunner, R. Schuhmacher et al., “The G protein α subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites,” Fungal Genetics and Biology, vol. 42, no. 9, pp. 749–760, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. S. Zeilinger, B. Reithner, V. Scala, I. Peissl, M. Lorito, and R. L. Mach, “Signal transduction by Tga3, a novel G protein α subunit of Trichoderma atroviride,” Applied and Environmental Microbiology, vol. 71, no. 3, pp. 1591–1597, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. R. do Nascimento Silva, A. S. Steindorff, C. J. Ulhoa, and C. R. Félix, “Involvement of G-alpha protein GNA3 in production of cell wall-degrading enzymes by Trichoderma reesei (Hypocrea jecorina) during mycoparasitism against Pythium ultimum,” Biotechnology Letters, vol. 31, no. 4, pp. 531–536, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. L. Li, S. J. Wright, S. Krystofova, G. Park, and K. A. Borkovich, “Heterotrimeric G protein signaling in filamentous fungi,” Annual Review of Microbiology, vol. 61, pp. 423–452, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. J. E. Buss, S. M. Mumby, P. J. Casey, A. G. Gilman, and B. M. Sefton, “Myristoylated alpha subunits of guanine nucleotide-binding regulatory proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 21, pp. 7493–7497, 1987. View at Google Scholar · View at Scopus
  26. R. E. West Jr., J. Moss, M. Vaughan, T. Liu, and T. Y. Liu, “Pertussis toxin-catalyzed ADP-ribosylation of transducin. Cysteine 347 is the ADP-ribose acceptor site,” The Journal of Biological Chemistry, vol. 260, no. 27, pp. 14428–14430, 1985. View at Google Scholar
  27. G. E. Turner and K. A. Borkovich, “Identification of a G protein α subunit from Neurospora crassa that is a member of the G(i) family,” Journal of Biological Chemistry, vol. 268, no. 20, pp. 14805–14811, 1993. View at Google Scholar · View at Scopus
  28. A. M. Kays and K. A. Borkovich, “Severe impairment of growth and differentiation in a Neurospora crassa mutant lacking all heterotrimeric Gα proteins,” Genetics, vol. 166, no. 3, pp. 1229–1240, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. M. C. Lorenz and J. Heitman, “Yeast pseudohyphal growth is regulated by GPA2, a G protein α homolog,” EMBO Journal, vol. 16, no. 23, pp. 7008–7018, 1997. View at Google Scholar · View at Scopus
  30. E. Regenfelder, T. Spellig, A. Hartmann, S. Lauenstein, M. Bölker, and R. Kahmann, “G proteins in Ustilago maydis: transmission of multiple signals?” EMBO Journal, vol. 16, no. 8, pp. 1934–1942, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. A. Lafon, K.-H. Han, J.-A. Seo, J.-H. Yu, and C. d'Enfert, “G-protein and cAMP-mediated signaling in aspergilli: a genomic perspective,” Fungal Genetics and Biology, vol. 43, no. 7, pp. 490–502, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. S. Krystofova and K. A. Borkovich, “The heterotrimeric G-protein subunits GNG-1 and GNB-1 form a Gβγ dimer required for normal female fertility, asexual development, and Gα protein levels in Neurospora crassa,” Eukaryotic Cell, vol. 4, no. 2, pp. 365–378, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. Q. Yang, S. I. Poole, and K. A. Borkovich, “A G-protein β subunit required for sexual and vegetative development and maintenance of normal Gα protein levels in Neurospora crassa,” Eukaryotic Cell, vol. 1, no. 3, pp. 378–390, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Versele, K. Lemaire, and J. M. Thevelein, “Sex and sugar in yeast: two distinct GPCR systems,” EMBO Reports, vol. 2, no. 7, pp. 574–579, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. K. A. Borkovich, L. A. Alex, O. Yarden et al., “Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism,” Microbiology and Molecular Biology Reviews, vol. 68, no. 1, pp. 1–108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. R. D. Kulkarni, M. R. Thon, H. Pan, and R. A. Dean, “Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea,” Genome Biology, vol. 6, no. 3, article R24, 2005. View at Google Scholar
  37. T. M. DeZwaan, A. M. Carroll, B. Valent, and J. A. Sweigard, “Magnaporthe grisea Pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues,” Plant Cell, vol. 11, no. 10, pp. 2013–2030, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Zheng, L. Zhou, T. Dou et al., “Genome-wide prediction of G protein-coupled receptors in Verticillium spp,” Fungal Biology, vol. 114, no. 4, pp. 359–368, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. E. M. Ross and T. M. Wilkie, “GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins,” Annual Review of Biochemistry, vol. 69, pp. 795–827, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. M. Sato, J. B. Blumer, V. Simon, and S. M. Lanier, “Accessory proteins for G proteins: partners in signaling,” Annual Review of Pharmacology and Toxicology, vol. 46, pp. 151–187, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. N. A. Lambert, C. A. Johnston, S. D. Cappell et al., “Regulators of G-protein signaling accelerate GPCR signaling kinetics and govern sensitivity solely by accelerating GTPase activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 15, pp. 7066–7071, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. D. R. Ballon, P. L. Flanary, D. P. Gladue, J. B. Konopka, H. G. Dohlman, and J. Thorner, “DEP-domain-mediated regulation of GPCR signaling responses,” Cell, vol. 126, no. 6, pp. 1079–1093, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. M. Versele, J. H. de Winde, and J. M. Thevelein, “A novel regulator of G protein signalling in yeast, Rgs2, downregulates glucose-activation of the cAMP pathway through direct inhibition of Gpa2,” EMBO Journal, vol. 18, no. 20, pp. 5577–5591, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. J.-H. Yu, J. Wieser, and T. H. Adams, “The Aspergillus FlbA RGS domain protein antagonizes G protein signaling to block proliferation and allow development,” EMBO Journal, vol. 15, no. 19, pp. 5184–5190, 1996. View at Google Scholar · View at Scopus
  45. K.-H. Han, J.-A. Seo, and J.-H. Yu, “A putative G protein-coupled receptor negatively controls sexual development in Aspergillus nidulans,” Molecular Microbiology, vol. 51, no. 5, pp. 1333–1345, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. W. Fang, Y. Pei, and M. J. Bidochka, “A regulator of a G protein signalling (RGS) gene, cag8, from the insect-pathogenic fungus Metarhizium anisopliae is involved in conidiation virulence and hydrophobin synthesis,” Microbiology, vol. 153, no. 4, pp. 1017–1025, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. H. Liu, A. Suresh, F. S. Willard, D. P. Siderovski, S. Lu, and N. I. Naqvi, “Rgs1 regulates multiple Gα subunits in Magnaporthe pathogenesis, asexual growth and thigmotropism,” EMBO Journal, vol. 26, no. 3, pp. 690–700, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. G. C. Segers, J. C. Regier, and D. L. Nuss, “Evidence for a role of the regulator of G-protein signaling protein CPRGS-1 in Gα subunit CPG-1-mediated regulation of fungal virulence, conidiation, and hydrophobin synthesis in the chestnut blight fungus Cryphonectria parasitica,” Eukaryotic Cell, vol. 3, no. 6, pp. 1454–1463, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. P. Wang, J. Cutler, J. King, and D. Palmer, “Mutation of the regulator of G protein signaling Crg1 increases virulence in Cryptococcus neoformans,” Eukaryotic Cell, vol. 3, no. 4, pp. 1028–1035, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. C. Xue, Y.-P. Hsueh, L. Chen, and J. Heitman, “The RGS protein Crg2 regulates both pheromone and cAMP signalling in Cryptococcus neoformans,” Molecular Microbiology, vol. 70, no. 2, pp. 379–395, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. S. Kasahara, P. Wang, and D. L. Nuss, “Identification of bdm-1, a gene involved in G protein β-subunit function and α-subunit accumulation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 1, pp. 412–417, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. J.-A. Seo and J.-H. Yu, “The phosducin-like protein PhnA is required for Gβγ-mediated signaling for vegetative growth, developmental control, and toxin biosynthesis in Aspergillus nidulans,” Eukaryotic Cell, vol. 5, no. 2, pp. 400–410, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. J. A. Salamon, R. Acuña, and A. L. Dawe, “Phosphorylation of phosducin-like protein BDM-1 by protein kinase 2 (CK2) is required for virulence and Gβ subunit stability in the fungal plant pathogen Cryphonectria parasitica,” Molecular Microbiology, vol. 76, no. 4, pp. 848–860, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. M. C. Overton and K. J. Blumer, “G-protein-coupled receptors function as oligomers in vivo,” Current Biology, vol. 10, no. 6, pp. 341–344, 2000. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Shi, M. F. Paige, J. Maley, and M. C. Loewen, “In vitro characterization of ligand-induced oligomerization of the S. cerevisiae G-protein coupled receptor, Ste2p,” Biochimica et Biophysica Acta, vol. 1790, no. 1, pp. 1–7, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. K. A. Schandel and D. D. Jenness, “Direct evidence for ligand-induced internalization of the yeast α-factor pheromone receptor,” Molecular and Cellular Biology, vol. 14, no. 11, pp. 7245–7255, 1994. View at Google Scholar · View at Scopus
  57. L. Chen and N. G. Davis, “Recycling of the yeast a-factor receptor,” Journal of Cell Biology, vol. 151, no. 3, pp. 731–738, 2000. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Davis, P. Dube, and J. B. Konopka, “Afr1p regulates the Saccharomyces cerevisiae α-factor receptor by a mechanism that is distinct from receptor phosphorylation and endocytosis,” Genetics, vol. 148, no. 2, pp. 625–635, 1998. View at Google Scholar · View at Scopus
  59. D. M. Rivers and G. F. Sprague Jr., “Autocrine activation of the pheromone response pathway in matα2—cells is attenuated by SST2- and ASG7-dependent mechanisms,” Molecular Genetics and Genomics, vol. 270, no. 3, pp. 225–233, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. N. Stoppacher, B. Reithner, M. Omann, S. Zeilinger, R. Krska, and R. Schuhmacher, “Profiling of trichorzianines in culture samples of Trichoderma atroviride by liquid chromatography/tandem mass spectrometry,” Rapid Communications in Mass Spectrometry, vol. 21, no. 24, pp. 3963–3970, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. M. Schmoll, A. Schuster, R. D. N. Silva, and C. P. Kubicek, “The G-alpha protein GNA3 of Hypocrea jecorina (anamorph Trichoderma reesei) regulates cellulase gene expression in the presence of light,” Eukaryotic Cell, vol. 8, no. 3, pp. 410–420, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. M. Komon-Zelazowska, T. Neuhof, R. Dieckmann et al., “Formation of atroviridin by Hypocrea atroviridis is conidiation associated and positively regulated by blue light and the G protein GNA3,” Eukaryotic Cell, vol. 6, no. 12, pp. 2332–2342, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. B. Reithner, R. Schuhmacher, N. Stoppacher, M. Pucher, K. Brunner, and S. Zeilinger, “Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk1 differentially affects mycoparasitism and plant protection,” Fungal Genetics and Biology, vol. 44, no. 11, pp. 1123–1133, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. K. Brunner, M. Omann, M. E. Pucher et al., “Trichoderma G protein-coupled receptors: functional characterisation of a cAMP receptor-like protein from Trichoderma atroviride,” Current Genetics, vol. 54, no. 6, pp. 283–299, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. M. Omann, S. Lehner, K. Brunner et al., “A cAMP receptor-like GPCR is involved in Trichoderma atroviride mycoparasitism,” in IOBC/WPRS Bulletin, pp. 105–108, IOBC/WPRS, 2009. View at Google Scholar