NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloë festucae and perennial ryegrass

Molecular Microbiology

Volumn 68, Issue 5, 2008, Pages 1165-1178

  Tanaka, Aiko ^a,c   Takemoto, Daigo ^a,c   Hyon, Gang Su ^b   Park, Pyoyun ^b   Scott, Barry ^a  

^a MASSEY UNIVERSITY   (New Zealand)

^b KOBE UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PROTEIN NOXA; PROTEIN RACA; RAC PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ALLELE; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENDOPHYTE; ENZYME ACTIVATION; EPICHLOE FESTUCAE; FUNGAL COLONIZATION; FUNGAL STRAIN; FUNGUS GROWTH; FUNGUS HYPHAE; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PERENNIAL RYEGRASS; PRIORITY JOURNAL; REGULATORY MECHANISM; SENESCENCE; SYMBIOSIS;

ASCOMYCOTA; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; LOLIUM; MOLECULAR SEQUENCE DATA; MONOMERIC GTP-BINDING PROTEINS; NADPH OXIDASE; PLANT DISEASES; RAC GTP-BINDING PROTEINS; REACTIVE OXYGEN SPECIES; SYMBIOSIS;

EPICHLOE FESTUCAE; FUNGI; LOLIUM PERENNE; MAMMALIA;

EID: 43449132091     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06217.x     Document Type: Article

References (46)

1. Aguirre, J., Rios-Momberg, M., Hewitt, D. Hansberg, W. (2005) Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol 13 : 111 118.
2. Bedard, K. Krause, K.H. (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87 : 245 313.
3. Bestwick, C.S., Brown, I.R., Bennett, M.H. Mansfield, J.W. (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9 : 209 221.
4. Bourne, H.R., Sanders, D.A. McCormick, F. (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349 : 117 127.
5. Boyce, K.J., Hynes, M.J. Andrianopoulos, A. (2001) The CDC42 homologue of the dimorphic fungus Penicillium marneffei is required for correct cell polarization during growth but not development. J Bacteriol 183 : 3447 3457.
6. Boyce, K.J., Hynes, M.J. Andrianopoulos, A. (2003) Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog. J Cell Sci 116 : 1249 1260.
7. Boyce, K.J., Hynes, M.J. Andrianopoulos, A. (2005) The Ras and Rho GTPases genetically interact to co-ordinately regulate cell polarity during development in Penicillium marneffei. Mol Microbiol 55 : 1487 1501.
8. Briggs, R.T., Drath, D.B., Karnovsky, M.L. Karnovsky, M.J. (1975) Localization of NADH oxidase on the surface of human polymorphonuclear leukocytes by a new cytochemical method. J Cell Biol 67 : 566 586.
9. Byrd, A.D., Schardl, C.L., Songlin, P.J., Mogen, K.L. Siegel, M.R. (1990) The β-tubulin gene of Epichloë typhina from perennial ryegrass (Lolium perenne). Curr Genet 18 : 347 354.
10. Chen, C. Dickman, M.B. (2004) Dominant active Rac and dominant negative Rac revert the dominant active Ras phenotype in Colletotrichum trifolii by distinct signalling pathways. Mol Microbiol 51 : 1493 1507.
11. Chen, C., Ha, Y.S., Min, J.Y., Memmott, S.D. Dickman, M.B. (2006) Cdc42 is required for proper growth and development in the fungal pathogen Colletotrichum trifolii. Eukaryot Cell 5 : 155 166.
12. Christensen, M.J., Bennett, R.J. Schmid, J. (2002) Growth of Epichloë/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycol Res 106 : 93 106.
13. Christensen, M.J., Bennett, R.J., Ansari, H.A., Koga, H., Johnson, R.D., Bryan, G.T., et al. (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45 : 84 93.
14. DerMardirossian, C. Bokoch, G.M. (2005) GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol 15 : 356 363.
15. Diebold, B.A. Bokoch, G.M. (2001) Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nature Immunol 2 : 211 215.
16. Hurtado, C.A., Beckerich, J.M., Gaillardin, C. Rachubinski, R.A. (2000) A Rac homolog is required for induction of hyphal growth in the dimorphic yeast Yarrowia lipolytica. J Bacteriol 182 : 2376 2386.
17. Itoh, Y., Johnson, R. Scott, B. (1994) Integrative transformation of the mycotoxin-producing fungus, Penicillium paxilli. Curr Genet 25 : 508 513.
18. Johnson, D.I. (1999) Cdc42: an essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol Mol Biol Rev 63 : 54 105.
19. Lambeth, J.D. (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4 : 181 189.
20. phox in complex with Rac.GTP. Mol Cell 6 : 899 907.
21. Latch, G.C.M. Christensen, M.J. (1985) Artificial infection of grasses with endophytes. Ann Appl Biol 107 : 17 24.
22. Mahlert, M., Leveleki, L., Hlubek, A., Sandrock, B. Bölker, M. (2006) Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Mol Microbiol 59 : 567 578.
23. Moon, C.D., Tapper, B.A. Scott, B. (1999) Identification of Epichloë endophytes in planta by a microsatellite-based PCR fingerprinting assay with automated analysis. Appl Env Microbiol 65 : 1268 1279.
24. Moon, C.D., Scott, B., Schardl, C.L. Christensen, M.J. (2000) The evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 92 : 1103 1118.
25. Munkres, K.D. (1990) Histochemical detection of superoxide radicals and hydrogen peroxide by Age-1 mutants of Neurospora. Fungal Genet Newsl 37 : 24 25.
26. Paduch, M., Jelen, F. Otlewski, J. (2001) Structure of small G proteins and their regulators. Acta Biochim Pol 48 : 829 850.
27. Park, H.O. Bi, E. (2007) Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol Mol Biol Rev 71 : 48 96.
28. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
29. Sanderson, K.E. Srb, A.M. (1965) Heterokaryosis and parasexuality in the fungus Ascochta imperfecta. Am J Bot 52 : 72 81.
30. Scott, B., Takemoto, D. Tanaka, A. (2007) Fungal endophyte production of reactive oxygen species is critical for maintaining the mutualistic symbiotic interaction between Epichloë festucae and perennial ryegrass. Plant Signal Behav 2 : 170 172.
31. Shinogi, T., Suzuki, T., Tagashira, M., Yamane, K., Yao, N., Uwo, M., et al. (2001) A low viscosity epoxy resin 'Quetol-651' as a substitute of Spurr's resin for hard biological materials in transmission electron microscopy. J Electron Microsc Technol Med Biol 16 : 1 10.
32. Shinogi, T., Suzuki, T., Kurihara, T., Narusaka, Y. Park, P. (2003) Microscopic detection of reactive oxygen species generation in the compatible and incompatible interactions of Alternaria alternata Japanese pear pathotype and host plants. J Gen Plant Pathol 69 : 7 16.
33. Spiers, A.G. Hopcroft, D.H. (1993) Black canker and leaf spot of Salix in New Zealand caused by Glomerella miyabeana (Colletotrichum gloeosporioides). Eur J For Pathol 23 : 92 102.
34. Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18 : 2807 2821.
35. Takemoto, D., Tanaka, A. Scott, B. (2007) NADPH oxidases in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet Biol 44 : 1065 1076.
36. Tan, Y.Y., Spiering, M.J., Scott, V., Lane, G.A., Christensen, M.J. Schmid, J. (2001) In planta regulation of extension of an endophytic fungus and maintenance of high metabolic rates in its mycelium in the absence of apical extension. Appl Environ Microbiol 67 : 5377 5383.
37. Tanaka, A., Tapper, B.A., Popay, A., Parker, E.J. Scott, B. (2005) A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 57 : 1036 1050.
38. Tanaka, A., Christensen, M.J., Takemoto, D., Park, P. Scott, B. (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic association. Plant Cell 18 : 1052 1066.
39. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for mulitple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24 : 4876 4882.
40. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11 : 1187 1194.
41. Torres, M.A. Dangl, J.L. (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8 : 397 403.
42. Vallim, M.A., Nichols, C.B., Fernandes, L., Cramer, K.L. Alspaugh, J.A. (2005) A Rac homolog functions downstream of Ras1 to control hyphal differentiation and high-temperature growth in the pathogenic fungus Cryptococcus neoformans. Eukaryot Cell 4 : 1066 1078.
43. Virag, A., Lee, M.P., Si, H. Harris, S.D. (2007) Regulation of hyphal morphogenesis by cdc42 and rac1 homologues in Aspergillus nidulans. Mol Microbiol 66 : 1579 1596.
44. Yamaguchi, Y., Ota, K. Ito, T. (2007) A novel Cdc42-interacting domain of the yeast polarity establishment protein Bem1. Implications for modulation of mating pheromone signaling. J Biol Chem 282 : 29 38.
45. Young, C., Itoh, Y., Johnson, R., Garthwaite, I., Miles, C.O., Munday-Finch, S.C. Scott, B. (1998) Paxilline-negative mutants of Penicillium paxilli generated by heterologous and homologous plasmid integration. Curr Genet 33 : 368 377.
46. Young, C.A., Bryant, M.K., Christensen, M.J., Tapper, B.A., Bryan, G.T. Scott, B. (2005) Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Mol Gen Genomics 274 : 13 29.