Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction

Plant Cell

Volumn 18, Issue 4, 2006, Pages 1052-1066

  Tanaka, Aiko ^a   Christensen, Michael J ^b   Takemoto, Daigo ^a   Park, Pyoyun ^c   Scott, Barry ^a  

^a MASSEY UNIVERSITY   (New Zealand)

^b AGRESEARCH GRASSLANDS   (New Zealand)

^c KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; OXYGEN; PATHOLOGY; PLANTS (BOTANY);

CLAVICIPITACEOUS FUNGAL ENDOPHYTE; EPICHLOE FESTUCAE; FUNGAL BIOMASSES; PERENNIAL RYEGRASS;

MUTAGENESIS;

FUNGI; MUTAGENS; OXYGEN; PATHOLOGY; PLANTS;

EPICHLOE FESTUCAE; FUNGI; LOLIUM PERENNE;

EID: 33745443572     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.039263     Document Type: Article

References (80)

1. Aguirre, J., Ríos-Momberg, M., Hewitt, D., and Hansberg, W. (2005). Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 13, 111-118.
2. Akiyama, K., Matsuzaki, K., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824-827.
3. Arnold, A.E., Mejia, L.C., Kyllo, D., Rojas, E.I., Maynard, Z., Robbins, N., and Herre, E.A. (2003). Fungal endophytes limit pathogen damage in a tropical tree. Proc. Natl. Acad. Sci. USA 100, 15649-15654.
4. Barelle, C.J., Bohula, E.A., Kron, S.J., Wessels, D., Soll, D.R., Schäfer, A., Brown, A.J., and Gow, N.A.R. (2003). Asynchronous cell cycle and asymmetric vacuolar inheritance in true hyphae of Candida albicans. Eukaryot. Cell 2, 398-410.
5. Bennett, J.W., and Lasure, L.L. (1985). Conventions for gene symbols. In Gene Manipulation in Fungi, J.W. Bennett and L.L. Lasure, eds (London: Academic Press), pp. 537-544.
6. Bestwick, C.S., Brown, I.R., Bennett, M.H., and 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.
7. Boyce, K.J., Hynes, M.J., and Andrianopoulos, A. (2003). Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog. J. Cell Sci. 116, 1249-1260.
8. Briggs, R.T., Drath, D.B., Karnovsky, M.L., and 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. Bush, L.P., Wilkinson, H.H., and Schardl, C.L. (1997). Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol. 114, 1-7.
10. Byrd, A.D., Schardl, C.L., Songlin, P.J., Mogen, K.L., and Siegel, M.R. (1990). The β-tubulin gene of Epichloe typhina from perennial ryegrass (Lolium perenne). Curr. Genet. 18, 347-354.
11. Carroll, A.M., Sweigard, J.A., and Valent, B. (1994). Improved vectors for selecting resistance to hygromycin. Fungal Genet. Newsl. 41, 22.
12. Chen, C., and 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.
13. phox. J. Biol. Chem. 279, 34250-34255.
14. Christensen, M.J. (1995). Variation in the ability of Acremonium endophytes of Lolium perenne, Festuca arundinacea and F. pratensis to form compatible associations in the three grasses. Mycol. Res. 99, 466-470.
15. Christensen, M.J., Ball, O.J.-P., Bennett, R.J., and Schardl, C.L. (1997). Fungal and host genotype effects on compatibility and vascular colonization by Epichloe festucae. Mycol. Res. 101, 493-501.
16. Christensen, M.J., Bennett, R.J., and Schmid, J. (2002). Growth of Epichloe/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycol. Res. 106, 93-106.
17. Clay, K. (2004). Fungi and the food of the gods. Nature 427, 401-402.
18. Clay, K., and Schardl, C. (2002). Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Nat. 160 (suppl.), S99-S127.
19. DeLeo, F.R., Yu, L., Burritt, J.B., Loetterle, L.R., Bond, C.W., Jesaitis, A.J., and Quinn, M.T. (1995). Mapping sites of interaction of p47-phox and flavocytochrome b with random-sequence peptide phage display libraries. Proc. Natl. Acad. Sci. USA 92, 7110-7114.
20. Doke, N. (1983). Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol. Plant Pathol. 23, 345-357.
21. - generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophthora infestans. Physiol. Plant Pathol. 27, 311-322.
22. Finegold, A.A., Shatwell, K.P., Segal, A.W., Klausner, R.D., and Dancis, A. (1996). Intramembrane bis-heme motif for transmembrane electron transport conserved in a yeast iron reductase and the human NADPH oxidase. J. Biol. Chem. 271, 31021-31024.
23. Foreman, J., Demidchik, V., Bothwell, J.H.F., Mylona, P., Miedema, H., Torres, M.A., Linstead, P., Costa, S., Brownlee, C., Jones, J.D.G., Davies, J.M., and Dolan, L. (2003). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442-446.
24. Grove, S.N., Bracker, C.E., and Morre, D.J. (1970). An ultrastructural basis for hyphal tip growth in Pythium ultimum. Am. J. Bot. 57, 245-266.
25. Harper, A.M., Chaplin, M.F., and Segal, A.W. (1985). Cytochrome b-245 from human neutrophils is a glycoprotein. Biochem. J. 227, 783-788.
26. Itoh, Y., Johnson, R., and Scott, B. (1994). Integrative transformation of the mycotoxin-producing fungus, Penicillium paxilli. Curr. Genet. 25, 508-513.
27. Karandashov, V., and Bucher, M. (2005). Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci. 10, 22-29.
28. Kawasaki, T., Henmi, K., Ono, E., Hatakeyama, S., Iwano, M., Satoh, H., and Shimamoto, K. (1999). The small GTP-binding protein Rac is a regulator of cell death in plants. Proc. Natl. Acad. Sci. USA 96, 10922-10926.
29. Koch, E., and Slusarenko, A. (1990). Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2, 437-445.
30. Koga, E., Christensen, M.J., and Bennett, R.J. (1993). Incompatibility of some grass/Acremonium endophyte associations. Mycol. Res. 97, 1237-1244.
31. Kornfeld, R., and Kornfeld, S. (1985). Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54, 631-664.
32. Kwak, J.M., Mori, I.C., Pei, Z.-M., Leonhardt, N., Torres, M.A., Dangl, J.L., Bloom, R.E., Bodde, S., Jones, J.D.G., and Schroeder, J.I. (2003). NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623-2633.
33. Lalucque, H., and Silar, P. (2003). NADPH oxidase: An enzyme for multicellularity? Trends Microbiol. 11, 9-12.
34. Lamb, C., and Dixon, R.A. (1997). The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
35. Lambeth, J.D. (2004). NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189.
36. Lambeth, J.D., Cheng, G., Arnold, R.S., and Edens, W.A. (2000). Novel homologs of gp91phox. Trends Biochem. Sci. 25, 459-461.
37. Lane, G.A., Christensen, M.J., and Miles, C.O. (2000). Coevolution of fungal endophytes with grasses: The significance of secondary metabolites. In Microbial Endophytes, C.W. Bacon and J.F.J. White, eds (New York: Marcel Dekker), pp. 341-388.
38. Lara-Ortiz, T., Riveros-Rosas, H., and Aguirre, J. (2003). Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol. Microbiol. 50, 1241-1255.
39. Latch, G.C.M., and Christensen, M.J. (1985). Artificial infection of grasses with endophytes. Ann. Appl. Biol. 107, 17-24.
40. Leuchtmann, A., Schardl, C.L., and Siegel, M.R. (1994). Sexual compatibility and taxonomy of a new species of Epichloe symbiotic with fine fescue grasses. Mycologia 86, 802-812.
41. Lodwig, E., and Poole, A. (2003). Metabolism of Rhizobium bacteroids. CRC Crit. Rev. Plant Sci. 22, 37-78.
42. Malagnac, F., Lalucque, H., Lepère, G., and Silar, P. (2004). Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet. Biol. 41, 982-997.
43. Moon, C.D., Scott, B., Schardl, C.L., and Christensen, M.J. (2000). The evolutionary origins of Epichloe endophytes from annual rye-grasses. Mycologia 92, 1103-1118.
44. Moon, C.D., Tapper, B.A., and Scott, B. (1999). Identification of Epichloe endophytes in planta by a microsatellite-based PCR fingerprinting assay with automated analysis. Appl. Environ. Microbiol. 65, 1268-1279.
45. Munkres, K.D. (1990). Histochemical detection of superoxide radicals and hydrogen peroxide by Age-1 mutants of Neurospora. Fungal Genet. Newsl. 37, 24-25.
46. Namiki, F., Matsunaga, M., Okuda, M., Inoue, I., Nishi, K., Fujita, Y., and Tsuge, T. (2001). Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol. Plant Microbe Interact. 14, 580-584.
47. Oldroyd, G.E., and Downie, J.A. (2004). Calcium, kinases and nodulation signalling in legumes. Nat. Rev. Mol. Cell Biol. 5, 566-576.
48. Panaccione, D.G., Johnson, R.D., Wang, J., Young, C.A., Damrongkool, P., Scott, B., and Schardl, C.L. (2001). Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proc. Natl. Acad. Sci. USA 98, 12820-12825.
49. Parniske, M. (2004). Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 7, 414-421.
50. Punt, P.J., Oliver, R.P., Dingemanse, M.A., Pouwels, P.H., and van den Hondel, C.A.M.J.J. (1987). Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56, 117-124.
51. Royer-Pokora, B., Kunkel, L.M., Monaco, A.P., Goff, S.C., Newburger, P.E., Baehner, R.L., Cole, F.S., Curnutte, J.T., and Orkin, S.H. (1986). Cloning the gene for an inherited human disorder-chronic granulomatous disease-on the basis of its chromosomal location. Nature 322, 32-38.
52. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
53. Sánchez, O., Navarro, R.E., and Aguirre, J. (1998). Increased transformation frequency and tagging of developmental genes in Aspergillus nidulans by restriction enzyme-mediated integration (REMI). Mol. Gen. Genet. 258, 89-94.
54. Sanderson, K.E., and Srb, A.M. (1965). Heterokaryosis and parasexuality in the fungus Ascochta imperfecta. Am. J. Bot. 52, 72-81.
55. Schardl, C.L. (2001). Epichloe festucae and related mutualistic symbionts of grasses. Fungal Genet. Biol. 33, 69-82.
56. Schardl, C.L., Leuchtmann, A., and Spiering, M.J. (2004). Symbioses of grasses with seedborne fungal endophytes. Annu. Rev. Plant Biol. 55, 315-340.
57. Schiestl, R.H., and Petes, T.D. (1991). Integration of DNA fragments by illegitimate recombination in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 88, 7585-7589.
58. Scott, B. (2001). Epichloe endophytes: Symbionts of grasses. Curr. Opin. Microbiol. 4, 393-398.
59. Shimizu-Sato, S., and Mori, H. (2001). Control of outgrowth and dormancy in axillary buds. Plant Physiol. 127, 1405-1413.
60. Shinogi, T., Suzuki, T., Kurihara, T., Narusaka, Y., and Park, P. (2003). Microscopic detection of reactive oxygen species generation in the compatible and incompatible interactions of Alternaria alternate Japanese pear pathotype and host plants. J. Gen. Plant Pathol. 69, 7-16.
61. Shinogi, T., Suzuki, T., Tagashira, M., Yamane, K., Yao, N., Uwo, M., Kawakami, S., Narusaka, Y., and Park, P. (2001). A low viscosity epoxy resin "Quetol-651" as a substitute of Spurr's resin for hard biological materials in transmission electron microscopy. J. Electr. Microsc. Technol. Med. Biol. 16, 1-10.
62. Simon-Plas, F., Elmayan, T., and Blein, J.-P. (2002). The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J. 31, 137-147.
63. Spiering, M.J., Moon, C.D., Wilkinson, H.H., and Schardl, C.L. (2005). Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum. Genetics 169, 1403-1414.
64. Spiering, M.J., Wilkinson, H.H., Blankenship, J.D., and Schardl, C.L. (2002). Expressed sequence tags and genes associated with loline alkaloid expression by the fungal endophyte Neotyphodium uncinatum. Fungal Genet. Biol. 36, 242-254.
65. Spiers, A.G., and Hopcroft, D.H. (1993). Black canker and leaf spot of Salix in New Zealand caused by Glomerella miyabeana (Colletotrichum gloeosporioldes). Eur. J. For. Pathol. 23, 92-102.
66. Suh, Y.-A., Arnold, R.S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., Chung, A.B., Griendling, K.K., and Lambeth, J.D. (1999). Cell transformation by the superoxide-generating oxidase Mox1. Nature 401, 79-82.
67. Taiz, L., and Zeiger, E. (1998). Plant Physiology. (Sunderland, MA: Sinauer Associates).
68. Tan, Y.Y., Spiering, M.J., Scott, V., Lane, G.A., Christensen, M.J., and 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.
69. Tanaka, A., Tapper, B.A., Popay, A., Parker, E.J., and 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.
70. Torres, M.A., Dangl, J.L., and Jones, J.D.G, (2002). Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99, 517-522.
71. Torres, M.A., Jones, J.D.G., and Dangl, J.L. (2005). Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 37, 1130-1134.
72. Torres, M.A., Onouchi, H., Hamada, S., Machida, C., Hammond-Kosack, K.E., and Jones, J.D.G. (1998). Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp97phox). Plant J. 14, 365-370.
73. Vignais, P.V. (2002). The superoxide-generating NADPH oxidase: Structural aspects and activation mechanism. CMLS Cell. Mol. Life Sci. 59, 1428-1459.
74. Wallach, T.M., and Segal, A.W. (1997). Analysis of glycosylation sites on gp91phox, the flavocytochrome of the NADPH oxidase, by site-directed mutagenesis and translation in vitro. Biochem. J. 321, 583-585.
75. Wang, J., Machado, C., Panaccione, D.G., Tsai, H.-F., and Schardl, C.L. (2004). The determinant step in ergot alkaloid biosynthesis by an endophyte of perennial ryegrass. Fungal Genet. Biol. 41, 189-198.
76. Weinzierl, G., Leveleki, L., Hassel, A., Kost, G., Wanner, G., and Bolker, M. (2002). Regulation of cell separation in the dimorphic fungus Ustilago maydis. Mol. Microbiol. 45, 219-231.
77. Wu, R., Hirai, A., Mundy, J., Nelson, R., and Rodriguez, R. (1991). Guidelines for nomenclature of cloned genes or DNA fragments in rice. Rice Genet. Newsl. 8, 51-53.
78. 2 accumulation and resistance to Phytophthora infestans. Plant Cell 15, 706-718.
79. Young, C., Itoh, Y., Johnson, R., Garthwaite, I., Miles, C.O., Munday-Finch, S.C., and Scott, B. (1998). Paxilline-negative mutants of Penicillium paxilli generated by heterologous and homologous plasmid integration. Curr. Genet. 33, 368-377.
80. Young, C.A., Bryant, M.K., Christensen, M.J., Tapper, B.A., Bryan, G.T., and 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. Genet. Genomics 274, 13-29.