An Extracellular Siderophore Is Required to Maintain the Mutualistic Interaction of Epichloë festucae with Lolium perenne

PLoS Pathogens

Volumn 9, Issue 5, 2013, Pages

  Johnson, Linda J ^a   Koulman, Albert ^b   Christensen, Michael ^a   Lane, Geoffrey A ^a   Fraser, Karl ^a   Forester, Natasha ^a   Johnson, Richard D ^a   Bryan, Gregory T ^a   Rasmussen, Susanne ^a  

^a AGRESEARCH GRASSLANDS   (New Zealand)

^b MRC HUMAN NUTRITION RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPICHLOENIN A; NONRIBOSOMAL PEPTIDE SYNTHETASE; SIDEROPHORE; UNCLASSIFIED DRUG;

AGRICULTURAL INOCULATION; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; EPICHLOE; FUNGUS HYPHAE; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOBLOTTING; MASS FRAGMENTOGRAPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PERENNIAL RYEGRASS; PLANT GROWTH; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; SPOROGENESIS; SYMBIOSIS; TRANSMISSION ELECTRON MICROSCOPY;

EPICHLOE; GENE DELETION; GENES, FUNGAL; IRON; LOLIUM; SIDEROPHORES; SYMBIOSIS;

EPICHLOE FESTUCAE; FUNGI; LOLIUM PERENNE;

EID: 84878480334     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003332     Document Type: Article

References (104)

1. Guerinot ML, (1994) Microbial iron transport. Annual Review of Microbiology 48: 743-772.
2. Beard JL, Dawson H, Pinero DJ, (1996) Iron metabolism: a comprehensive review. Nutrition Reviews 54: 295-317.
3. Curie C, Briat JF, (2003) Iron transport and signaling in plants. Annual Review of Plant Biology 54: 183-206.
4. Halliwell B, Gutteridge JMC, (1992) Biologically Relevant Metal Ion-Dependent Hydroxyl Radical Generation an Update. FEBS Letters 307: 108-112.
5. Expert D (1999) Withholding and exchanging iron: Interactions between Erwinia spp. and their plant hosts. In: Webster RK, editor. Annual Review of Phytopathology. Palo Alto, California: Annual Reviews Inc., pp. 307-334.
6. Haas H (2004) Molecular genetics of iron uptake and homeostasis in fungi. In: Brambl R, Marzluf GA, editors. The Mycota III Biochemistry and Molecular Biology. Berlin, Germany: Springer-Verlag.
7. Schaible UE, Kaufmann SHE, (2004) Iron and microbial infection. Nature Reviews: Microbiology 2: 946-953.
8. Jeong J, Guerinot ML, (2009) Homing in on iron homeostasis in plants. Trends in Plant Science 14: 280-285.
9. Clifton MC, Corrent C, Strong RK, (2009) Siderocalins: Siderophore-binding proteins of the innate immune system. Bio Metals 22: 557-564.
10. Ganz T, (2009) Iron in innate immunity: starve the invaders. Current Opinion in Immunology 21: 63-67.
11. Haas H, Eisendle M, Turgeon BG, (2008) Siderophores in fungal physiology and virulence. Annual Review of Phytopathology 46: 149-187.
12. Johnson L, (2008) Iron and siderophores in fungal-host interactions. Mycological Research 112: 170-183.
13. Hider RC, Kong X, (2010) Chemistry and biology of siderophores. Natural Product Reports 27: 637-657.
14. Eisendle M, Oberegger H, Zadra I, Haas H, (2003) The siderophore system is essential for viability of Aspergillus nidulans: functional analysis of two genes encoding l-ornithine N5-monooxygenase (sidA) and a non-ribosomal peptide synthetase (sidC). Molecular Microbiology 49: 359-375.
15. Eichhorn H, Lessing F, Winterberg B, Schirawski J, Kamper J, et al. (2006) A Ferroxidation/Permeation Iron Uptake System Is Required for Virulence in Ustilago maydis. Plant Cell 18: 3332-3345.
16. Schrettl M, Bignell E, Kragl C, Joechl C, Rogers T, et al. (2004) Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. Journal of Experimental Medicine 200: 1213-1219.
17. Hissen AHT, Wan ANC, Warwas ML, Pinto LJ, Moore MM, (2005) The Aspergillus fumigatus Siderophore Biosynthetic Gene sidA, Encoding L-Ornithine N5-Oxygenase, Is Required for Virulence. Infection and Immunity 73: 5493-5503.
18. Oide S, Krasnoff SB, Gibson DM, Turgeon BG, (2007) Intracellular siderophores are essential for ascomycete sexual development in heterothallic Cochliobolus heterostrophus and homothallic Gibberella zeae. Eukaryotic Cell 6: 1339-1353.
19. Oide S, Moeder W, Krasnoff S, Gibson D, Haas H, et al. (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: 2836-2853.
20. Hof C, Eisfeld K, Welzel K, Antelo L, Foster AJ, et al. (2007) Ferricrocin synthesis in Magnaporthe grisea and its role in pathogenicity in rice. Molecular Plant Pathology 8: 163-172.
21. Eisendle M, Schrettl M, Kragl C, Muller D, Illmer P, et al. (2006) The intracellular siderophore ferricrocin is involved in iron storage, oxidative-stress resistance, germination, and sexual development in Aspergillus nidulans. Eukaryotic Cell 5: 1596-1603.
22. Kaplan J, McVey Ward D, Crisp RJ, Philpott CC, (2006) Iron-dependent metabolic remodeling in S. cerevisiae. Biochimica et Biophysica Acta 1763: 646-651.
23. Kosman DJ, (2003) Molecular mechanisms of iron uptake in fungi. Molecular Microbiology 47: 1185-1197.
24. Askwith C, Kaplan J, (1997) An oxidase-permease-based iron transport system in Schizosaccharomyces pombe and its expression in Saccharomyces cerevisiae. Journal of Biological Chemistry 272: 401-405.
25. Greenshields DL, Liu G, Feng J, Selvaraj G, Wei Y, (2007) The siderophore biosynthetic gene SID1, but not the ferroxidase gene FET3, is required for full Fusarium graminearum virulence. Molecular Plant Pathology 8: 411-421.
26. Mei B, Budde AD, Leong SA, (1993) sid1, A gene initiating siderophore biosynthesis in Ustilago maydis: molecular characterization, regulation by iron, and role in phytopathogenicity. Proceedings of the National Academy of Sciences, USA 90: 903-907.
27. Roman DG, Dancis A, Anderson GJ, Klausner RD, Roman DG, et al. (1993) The fission yeast ferric reductase gene frp1+ is required for ferric iron uptake and encodes a protein that is homologous to the gp91-phox subunit of the human NADPH phagocyte oxidoreductase. Molecular and Cellular Biology 13: 4342-4350.
28. Schwecke T, Goettling K, Durek P, Duenas I, Kaeufer NF, et al. (2006) Nonribosomal peptide synthesis in Schizosaccharomyces pombe and the Architectures of ferrichrome-type siderophore synthetases in fungi. Chem Bio Chem 7: 612-622.
29. Hwang LH, Mayfield JA, Rine J, Sil A, (2008) Histoplasma requires SID1, a member of an iron-regulated siderophore gene cluster, for host colonization. PLoS Pathogens 4: e1000044.
30. Jung WH, Sham A, White R, Kronstad JW, (2006) Iron regulation of the major virulence factors in the AIDS-associated pathogen Cryptococcus neoformans. PLoS Biology 4: 2282-2295.
31. Ramanan N, Wang Y, (2000) A high-affinity iron permease essential for Candida albicans virulence. Science 288: 1062-1064.
32. Van Der Helm D, Winkelmann G (1994) Hydroxamates and polycarboxylates as iron transport agents (siderophores) in fungi. In: Winkelmann G, Winge DR, editors. Mycology Series; Metal ions in fungi. New York, New York: Marcel Dekker, Inc. pp. 39-98.
33. Finking R, Marahiel MA, (2004) Biosynthesis of nonribosomal peptides. Annual Review of Microbiology 58: 453-488.
34. Yuan WM, Gentil GD, Budde AD, Leong SA, (2001) Characterization of the Ustilago maydis sid2 gene, encoding a multidomain peptide synthetase in the ferrichrome biosynthetic gene cluster. Journal of Bacteriology 183: 4040-4051.
35. Winterberg B, Uhlmann S, Linne U, Lessing F, Marahiel MA, et al. (2010) Elucidation of the complete ferrichrome A biosynthetic pathway in Ustilago maydis. Molecular Microbiology 75: 1260-1271.
36. Schrettl M, Bignell E, Kragl C, Sabiha Y, Loss O, et al. (2007) Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathogens 3: 1195-1207.
37. Hof C, Eisfeld K, Antelo L, Foster AJ, Anke H, (2009) Siderophore synthesis in Magnaporthe grisea is essential for vegetative growth, conidiation and resistance to oxidative stress. Fungal Genetics and Biology 46: 321-332.
38. Haselwandter K, (1995) Mycorrhizal fungi siderophore production. Critical Reviews in Biotechnology 15: 287-291.
39. Haselwandter K, Winkelmann G, (2002) Ferricrocin-an ectomycorrhizal siderophore of Cenococcum geophilum. BioMetals 15: 73-77.
40. Haselwandter K, Passler V, Reiter S, Schmid DG, Nicholson G, et al. (2006) Basidiochrome- a novel siderophore of the orchidaceous mycorrhizal fungi Ceratobasidium and Rhizoctonia spp. Bio Metals 19: 335-343.
41. Hordt W, Romheld V, Winkelmann G, (2000) Fusarinines and dimerum acid, mono- and dihydroxamate siderophores from Penicillium chrysogenum, improve iron utilization by strategy I and strategy II plants. Bio Metals 13: 37-46.
42. Schardl CL, (2010) The epichloae, symbionts of the grass subfamily Poideae. Annals of the Missouri Botanical Garden 97: 646-665.
43. Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, et al. (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genetics and Biology 45: 84-93.
44. Schardl CL, Leuchtmann A, Spiering MJ, (2004) Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 55: 315-340.
45. Arachevaleta M, Bacon CW, Hoveland CS, Radcliffe DE, (1989) Effect of the tall fescue endophyte on plant response to environmental stress. Agronomy Journal 81: 83-90.
46. Kimmons CA, Gwinn KD, Bernard EC, (1990) Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Disease 74: 757-761.
47. Gwinn KD, Gavin AM, (1992) Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease. Plant Disease 76: 911-914.
48. Clay K, Holah J, (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285: 1742-1744.
49. Lane GA, Christensen MJ, Miles CO (2000) Chapter 14. Coevolution of fungal endophytes with grasses: the significance of secondary metabolites. In: Bacon CWW, J. F, editor. Microbial Endophytes. New York: Marcel Dekker. pp. 341-388.
50. Koulman A, Cao M, Faville M, Lane G, Mace W, et al. (2009) Semi-quantitative and structural metabolic phenotyping by direct infusion ion trap mass spectrometry and its application in genetical metabolomics. Rapid Communications in Mass Spectrometry 23: 2253-2263.
51. Johnson R, Voisey C, Johnson L, Pratt J, Fleetwood D, et al. (2007) Distribution of NRPS gene families within the Neotyphodium/Epichloe complex. Fungal Genetics and Biology 44: 1180-1190.
52. Lee TV, Johnson LJ, Johnson RD, Koulman A, Lane GA, et al. (2010) Structure of a Eukaryotic Nonribosomal Peptide Synthetase Adenylation Domain That Activates a Large Hydroxamate Amino Acid in Siderophore Biosynthesis. Journal of Biological Chemistry 285: 2415-2427.
53. Koulman A, Lee TV, Fraser K, Johnson L, Arcus V, et al. (2012) Identification of extracellular siderophores and a related peptide from the endophytic fungus Epichloë festucae in culture and endophyte-infected Lolium perenne. Phytochemistry 75: 128-139.
54. Thorstensen K, (1988) Hepatocytes and reticulocytes have different mechanisms for the uptake of iron from transferrin. Journal of Biological Chemistry 263: 16837-16841.
55. Richardson DR, Baker E, (1994) Two saturable mechanisms of iron uptake from transferrin in human melanoma cells: the effect of transferrin concentration, chelators, and metabolic probes on transferrin and iron uptake. Journal of Cellular Physiology 161: 160-168.
56. Plattner HJ, Diekmann H (1994) Enzymology of siderophore biosynthesis in fungi. In: Winkelmann G, Winge DR, editors. Metal ions in fungi. New York: Marcel Decker. pp. 99-117.
57. Bushley K, Ripoll D, Turgeon BG, (2008) Module evolution and substrate specificity of fungal nonribosomal peptide synthetases involved in siderophore biosynthesis. BMC Evolutionary Biology 8: 328.
58. Harrington BJ, Hageage GJ Jr, (1991) Calcofluor white: Tips for improving its use. Clinical Microbiology Newsletter 13: 3-5.
59. Schardl CL, Phillips TD, (1997) Protective grass endophytes: where are they from and where are they going? Plant Disease 81: 430-437.
60. Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, et al. (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytologist 173: 787-797.
61. Koulman A, Lane GA, Christensen MJ, Fraser K, Tapper BA, (2007) Peramine and other fungal alkaloids are exuded in the guttation fluid of endophyte-infected grasses. Phytochemistry 68: 355-360.
62. Rowan DD, (1993) Lolitrems, paxilline, and peramine: mycotoxins of the ryegrass/endophyte interaction. Agriculture, Ecosystems and Environment 44: 103-122.
63. Craven KD, Blankenship JD, Leuchtmann A, Hignight K, Schardl CL, (2001) Hybrid fungal endophytes symbiotic with the grass Lolium pratense. Sydowia 53: 44-73.
64. Spiering MJ, Lane GA, Christensen MJ, Schmid J, (2005) Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants. Phytochemistry 66: 195-202.
65. Malinowski DP, Zuo H, Belesky DP, Alloush GA, (2005) Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected with Neotyphodium spp. endophytes. Plant and Soil 267: 1-12.
66. Liu Q, Parsons AJ, Xue HF, Ryan GD, Newman JA, et al. (2011) Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Functional Ecology 25: 910-920.
67. Courty PE, Hoegger PJ, Kilaru S, Kohler A, Buee M, et al. (2009) Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytologist 182: 736-750.
68. Haas H, Zadra I, Stoeffler G, Angermayr K, (1999) The Aspergillus nidulans GATA factor SREA is involved in regulation of siderophore biosynthesis and control of iron uptake. Journal of Biological Chemistry pp. 19, 1999.
69. Schrettl M, Kim HS, Eisendle M, Kragl C, Nierman WC, et al. (2008) SreA-mediated iron regulation in Aspergillus fumigatus. Molecular Microbiology 70: 27-43.
70. Mercier A, Pelletier B, Labbe S, (2006) A transcription factor cascade involving Fep1 and the CCAAT-binding factor Php4 regulates gene expression in response to iron deficiency in the fission yeast Schizosaccharomyces pombe. Eukaryotic Cell 5: 1866-1881.
71. Hortschansky P, Eisendle M, Al-Abdallah Q, Schmidt AD, Bergmann S, et al. (2007) Interaction of HapX with the CCAAT-binding complex-a novel mechanism of gene regulation by iron. EMBO Journal 26: 3157-3168.
72. Schrettl M, Beckmann N, Varga J, Heinekamp T, Jacobsen ID, et al. (2010) HapX-mediated adaption to iron starvation is crucial for virulence of Aspergillus fumigatus. PLoS Pathogens 6: e1001124.
73. Hsu P-C, Yang C-Y, Lan C-Y, (2011) Candida albicans Hap43 Is a Repressor Induced under Low-Iron Conditions and Is Essential for Iron-Responsive Transcriptional Regulation and Virulence. Eukaryotic Cell 10: 207-225.
74. Takemoto D, Tanaka A, Scott B, (2006) A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18: 2807-2821.
75. Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B, (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18: 1052-1066.
76. Tanaka A, Takemoto D, Hyon GS, Park P, Scott B, (2008) NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloe festucae and perennial ryegrass. Molecular Microbiology 68: 1165-1178.
77. Takemoto D, Kamakura S, Saikia S, Becker Y, Wrenn R, et al. (2011) Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex. Proceedings of the National Academy of Sciences, USA 108: 2861-2866.
78. Howard DH, (1999) Acquisition, transport, and storage of iron by pathogenic fungi. Clinical Microbiology Reviews 12: 394-404.
79. Tan YY, Spiering MJ, Scott V, Lane GA, Christensen MJ, et al. (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. Applied and Environmental Microbiology 67: 5377-5383.
80. Lee B, Kroken S, Chou DYT, Robbertse B, Yoder OC, et al. (2005) Functional analysis of all nonribosomal peptide synthetases in Cochliobolus heterostrophus reveals a factor, NPS6, involved in virulence and resistance to oxidative stress. Eukaryotic Cell 4: 545-555.
81. Pujol-Carrion N, De La Torre-Ruiz MA, (2010) Glutaredoxins Grx4 and Grx3 of Saccharomyces cerevisiae play a role in actin dynamics through their trx domains, which contributes to oxidative stress resistance. Applied and Environmental Microbiology 76: 7826-7835.
82. Moon CD, Scott B, Schardl CL, Christensen MJ, (2000) The evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 92: 1103-1118.
83. Moon CD, Tapper BA, Scott B, (1999) Identification of Epichloë endophytes in planta by a microsatellite- based PCR fingerprinting assay with automated analysis. Applied and Environmental Microbiology 65: 1268-1279.
84. Mantle PG, Nisbet LJ, (1976) Differentiation of Claviceps purpurea in axenic culture. Journal of General Microbiology 93: 321-334.
85. Latch GCM, Christensen MJ, (1985) Artificial infection of grasses with endophytes. Annals of Applied Biology 107: 17-24.
86. Tanaka A, Tapper BA, Popay A, Parker EJ, 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. Molecular Microbiology 57: 1036-1050.
87. Gwinn KD, Collins-Shepard MH, Reddick BB, (1991) Tissue print-immunoblot, an accurate method for the detection of Acremonium coenophialum in tall fescue. Phytopathology 81: 747-748.
88. Christensen MJ, Leuchtmann A, Rowan DD, Tapper BA, (1993) Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (F. pratensis) and perennial rye-grass (Lolium perenne). Mycological Research 97: 1083-1092.
89. Tanaka A, Tapper BA, Popay A, Parker EJ, 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. Molecular Microbiology 57: 1036-1050.
90. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
91. Yoder OC, (1988) Cochliobolus heterostrophus, cause of southern leaf blight. Advances in Plant Pathology 6: 93-112.
92. Denning DW, Clemons KV, Hanson LH, Stevens DA, (1990) Restriction endonuclease analysis of total cellular DNA of Aspergillus fumigatus isolates of geographically and epidemiologically diverse origin. Journal of Infectious Diseases 162: 1151-1158.
93. Young C, Itoh Y, Johnson R, Garthwaite I, Miles CO, et al. (1998) Paxilline-negative mutants of Penicillium paxilli generated by heterologous and homologous plasmid integration. Current Genetics 33: 368-377.
94. Young CA, Bryant MK, Christensen MJ, Tapper BA, Bryan GT, et al. (2005) Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Molecular Genetics and Genomics 274: 13-29.
95. Namiki F, Matsunaga M, Okuda M, Inoue I, Nishi K, et al. (2001) Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Molecular Plant-Microbe Interactions 14: 580-584.
96. Vollmer SJ, Yanofsky C, (1986) Efficient cloning of genes of Neurospora crassa. Proceedings of the National Academy of Sciences, USA 83: 4869-4873.
97. Itoh Y, Johnson R, Scott B, (1994) Integrative transformation of the mycotoxin-producing fungus, Penicillium paxilli. Current Genetics 25: 508-513.
98. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
99. Schwarzer D, Finking R, Marahiel MA, (2003) Nonribosomal peptides: from genes to products. Natural Product Reports 20: 275-287.
100. McCormack P, Worsfold PJ, Gledhill M, (2003) Separation and detection of siderophores produced by marine bacterioplankton using high-performance liquid chromatography with electrospray ionization mass spectrometry. Analytical Chemistry 75: 2647-2652.
101. Gallagher RT, Hawkes AD, Stewart JM, (1985) Rapid determination of the neurotoxin lolitrem B in perennial ryegrass by high-performance liquid chromatography with fluorescence detection. Journal of Chromatography A 321: 217-226.
102. Spiering MJ, Davies E, Tapper BA, Schmid J, Lane GA, (2002) Simplified extraction of ergovaline and peramine for analysis of tissue distribution in endophyte-infected grass tillers. Journal of Agricultural and Food Chemistry 50: 5856-5862.
103. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB, (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant Journal 11: 1187-1194.
104. Eaton CJ, Jourdain I, Foster SJ, Hyams JS, Scott B, (2008) Functional analysis of a fungal endophyte stress-activated MAP kinase. Current Genetics 53: 163-174.