A core gene set describes the molecular basis of Mutualism and Antagonism in Epichloë spp

Molecular Plant-Microbe Interactions

Volumn 28, Issue 3, 2015, Pages 218-231

  Eaton, Carla J ^a   Dupont, Pierre Yves ^a   Solomon, Peter ^b   Clayton, William ^a   Scott, Barry ^a   Cox, Murray P ^a  

^a MASSEY UNIVERSITY   (New Zealand)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; LOLIUM PERENNE;

ERGOT ALKALOID; FUNGAL PROTEIN; INDOLE ALKALOID; LOLITREM B; MYCOTOXIN;

CELL WALL; CHEMISTRY; DOWN REGULATION; ENDOPHYTE; EPICHLOE; FUNGUS HYPHAE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SEQUENCING; HOST PATHOGEN INTERACTION; LOLIUM; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; PLANT; PLANT LEAF; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SYMBIOSIS; UPREGULATION;

CELL WALL; DOWN-REGULATION; ENDOPHYTES; EPICHLOE; ERGOT ALKALOIDS; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOST-PATHOGEN INTERACTIONS; HYPHAE; INDOLE ALKALOIDS; LOLIUM; MULTIGENE FAMILY; MYCOTOXINS; PLANT LEAVES; PLANT SHOOTS; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; SYMBIOSIS; UP-REGULATION;

EID: 84923177100     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-09-14-0293-FI     Document Type: Article

References (80)

1. Ambrose, K. V., Koppenhofer, A. M., and Belanger, F. C. 2014. Horizontal gene transfer of a bacterial insect toxin gene into the Epichloë fungal symbionts of grasses. Sci. Rep. 4:5562.
2. Bowman, S. M., and Free, S. J. 2006. The structure and synthesis of the fungal cell wall. BioEssays 28:799-808.
3. Bronstein, J. L. 1994. Conditional outcomes in mutualistic interactions. Trends Ecol. Evol. 9:214-217.
4. Bryant, M. K., Schardl, C. L., Hesse, U., and Scott, B. 2009. Evolution of a subtilisin-like protease gene family in the grass endophytic fungus Epichloë festucae. BMC Evol. Biol. 9:168.
5. Bushley, K. E., Raja, R., Jaiswal, P., Cumbie, J. S., Nonogaki, M., Boyd, A. E., Owensby, C. A., Knaus, B. J., Elser, J., Miller, D., Di, Y., McPhail, K. L., and Spatafora, J. W. 2013. The genome of Tolypocladium inflatum: Evolution, organization, and expression of the cyclosporin biosynthetic gene cluster. PLoS Genet. 9:e1003496. Published online.
6. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. 2009. The Carbohydrate-Active EnZymes database (CAZy): An expert resource for glycogenomics. Nucleic Acids Res. 37:D233-D238.
7. Carlson, M., and Botstein, D. 1982. Two differentially regulated mRNAs with different 5 ends encode secreted with intracellular forms of yeast invertase. Cell 28:145-154.
8. Carpita, N. C. 1996. Structure and biogenesis of the cell walls of grasses. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:445-476.
9. Coleman, M., Henricot, B., Arnau, J., and Oliver, R. P. 1997. Starvationinduced genes of the tomato pathogen Cladosporium fulvum are also induced during growth in planta. Mol. Plant-Microbe Interact. 10:1106-1109.
10. Damveld, R. A., Arentshorst, M., VanKuyk, P. A., Klis, F. M., van den Hondel, C. A., and Ram, A. F. 2005. Characterisation of CwpA, a putative glycosylphosphatidylinositol-anchored cell wall mannoprotein in the filamentous fungus Aspergillus niger. Fungal Genet. Biol. 42:873-885.
11. de Jonge, R., van Esse, H. P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., van der Krol, S., Shibuya, N., Joosten, M. H., and Thomma, B. P. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953-935.
12. Di Pietro, A., González-Roncero, I., and Ruiz-Roldán, M. C. 2009. From tools of survival to weapons of destruction: The role of cell-wall degrading enzymes in plant infection. Pages 275-306 in: Plant Relationships. H. B. Deising, ed. Springer-Verlag, Berlin.
13. Eaton, C. J., Cox, M. P., Ambrose, B., Becker, M., Hesse, U., Schardl, C. L., and Scott, B. 2010. Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis. Plant Physiol. 153:1780-1794.
14. Egger, K. N., and Hibbett, D. S. 2004. The evolutionary implications of exploitation in mycorrhizas. Can. J. Bot. 82:1110-1121.
15. Fleetwood, D. J., Scott, B., Lane, G. A., Tanaka, A., and Johnson, R. D. 2007. A complex ergovaline gene cluster in Epichloë endophytes of grasses. Appl. Environ. Microbiol. 73:2571-2579.
16. Giesbert, S., Lepping, H.-B., Tenberge, K. B., and Tudzynski, P. 1998. The xylanolytic system of Claviceps purpurea: Cytological evidence for secretion of xylanases in infected rye tissue and molecular characterization of two xylanase genes. Phytopathology 88:1020-1030.
17. González-Candelas, L., and Kolattukudy, P. E. 1992. Isolation and analysis of a novel inducible pectate lyase gene from the phytopathogenic fungus Fusarium solani f. Sp. Pisi (Nectria haematococca, mating population VI). J. Bacteriol. 174:6343-6349.
18. Grobler, J., Bauer, F., Subden, R. E., and Van Vuuren, H. J. 1995. The mae1 gene of Schizosaccharomyces pombe encodes a permease for malate and other C4 dicarboxylic acids. Yeast 11:1485-1491.
19. Guo, W., Gonzalez-Candelas, L., and Kolattukudy, P. E. 1995a. Cloning of a new pectate lyase gene pelC from Fusarium solani f. Sp. Pisi (Nectria haematococca, mating type VI) and characterization of the gene product expressed in Pichia pastoris. Arch. Biochem. Biophys. 323:352-360.
20. Guo, W., Gonzalez-Candelas, L., and Kolattukudy, P. E. 1995b. Cloning of a novel constitutively expressed pectate lyase gene pelB from Fusarium solani f. Sp. Pisi (Nectria haematococca, mating type VI) and characterization of the gene product expressed in Pichia pastoris. J. Bacteriol. 177:7070-7077.
21. Guo, W., Gonzalez-Candelas, L., and Kolattukudy, P. E. 1996. Identification of a novel pelD gene expressed uniquely in planta by Fusarium solani f. Sp. Pisi (Nectria haematococca, mating type VI) and characterization of its protein product as an endo-pectate lyase. Arch. Biochem. Biophys. 332:305-312.
22. Heier, C., Taschler, U., Rengachari, S., Oberer, M., Wolinski, H., Natter, K., Kohlwein, S. D., Leber, R., and Zimmermann, R. 2010. Identification of Yju3p as functional orthologue of mammalian monoglyceride lipase in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1801:1063-1071.
23. Hunt, M. G., Rasmussen, S., Newton, P. C. D., Parsons, A. J., and Newman, J. A. 2005. Near-term impacts of elevated CO2, nitrogen and fungal endophyte-infection on Lolium perenne L. growth, chemical composition and alkaloid production. Plant Cell Environ. 28:1345-1354.
24. Ilangumaran, S., Robinson, P. J., and Hoessli, D. C. 1999. Signaling through GPI-anchored receptors. In: GPI-Anchored Membrane Proteins and Carbohydrates. D. C. Hoessli and S. Ilangumaran, eds. Landes Bio-Science. R. G. Landes, Austin, TX, U. S. A.
25. Iraqui, I., Vissers, S., Cartiaux, M., and Urrestarazu, A. 1998. Characterisation of Saccharomyces cerevisiae ARO8 and ARO9 genes encoding aromatic aminotransferases I and II reveals a new aminotransferase subfamily. Mol. Gen. Genet. 257:238-248.
26. Johnson, L. J., Koulman, A., Christensen, M., Lane, G. A., Fraser, K., Forester, N., Johnson, R. D., Bryan, G. T., and Rasmussen, S. 2013. An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne. PLoS Pathog. 9:e1003332. Published Online.
27. Published online. Johnsen, U., Dambeck, M., Zaiss, H., Fuhrer, T., Soppa, J., Sauer, U., and Schonheit, P. 2009. D-xylose degradation pathway in the halophilic archaeon Haloferax volcanii. J. Biol. Chem. 284:27290-27303.
28. Kars, I., McCalman, M., Wagemakers, L., and Van Kan, J. A. L. 2005. Functional analysis of Botrytis cinerea pectin methylesterase genes by PCR-based targeted mutagenesis: Bcpme1 and Bcpme2 are dispensable for virulence of strain B05. 10. Mol. Plant Pathol. 6:641-652.
29. Kayano, Y., Tanaka, A., Akano, F., Scott, B., and Takemoto, D. 2013. Differential roles of NADPH oxidases and associated regulators in polarized growth, conidiation and hyphal fusion in the symbiotic fungus Epichloë festucae. Fungal Genet. Biol. 56:87-97.
30. Lam, C. K., Belanger, F. C., White, J. F., Jr., and Daie, J. 1995. Invertase activity in Epichloë/Acremonium fungal endophytes and its possible role in choke disease. Mycol. Res. 99:867-873.
31. Latch, G. C. M., and Christensen, M. J. 1985. Artificial infection of grasses with endophytes. Ann. Appl. Biol. 107:17-24.
32. Leuchtmann, A., Bacon, C. W., Schardl, C. L., White, J. F., Jr., and Tadych, M. 2014. Nomenclatural realignment of Neotyphodium species with genus Epichloë. Mycologia 106:202-215.
33. Lowe, R. G., Lord, M., Rybak, K., Trengove, R. D., Oliver, R. P., and Solomon, P. S. 2009. Trehalose biosynthesis is involved in sporulation of Stagonospora nodorum. Fungal Genet. Biol. 46:381-389.
34. Martin, F., Aerts, A., Ahren, D., Brun, A., Danchin, E. G., Duchaussoy, F., Gibon, J., Kohler, A., Lindquist, E., Pereda, V., Salamov, A., Shapiro, H. J., Wuyts, J., Blaudez, D., Buee, M., Brokstein, P., Canback, B., Cohen, D., Courty, P. E., Coutinho, P. M., Delaruelle, C., Detter, J. C., Deveau, A., DiFazio, S., Duplessis, S., Fraissinet-Tachet, L., Lucic, E., Frey-Klett, P., Fourrey, C., Feussner, I., Gay, G., Grimwood, J., Hoegger, P. J., Jain, P., Kilaru, S., Labbe, J., Lin, Y. C., Legue, V., Le Tacon, F., Marmeisse, R., Melayah, D., Montanini, B., Muratet, M., Nehls, U., Niculita-Hirzel, H., Oudot-Le Secq, M. P., Peter, M., Quesneville, H., Rajashekar, B., Reich, M., Rouhier, N., Schmutz, J., Yin, T., Chalot, M., Henrissat, B., Kues, U., Lucas, S., Van de Peer, Y., Podila, G. K., Polle, A., Pukkila, P. J., Richardson, P. M., Rouze, P., Sanders, I. R., Stajich, J. E., Tunlid, A., Tuskan, G., and Grigoriev, I. V. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88-92.
35. Mathioni, S. M., Belo, A., Rizzo, C. J., Dean, R. A., and Donofrio, N. M. 2011. Transcriptome profiling of the rice blast fungus during invasive plant infection and in vitro stresses. BMC Genomics 12:49.
36. Maundrell, K. 1990. nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine. J. Biol. Chem. 265:10857-10864.
37. Meinhardt, L. W., Costa, G. G., Thomazella, D. P., Teixeira, P. J., Carazzolle, M. F., Schuster, S. C., Carlson, J. E., Guiltinan, M. J., Mieczkowski, P., Farmer, A., Ramaraj, T., Crozier, J., Davis, R. E., Shao, J., Melnick, R. L., Pereira, G. A., and Bailey, B. A. 2014. Genome and secretome analysis of the hemibiotrophic fungal pathogen, Moniliophthora roreri, which causes frosty pod rot disease of cacao: Mechanisms of the biotrophic and necrotrophic phases. BMC Genomics 15:164.
38. Miller, S. M., and Magasanik, B. 1990. Role of NAD-linked glutamate dehydrogenase in nitrogen metabolism in Saccharomyces cerevisiae. J. Bacteriol. 172:4927-4935.
39. Miller, S. M., and Magasanik, B. 1991. Role of the complex upstream region of the GDH2 gene in nitrogen regulation of the NAD-linked glutamate dehydrogenase in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:6229-6247.
40. Moy, M., Belanger, F., Duncan, R., Freehoff, A., Leary, C., Meyer, W., Sullivan, R., and White, J. F., Jr. 2000. Identification of epiphyllous mycelial nets on leaves of grasses infected by clavicipitaceous endophytes. Symbiosis 28:291-302.
41. O'Connell, R. J., Thon, M. R., Hacquard, S., Amyotte, S. G., Kleemann, J., Torres, M. F., Damm, U., Buiate, E. A., Epstein, L., Alkan, N., Altmuller, J., Alvarado-Balderrama, L., Bauser, C. A., Becker, C., Birren, B. W., Chen, Z., Choi, J., Crouch, J. A., Duvick, J. P., Farman, M. A., Gan, P., Heiman, D., Henrissat, B., Howard, R. J., Kabbage, M., Koch, C., Kracher, B., Kubo, Y., Law, A. D., Lebrun, M. H., Lee, Y. H., Miyara, I., Moore, N., Neumann, U., Nordstrom, K., Panaccione, D. G., Panstruga, R., Place, M., Proctor, R. H., Prusky, D., Rech, G., Reinhardt, R., Rollins, J. A., Rounsley, S., Schardl, C. L., Schwartz, D. C., Shenoy, N., Shirasu, K., Sikhakolli, U. R., Stuber, K., Sukno, S. A., Sweigard, J. A., Takano, Y., Takahara, H., Trail, F., van der Does, H. C., Voll, L. M., Will, I., Young, S., Zeng, Q., Zhang, J., Zhou, S., Dickman, M. B., Schulze-Lefert, P., Ver Loren van Themaat, E., Ma, L. J., and Vaillancourt, L. J. 2012. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat. Genet. 44:1060-1067.
42. Oeser, B., Heidrich, P. M., Muller, U., Tudzynski, P., and Tenberge, K. B. 2002. Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/ rye interaction. Fungal Genet. Biol. 36:176-186.
43. Ozcan, S., Vallier, L. G., Flick, J. S., Carlson, M., and Johnston, M. 1997. Expression of the SUC2 gene of Saccharomyces cerevisiae is induced by low levels of glucose. Yeast 13:127-137.
44. Parniske, M. 2008. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat. Rev. Microbiol. 6:763-775.
45. Plett, J. M., Kemppainen, M., Kale, S. D., Kohler, A., Legue, V., Brun, A., Tyler, B. M., Pardo, A. G., and Martin, F. 2011. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr. Biol. 21:1197-1203.
46. Praekelt, U. M., and Meacock, P. A. 1992. MOL1, a Saccharomyces cerevisiae gene that is highly expressed in early stationary phase during growth on molasses. Yeast 8:699-710.
47. Praekelt, U. M., Byrne, K. L., and Meacock, P. A. 1994. Regulation of THI4 (MOL1), a thiamine-biosynthetic gene of Saccharomyces cerevisiae. Yeast 10:481-490.
48. Rasmussen, S., Lane, G. A., Mace, W., Parsons, A. J., Fraser, K., and Xue, H. 2012a. The use of genomics and metabolomics methods to quantify fungal endosymbionts and alkaloids in grasses. Methods Mol. Biol. 860:213-226.
49. Rasmussen, S., Liu, Q., Parsons, A. J., Xue, H., Sinclair, B., and Newman, J. A. 2012b. Grass-endophyte interactions: A note on the role of monosaccharide transport in the Neotyphodium lolii-Lolium perenne symbiosis. New Phytol. 196:7-12.
50. Regenberg, B., Holmberg, S., Olsen, L. D., and Kielland-Brandt, M. C. 1998. Dip5p mediates high-affinity and high-capacity transport of Lglutamate and L-aspartate in Saccharomyces cerevisiae. Curr. Genet. 33:171-177.
51. Rep, M. 2005. Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol. Lett. 253:19-27.
52. Rittenour, W. R., and Harris, S. D. 2013. Glycosylphosphatidylinositolanchored proteins in Fusarium graminearum: Inventory, variability, and virulence. PLoS One 8:e81603. Published online.
53. Robin, J. B., Arffa, R. C., Avni, I., and Rao, N. A. 1986. Rapid visualization of three common fungi using fluorescein-conjugated lectins. Invest. Ophthalmol. Visual Sci. 27:500-506.
54. Saikia, S., Takemoto, D., Tapper, B. A., Lane, G. A., Fraser, K., and Scott, B. 2012. Functional analysis of an indole-diterpene gene cluster for lolitrem B biosynthesis in the grass endosymbiont Epichloë festucae. FEBS (Fed. Eur. Biochem. Soc.) Lett. 586:2563-2569.
55. Schardl, C. L. 2001. Epichloë 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. Schardl, C. L., Panaccione, D. G., and Tudzynski, P. 2006. Ergot alkaloids-biology and molecular biology. Pages 425-443 in: Alkaloids: Chemistry and Biology. G. A. Cordell, ed. Academic Press, San Diego, CA, U. S. A.
58. Schardl, C. L., Young, C. A., Hesse, U., Amyotte, S. G., Andreeva, K., Calie, P. J., Fleetwood, D. J., Haws, D. C., Moore, N., Oeser, B., Panaccione, D. G., Schweri, K. K., Voisey, C. R., Farman, M. L., Jaromczyk, J. W., Roe, B. A., O'Sullivan, D. M., Scott, B., Tudzynski, P., An, Z.-Q., Arnaoudova, E. G., Bullock, C. T., Charlton, N. D., Chen, L., Cox, M., Dinkins, R. D., Florea, S., Glenn, A. E., Gordon, A., Güldener, U., Harris, D. R., Hollin, W., Jaromczyk, J., Johnson, R. D., Khan, A. K., Leistner, E., Leuchtmann, A., Li, C., Liu, J.-G., Liu, J., Liu, M., Mace, W., Machado, C., Nagabhyru, P., Pan, J., Schmid, J., Sugawara, K., Steiner, U., Takach, J. E., Tanaka, E., Webb, J. S., Wilson, E. V., Wiseman, J. L., Yoshida, R., and Zheng, Z. 2013. Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet. 9:e1003323. Published online.
59. Schauer, N., Steinhauser, D., Strelkov, S., Schomburg, D., Allison, G., Moritz, T., Lundgren, K., Roessner-Tunali, U., Forbes, M. G., Willmitzer, L., Fernie, A. R., and Kopka, J. 2005. GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS (Fed. Eur. Biochem. Soc.) Lett. 579:1332-1337.
60. Scott, B., Becker, Y., Becker, M., and Cartwright, G. 2012. Morphogenesis, growth and development of the grass symbiont Epichloë festucae. Pages 243-264 in: Morphogenesis and Pathogenicity in Fungi. J. P. Martin and A. Di Pietro, eds. Springer-Verlag, Heidelberg, Germany.
61. Skamnioti, P., and Gurr, S. J. 2007. Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19:2674-2689.
62. Solomon, P. S., Thomas, S. W., Spanu, P. D., and Oliver, R. P. 2003. The utilisation of di/tripeptides by Stagonospora nodorum is dispensable for wheat infection. Physiol. Mol. Plant Pathol. 63:191-199.
63. Spiering, M. J., Davies, E., Tapper, B. A., Schmid, J., and Lane, G. A. 2002. Simplified extraction of ergovaline and peramine for analysis of tissue distribution in endophyte-infected grass tillers. J. Agric. Food Chem. 50:5856-5862.
64. Storey, J. D., and Tibshirani, R. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U. S. A. 100:9440-9445.
65. 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.
66. Tanaka, A., Christensen, M. J., Takemoto, D., Park, P., and Scott, B. 2006. Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic association. Plant Cell 18:1052-1066.
67. Tanaka, A., Cartwright, G. M., Saikia, S., Kayano, Y., Takemoto, D., Kato, M., Tsuge, T., and Scott, B. 2013. ProA, a transcriptional regulator of fungal fruiting body development, regulates leaf hyphal network development in the Epichloë festucae-Lolium perenne symbiosis. Mol. Microbiol. 90:551-568.
68. Tisserant, E., Kohler, A., Dozolme-Seddas, P., Balestrini, R., Benabdellah, K., Colard, A., Croll, D., Da Silva, C., Gomez, S. K., Koul, R., Ferrol, N., Fiorilli, V., Formey, D., Franken, P., Helber, N., Hijri, M., Lanfranco, L., Lindquist, E., Liu, Y., Malbreil, M., Morin, E., Poulain, J., Shapiro, H., van Tuinen, D., Waschke, A., Azcon-Aguilar, C., Becard, G., Bonfante, P., Harrison, M. J., Kuster, H., Lammers, P., Paszkowski, U., Requena, N., Rensing, S. A., Roux, C., Sanders, I. R., Shachar-Hill, Y., Tuskan, G., Young, J. P., Gianinazzi-Pearson, V., and Martin, F. 2012. The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol. 193:755-769.
69. Valette-Collet, O., Cimerman, A., Reignault, P., Levis, C., and Boccara, M. 2003. Disruption of Botrytis cinerea pectin methylesterase gene Bcpme1 reduces virulence on several host plants. Mol. Plant-Microbe Interact. 16:360-367.
70. van den Ackerveken, G. F. J. M., Dunn, R. M., Cozijnsen, A. J., Vossen, J. P. M. J., van den Broek, H. W. J., and de Wit, P. J. G. M. 1994.
71. Nitrogen limitation induces expression of the avirulence gene avr9 in the tomato pathogen Cladosporium fulvum. Mol. Gen. Genet. 243:277-285.
72. van Esse, H. P., Bolton, M. D., Stergiopoulos, I., de Wit, P. J., and Thomma, B. P. 2007. The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol. Plant-Microbe Interact. 20:1092-1101.
73. van Hove, L. W. A., Heeres, P., and Bossen, M. E. 2002. The annual variation in stomatal ammonia compensation point of rye grass (Lolium perenne L.) leaves in an intensively managed grassland. Atmosph. Environ. 36:2965-2977.
74. Vincent, D., Du Fall, L. A., Livk, A., Mathesius, U., Lipscombe, R. J., Oliver, R. P., Friesen, T. L., and Solomon, P. S. 2012. A functional genomics approach to dissect the mode of action of the Stagonospora nodorum effector protein SnToxA in wheat. Mol. Plant Pathol. 13:467-482.
75. Wang, C., and St Leger, R. J. 2007. The MAD1 adhesin of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. Eukaryot. Cell 6:808-816.
76. Wightman, R., and Meacock, P. A. 2003. The THI5 gene family of Saccharomyces cerevisiae: Distribution of homologues among the hemiascomycetes and functional redundancy in the aerobic biosynthesis of thiamin from pyridoxine. Microbiology 149:1447-1460.
77. Yoko-o, T., Matsui, Y., Yagisawa, H., Nojima, H., Uno, I., and Toh-e, A. 1993. The putative phosphoinositide-specific phospholipase C gene, PLC1, of the yeast Saccharomyces cerevisiae is important for cell growth. Proc. Natl. Acad. Sci. U. S. A. 90:1804-1808.
78. 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. Gen. Genomics 274:13-29.
79. Young, C. A., Felitti, S., Shields, K., Spangenberg, G., Johnson, R. D., Bryan, G. T., Saikia, S., and Scott, B. 2006. A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii. Fungal Genet. Biol. 43:679-693.
80. Zhao, Z., Liu, H., Wang, C., and Xu, J. R. 2014. Correction: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 15:6.