American Journal of Potato Research

, Volume 91, Issue 5, pp 517–524 | Cite as

A Draft Genome Sequence Reveals the Helminthosporium solani Arsenal for Cell Wall Degradation

  • Chakradhar Mattupalli
  • Jeremy D. Glasner
  • Amy O. Charkowski
Article
First Online:

Abstract

Helminthosporium solani is a slow-growing fungal pathogen belonging to the family Massarinaceae. It causes blemishes on potato tubers, affecting processing and fresh market trade. Despite its worldwide distribution, little is known about the biology of H. solani. Here we report the generation of a draft genome sequence of H. solani with an estimated genome size of ~35 megabases, for use in phylogenetic and pathogenicity studies of this fungal pathogen. This sequence is also the first reference genome within the family Massarinaceae. We identified a large suite of genes in the H. solani genome that encode putative cell wall degrading enzymes. Based on comparison with other genomes, we speculate that H. solani is a hemibiotroph or necrotroph. The presence of a large number of genes in the glycoside hydrolase (GH) 10 and 43 families, which aid in the hydrolysis of glucoronoarabinoxylan, also suggests that H. solani may be able to survive on grass hosts and indicates the need to re-examine the life cycle and host range of this pathogen.

Keywords

Silver scurf Massarinaceae Glycoside hydrolases 

Resumen

Helminthosporium solani, es un hongo patógeno de lento crecimiento que pertenece a la familia Massarinaceae. Causa manchas en los tubérculos de papa, afectando el mercado en fresco y de procesamiento. A pesar de su distribución mundial, se sabe poco de la biología de H. solani. Aquí reportamos la generación de una secuencia preliminar del genomio de H. solani, con un tamaño genómico estimado de ~35 megabases, para uso en estudios filogenéticos y de patogenicidad de este patógeno fúngico. Esta secuencia también es la primera referencia genómica dentro de la familia Massarinaceae. Identificamos un gran conjunto de genes en el genómio de H. solani que codifican supuestamente para enzimas degradadoras de pared celular. Con base en la comparación con otros genomios, especulamos que H. solani es un hemibiótrofo o necrótrofo. La presencia de un gran número de genes en las familias 10 y 43 de glicósido hidrolasa (GH), que ayudan en la hidrólisis de glucoronoarabinoxilano, también sugiere que H. solani pudiera ser capaz de sobrevivir en pastos hospedantes o en desechos, e indica la necesidad de reexaminar el ciclo biológico y la amplitud de hospederos de este patógeno.

This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We thank Jason L. Kingstad for assisting with blast searches and construction of phylogenetic trees. We also thank Samantha Sparrow for conducting co-inoculation assays. This work was funded by the Ceres Trust and the Wisconsin Potato and Vegetable Growers Association.

All the experiments performed complied with the current regulations of the United States of America.

References

  1. Albersheim, P., A. Darvill, K. Roberts, R. Sederoff, and A. Staehelin. 2011. Plant cell walls: From chemistry to biology. New York: Garland Science, Taylor and Francis group.Google Scholar
  2. Altschul, S.F., W. Gish, W. Miller, E.W. Myers, and D.J. Lipman. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.CrossRefPubMedGoogle Scholar
  3. Amselem, J., C.A. Cuomo, J.A. van Kan, M. Viaud, E.P. Benito, A. Couloux, P.M. Coutinho, R.P. de Vries, P.S. Dyer, S. Fillinger, E. Fournier, L. Gout, M. Hahn, L. Kohn, N. Lapalu, K.M. Plummer, J.M. Pradier, E. Quévillon, A. Sharon, A. Simon, A. ten Have, B. Tudzynski, P. Tudzynski, P. Wincker, M. Andrew, V. Anthouard, R.E. Beever, R. Beffa, I. Benoit, O. Bouzid, B. Brault, Z. Chen, M. Choquer, J. Collémare, P. Cotton, E.G. Danchin, C. Da Silva, A. Gautier, C. Giraud, T. Giraud, C. Gonzalez, S. Grossetete, U. Güldener, B. Henrissat, B.J. Howlett, C. Kodira, M. Kretschmer, A. Lappartient, M. Leroch, C. Levis, E. Mauceli, C. Neuvéglise, B. Oeser, M. Pearson, J. Poulain, N. Poussereau, H. Quesneville, C. Rascle, J. Schumacher, B. Ségurens, A. Sexton, E. Silva, C. Sirven, D.M. Soanes, N.J. Talbot, M. Templeton, C. Yandava, O. Yarden, Q. Zeng, J.A. Rollins, M.H. Lebrun, and M. Dickman. 2011. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genetics 7: e1002230.PubMedCentralCrossRefPubMedGoogle Scholar
  4. Ashburner, M., C.A. Ball, J.A. Blake, D. Botstein, H. Butler, J.M. Cherry, A.P. Davis, K. Dolinski, S.S. Dwight, J.T. Eppig, M.A. Harris, D.P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J.C. Matese, J.E. Richardson, M. Ringwald, G.M. Rubin, and G. Sherlock. 2000. Gene Ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 25: 25–29.PubMedCentralCrossRefPubMedGoogle Scholar
  5. Blin, K., M.H. Medema, D. Kazempour, M.A. Fischbach, R. Breitling, E. Takano, and T. Weber. 2013. antiSMASH 2.0—a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Research 41: W204–W212.PubMedCentralCrossRefPubMedGoogle Scholar
  6. Bok, J.W., and N.P. Keller. 2012. Fast and easy method for construction of plasmid vectors using modified quick-change mutagenesis. Methods in Molecular Biology 944: 163–174.PubMedCentralPubMedGoogle Scholar
  7. Borodovsky, M., and A. Lomsadze. 2011. Eukaryotic gene prediction using GeneMark.hmm-E and GeneMark-ES. Current Protocols in Bioinformatics. doi: 10.1002/0471250953.bi0406s35.PubMedCentralGoogle Scholar
  8. Bucher, V.V.C., S.B. Pointing, K.D. Hyde, and C.A. Reddy. 2004. Production of wood decay enzymes, loss of mass, and lignin solubilization in wood by diverse tropical freshwater fungi. Microbial Ecology 48: 331–337.CrossRefPubMedGoogle Scholar
  9. Burke, O.D. 1938. The silver scurf disease of potatoes. Bulletin of Cornell University Agricultural Experimental Station 692: 1–30.Google Scholar
  10. Cantarel, B.L., P.M. Coutinho, C. Rancurel, T. Bernard, V. Lombard, and B. Henrissat. 2008. The carbohydrate-active enzyme database (CAZy): an expert resource for glycogenomics. Nucleic Acid Research 37: D233–D238.CrossRefGoogle Scholar
  11. Carnegie, S.F., A.M. Cameron, and P. Haddon. 1996. The potato store—a source of infection. Abstracts of the 13th Triennial Conference of the European Association for Potato Research, Wageningen, The Netherlands. 672–673.Google Scholar
  12. Cunha, M.G., and D.M. Rizzo. 2004. Occurrence and epidemiological aspects of potato silver scurf in California. Horticultura Brasileira 22: 690–695.CrossRefGoogle Scholar
  13. de Wit, P.J., A. van der Burgt, B. Ökmen, I. Stergiopoulos, K.A. Abd-Elsalam, A.L. Aerts, A.H. Bahkali, H.G. Beenen, P. Chettri, M.P. Cox, E. Datema, R.P. de Vries, B. Dhillon, A.R. Ganley, S.A. Griffiths, Y. Guo, R.C. Hamelin, B. Henrissat, M.S. Kabir, M.K. Jashni, G. Kema, S. Klaubauf, A. Lapidus, A. Levasseur, E. Lindquist, R. Mehrabi, R.A. Ohm, T.J. Owen, A. Salamov, A. Schwelm, E. Schijlen, H. Sun, H.A. van den Burg, R.C. van Ham, S. Zhang, S.B. Goodwin, I.V. Grigoriev, J. Collemare, and R.E. Bradshaw. 2012. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genetics 8(11): e1003088.PubMedCentralCrossRefPubMedGoogle Scholar
  14. Ellwood, S.R., Z. Liu, R.A. Syme, Z. Lai, J.K. Hane, F. Keiper, C.S. Moffat, R.P. Oliver, and T.L. Friesen. 2010. A first genome assembly of the barley fungal pathogen Pyrenophora teres f. teres. Genome Biology 11: R109.PubMedCentralCrossRefPubMedGoogle Scholar
  15. Elson, M.K., D.A. Schisler, and M.A. Jackson. 1998. Carbon-to-nitrogen ratio, carbon concentration, and amino acid composition of growth media influence conidiation of Helminthosporium solani. Mycologia 90: 406–413.CrossRefGoogle Scholar
  16. Eriksson, O.E., and D.L. Hawksworth. 2003. Saccharicola, a new genus for two Leptosphaeria species on sugar cane. Mycologia 95: 426–433.CrossRefPubMedGoogle Scholar
  17. Errampalli, D., J.M. Saunders, and J.D. Holley. 2001. Emergence of silver scurf (Helminthosporium solani) as an economically important disease of potato. Plant Pathology 50: 141–153.CrossRefGoogle Scholar
  18. Geary, B., D.A. Johnson, P.B. Hamm, S. James, and K.A. Rykbost. 2007. Potato silver scurf affected by tuber seed treatments and locations, and occurrence of fungicide resistant isolates of Helminthosporium solani. Plant Disease 91: 315–320.CrossRefGoogle Scholar
  19. Gibson, D.M., B.C. King, M.L. Hayes, and G.C. Bergstrom. 2011. Plant pathogens as a source of diverse enzymes for lignocelluloses digestion. Current Opinion in Microbiology 14: 264–270.CrossRefPubMedGoogle Scholar
  20. Gijzen, M., and T. Nürnberger. 2006. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67: 1800–1807.CrossRefPubMedGoogle Scholar
  21. Goodwin, S.B., S.B. M’barek, B. Dhillon, A.H. Wittenberg, C.F. Crane, J.K. Hane, A.J. Foster, T.A. Van der Lee, J. Grimwood, A. Aerts, J. Antoniw, A. Bailey, B. Bluhm, J. Bowler, J. Bristow, A. van der Burgt, B. Canto-Canché, A.C. Churchill, L. Conde-Ferràez, H.J. Cools, P.M. Coutinho, M. Csukai, P. Dehal, P. De Wit, B. Donzelli, H.C. van de Geest, R.C. van Ham, K.E. Hammond-Kosack, B. Henrissat, A. Kilian, A.K. Kobayashi, E. Koopmann, Y. Kourmpetis, A. Kuzniar, E. Lindquist, V. Lombard, C. Maliepaard, N. Martins, R. Mehrabi, J.P. Nap, A. Ponomarenko, J.J. Rudd, A. Salamov, J. Schmutz, H.J. Schouten, H. Shapiro, I. Stergiopoulos, S.F. Torriani, H. Tu, R.P. de Vries, C. Waalwijk, S.B. Ware, A. Wiebenga, L.H. Zwiers, R.P. Oliver, I.V. Grigoriev, and G.H. Kema. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genetics 7: e1002070.PubMedCentralCrossRefPubMedGoogle Scholar
  22. Gorfer, M., M. Blumhoff, S. Klaubauf, A. Urban, E. Inselsbacher, D. Bandian, B. Mitter, A. Sessitsch, W. Wanek, and J. Strauss. 2011. Community profiling and gene expression of fungal assimilatory nitrate reductases in agricultural soils. The ISME Journal 5: 1771–1783.PubMedCentralCrossRefPubMedGoogle Scholar
  23. Goth, R.W., and R.E. Webb. 1983. Maintenance and growth of Helminthosporium solani. American Potato Journal 60: 281–287.CrossRefGoogle Scholar
  24. Hane, J.K., R.G. Lowe, P.S. Solomon, K.C. Tan, C.L. Schoch, J.W. Spatafora, P.W. Crous, C. Kodira, B.W. Birren, J.E. Galagan, S.F. Torriani, B.A. McDonald, and R.P. Oliver. 2007. Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19: 3347–3368.PubMedCentralCrossRefPubMedGoogle Scholar
  25. Holley, J.D., and L.M. Kawchuk. 1996. Distribution of thiabendazole and thiophanate-methyl resistant strains of Helminthosporium solani and Fusarium sambucinum in Alberta potato storages. Canadian Plant Disease Survey 76: 21–27.Google Scholar
  26. Islam, M.S., M.S. Haque, M.M. Islam, E.M. Emdad, A. Halim, Q.M. Hossen, M.Z. Hossain, B. Ahmed, S. Rahim, M.S. Rahman, M.M. Alam, S. Hou, X. Wan, J.A. Saito, and M. Alam. 2012. Tools to kill: genome of one of the most destructive plant pathogenic fungi Macrophomina phaseolina. BMC Genomics 13: 493.PubMedCentralCrossRefPubMedGoogle Scholar
  27. Jellis, G.J., and G.S. Taylor. 1974. The relative importance of silver scurf and black dot: two disfiguring diseases of potato tubers. ADAS Quarterly Review 14: 53–61.Google Scholar
  28. Jellis, G.J., and G.S. Taylor. 1977. The development of silver scurf (Helminthosporium solani) disease of potato. Annals of Applied Biology 86: 19–28.CrossRefGoogle Scholar
  29. Kamara, A.M., and J.E. Huguelet. 1972. Host range and overwintering of Helminthosporium solani. American Potato Journal 49: 365.Google Scholar
  30. King, B.C., K.D. Waxman, N.V. Nenni, L.P. Walker, G.C. Bergstrom, and D.M. Gibson. 2011. Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi. Biotechnology for Biofuels 4: 4.PubMedCentralCrossRefPubMedGoogle Scholar
  31. Kirk, P.M., P.F. Cannon, D.W. Minter, and J.A. Stalpers. 2008. Ainsworth and Bisby’s Dictionary of the fungi. Wallingford: CAB International.Google Scholar
  32. Liew, C.Y., A. Aptroot, and K.D. Hyde. 2002. An evaluation of the monophyly of Massarina based on ribosomal DNA sequences. Mycologia 94: 803–813.CrossRefPubMedGoogle Scholar
  33. Loria, R., and G.A. Secor. 2001. In Compendium of potato diseases, ed. W.R. Stevenson, R. Loria, G.D. Franc, and D.P. Weingartner, 40–41. St. Paul: American Phytopathological Society press.Google Scholar
  34. Manning, V.A., I. Pandelova, B. Dhillon, L.J. Wilhelm, S.B. Goodwin, A.M. Berlin, M. Figueroa, M. Freitag, J.K. Hane, B. Henrissat, W.H. Holman, C.D. Kodira, J. Martin, R.P. Oliver, B. Robbertse, W. Schackwitz, D.C. Schwartz, J.W. Spatafora, B.G. Turgeon, C. Yandava, S. Young, S. Zhou, Q. Zeng, I.V. Grigoriev, L.J. Ma, and L.M. Ciuffetti. 2013. Comparative genomics of a plant-pathogenic fungus, Pyrenophora tritici-repentis, reveals transduplication and the impact of repeat elements on pathogenicity and population divergence. G3 (Bethesda) 3: 41–63.CrossRefGoogle Scholar
  35. Margulies, M., M. Egholm, W.E. Altman, S. Attiya, J.S. Bader, L.A. Bemben, J. Berka, M.S. Braverman, Y.J. Chen, Z. Chen, S.B. Dewell, L. Du, J.M. Fierro, X.V. Gomes, B.C. Godwin, W. He, S. Helgesen, C.H. Ho, G.P. Irzyk, S.C. Jando, M.L. Alenquer, T.P. Jarvie, K.B. Jirage, J.B. Kim, J.R. Knight, J.R. Lanza, J.H. Leamon, S.M. Lefkowitz, M. Lei, J. Li, K.L. Lohman, H. Lu, V.B. Makhijani, K.E. McDade, M.P. McKenna, E.W. Myers, E. Nickerson, J.R. Nobile, R. Plant, B.P. Puc, M.T. Ronan, G.T. Roth, G.J. Sarkis, J.F. Simons, J.W. Simpson, M. Srinivasan, K.R. Tartaro, A. Tomasz, K.A. Vogt, G.A. Volkmer, S.H. Wang, Y. Wang, M.P. Weiner, P. Yu, R.F. Begley, and J.M. Rothberg. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376–380.PubMedCentralPubMedGoogle Scholar
  36. Martinez, C., D. Rioux, and R.J. Tweddell. 2004. Ultrastructure of the infection process of potato tuber by Helminthosporium solani, causal agent of potato silver scurf. Mycological Research 108: 828–836.CrossRefPubMedGoogle Scholar
  37. Martinez, D., R.M. Berka, B. Henrissat, M. Saloheimo, M. Arvas, S.E. Baker, J. Chapman, O. Chertkov, P.M. Coutinho, D. Cullen, E.G. Danchin, I.V. Grigoriev, P. Harris, M. Jackson, C.P. Kubicek, C.S. Han, I. Ho, L.F. Larrondo, A.L. de Leon, J.K. Magnuson, S. Merino, M. Misra, B. Nelson, N. Putnam, B. Robbertse, A.A. Salamov, M. Schmoll, A. Terry, N. Thayer, A. Westerholm-Parvinen, C.L. Schoch, J. Yao, R. Barabote, M.A. Nelson, C. Detter, D. Bruce, C.R. Kuske, G. Xie, P. Richardson, D.S. Rokhsar, S.M. Lucas, E.M. Rubin, N. Dunn-Coleman, M. Ward, and T.S. Brettin. 2008. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nature Biotechnology 26: 553–560.CrossRefPubMedGoogle Scholar
  38. Mattupalli, C., R.K. Genger, and A.O. Charkowski. 2013. Evaluating incidence of Helminthosporium solani and Colletotrichum coccodes on asymptomatic organic potatoes and screening potato lines for resistance to silver scurf. American Journal of Potato Research 90: 369–377.CrossRefGoogle Scholar
  39. Merida, C.L., and R. Loria. 1994. Survival of Helminthosporium solani in soil and in vitro colonization of senescent plant tissue. American Potato Journal 71: 591–598.CrossRefGoogle Scholar
  40. Ohm, R.A., N. Feau, B. Henrissat, C.L. Schoch, B.A. Horwitz, K.W. Barry, B.J. Condon, A.C. Copeland, B. Dhillon, F. Glaser, C.N. Hesse, I. Kosti, K. LaButti, E.A. Lindquist, S. Lucas, A.A. Salamov, R.E. Bradshaw, L. Ciuffetti, R.C. Hamelin, G.H. Kema, C. Lawrence, J.A. Scott, J.W. Spatafora, B.G. Turgeon, P.J. de Wit, S. Zhong, S.B. Goodwin, and I.V. Grigoriev. 2012. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathogens 8: e1003037.PubMedCentralCrossRefPubMedGoogle Scholar
  41. Oliver, C., M.L. Berbee, R.A. Shoemaker, and R. Loria. 2000. Molecular phylogenetic support from ribosomal DNA sequences for origin of Helminthosporium from Leptosphaeria-like loculoascomycete ancestors. Mycologia 92: 736–746.CrossRefGoogle Scholar
  42. Olivier, C., and R. Loria. 1998. Detection of Helminthosporium solani from soil and plant tissue with species-specific PCR primers. FEMS Microbiology Letters 168: 235–241.CrossRefGoogle Scholar
  43. Read, P.J., and G.A. Hide. 1984. Effects of silver scurf (Helminthosporium solani) on seed potatoes. Potato Research 27: 145–154.CrossRefGoogle Scholar
  44. Richards, T.A., G. Leonard, D.M. Soanes, and N.J. Talbot. 2011. Gene transfer into the fungi. Fungal Biology Reviews 25: 98–110.CrossRefGoogle Scholar
  45. Rivera-Varas, V.V., T.A. Freeman, N.C. Gudmestad, and G.A. Secor. 2007. Mycoparasitism of Helminthosporium solani by Acremonium strictum. Phytopathology 97: 1331–1337.CrossRefPubMedGoogle Scholar
  46. Rodriguez, D.A., G.A. Secor, N.C. Gudmestad, and K. Grafton. 1995. Screening tuber-bearing Solanum species for resistance to Helminthosporium solani. American Potato Journal 72: 669–679.CrossRefGoogle Scholar
  47. Rouxel, T., J. Grandaubert, J.K. Hane, C. Hoede, A.P. van de Wouw, A. Couloux, V. Dominguez, V. Anthouard, P. Bally, S. Bourras, A.J. Cozijnsen, L.M. Ciuffetti, A. Degrave, A. Dilmaghani, L. Duret, I. Fudal, S.B. Goodwin, L. Gout, N. Glaser, J. Linglin, G.H. Kema, N. Lapalu, C.B. Lawrence, K. May, M. Meyer, B. Ollivier, J. Poulain, C.L. Schoch, A. Simon, J.W. Spatafora, A. Stachowiak, B.G. Turgeon, B.M. Tyler, D. Vincent, J. Weissenbach, J. Amselem, H. Quesneville, R.P. Oliver, P. Wincker, M.H. Balesdent, and B.J. Howlett. 2011. Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nature Communications. doi: 10.1038/ncomms1189.PubMedCentralPubMedGoogle Scholar
  48. Sethuraman, K., G. Ramakrishnan, and A. Balasubramanian. 1997. A leaf spot disease of Solanum elaeagnifolium caused by Helminthosporium solani. The Madras Agricultural Journal 84: 561.Google Scholar
  49. Simonis, J.L., H.A. Raja, and C.A. Shearer. 2008. Extracellular enzymes and soft rot decay: are ascomycetes important degraders in fresh water? Fungal Diversity 31: 135–146.Google Scholar
  50. Sin, M.K.W., K.D. Hyde, and S.B. Pointing. 2002. Comparative enzyme production by fungi from diverse lignocellulosic substrates. Journal of Microbiology 40: 241–244.Google Scholar
  51. Soanes, D.M., I. Alam, M. Cornell, H.M. Wong, C. Hedeler, N.W. Paton, M. Rattray, S.J. Hubbard, S.G. Oliver, and N.J. Talbot. 2008. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS One. doi: 10.1371/journal.pone.0002300.PubMedCentralPubMedGoogle Scholar
  52. Stergiopoulos, I., J. Collemare, R. Mehrabi, and P.J. De Wit. 2013. Phytotoxic secondary metabolites and peptides produced by plant pathogenic Dothideomycete fungi. FEMS Microbiology Reviews 37: 67–93.CrossRefPubMedGoogle Scholar
  53. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.PubMedCentralCrossRefPubMedGoogle Scholar
  54. Tao, T. 2010. Standalone BLAST Setup for Windows PC. [Updated 2012 Oct 10] In: BLAST® Help [Internet]. Bethesda: National Center for Biotechnology Information (US); 2008-. Available from: http://www.ncbi.nlm.nih.gov/books/NBK52637/.
  55. Thompson, J.D., D.G. Higgins, and T.J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.PubMedCentralCrossRefPubMedGoogle Scholar
  56. van den Brink, J., and R.P. de Vries. 2011. Fungal enzyme sets for plant polysaccharide degradation. Applied Microbiology and Biotechnology 91: 1477–1492.PubMedCentralCrossRefPubMedGoogle Scholar
  57. Vogel, J. 2008. Unique aspects of the grass cell wall. Current Opinion in Plant Biology 11: 301–307.CrossRefPubMedGoogle Scholar
  58. Wenzl, P., L. Wong, K. Kwang-won, and R.A. Jefferson. 2005. A functional screen identifies lateral transfer of β-glucuronidase (gus) from bacteria to fungi. Molecular Biology and Evolution 22: 308–316.CrossRefPubMedGoogle Scholar
  59. Zdobnov, E.M., and R. Apweiler. 2001. InterPro Scan- an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847–848.CrossRefPubMedGoogle Scholar
  60. Zhang, Y., C.L. Schoch, J. Fournier, P.W. Crous, J. de Gruyter, J.H. Woudenberg, K. Hirayama, K. Tanaka, S.B. Pointing, J.W. Spatafora, and K.D. Hyde. 2009. Multi-locus phylogeny of Pleosporales: a taxonomic, ecological and evolutionary re-evaluation. Studies in Mycology 64: 85–102.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Potato Association of America 2014

Authors and Affiliations

  • Chakradhar Mattupalli
    • 1
    • 3
  • Jeremy D. Glasner
    • 2
  • Amy O. Charkowski
    • 1
  1. 1.Department of Plant PathologyUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Biotechnology CenterUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.PhylloTech LLCMadisonUSA

Personalised recommendations