The genome of the saprophytic fungus Verticillium tricorpus reveals a complex effector repertoire resembling that of its pathogenic relatives

Molecular Plant-Microbe Interactions

Volumn 28, Issue 3, 2015, Pages 362-373

  Seidl, Michael F ^a   Faino, Luigi ^a   Shi Kunne, Xiaoqian ^a   Van Den Berg, Grardy C M ^a   Bolton, Melvin D ^b   Thomma, Bart P H J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; VERTICILLIUM DAHLIAE; VERTICILLIUM TRICORPUS;

COMPARATIVE STUDY; DNA SEQUENCE; FUNGAL GENOME; GENETICS; GENOMICS; KARYOTYPING; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT DISEASE; SEEDLING; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; TOMATO; VERTICILLIUM;

BASE SEQUENCE; GENOME, FUNGAL; GENOMICS; KARYOTYPING; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PLANT DISEASES; SEEDLING; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; VERTICILLIUM;

EID: 84923132280     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-14-0173-R     Document Type: Article

References (80)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Bolton, M. D., van Esse, H. P., Vossen, J. H., de Jonge, R., Stergiopoulos, I., Stulemeijer, I. J. E., van den Berg, G. C. M., Borrás-Hidalgo, O., Dekker, H. L., de Koster, C. G., de Wit, P. J. G. M., Joosten, M. H. A. J., and Thomma, B. P. H. J. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69:119-136.
4. Brown, N. A., Antoniw, J., and Hammond-Kosack, K. E. 2012. The predicted secretome of the plant pathogenic fungus Fusarium graminearum: A refined comparative analysis. PLoS ONE 7:e33731. Published online.
5. Choi, J., Park, J., Kim, D., Jung, K., Kang, S., and Lee, Y.-H. 2010. Fungal secretome database: Integrated platform for annotation of fungal secretomes. BMC Genomics 11:105.
6. Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J., Talon, M., and Robles, M. 2005. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-3676.
7. de Jonge, R., and Thomma, B. P. H. J. 2009. Fungal LysM effectors: Extinguishers of host immunity? Trends Microbiol. 17:151-157.
8. de Jonge, R., Peter van Esse, H., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., van der Krol, S., Shibuya, N., Joosten, M. H. A. J., and Thomma, B. P. H. J. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953-955.
9. de Jonge, R., Bolton, M. D., and Thomma, B. P. 2011. How filamentous pathogens co-opt plants: The ins and outs of fungal effectors. Curr. Opin. Plant Biol. 14:400-406.
10. de Jonge, R., Peter van Esse, H., Maruthachalam, K., Bolton, M. D., Santhanam, P., Saber, M. K., Zhang, Z., Usami, T., Lievens, B., Subbarao, K. V., and Thomma, B. P. H. J. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. U. S. A. 109:5110-5115.
11. de Jonge, R., Bolton, M. D., Kombrink, A., van den Berg, G. C. M., Yadeta, K. A., and Thomma, B. P. H. J. 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 23:1271-1282.
12. Dyrløv Bendtsen, J., Nielsen, H., Heijne, von, G., and Brunak, S. 2004. Improved prediction of signal peptides: SignalP 3. 0. J. Mol. Biol. 340:783-795.
13. Emanuelsson, O., Nielsen, H., Brunak, S., and Heijne, von, G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300:1005-1016.
14. Faino, L., and Thomma, B. P. H. J. 2014. Get your high-quality low-cost genome sequence. Trends Plant Sci. 19:288-291.
15. Felsenstein, J. 2002. PHYLIP (Phylogeny Inference Package) version 3. 6a3. Department of Genome Sciences, University of Washington, Seattle.
16. Fradin, E. F., and Thomma, B. P. H. J. 2006. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. alboatrum. Mol. Plant Pathol. 7:71-86.
17. Fradin, E. F., Zhang, Z., Juarez Ayala, J. C., Castroverde, C. D. M., Nazar, R. N., Robb, J., Liu, C.-M., and Thomma, B. P. H. J. 2009. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol. 150:320-332.
18. Fulnecková, J., Sevcíková, T., Fajkus, J., Lukesová, A., Lukes, M., Vlcek, C., Lang, B. F., Kim, E., Elias, M., and Sykorová, E. 2013. A broad phylogenetic survey unveils the diversity and evolution of telomeres in eukaryotes. Genome Biol Evol. 5:468-483.
19. Gaderer, R., Bonazza, K., and Seidl-Seiboth, V. 2014. Cerato-platanins: A fungal protein family with intriguing properties and application potential. Appl. Microbiol. Biotechnol. 98:4795-4803.
20. Gijzen, M., and Nürnberger, T. 2006. Nep1-like proteins from plant pathogens: Recruitment and diversification of the NPP1 domain across taxa. Phytochemistry. 67:1800-1807.
21. Gnerre, S., Maccallum, I., Przybylski, D., Ribeiro, F. J., Burton, J. N., Walker, B. J., Sharpe, T., Hall, G., Shea, T. P., Sykes, S., Berlin, A. M., Aird, D., Costello, M., Daza, R., Williams, L., Nicol, R., Gnirke, A., Nusbaum, C., Lander, E. S., and Jaffe, D. B. 2011. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl. Acad. Sci. U. S. A. 108:1513-1518.
22. Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., and Regev, A. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29:644-652.
23. Gurevich, A., Saveliev, V., Vyahhi, N., and Tesler, G. 2013. QUAST: Quality assessment tool for genome assemblies. Bioinformatics 29:1072-1075.
24. Guyon, K., Balagué, C., Roby, D., and Raffaele, S. 2014. Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum. BMC Genomics 15:336.
25. Haas, B. J., Delcher, A. L., Mount, S. M., Wortman, J. R., Smith, R. K., Hannick, L. I., Maiti, R., Ronning, C. M., Rusch, D. B., Town, C. D., Salzberg, S. L., and White, O. 2003. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31:5654-5666.
26. Holt, C., and Yandell, M. 2011. MAKER2: An annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12:491.
27. Horton, P., Park, K.-J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C. J., and Nakai, K. 2007. WoLF PSORT: Protein localization predictor. Nucleic Acids Res. 35:W585-7.
28. Inderbitzin, P., and Subbarao, K. V. 2014. Verticillium systematics and evolution: How confusion impedes verticillium wilt management and how to resolve it. Phytopathology 104:564-574.
29. Inderbitzin, P., Bostock, R. M., Davis, R. M., Usami, T., Platt, H. W., and Subbarao, K. V. 2011. Phylogenetics and taxonomy of the fungal vascular wilt pathogen Verticillium, with the descriptions of five new species. A. Idnurm, ed. PLoS ONE 6:e28341. Published online.
30. Isaac, I. 1956. Some soil factors affecting Verticillium wilt of antirrhinum. Annals of Applied Biology. 44:105-112.
31. Isaac, I. 1967. Speciation in Verticillium. Annu. Rev. Phytopathol. 5:201-222.
32. Jones, P., Binns, D., Chang, H.-Y., Fraser, M., Li, W., McAnulla, C., McWilliam, H., Maslen, J., Mitchell, A., Nuka, G., Pesseat, S., Quinn, A. F., Sangrador-Vegas, A., Scheremetjew, M., Yong, S.-Y., Lopez, R., and Hunter, S. 2014. InterProScan 5: Genome-scale protein function classification. Bioinformatics 30:1236-1240.
33. Jurka, J., Kapitonov, V. V., Pavlicek, A., Klonowski, P., Kohany, O., and Walichiewicz, J. 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110:462-467.
34. Katoh, K., Misawa, K., Kumar, S., and Miyata, T. 2002. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059-3066.
35. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., and Salzberg, S. L. 2013. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14:R36.
36. Klimes, A., Amyotte, S. G., Grant, S., Kang, S., and Dobinson, K. F. 2008. Microsclerotia development in Verticillium dahliae: Regulation and differential expression of the hydrophobin gene VDH1. Fungal Genet. Biol. 45:1525-1532.
37. Klosterman, S. J., Atallah, Z. K., Vallad, G. E., and Subbarao, K. V. 2009. Diversity, pathogenicity, and management of Verticillium species. Annu. Rev. Phytopathol. 47:39-62.
38. Klosterman, S. J., Subbarao, K. V., Kang, S., Veronese, P., Gold, S. E., Thomma, B. P. H. J., Chen, Z., Henrissat, B., Lee, Y.-H., Park, J., Garcia-Pedrajas, M. D., Barbara, D. J., Anchieta, A., de Jonge, R., Santhanam, P., Maruthachalam, K., Atallah, Z., Amyotte, S. G., Paz, Z., Inderbitzin, P., Hayes, R. J., Heiman, D. I., Young, S., Zeng, Q., Engels, R., Galagan, J., Cuomo, C. A., Dobinson, K. F., and Ma, L.-J. 2011. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. J. L. Dangl, ed. PLoS Pathog. 7:e1002137. Published online.
39. Kombrink, A. 2014. Functional analysis of LysM effectors secreted by fungal plant pathogens. PhD thesis. Wageningen University, The Netherlands.
40. Kombrink, A., and Thomma, B. P. H. J. 2013. LysM effectors: Secreted proteins supporting fungal life. PLoS Pathog. 9:e1003769. Published online.
41. Koren, S., Schatz, M. C., Walenz, B. P., Martin, J., Howard, J. T., Ganapathy, G., Wang, Z., Rasko, D. A., McCombie, W. R., Jarvis, E. D., and Adam M Phillippy. 2012. Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat. Biotechnol. 30:693-700.
42. Korf, I. 2004. Gene finding in novel genomes. BMC Bioinformatics 5:59.
43. Krogh, A., Larsson, B., Heijne, von, G., and Sonnhammer, E. L. 2001. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305:567-580.
44. Li, L., Stoeckert, C. J., and Roos, D. S. 2003. OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189.
45. Lukashin, A. V., and Borodovsky, M. 1998. GeneMark. hmm: New solutions for gene finding. Nucleic Acids Res. 26:1107-1115.
46. Marshall, R., Kombrink, A., Motteram, J., Loza-Reyes, E., Lucas, J., Hammond-Kosack, K. E., Thomma, B. P. H. J., and Rudd, J. J. 2011.
47. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol. 156:756-769.
48. Mehrabi, R., Taga, M., Aghaee, M., de Wit, P. J. G. M., and Kema, G. H. J. 2012. Karyotyping methods for fungi. Methods Mol. Biol. 835:591-602.
49. Mentlak, T. A., Kombrink, A., Shinya, T., Ryder, L. S., Otomo, I., Saitoh, H., Terauchi, R., Nishizawa, Y., Shibuya, N., Thomma, B. P. H. J., and Talbot, N. J. 2012. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24:322-335.
50. Metzker, M. L. 2010. Sequencing technologies-The next generation. Nat. Rev. Genet. 11:31-46.
51. Nguyen Ba, A. N., Pogoutse, A., Provart, N., and Moses, A. M. 2009. NLStradamus: A simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 10:202.
52. Parra, G., Bradnam, K., and Korf, I. 2007. CEGMA: A pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061-1067.
53. Parra, G., Bradnam, K., Ning, Z., Keane, T., and Korf, I. 2009. Assessing the gene space in draft genomes. Nucleic Acids Res. 37:289-297.
54. Petersen, T. N., Brunak, S., Heijne, von, G., and Nielsen, H. 2011. SignalP 4. 0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786.
55. Pignatelli, M., Serras, F., Moya, A., Guigó, R., and Corominas, M. 2009. CROC: Finding chromosomal clusters in eukaryotic genomes. Bioinformatics 25:1552-1553.
56. Powell, M., Gundersen, B., Miles, C., Coats, K., and Inglis, D. A. 2013. First report of Verticillium wilt on lettuce (Lactuca sativa) in Washington caused by Verticillium tricorpus. Plant Dis. 97:996-996.
57. Qin, Q. M., Qin, Q.-M., Vallad, G. E., Vallad, G. E., Subbarao, K. V., and Subbarao, K. V. 2008. Characterization of Verticillium dahliae and V. tricorpus isolates from lettuce and artichoke. Plant Dis. 92:69-77.
58. Raffaele, S., and Kamoun, S. 2012. Genome evolution in filamentous plant pathogens: Why bigger can be better. Nat. Rev. Microbiol. 10:417-430.
59. Raffaele, S., Farrer, R. A., Cano, L. M., Studholme, D. J., MacLean, D., Thines, M., Jiang, R. H. Y., Zody, M. C., Kunjeti, S. G., Donofrio, N. M., Meyers, B. C., Nusbaum, C., and Kamoun, S. 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330:1540-1543.
60. Rovenich, H., Boshoven, J. C., and Thomma, B. P. 2014. Filamentous pathogen effector functions: Of pathogens, hosts and microbiomes. Curr. Opin. Plant Biol. 20C:96-103.
61. Santhanam, P., van Esse, H. P., Albert, I., Faino, L., Nürnberger, T., and Thomma, B. P. H. J. 2013. Evidence for functional diversification within a fungal NEP1-like protein family. Mol. Plant-Microbe Interact. 26:278-286.
62. Saunders, D. G. O., Win, J., Cano, L. M., Szabo, L. J., Kamoun, S., and Raffaele, S. 2012. Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi. J. E. Stajich, ed. PLoS ONE 7:e29847. Published online.
63. Sánchez-Vallet, A., Saleem-Batcha, R., Kombrink, A., Hansen, G., Valkenburg, D.-J., Thomma, B. P., and Mesters, J. R. 2013. Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. Elife 2:e00790. Published online.
64. Schadt, E. E., Turner, S., and Kasarskis, A. 2010. A window into thirdgeneration sequencing. Hum. Mol. Genet. 19:R227-40.
65. Schulz, M. H., Zerbino, D. R., Vingron, M., and Birney, E. 2012. Oases: Robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28:1086-1092.
66. Seidl, M. F., and Thomma, B. P. H. J. 2014. Sex or no sex: Evolutionary adaptation occurs regardless. Bioessays 36:335-345.
67. Seidl, M. F., Van den Ackerveken, G., Govers, F., and Snel, B. 2011. A domain-centric analysis of oomycete plant pathogen genomes reveals unique protein organization. Plant Physiol. 155:628-644.
68. Smit, A. F. A., and Hubley, R. 2008. RepeatModeler Open-1. 0.
69. Smit, A. F. A., Hubley, R., and Green, P. 1996. RepeatMasker Open-3. 0.
70. Stamatakis, A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
71. Stamatakis, A., Hoover, P., and Rougemont, J. 2008. A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol. 57:758-771.
72. Stanke, M., Steinkamp, R., Waack, S., and Morgenstern, B. 2004. AUGUSTUS: A web server for gene finding in eukaryotes. Nucleic Acids Res. 32:W309-12.
73. Talbot, N. J., Ebbole, D. J., and Hamer, J. E. 1993. Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575-1590.
74. Thomma, B. P. H. J., Nurnberger, T., and Joosten, M. H. A. J. 2011. Of PAMPs and effectors: The blurred PTI-ETI dichotomy. Plant Cell 23:4-15.
75. Trapnell, C., Pachter, L., and Salzberg, S. L. 2009. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111.
76. Tritt, A., Eisen, J. A., Facciotti, M. T., and Darling, A. E. 2012. An integrated pipeline for de novo assembly of microbial genomes. PLoS ONE 7:e42304. Published online.
77. Wicker, T., Oberhaensli, S., Parlange, F., Buchmann, J. P., Shatalina, M., Roffler, S., Ben-David, R., Doležel, J., Simková, H., Schulze-Lefert, P., Spanu, P. D., Bruggmann, R., Amselem, J., Quesneville, H., Ver Loren van Themaat, E., Paape, T., Shimizu, K. K., and Keller, B. 2013. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nat. Genet. 45:1092-1096.
78. Yin, Y., Mao, X., Yang, J., Chen, X., Mao, F., and Xu, Y. 2012. dbCAN: A web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 40:W445-51.
79. Zdobnov, E. M., and Apweiler, R. 2001. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847-848.
80. Zhao, Z., Liu, H., Wang, C., and Xu, J.-R. 2013. Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 14:274.