A gapless genome sequence of the fungus Botrytis cinerea

Molecular Plant Pathology

Volumn 18, Issue 1, 2017, Pages 75-89

  Van Kan, Jan A L ^a   Stassen, Joost H M ^a,i   Mosbach, Andreas ^b   Van Der Lee, Theo A J ^a   Faino, Luigi ^a   Farmer, Andrew D ^c,d   Papasotiriou, Dimitrios G ^e   Zhou, Shiguo ^f   Seidl, Michael F ^a   Cottam, Eleanor ^g   Edel, Dominique ^b   Hahn, Matthias ^h   Schwartz, David C ^f   Dietrich, Robert A ^d   Widdison, Stephanie ^g   Scalliet, Gabriel ^b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b SYNGENTA CROP PROTECTION AG   (Switzerland)

^c NATIONAL CENTER FOR GENOME RESOURCES   (United States)

^d SYNGENTA BIOTECHNOLOGY INC   (United States)

^e JEALOTT S HILL INTERNATIONAL RESEARCH CENTRE   (United Kingdom)

^f UNIVERSITY OF WISCONSIN MADISON   (United States)

^g Jealott's Hill International Research Centre   (United Kingdom)

^h Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

ⁱ UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

genetic map; grey mould; optical map; SMRT sequencing

Indexed keywords

FUNGICIDE; PROTEOME;

ANTIFUNGAL RESISTANCE; BASE PAIRING; BOTRYTIS; CHROMOSOMAL MAPPING; CHROMOSOME; CYTOLOGY; DNA SEQUENCE; DRUG EFFECTS; FUNGAL GENE; FUNGAL GENOME; GENE LOCUS; GENETIC LINKAGE; GENETIC RECOMBINATION; GENETICS; MEIOSIS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPTOGENETICS; PROTEOMICS; REPRODUCIBILITY; SINGLE NUCLEOTIDE POLYMORPHISM;

BASE PAIRING; BASE SEQUENCE; BOTRYTIS; CHROMOSOME MAPPING; CHROMOSOMES, FUNGAL; DRUG RESISTANCE, FUNGAL; EVOLUTION, MOLECULAR; FUNGICIDES, INDUSTRIAL; GENES, FUNGAL; GENETIC LINKAGE; GENETIC LOCI; GENOME, FUNGAL; MEIOSIS; MOLECULAR SEQUENCE ANNOTATION; OPEN READING FRAMES; OPTOGENETICS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEOME; PROTEOMICS; RECOMBINATION, GENETIC; REPRODUCIBILITY OF RESULTS; SEQUENCE ANALYSIS, DNA;

EID: 84976911414     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12384     Document Type: Article

References (66)

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. Amselem, J., Cuomo, C.A., van Kan, J.A.L., Viaud, M., Benito, E.P., Couloux, A., Coutinho, P.M., de Vries, R.P., Dyer, P.S., Fillinger, S., Fournier, E., Gout, L., Hahn, M., Kohn, L., Lapalu, N., Plummer, K.M., Pradier, J.-M., Quévillon, E., Sharon, A., Simon, A., ten Have, A., Tudzynski, B., Tudzynski, P., Wincker, P., Andrew, M., Anthouard, V., Beever, R.E., Beffa, R., Benoit, I., Bouzid, O., Brault, B., Chen, Z., Choquer, M., Collémare, J., Cotton, P., Danchin, E.G., Da Silva, C., Gautier, A., Giraud, C., Giraud, T., Gonzalez, C., Grossetete, S., Güldener, U., Henrissat, B., Howlett, B.J., Kodira, C., Kretschmer, M., Lappartient, A., Leroch, M., Levis, C., Mauceli, E., Neuvéglise, C., Oeser, B., Pearson, M., Poulain, J., Poussereau, N., Quesneville, H., Rascle, C., Schumacher, J., Ségurens, B., Sexton, A., Silva, E., Sirven, C., Soanes, D.M., Talbot, N.J., Templeton, M., Yandava, C., Yarden, O., Zeng, Q., Rollins, J.A., Lebrun, M.-H. and Dickman, M. (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7, e1002230.
3. Amselem, J., Lebrun M.-H. and Quesneville, H. (2015) Whole genome comparative analysis of transposable elements provides new insight into mechanisms of their inactivation in fungal genomes. BMC Genomics, 16, 141.
4. Antal, Z., Rascle, C., Cimerman, A., Viaud, M., Billon-Grand, G., Choquer, M. and Bruel, C. (2012) The Homeobox BcHOX8 gene in Botrytis cinerea regulates vegetative growth and morphology. PLoS One, 7, e48134.
5. Arazoe, T., Miyoshi, K., Yamato, T., Ogawa, T., Ohsato, S., Arie, T. and Kuwata, S. (2015) Tailor-made CRISPR/Cas system for highly efficient targeted gene replacement in the rice blast fungus. Biotechnol. Bioeng. 112, 2543–2549.
6. Canessa, P., Schumacher, J., Hevia, M.A., Tudzynski, P. and Larrondo, L.F. (2013) Assessing the effects of light on differentiation and virulence of the plant pathogen Botrytis cinerea: characterization of the White Collar complex. PLoS One, 8, e84223.
7. Chin, C.S., Alexander, D.H., Marks, P., Klammer, A.A., Drake, J., Heiner, C., Clum, A., Copeland, A., Huddleston, J., Eichler, E.E., Turner, S.W. and Korlach, J. (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods, 10, 563–569.
8. Coleman, J.J., Rounsley, S.D., Rodriguez-Carres, M., Kuo, A., Wasmann, C.C., Grimwood, J., Schmutz, J., Taga, M., White, G.J., Zhou, S., Schwartz, D.C., Freitag, M., Ma, L.-J., Danchin, E.G.J., Henrissat, B., Coutinho, P.M., Nelson, D.R., Straney, D., Napoli, C.A., Barker, B.M., Gribskov, M., Rep, M., Kroken, S., Molnár, I., Rensing, C., Kennell, J.C., Zamora, J., Farman, M.L., Selker, E.U., Salamov, A., Shapiro, H., Pangilinan, J., Lindquist, E., Lamers, C., Grigoriev, I.V., Geiser, D.M., Covert, S.F., Temporini, E., and VanEtten, H.D. (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet., 5, e1000618.
9. Croll, D., Lendenmann, M.H., Stewart, E. and McDonald, B.A. (2015) The impact of recombination hotspots on genome evolution of a fungal plant pathogen. Genetics, 201, 1213–1228.
10. Dalmais, B., Schumacher, J., Moraga, J., Le Pecheur, P., Tudzynski, B., Collado, I.G. and Viaud, M. (2011) The Botrytis cinerea phytotoxin botcinic acid requires two polyketide synthases for production and has a redundant role in virulence with botrydial. Mol. Plant Pathol. 12, 564–579.
11. Dean, R., van Kan, J.A.L., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D., Rudd, J.J., Dickman, M., Kahmann, R. and Ellis, J. (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13, 414–430.
12. Dimalanta, E.T., Lim, A., Runnheim, R., Lamers, C., Churas, C., Forrest, D.K., de Pablo, J.J., Graham, M.D., Coppersmith, S.N., Goldstein, S. and Schwartz, D.C. (2004) A microfluidic system for large DNA molecule arrays. Anal. Chem. 76, 5293–5301.
13. Elad, Y., Pertot, I., Cotes Prado, A.M. and Stewart, A. (2015) Plant hosts of Botrytis spp. In: Botrytis – The Fungus, the Pathogen and its Management in Agricultural Systems (Fillinger, S. and Elad, Y., eds.), pp. 413–486. Berlin: Springer.
14. English, A.C., Richards, S., Han, Y., Wang, M., Vee, V., Qu, J., Qin, X., Muzny, D.M., Reid, J.G., Worley, K.C. and Gibbs, R.A. (2012) Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology. PLoS One, 7, e47768.
15. Faino, L., Seidl, M.F., Datema, E., van den Berg, G.C.M., Janssen, A., Wittenberg, A.H.J. and Thomma, B.P.H.J. (2015) Single-Molecule Real-Time sequencing combined with optical mapping yields completely finished fungal genome. mBio, 6, e00936–15.
16. Faretra, F., Antonacci, E. and Pollastro, S. (1988) Sexual behavior and mating system of Botryotinia fuckeliana, teleomorph of Botrytis cinerea. J. Gen. Microbiol. 134, 2543–2550.
17. Finkers, R., van Heusden, A.W., Meijer-Dekens, F., van Kan, J.A.L., Maris, P. and Lindhout, P. (2007) The construction of a Solanum habrochaites LYC4 introgression line population and the identification of QTLs for resistance to Botrytis cinerea. Theor. Appl. Genet. 114, 1071–1080.
18. Ganley, A.R.D. and Kobayashi, T. (2007) Highly efficient concerted evolution in the ribosomal DNA repeats: total rDNA repeat variation revealed by whole-genome shotgun sequence data. Genome Res. 17, 184–191.
19. 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. USA, 108, 1513–1518.
20. Gonzalez, M., Brito, N., Frias, M. and Gonzalez, C. (2013) Botrytis cinerea protein O-mannosyltransferases play critical roles in morphogenesis, growth, and virulence. PLoS One, 8, e65924.
21. 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., Regev, A. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652.
22. Gronover, C.S., Schumacher, J., Hantsch, P. and Tudzynski, B. (2005) A novel seven-helix transmembrane protein BTP1 of Botrytis cinerea controls the expression of GST-encoding genes, but is not essential for pathogenicity. Mol. Plant Pathol. 6, 243–256.
23. 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., White, O. (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654–5666.
24. Haas, B.J., Salzberg, S.L., Zhu, W., Pertea, M., Allen, J.E., Orvis, J., White, O., Buell, C.R., Wortman, J.R. (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, R7.
25. Hahn, M. (2014) The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. J. Chem. Biol. 7, 133–141.
26. Huang, X.Q. and Madan, A. (1999) CAP3: a DNA sequence assembly program. Genome Res. 9, 868–877.
27. van Kan, J.A.L. (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 11, 247–253.
28. van Kan, J.A.L., Goverse, A. and van der Vlugt-Bergmans, C.J.B. (1993) Electrophoretic karyotype analysis of Botrytis cinerea. Neth. J. Plant Pathol. 99, 119–128.
29. van Kan, J.A.L., van't Klooster, J.W., Dees, D.C.T., Wagemakers, C.A.M. and van der Vlugt-Bergmans, C.J.B. (1997) Cutinase A of Botrytis cinerea is expressed, but not essential, during penetration of gerbera and tomato. Mol. Plant–Microbe Interact. 10, 30–38.
30. van Kan, J.A.L., Shaw, M.A. and Grant-Downton, R.T. (2014) Botrytis species: relentless necrotrophic thugs or endophytes gone rogue? Mol. Plant Pathol. 15, 957–961.
31. Korf, I. (2004) Gene finding in novel genomes. BMC Bioinformatics, 5, 59.
32. Leroch, M., Plesken, C., Weber, R.W.S., Kauff, F., Scalliet, G. and Hahn, M. (2013) Gray mold populations in German strawberry fields are resistant to multiple fungicides and dominated by a novel clade closely related to Botrytis cinerea. Appl. Environ. Microbiol. 79, 159–167.
33. Leroux, P., Fritz, R., Debieu, D., Albertini, C., Lanen, C., Bach, J., Gredt, M. and Chapeland, F. (2002) Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Manag. Sci. 58, 876–888.
34. Leroux, P., Gredt, M., Leroch, M. and Walker, A.S. (2010) Exploring mechanisms of resistance to respiratory inhibitors in field strains of Botrytis cinerea, the causal agent of gray mold. Appl. Environ. Microbiol. 76, 6615–6630.
35. Ma, L.J., van der Does, H.C., Borkovich, K.A., Coleman, J.J., Daboussi, M.J., Di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B., Houterman, P.M., Kang, S., Shim, W.B., Woloshuk, C., Xie, X., Xu, J.R., Antoniw, J., Baker, S.E., Bluhm, B.H., Breakspear, A., Brown, D.W., Butchko, R.A., Chapman, S., Coulson, R., Coutinho, P.M., Danchin, E.G., Diener, A., Gale, L.R., Gardiner, D.M., Goff, S., Hammond-Kosack, K.E., Hilburn, K., Hua-Van, A., Jonkers, W., Kazan, K., Kodira, C.D., Koehrsen, M., Kumar, L., Lee, Y.H., Li, L., Manners, J.M., Miranda-Saavedra, D., Mukherjee, M., Park, G., Park, J., Park, S.Y., Proctor, R.H., Regev, A., Ruiz-Roldan, M.C., Sain, D., Sakthikumar, S., Sykes, S., Schwartz, D.C., Turgeon, B.G., Wapinski, I., Yoder, O., Young, S., Zeng, Q., Zhou, S., Galagan, J., Cuomo, C.A., Kistler, H.C., and Rep, M. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature, 464, 367–373.
36. Nødvig, C.S., Nielsen, J.B., Kogle, M.E. and Mortensen, U.H. (2015) A CRISPR-Cas9 system for genetic engineering of filamentous fungi. PLoS One, 10, e0133085.
37. Pinedo, C., Wang, C.M., Pradier, J.-M., Dalmais, B., Choquer, M., Le Pecheur, P., Morgant, G., Collado, I.G., Cane, D.E. and Viaud, M. (2008) Sesquiterpene synthase from the botrydial biosynthetic gene cluster of the phytopathogen Botrytis cinerea. ACS Chem. Biol. 3, 791–801.
38. Parra, G., Bradnam, K. and Korf, I. (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics, 23:1061–1067.
39. Ribeiro, F.J., Przybylski, D., Yin, S.Y., Sharpe, T., Gnerre, S., Abouelleil, A., Berlin, A.M., Montmayeur, A., Shea, T.P., Walker, B.J., Young, S.K., Russ, C., Nusbaum, C., MacCallum, I. and Jaffe, D.B. (2012) Finished bacterial genomes from shotgun sequence data. Genome Res. 22, 2270–2277.
40. Rui, O. and Hahn, M. (2007) The Slt2-type MAP kinase Bmp3 of Botrytis cinerea is required for normal saprotrophic growth, conidiation, plant surface sensing and host tissue colonization. Mol. Plant Pathol. 8, 173–184.
41. Schumacher, J., Simon, A., Cohrs, K.C., Viaud, M. and Tudzynski, P. (2014) The transcription factor BcLTF1 regulates virulence and light responses in the necrotrophic plant pathogen Botrytis cinerea. PLoS Genet. 10, e1004040.
42. Schwartz, D.C. and Cantor, C.R. (1984) Separation of yeast chromosome-sized DNAs by pulsed-field gradient gel-electrophoresis. Cell, 37, 67–75.
43. Seidl, M.F., Faino, L., Shi-Kunne, X., van den Berg, G.C.M., Bolton, M.D. and Thomma, B.P.H.J. (2015) The genome of the saprophytic fungus Verticillium tricorpus reveals a complex effector repertoire resembling that of its pathogenic relatives. Mol. Plant–Microbe Interact. 28, 362–373.
44. Shirane, N., Masuka, M. and Hayashi, Y. (1989) Light microscopic observation of nuclei and mitotic chromosomes of Botrytis species. Phytopathology, 79, 728–730.
45. 2 transcription factor involved in the regulation of secondary metabolism gene clusters. Fung. Genet. Biol. 52, 9–19.
46. Smith, K.M., Galazka, J.M., Phatale, P.A., Connolly, L.R. and Freitag, M. (2012) Centromeres of filamentous fungi. Chromosome Res. 20, 635–656.
47. Sowley, E.N.K., Dewey, F.M. and Shaw, M.W. (2009) Persistent, symptomless, systemic, and seed-borne infection of lettuce by Botrytis cinerea. Eur. J. Plant Pathol. 126, 61–71.
48. Spatafora, J., Stajich, J. and Grigoriev, I. (2013) 1000 Fungal Genomes project. Phytopathology, 103, 137.
49. Staats, M. and van Kan, J.A.L. (2012) Genome update of Botrytis cinerea strains B05.10 and T4. Eukaryotic Cell, 11, 1413–1414.
50. Stanke, M., Keller, O., Gunduz, I., Hayes, A., Waack, S. and Morgenstern, B. (2006) AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435–W439.
51. Stefanato, F.L., Abou-Mansour, E., Buchala, A., Kretschmer, M., Mosbach, A., Hahn, M., Bochet, C.G., Metraux, J.P. and Schoonbeek, H.-J. (2009) The ABC transporter BcatrB from Botrytis cinerea exports camalexin and is a virulence factor on Arabidopsis thaliana. Plant J. 58, 499–510.
52. Teague, B., Waterman, M.S., Goldstein, S., Potamousis, K., Zhou, S., Reslewic, S., Sarkar, D., Valouev, A., Churas, C., Kidd, J.M., Kohn, S., Runnhein, R., Lamers, C., Forrest, D., Newton, M.A., Eichler, E.E., Kent-First, M., Surti, U., Livny, M., and Schwartz, D.C. (2010) High-resolution human genome structure by single molecule analysis. Proc. Natl. Acad. Sci. USA, 107, 10 848–10 853.
53. Terhem, R.B. (2015) Sexual development of Botrytis species. PhD Thesis, Wageningen University.
54. Ter-Hovhannisyan, V., Lomsadze, A., Chernoff, Y.O. and Borodovsky, M. (2008) Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 18, 1979–1990.
55. Thomma, B.P.H.J., Seidl, M.F., Shi-Kunne, X., Cook, D., Bolton, M.D., van Kan, J.A.L. and Faino, L. (2016) Mind the gap; seven reasons to close fragmented genome assemblies. Fung. Genet. Biol. 90, 24–30.
56. Turrion-Gomez, J.L., Eslava, A.P. and Benito, E.P. (2010) The flavohemoglobin BCFHG1 is the main NO detoxification system and confers protection against nitrosative conditions but is not a virulence factor in the fungal necrotroph Botrytis cinerea. Fung. Genet. Biol. 47, 484–496.
57. Valouev, A., Schwartz, D., Zhou, S. and Waterman, M.S. (2006a) An algorithm for assembly of ordered restriction maps from single DNA molecules. Proc. Natl. Acad. Sci. USA, 103, 15 770–15 775.
58. Valouev, A., Zhang, Y., Schwartz, D.C. and Waterman, M.S. (2006b) Refinement of optical map assemblies. Bioinformatics, 22, 1217–1224.
59. Valouev, A., Li, L., Liu, Y., Schwartz, D.C., Yang, Y., Zhang, Y. and Waterman, M.S. (2006c) Alignment of optical maps. J. Comput. Biol. 13, 442–446.
60. Viefhues, A., Heller, J., Temme, N. and Tudzynski, P. (2014) Redox systems in Botrytis cinerea: impact on development and virulence. Mol. Plant–Microbe Interact. 27, 858–874.
61. Wang, Z. and Sachs, M.S. (1996) Ribosome stalling is responsible for arginine-specific translational attenuation in Neurospora crassa. Mol. Cell. Biol. 17, 4904–4913.
62. Wang, Z., Fang, P. and Sachs, M.S. (1998) The evolutionarily conserved eukaryotic arginine attenuator peptide regulates the movement of ribosomes that have translated it. Mol. Cell. Biol. 18, 7528–7536.
63. Wang, Z., Gaba, A. and Sachs, M.S. (1999) A highly conserved mechanism of regulated ribosome stalling mediated by fungal arginine attenuator peptides that appears independent of the charging status of arginyl-tRNAs. J. Biol. Chem. 274, 37 565–37 574.
64. Weiberg, A., Wang, M., Lin, F.M., Zhao, H.W., Zhang, Z.H., Kaloshian, I., Huang H.D. and Jin, H.L. (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science, 342, 118–123.
65. Williamson, B., Tudzynski, B., Tudzynski, P. and van Kan, J.A.L. (2007) Botrytis cinerea: the cause of grey mould disease. Mol. Plant Pathol. 8, 561–580.
66. Zhou, S., Herschleb, J., and Schwartz, D.C. (2007) A single molecule system for whole genome analysis. In: New High Throughput Technologies for DNA Sequencing and Genomics, Vol. 2 (Mitchelson, K.R., ed), pp. 265–300. Amsterdam: Elsevier Scientific Publishers.