The genome and transcriptome of the pine saprophyte Ophiostoma piceae, and a comparison with the bark beetle-associated pine pathogen Grosmannia clavigera

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Haridas, Sajeet ^a   Wang, Ye ^a   Lim, Lynette ^a   Massoumi Alamouti, Sepideh ^a   Jackman, Shaun ^b   Docking, Rod ^b   Robertson, Gordon ^b   Birol, Inanc ^b   Bohlmann, Jörg ^c   Breuil, Colette ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CANADA'S MICHAEL SMITH GENOME SCIENCES CENTRE   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Genome; Ophiostoma piceae; Saprobe; Transcriptome; Wood staining fungus

Indexed keywords

FATTY ACID; MANNOSE; TERPENE; TERPENE DERIVATIVE; TRANSCRIPTOME; TRIACYLGLYCEROL;

ARTICLE; BARK; CARBON SOURCE; CONTROLLED STUDY; ECOLOGICAL NICHE; EXON; FUNGAL GENOME; FUNGAL PLANT DISEASE; FUNGUS; FUNGUS GROWTH; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENOME SIZE; GROSMANNIA CLAVIGERA; MELANOGENESIS; MULTIGENE FAMILY; NONHUMAN; OPHIOSTOMA; OPHIOSTOMA PICEAE; PINE; PLANT DEFENSE; SAPROTROPH; UPREGULATION; WOOD;

ANIMALS; BEETLES; GENOME, FUNGAL; MANNOSE; MOLECULAR SEQUENCE ANNOTATION; OLEIC ACID; OPHIOSTOMA; PINUS; SPECIES SPECIFICITY; TRANSCRIPTOME; TRIGLYCERIDES; WOOD;

ASCOMYCOTA; CLAVIGERA; COLEOPTERA; CONIFEROPHYTA; FUNGI; OPHIOSTOMA PICEAE; PINUS MUGO; SCOLYTINAE;

EID: 84878370770     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-373     Document Type: Article

References (67)

1. Seifert K. Sapstain of commercial lumber by species of Ophiostoma and Ceratocystis. Ceratocystis and Ophiostoma: taxonomy, ecology, and pathogenicity 1993, 141-151. St Paul, Minnesota: APS Press, Wingfield M, Seifert K, Webber J.
2. Harrington TC. Diseases of conifers caused by species of Ophiostoma and Leptographium. Ceratocystis and Ophiostoma: taxonomy, ecology, and pathogenicity 1993, 161-172. St Paul, Minnesota: APS Press, Wingfield M, Seifert K, Webber J.
3. Münch E. Die bläufaule des nadelholzes. I-II. Naturwiss Z Forst-landw 1907, 5:531-573.
4. Upadhyay H. Classification of the Ophiostomatoid fungi. Ceratocystis and Ophiostoma: taxonomy, ecology, and pathogenicity 1993, 7-13. St Paul, Minnesota: APS Press, Wingfield M, Seifert K, Webber J.
5. Krokene P, Solheim H. Pathogenicity of four blue-stain fungi associated with aggressive and nonaggressive bark beetles. Phytopathology 1998, 88(1):39-44. 10.1094/PHYTO.1998.88.1.39, 18944997.
6. Uzunovic A, Yang D, Gagne P, Breuil C, Bernier L, Byrne A, Gignac M, Kim SH. Fungi that cause sapstain in Canadian softwoods. Can J Microbiol 1999, 45(11):914-922.
7. Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, Ebata T, Safranyik L. Mountain pine beetle and forest carbon feedback to climate change. Nature 2008, 452(7190):987-990. 10.1038/nature06777, 18432244.
8. DiGuistini S, Wang Y, Liao NY, Taylor G, Tanguay P, Feau N, Henrissat B, Chan SK, Hesse-Orce U, Alamouti SM, Tsui CKM, Docking RT, Levasseur A, Haridas S, Robertson G, Birol I, Holt RA, Marra MA, Hamelin RC, Hirst M, Jones SJM, Bohlmann J, Breuil C. Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proc Natl Acad Sci USA 2011, 108(6):2504-2509. 10.1073/pnas.1011289108, 3038703, 21262841.
9. Felsenstein J. Confidence-limits on phylogenies - an approach using the bootstrap. Evolution 1985, 39(4):783-791.
10. Harrington TC. Ecology and evolution of mycophagous bark beetles and their fungal partners. Ecology and Evolutionary Advances in Insect-Fungal Associations 2005, 251-291. United Kingdom: Oxford University Press, Vega F, Blackwell M.
11. Chung WH, Kim JJ, Yamaoka Y, Uzunovic A, Masuya H, Breuil C. Ophiostoma breviusculum sp. nov. (Ophiostomatales, Ascomycota) is a new species in the Ophiostoma piceae complex associated with bark beetles infesting larch in Japan. Mycologia 2006, 98(5):801-814. 10.3852/mycologia.98.5.801, 17256583.
12. DiGuistini S, Ralph SG, Lim YW, Holt R, Jones S, Bohlmann J, Breuil C. Generation and annotation of lodgepole pine and oleoresin-induced expressed sequences from the blue-stain fungus Ophiostoma clavigerum, a Mountain pine beetle-associated pathogen. FEMS Microbiol Lett 2007, 267(2):151-158. 10.1111/j.1574-6968.2006.00565.x, 17328114.
13. Fleet C, Breuil C, Uzunovic A. Nutrient consumption and pigmentation of deep and surface colonizing sapstaining fungi in Pinus contorta. Holzforschung 2001, 55(4):340-346.
14. Zabel R, Morrell J. Wood stains and discolorations. Wood Microbiology: decay and its prevention 1992, 326-343. San Diego, California: Academic Press, Inc, Zabel R, Morrell J.
15. Behrendt C, Blanchette R, Farrell R. Biological-control of blue-stain fungi in wood. Phytopathology 1995, 85(1):92-97.
16. Uzunovic A, Byrne T, Gignac M, Yang D. Microbial discolorations. Wood Discolorations and their Prevention; with an Emphasis on Bluestain 2008, 16-41. British Columbia: FPInnovations, Uzunovic A, Byrne T, Gignac M, Yang D, Special publication AP-50 ISSN#0824-2119.
17. Scheffer T. Microbiological degradation. Wood Deterioration and its Prevention by Preservative Treatments 1973, 31-106. NY: Syracuse University Press, Nicholas D.
18. Franceschi VR, Krokene P, Christiansen E, Krekling T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 2005, 167(2):353-375. 10.1111/j.1469-8137.2005.01436.x, 15998390.
19. Keeling CI, Bohlmann J. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 2006, 170(4):657-675. 10.1111/j.1469-8137.2006.01716.x, 16684230.
20. Bohlmann J. Pine terpenoid defences in the mountain pine beetle epidemic and in other conifer pest interactions: specialized enemies are eating holes into a diverse, dynamic and durable defence system. Tree Physiol 2012, 32(8):943-945. 10.1093/treephys/tps065, 22874830.
21. Wang Y, Lim L, DiGuistini S, Robertson G, Bohlmann J, Breuil C. A specialized ABC efflux transporter GcABC-G1 confers monoterpene resistance to Grosmannia clavigera, a bark beetle-associated fungal pathogen of pine trees. New Phytol 2013, 197(3):886-898. 10.1111/nph.12063, 23252416.
22. Clark EL, Carroll AL, Huber DPW. Differences in the constitutive terpene profile of lodgepole pine across a geographical range in British Columbia, and correlation with historical attack by mountain pine beetle. Can Entomol 2010, 142(6):557-573.
23. Turtola S, Manninen A, Holopainen J, Levula T, Raitio H, Kainulainen P. Secondary metabolite concentrations and terpene emissions of Scots pine xylem after long-term forest fertilization RID B-1656-2008. J Environ Qual 2002, 31(5):1694-1701. 10.2134/jeq2002.1694, 12371188.
24. Eberhardt TL, Sheridan PM, Mahfouz JM. Monoterpene persistence in the sapwood and heartwood of longleaf pine stumps: assessment of differences in composition and stability under field conditions. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 2009, 39(7):1357-1365.
25. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I. ABySS: a parallel assembler for short read sequence data. Genome Res 2009, 19(6):1117-1123. 10.1101/gr.089532.108, 2694472, 19251739.
26. Slater GS, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinforma 2005, 6:31.
27. Parra G, Bradnam K, Korf I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 2007, 23(9):1061-1067. 10.1093/bioinformatics/btm071, 17332020.
28. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29(7):644-652. 10.1038/nbt.1883, 3571712, 21572440.
29. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CP, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B, et al. The genome sequence of the filamentous fungus Neurospora crassa. Nature 2003, 422(6934):859-868. 10.1038/nature01554, 12712197.
30. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, Danchin EG, Grigoriev IV, Harris P, Jackson M, Kubicek CP, Han CS, Ho I, Larrondo LF, de Leon AL, Magnuson JK, Merino S, Misra M, Nelson B, Putnam N, Robbertse B, Salamov AA, Schmoll M, Terry A, Thayer N, Westerholm-Parvinen A, Schoch CL, Yao J, Barabote R, Nelson MA, Detter C, Bruce D, Kuske CR, Xie G, Richardson P, Rokhsar DS, Lucas SM, Rubin EM, Dunn-Coleman N, Ward M, Brettin TS, et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 2008, 26(5):553-560. 10.1038/nbt1403, 18454138.
31. Holt C, Yandell M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinforma 2011, 12:491.
32. Massoumi Alamouti S, Tsui CK, Breuil C. Multigene phylogeny of filamentous ambrosia fungi associated with ambrosia and bark beetles. Mycol Res 2009, 113(Pt 8):822-835.
33. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, Condon BJ, Copeland AC, Dhillon B, Glaser F, Hesse CN, Kosti I, LaButti K, Lindquist EA, Lucas S, Salamov AA, Bradshaw RE, Ciuffetti L, Hamelin RC, Kema GHJ, Lawrence C, Scott JA, Spatafora JW, Turgeon BG, de Wit PJGM, Zhong S, Goodwin SB, Grigoriev IV. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen dothideomycetes fungi. PLoS Pathog 2012, 8(12):e1003037. 10.1371/journal.ppat.1003037, 3516569, 23236275.
34. Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH, Fedorova ND. SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol 2010, 47(9):736-741. 10.1016/j.fgb.2010.06.003, 2916752, 20554054.
35. Lah L, Haridas S, Bohlmann J, Breuil C. The cytochromes P450 of Grosmannia clavigera: Genome organization, phylogeny, and expression in response to pine host chemicals. Fungal Genet Biol 2013, 50:72-81.
36. Butler MJ, Day AW. Fungal melanins: a review. Can J Microbiol 1998, 44(12):1115-1136.
37. Wang H, Breuil C. A second reductase gene involved in melanin biosynthesis in the sap-staining fungus Ophiostoma floccosum. Mol Genet Genomics 2002, 267(5):557-563. 10.1007/s00438-002-0694-1, 12172794.
38. Loppnau P, Tanguay P, Breuil C. Isolation and disruption of the melanin pathway polyketide synthase gene of the softwood deep stain fungus Ceratocystis resinifera. Fungal Genet Biol 2004, 41(1):33-41. 10.1016/j.fgb.2003.08.008, 14643257.
39. Brasier C. The genetic system as a fungal taxonomic tool: gene flow, molecular variation and sibling species in the " Ophiostoma piceae - Ophiostoma ulmi" complex and its taxonomic and ecological significance. Ceratocystis and Ophiostoma: taxonomy, ecology, and pathogenicity 1993, 77-92. St Paul, Minnesota: APS Press, Wingfield M, Seifert K, Webber J.
40. Tsui CK, Diguistini S, Wang Y, Feau N, Dhillon B, Bohlmann J, Hamelin RC. Unequal recombination and evolution of the Mating-Type (MAT) loci in the pathogenic fungus Grosmannia clavigera and relatives. G3 (Bethesda, Md.) 2013, 3(3):465-480.
41. Gao Y, Breuil C, Chen T. Utilization of triglycerides, fatty acids and resin acids in lodgepole pine wood by a sapstaining fungus O. piceae. Material und Organismen 1994, 28:105-118.
42. MacPherson S, Larochelle M, Turcotte B. A fungal family of transcriptional regulators: The zinc cluster proteins. Microbiol Mol Biol Rev 2006, 70(3):583-+. 1594591, 16959962.
43. Asch DK, Orejas M, Geever RF, Case ME. Comparative studies of the quinic acid (qa) cluster in several Neurospora species with special emphasis on the qa-x-qa-2 intergenic region. Mol Gen Genet 1991, 230(3):337-344. 10.1007/BF00280289, 1685010.
44. Giles NH, Geever RF, Asch DK, Avalos J, Case ME. The Wilhelmine E. Key 1989 invitational lecture. Organization and regulation of the qa (quinic acid) genes in Neurospora crassa and other fungi. J Hered 1991, 82(1):1-7. 10.1093/jhered/82.1.1, 1825499.
45. Schirp A, Farrell R, Kreber B, Singh A. Advances in understanding the ability of sapstaining fungi to produce cell wall-degrading enzymes. Wood Fiber Sci 2003, 35(3):434-444.
46. Yu J, Keller N. Regulation of secondary metabolism in filamentous fungi. Annu Rev Phytopathol 2005, 43:437-458. 10.1146/annurev.phyto.43.040204.140214, 16078891.
47. Wang Y, DiGuistini S, Wang TCT, Bohlmann J, Breuil C. Agrobacterium-meditated gene disruption using split-marker in Grosmannia clavigera, a mountain pine beetle associated pathogen. Curr Genet 2010, 56(3):297-307. 10.1007/s00294-010-0294-2, 20229292.
48. Fischer C, Holl W. Food Reserves of Scots Pine (Pinus-Sylvestris L) .2. Seasonal-Changes and Radial-Distribution of Carbohydrate and Fat Reserves in Pine Wood. Trees-Structure and Function 1992, 6(3):147-155.
49. Gao Y, Breuil C. Extracellular Lipase Production by a Sapwood-Staining Fungus, Ophiostoma-Piceae. World J Microbiol Biotechnol 1995, 11(6):638-642.
50. Coleman JJ, Mylonakis E. Efflux in fungi: La piece de resistance. PLoS Pathog 2009, 5(6):e1000486. 10.1371/journal.ppat.1000486, 2695561, 19557154.
51. Abraham L, Hoffman B, Gao Y, Breuil C. Action of Ophiostoma piceae proteinase and lipase on wood nutrients. Can J Microbiol 1998, 44(7):698-701.
52. Breuil C, Yagodnik C, ABRAHAM L. Staining fungi growing in softwood produce proteinases and aminopeptidases. Material Und Organismen 1995, 29(1):15-25.
53. Abreu C, Sanguinetti M, Amillis S, Ramon A. UreA, the major urea/H + symporter in Aspergillus nidulans. Fungal Genet Biol 2010, 47(12):1023-1033. 10.1016/j.fgb.2010.07.004, 20633690.
54. Abraham L, Breuil C, Bradshaw D, Morris P, Byrne T. Proteinases as potential targets for new generation anti-sapstain chemicals. For Prod J 1997, 47(9):57-62.
55. Raffa K, Smalley E. Interaction of Pre-Attack and Induced Monoterpene Concentrations in Host Conifer Defense Against Bark Beetle Fungal Complexes. Oecologia 1995, 102(3):285-295.
56. Haridas S, Gantt JS. The mitochondrial genome of the wood-degrading basidiomycete Trametes cingulata. FEMS Microbiol Lett 2010, 308(1):29-34. 10.1111/j.1574-6968.2010.01979.x, 20455947.
57. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. Versatile and open software for comparing large genomes. Genome Biol 2004, 5(2):R12. 10.1186/gb-2004-5-2-r12, 395750, 14759262.
58. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 2011, 27(6):863-864. 10.1093/bioinformatics/btr026, 3051327, 21278185.
59. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012, 7(3):562-578. 10.1038/nprot.2012.016, 3334321, 22383036.
60. Korf I. Gene finding in novel genomes. BMC Bioinforma 2004, 5:59.
61. Stanke M, Waack S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 2003, 19(Suppl 2):ii215-ii225. 10.1093/bioinformatics/btg1080, 14534192.
62. Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res 2008, 18(12):1979-1990. 10.1101/gr.081612.108, 2593577, 18757608.
63. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21(18):3674-3676. 10.1093/bioinformatics/bti610, 16081474.
64. Pavesi A, Conterio F, Bolchi A, Dieci G, Ottonello S. Identification of new eukaryotic tRNA genes in genomic DNA databases by a multistep weight matrix analysis of transcriptional control regions. Nucleic Acids Res 1994, 22(7):1247-1256. 10.1093/nar/22.7.1247, 523650, 8165140.
65. McInerney JO. GCUA: general codon usage analysis. Bioinformatics 1998, 14(4):372-373. 10.1093/bioinformatics/14.4.372, 9632833.
66. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 2000, 300(4):1005-1016. 10.1006/jmbi.2000.3903, 10891285.
67. Kall L, Krogh A, Sonnhammer EL. Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server. Nucleic Acids Res 2007, 35:W429-W432. 10.1093/nar/gkm256, 1933244, 17483518.