RNA-seq analyses of gene expression in the microsclerotia of Verticillium dahliae

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Duressa, Dechassa ^a   Anchieta, Amy ^a   Chen, Dongquan ^b   Klimes, Anna ^c,d,e   Garcia Pedrajas, Maria D ^f   Dobinson, Katherine F ^c,d   Klosterman, Steven J ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

^d AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^e WESTERN NEW ENGLAND UNIVERSITY   (United States)

^f INSTITUTO DE HORTOFRUTICULTURA SUBTROPICAL Y MEDITERRÁNEA LA MAYORA   (Spain)

Author keywords

Gene expression; Microsclerotia; Morphogenesis; RNA seq; Verticillium dahliae

Indexed keywords

ARTICLE; BIOGENESIS; CELL GROWTH; CONTROLLED STUDY; FUNGAL CELL; FUNGAL GENE; FUNGAL STRAIN; FUNGAL STRUCTURES; FUNGUS CULTURE; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCATION; MELANOGENESIS; MICROARRAY ANALYSIS; MICROSCLEROTIA; MORPHOGENESIS; NONHUMAN; NORTHERN BLOTTING; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SCYTALONE DEHYDRATASE GENE; SEQUENCE ANALYSIS; TETRAHYDROXYNAPHTHALENE REDUCTASE GENE; VERTICILLIUM DAHLIAE;

FUNGI; VERTICILLIUM DAHLIAE;

COMPUTATIONAL BIOLOGY; DATA MINING; GENE EXPRESSION REGULATION, FUNGAL; GENE LIBRARY; GENES, FUNGAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, FUNGAL; SEQUENCE ANALYSIS, RNA; VERTICILLIUM;

EID: 84883550378     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-607     Document Type: Article

References (59)

1. Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV. Diversity, pathogenicity, and management of Verticillium species. Ann Rev Phytopathol 2009, 47:39-62.
2. Pegg GF, Brady BL. Verticillium Wilts 2002, Wallingford: CABI Publishing.
3. Wilhelm S. Longevity of the Verticillium wilt fungus in the laboratory and field. Phytopathology 1955, 45:180-181.
4. Schreiber LR, Green RJ. Effect of root exudates on germination of conidia and microsclerotia of Verticillium albo-atrum inhibited by the soil fungistatic principle. Phytopathology 1963, 53:260-264.
5. Fitzell R, Evans G, Fahy PC. Studies on the colonization of plant roots by Verticillium dahliae Klebahn with use of immunofluorescent staining. Austr J Bot 1980, 28:357-368.
6. Butler MJ, Day AW. Fungal melanins: a review. Can J Microbiol 1998, 44:1115-1136.
7. Wheeler MH. Comparisons of fungal melanin biosynthesis in ascomycetous, imperfect and basidiomycetous fungi. Trans Br Mycological Soc 1983, 81:29-36.
8. Bell AA, Wheeler MH. Biosynthesis and functions of fungal melanins. Ann Rev Phytopathol 1986, 24:411-451.
9. Bell AA, Puhalla JE, Tolmsoff WJ, Stipanovic RD. Use of mutants to establish (+)-scytalone as an intermediate in melanin biosynthesis by Verticillium dahliae. Can J Microbiol 1976, 22:787-799. 10.1139/m76-115, 945120.
10. Gordee RS, Porter CL. Structure, germination and physiology of microsclerotia of Verticillium albo-atrum. Mycologia 1961, 53:171-182.
11. Debode J, Maeyer KD, Perneel M, Pannecoucque J, Backer GD, Höfte M. Biosurfactants are involved in the biological control of Verticillium microsclerotia by Pseudomonas spp. J Appl Microbiol 2007, 103:1184-1196. 10.1111/j.1365-2672.2007.03348.x, 17897223.
12. Hawke MA, Lazarovits G. Production and manipulation of individual microsclerotia of Verticillium dahliae for use in studies of survival. Phytopathology 1994, 84:883-890.
13. Coley-Smith JR, Cooke RC. Survival and germination of fungal sclerotia. Ann Rev Phytopathol 1971, 9:65-92.
14. Gao F, Zhou B-J, Li G-Y, Jia P-S, Li H, Zhao Y-L, Zhao P, Xia G-X, Guo H-S. A glutamic acid-rich protein identified in Verticillium dahliae from an insertional mutagenesis affects microsclerotial formation and pathogenicity. PLoS ONE 2010, 5:e15319. 10.1371/journal.pone.0015319, 2998422, 21151869.
15. Maruthachalam K, Klosterman SJ, Kang S, Hayes RJ, Subbarao KV. Identification of pathogenicity-related genes in the vascular wilt fungus Verticillium dahliae by Agrobacterium tumefaciens-mediated T-DNA insertional mutagenesis. Mol Biotechnol 2011, 49:209-221. 10.1007/s12033-011-9392-8, 3183274, 21424547.
16. Tzima AK, Paplomatas EJ, Rauyaree P, Kang S. Roles of the catalytic subunit of cAMP-dependent protein kinase A in virulence and development of the soilborne plant pathogen. Fungal Genet Biol 2010, 7:406-415.
17. Klimes A, Dobinson KF. A hydrophobin gene, VDH1, is involved in microsclerotial development and spore viability in the plant pathogen Verticillium dahliae. Fungal Genet Biol 2006, 43:283-294. 10.1016/j.fgb.2005.12.006, 16488633.
18. Neumann MJ, Dobinson KF. Sequence tag analysis of gene expression during pathogenic growth and microsclerotia development in the vascular wilt pathogen Verticillium dahliae. Fungal Genet Biol 2003, 38:54-62. 10.1016/S1087-1845(02)00507-8, 12553936.
19. Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE, Thomma BPHJ, Chen Z, Henrissat B, Lee Y-H, Park J, Garcia-Pedrajas MD, Barbara DJ, Anchieta A, de Jonge R, Santhanam P, Maruthachalam K, Atallah Z, Amyotte SG, Paz Z, Inderbitzin P, Hayes RJ, Heiman DI, Young S, Zeng Q, Engels R, Galagan J, Cuomo CA, Dobinson KF, Ma L-J. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog 2011, 7:e1002137. 10.1371/journal.ppat.1002137, 3145793, 21829347.
20. Klimes A. Identification and characterization of genes associated with microsclerotial development in the plant pathogen Verticillium dahliae. PhD Thesis 2006, University of Western Ontario.
21. Chet I, Henis Y. Sclerotial morphogenesis in fungi. Ann Rev Phytopathol 1975, 13:169-192.
22. Eliahu N, Igbaria A, Rose MS, Horwitz BA, Lev S. Melanin biosynthesis in the maize pathogen Cochliobolus heterostrophus depends on two mitogen-activated protein kinases, Chk1 and Mps1, and the transcription factor Cmr1. Eukaryot Cell 2007, 6:421-429. 10.1128/EC.00264-06, 1828933, 17237364.
23. Tsuji G, Kenmochi Y, Takano Y, Sweigard J, Farrall L, Furusawa I, Horino O, Kubo Y. Novel fungal transcriptional activators, Cmr1p of Colletotrichum lagenarium and Pig1p of Magnaporthe grisea, contain Cys2His2 zinc finger and Zn(II)2Cys6 binuclear cluster DNA-binding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol Microbiol 2000, 38:940-954.
24. Woo PCY, Tam EWT, Chong KTK, Cai JJ, Tung ETK, Ngan AHY, Lau SKP, Yuen K-Y. High diversity of polyketide synthase genes and the melanin biosynthesis gene cluster in Penicillium marneffei. FEBS J 2010, 277:3750-3758. 10.1111/j.1742-4658.2010.07776.x, 20718860.
25. Yu J, Chang P-K, Ehrlich KC, Cary JW, Montalbano B, Dyer JM, Bhatnagar D, Cleveland TE. Characterization of the critical amino acids of an Aspergillus parasiticus cytochrome P-450 monooxygenase encoded by ordA that is involved in the biosynthesis of aflatoxins B1, G1, B2, and G2. Appl Environ Microbiol 1998, 64:4834-4841. 90931, 9835571.
26. Bourges N, Groppi A, Barreau C, Clave C, Begueret J. Regulation of gene expression during the vegetative incompatibility reaction in Podospora anserina: Characterization of three induced genes. Genetics 1998, 150:633-641. 1460364, 9755195.
27. Dementhon K, Paoletti M, Pinan-Lucarre B, Loubradou-Bourges N, Sabourin M, Saupe SJ, Clave C. Rapamycin mimics the incompatibility reaction in the fungus Podospora anserina. Eukaryot Cell 2003, 2:238-246. 10.1128/EC.2.2.238-246.2003, 154840, 12684373.
28. Puyesky M, Benhamou N, Noyola PP, Bauw G, Ziv T, Van Montagu M, Herrera-Estrella A, Horwitz BA. Developmental regulation of cmp1, a gene encoding a multidomain conidiospore surface protein of Trichoderma. Fungal Genet Biol 1999, 27:88-99. 10.1006/fgbi.1999.1134, 10413618.
29. Walker SK, Garrill A. Actin microfilaments in fungi. Mycologist 2006, 20:26-31.
30. Feoktistova A, McCollum D, Ohi R, Gould KL. Identification and characterization of Schizosaccharomyces pombe asp1+, a gene that interacts with mutations in the Arp2/3 complex and actin. Genetics 1999, 152:895-908. 1460656, 10388810.
31. Mouassite M, Camougrand N, Schwob E, Demaison G, Laclau M, Guérin M. The 'SUN' family: yeast SUN4/SCW3 is involved in cell septation. Yeast 2000, 16:905-919. 10.1002/1097-0061(200007)16:10<905::AID-YEA584>3.0.CO;2-1, 10870102.
32. Robbertse B, Yoder OC, Nguyen A, Schoch CL, Turgeon BG. Deletion of all Cochliobolus heterostrophus monofunctional catalase-encoding genes reveals a role for one in sensitivity to oxidative stress but none with a role in virulence. Mol Plant-Microbe Interact 2003, 16:1013-1021. 10.1094/MPMI.2003.16.11.1013, 14601669.
33. Papapostolou I, Georgiou CD. Hydrogen peroxide is involved in the sclerotial differentiation of filamentous phytopathogenic fungi. J Appl Microbiol 2010, 109:1929-1936. 10.1111/j.1365-2672.2010.04822.x, 20681971.
34. Kimpel E, Osiewacz HD. PaGrg1, a glucose-repressible gene of Podospora anserina that is differentially expressed during lifespan. Curr Genet 1999, 35:557-563. 10.1007/s002940050453, 10369964.
35. Walther TC, Brickner JH, Aguilar PS, Bernales S, Pantoja C, Walter P. Eisosomes mark static sites of endocytosis. Nature 2006, 439:998-1003. 10.1038/nature04472, 16496001.
36. Brandt WH. Morphogenesis in Verticillium: Effect of light and ultraviolet radiation on microsclerotia and melanin. Can J Bot 1964, 42:1017-1023.
37. Griffiths DA. The fine structure of developing microsclerotia of Verticillium dahliae Kleb. Arch Microbiol 1970, 74:207-212.
38. Klimes A, Amyotte SG, Grant S, Kang S, Dobinson KF. Microsclerotia development in Verticillium dahliae: Regulation and differential expression of the hydrophobin gene VDH1. Fungal Genet Biol 2008, 45:1525-1532. 10.1016/j.fgb.2008.09.014, 18951989.
39. Fradin EF, Thomma BPHJ. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol 2006, 7:71-86. 10.1111/j.1364-3703.2006.00323.x, 20507429.
40. Thompson JE, Fahnestock S, Farrall L, Liao D-I, Valent B, Jordan DB. The second naphthol reductase of fungal melanin biosynthesis in Magnaporthe grisea: tetrahydroxynaphthalene reductase. J Biol Chem 2000, 275:34867-34872. 10.1074/jbc.M006659200, 10956664.
41. Butler MJ, Gardiner RB, Day AW. Melanin synthesis by Sclerotinia sclerotiorum. Mycologia 2009, 101:296-304. 10.3852/08-120, 19537203.
42. Henson JM, Butler MJ, Day AW. The dark side of the mycelium: Melanins of phytopathogenic fungi. Ann Rev Phytopathol 1999, 37:447-471.
43. Tsai H-F, Wheeler MH, Chang YC, Kwon-Chung KJ. A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J Bacteriol 1999, 181:6469-6477. 103784, 10515939.
44. Fujii I, Yasuoka Y, Tsai H-F, Chang YC, Kwon-Chung KJ, Ebizuka Y. Hydrolytic polyketide shortening by ayg1p, a novel enzyme involved in fungal melanin biosynthesis. J Biol Chem 2004, 279:44613-44620. 10.1074/jbc.M406758200, 15310761.
45. Karapapa VK, Bainbridge BW, Heale JB. Morphological and molecular characterization of Verticillium longisporum comb. nov., pathogenic to oilseed rape. Mycol Res 1997, 101:1281-1294.
46. Dementhon K, Iyer G, Glass NL. VIB-1 is required for expression of genes necessary for programmed cell death in Neurospora crassa. Eukaryot Cell 2006, 5:2161-2173. 10.1128/EC.00253-06, 1694810, 17012538.
47. Paoletti M, Clave C. The fungus-specific HET domain mediates programmed cell death in Podospora anserina. Eukaryot Cell 2007, 6:2001-2008. 10.1128/EC.00129-07, 2168401, 17873080.
48. Baladron V, Ufano S, Dueñas E, Martín-Cuadrado AB, del Rey F, Vazquez de Aldana CR. Eng1p, an endo-1,3-β-glucanase localized at the daughter side of the septum, is involved in cell separation in Saccharomyces cerevisiae. Eukaryot Cell 2002, 1:774-786. 10.1128/EC.1.5.774-786.2002, 126745, 12455695.
49. Jorge JA, Polizeli ML, Thevelein JM, Terenzi HF. Trehalases and trehalose hydrolysis in fungi. FEMS Microbiol Lett 1997, 154:165-171. 10.1111/j.1574-6968.1997.tb12639.x, 9311112.
50. Parrou JL, Jules M, Beltran G, François J. Acid trehalase in yeasts and filamentous fungi: Localization, regulation and physiological function. FEMS Yeast Res 2005, 5:503-511. 10.1016/j.femsyr.2005.01.002, 15780651.
51. Dekker N, Speijer D, Grun CH, van den Berg M, de Haan A, Hochstenbach F. Role of the alpha-glucanase Agn1p in fission-yeast cell separation. Mol Biol Cell 2004, 15:3903-3914. 10.1091/mbc.E04-04-0319, 491845, 15194814.
52. Blair DE, Hekmat O, Schuttelkopf W, Shrestha B, Tokuyasu K, Withers SG, van Aalten DMF. Structure and mechanism of chitin deacetylase from the fungal pathogen Colletotrichum lindemuthianum. Biochemistry 2006, 45:9416-9426. 10.1021/bi0606694, 16878976.
53. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111. 10.1093/bioinformatics/btp120, 2672628, 19289445.
54. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:511-515. 10.1038/nbt.1621, 3146043, 20436464.
55. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold BJ. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628. 10.1038/nmeth.1226, 18516045.
56. Xing Y, Yu T, Wu YN, Roy M, Kim J, Lee C. An expectation-maximization algorithm for probabilistic reconstructions of full-length isoforms from splice graphs. Nucleic Acids Res 2006, 34:3150-3160. 10.1093/nar/gkl396, 1475746, 16757580.
57. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-476. 10.1038/nature07509, 2593745, 18978772.
58. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36. 10.1093/nar/30.9.e36, 113859, 11972351.
59. Bennett JW, Lasure LL. Growth media 1991, San Diego: Academic.