The Sclerotinia sclerotiorum Mating Type Locus (MAT) Contains a 3.6-kb Region That Is Inverted in Every Meiotic Generation

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Chitrampalam, Periasamy ^a,b   Inderbitzin, Patrik ^a   Maruthachalam, Karunakaran ^a   Wu, Bo Ming ^a,c   Subbarao, Krishna V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; FUNGAL GENE; FUNGAL STRAIN; FUNGUS CULTURE; FUNGUS ISOLATION; GENE EXPRESSION; GENE LOCUS; INVERTED REPEAT; MAT GENE; MAT1 1 1 GENE; MAT1 1 5 GENE; MAT1 2 1 GENE; MAT1 2 4 GENE; MEIOSIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SCLEROTINIA SCLEROTIORUM; SOUTHERN BLOTTING;

ASCOMYCOTA; EVOLUTION, MOLECULAR; FERTILITY; GENE DOSAGE; GENE EXPRESSION REGULATION, FUNGAL; GENES, MATING TYPE, FUNGAL; GENETIC LOCI; LETTUCE; MEIOSIS; MYCELIUM; SEQUENCE ANALYSIS, DNA; SEQUENCE INVERSION; SPORES, FUNGAL;

EID: 84874082882     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056895     Document Type: Article

References (71)

1. Boland GJ, Hall R, (1994) Index of plant hosts of Sclerotinia sclerotiorum. Can J Plant Pathol 16: 93-108.
2. Purdy LH, (1979) Sclerotinia sclerotiorum: History, diseases and symptomatology, host range, geographic distribution, and impact. Phytopathology 69: 875-880.
3. Wu BM, Subbarao KV, (2006) Analyses of lettuce drop incidence and population structure of Sclerotinia sclerotiorum and S. minor. Phytopathology 96: 1322-1329.
4. Subbarao KV, (1998) Progress toward integrated management of lettuce drop. Plant Disease 82: 1068-1078.
5. Adams PB, Ayers WA, (1979) Ecology of Sclerotinia species. Phytopathology 69: 896-899.
6. Bourdôt GW, Hurrell GA, Saville DJ, DeJong DMD, (2001) Risk analysis of Sclerotinia sclerotiorum for biological control of Cirsium arvense in pasture: ascospore dispersal. Biocontrol Sci Technol 11: 119-139.
7. Bolton MD, Thomma BPHJ, Nelson BD, (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7: 1-16.
8. Codron D, (1974) Etude ultrastructurale de quelques points du développement des asques du Sclerotinia sclerotiorum (Lib.) de Bary. Annales des Sciences Naturelles, Botanique 12.
9. Ford EJ, Miller RV, Gray H, Sherwood JE, (1995) Heterokaryon formation and vegetative compatibility in Sclerotinia sclerotiorum. Mycol Res 99: 241-247.
10. Drayton FL, Groves JW, (1952) Stromatinia narcissi, a new, sexually dimorphic discomycete. Mycologia 44: 119-140.
11. Turgeon BG, Christiansen SK, Yoder OC (1993) Mating type genes in ascomycetes and their imperfect relatives. In: Reynolds DR, Taylor JW, editors. The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. Wallingford: CAB International. pp 199-215.
12. Debuchy R, Berteaux-Lecellier V, Silar P (2010) Mating systems and sexual morphogenesis in ascomycetes. In: Borkovich KA, Ebbole D, editors. Cellular and molecular biology of flamentous fungi. Washington, DC: ASM Press. pp 501-535.
13. Lu S-W, Yun S-H, Lee T, Turgeon BG, (2011) Altering sexual reproductive mode by interspecific exchange of MAT loci. Fungal Genet Biol 48: 714-724.
14. Metzenberg RL, Glass NL, (1990) Mating type and mating strategies in Neurospora. BioEssays 12: 53-59.
15. Martin T, Lu S-W, van Tilbeurgh H, Ripoll DR, Dixelius C, et al. (2010) Tracing the origin of the fungal α1 domain places its ancestor in the HMG-box superfamily: implication for fungal mating-type evolution. PLoS ONE 5: e15199.
16. Turgeon BG, Yoder OC, (2000) Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet Biol 31: 1-5.
17. Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, et al. (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7: e1002230.
18. Samuels GJ, Lodge DJ, (1996) Three species of Hypocrea with stipitate stromata and Trichoderma anamorphs. Mycologia 88: 302-315.
19. Faretra F, Pollastro S, (1996) Genetic studies of the phytopathogenic fungus Botryotinia fuckeliana (Botrytis cinerea) by analysis of ordered tetrads. Mycol Res 100: 620-624.
20. Leslie JF, Hwang F, Doe FJ, (1986) Homothallic and heterothallic isolates of Fusarium subglutinans. Phytopathology 76: 1142.
21. Mathieson MJ, (1952) Ascospore dimorphism and mating type in Chromocrea spinulosa (Fuckel) Petch n. comb. Ann Bot 16: 449-466.
22. Uhm JY, Fujii H, (1983) Heterothallism and mating type mutation in Sclerotinia trifoliorum. Phytopathology 73: 569-572.
23. Harrington TC, McNew DL, (1997) Self-fertility and uni-directional mating-type switching in Ceratocystis coerulescens, a filamentous ascomycete. Curr Genet 32: 52-59.
24. Yun SH, Berbee ML, Yoder OC, Turgeon BG, (1999) Evolution of fungal self-fertile reproductive life style from self-sterile ancestors. Proc Natl Acad Sci U S A 96: 5592-5597.
25. Inderbitzin P, Harkness J, Turgeon BG, Berbee ML, (2005) Lateral transfer of mating system in Stemphylium. Proc Natl Acad Sci U S A 102: 11390-11395.
26. Inderbitzin P, Shoemaker RA, O'Neill NR, Turgeon BG, Berbee ML, (2006) Systematics and mating systems of two fungal pathogens of opium poppy: the heterothallic Crivellia papaveracea with a Brachycladium penicillatum asexual state and a homothallic species with a B. papaveris asexual state. Can J Bot 84: 1304-1326.
27. Woudenberg JHC, De Gruyter J, Crous PW, Zwiers L-H, (2012) Analysis of the mating-type loci of co-occurring and phylogenetically related species of Ascochyta and Phoma. Mol Plant Pathol 13: 350-362.
28. Herskowitz I, (1989) A regulatory hierarchy for cell specialization in yeast. Nature 342: 749-757.
29. Bobrowicz P, Pawlak R, Correa A, Bell-Pedersen D, Ebbole DJ, (2002) The Neurospora crassa pheromone precursor genes are regulated by the mating type locus and the circadian clock. Mol Microbiol 45: 795-804.
30. Bistis GN, (1981) Chemotropic interactions between trichogynes and conidia of different mating-type in Neurospora crassa. Mycologia 73: 959-975.
31. Bidard F, Aït Benkhali J, Coppin E, Imbeaud S, Grognet P, et al. (2011) Genome-wide gene expression profiling of fertilization competent mycelium in opposite mating types in the heterothallic fungus Podospora anserina. PLoS ONE 6: e21476.
32. Arnaise S, Debuchy R, Picard M, (1997) What is a bona fide mating-type gene? Internuclear complementation of mat mutants in Podospora anserina. Mol Gen Genet 256: 169-178.
33. Zickler D, Arnaise S, Coppin E, Debuchy R, Picard M, (1995) Altered mating-type identity in the fungus Podospora anserina leads to selfish nuclei, uniparental progeny, and haploid meiosis. Genetics 140: 493-503.
34. Shiu PK, Glass NL, (2000) Cell and nuclear recognition mechanisms mediated by mating type in filamentous ascomycetes. Curr Opin Microbiol 3: 183-188.
35. Debuchy R, (1999) Internuclear recognition: a possible connection between Euascomycetes and Homobasidiomycetes. Fungal Genet Biol 27: 218-223.
36. Glass NL, Kaneko I, (2003) Fatal Attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot Cell 2: 1-8.
37. Klix V, Nowrousian M, Ringelberg C, Loros JJ, Dunlap JC, et al. (2010) Functional characterization of MAT1-1-specific mating-type genes in the homothallic ascomycete Sordaria macrospora provides new insights into essential and nonessential sexual regulators. Eukaryot Cell 9: 894-905.
38. Keszthelyi A, Jeney A, Kerényi Z, Mendes O, Waalwijk C, et al. (2007) Tagging target genes of the MAT1-2-1 transcription factor in Fusarium verticillioides (Gibberella fujikuroi MP-A). Antonie Van Leeuwenhoek 91: 373-391.
39. Pöggeler S, Nowrousian M, Ringelberg C, Loros J, Dunlap J, et al. (2006) Microarray and real-time PCR analyses reveal mating type-dependent gene expression in a homothallic fungus. Mol Genet Genomics 275: 492-503.
40. Uhm JY, Fujii H, (1983) Ascospore dimorphism in Sclerotinia trifoliorum and cultural characters of strains from different-sized spores. Phytopathology 73: 565-569.
41. Yoder OC, Valent B, Chumley F, (1986) Genetic nomenclature and practice for plant pathogenic fungi. Phytopathology 76: 383-385.
42. Raju NB, (1980) Meiosis and ascospore genesis in Neurospora. Eur J Cell Biol 23: 208-223.
43. Raju NB, (2009) Neurospora as a model fungus for studies in cytogenetics and sexual biology at Stanford. J Biosci 34: 139-159.
44. Wu BM, Peng Y-L, Qin Q-M, Subbarao KV, (2007) Incubation of excised apothecia enhances ascus maturation of Sclerotinia sclerotiorum. Mycologia 99: 33-41.
45. Ekins M, Aitken EA, Coulter KC, (2006) Homothallism in Sclerotinia minor. Mycol Res 110: 1193-1199.
46. Flores M, Morales L, Gonzaga-Jauregui C, Domínguez-Vidaña R, Zepeda C, et al. (2007) Recurrent DNA inversion rearrangements in the human genome. Proc Natl Acad Sci U S A 104: 6099-6106.
47. Hurles ME, Lupski JR (2006) Recombination hotspots in nonallelic homologous recombination. In: Lupski JR, Stankiewicz P, editors. Genomic Disorders: The genomic basis of disease. Totowa, NJ: Humana Press. pp 341-355.
48. Hoang ML, Tan FJ, Lai DC, Celniker SE, Hoskins RA, et al. (2010) Competitive repair by naturally dispersed repetitive DNA during non-allelic homologous recombination. PLoS Genet 6: e1001228.
49. Haber JE, (2012) Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics 191: 33-64.
50. Holst-Jensen A, Kohn LM, Schumacher T (1997) Nuclear rDNA phylogeny of the Sclerotiniaceae Mycologia. 89: 885-899.
51. Andrew M, Barua R, Short SM, Kohn LM, (2012) Evidence for a common toolbox based on necrotrophy in a fungal lineage spanning necrotrophs, biotrophs, endophytes, host generalists and specialists. PLoS ONE 7: e29943.
52. Yun SH, Arie T, Kaneko I, Yoder OC, Turgeon BG, (2000) Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet Biol 31: 7-20.
53. Simon M, Zieg J, Silverman M, Mandel G, Doolittle R, (1980) Phase Variation: Evolution of a Controlling Element. Science 209: 1370-1374.
54. Puig M, Cáceres M, Ruiz A, (2004) Silencing of a gene adjacent to the breakpoint of a widespread Drosophila inversion by a transposon-induced antisense RNA. Proc Natl Acad Sci U S A 101: 9013-9018.
55. Guillén Y, Ruiz A, (2012) Gene alterations at Drosophila inversion breakpoints provide prima facie evidence for natural selection as an explanation for rapid chromosomal evolution. BMC Genomics 13: 53.
56. Leubner-Metzger G, Horwitz BA, Yoder OC, Turgeon BG, (1997) Transcripts at the mating type locus of Cochliobolus heterostrophus. Mol Gen Genet 256: 661-673.
57. Glass NL, Vollmer SJ, Staben C, Grotelueschen J, Metzenberg RL, et al. (1988) DNAs of the two mating-type alleles of Neurospora crassa are highly dissimilar. Science 241: 570-573.
58. Perkins DD, (1987) Mating-type switching in filamentous ascomycetes. Genetics 115: 215-216.
59. Raju NB, Perkins DD, (2000) Programmed ascospore death in the homothallic ascomycete Coniochaeta tetraspora. Fungal Genet Biol 30: 213-221.
60. Witthuhn RC, Harrington TC, Wingfield BD, Steimel JP, Wingfield MJ, (2000) Deletion of the MAT-2 mating-type gene during uni-directional mating-type switching in Ceratocystis. Curr Genet 38: 48-52.
61. Turgeon BG, Debuchy R (2007) Cochliobolus and Podospora: Mechanisms of sex determination and the evolution of reproductive lifestyle. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA, editors. Sex in Fungi: Molecular determination and evolutionary implications. Washington, DC: ASM Press. pp 93-121.
62. Sambrook J, Russell DW (2001) Molecular Cloning. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
63. Garza E, Finan C, Iverson A, Zhou S, (2011) Extension temperature of 60°C required for PCR amplification of large DNA fragments (>5 kb) from a low GC bacterium Clostridium acetobutylicum. World J Microbiol and Biotechnol 27: 449-451.
64. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, et al. (2010) Geneious v4.8.5. Available: http://www.geneious.com.
65. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4., Sunderland, Massachusetts: Sinauer Associates.
66. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
67. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
68. Betley JN, Frith MC, Graber JH, Choo S, Deshler JO, (2002) A ubiquitous and conserved signal for RNA localization in chordates. Curr Biol 12: 1756-1761.
69. Malvárez G, Carbone I, Grünwald NJ, Subbarao KV, Kohn LM, (2007) New populations of Sclerotinia sclerotiorum from lettuce in California and peas and lentils in Washington. Phytopathology 97: 470-483.
70. Selden RF, Schatz DG (1989) Analysis of DNA sequences by blotting and hybridization. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG et al., editors. Short protocols in molecular biology. New York: Wiley. pp 75-79.
71. Schafer MR, Kohn LM, (2006) An optimized method for mycelial compatibility testing in Sclerotinia sclerotiorum. Mycologia 98: 593-597.