Recombination and lineage-specific gene loss in the aflatoxin gene cluster of Aspergillus flavus

Molecular Ecology

Volumn 18, Issue 23, 2009, Pages 4870-4887

  Moore, Geromy G ^a   Singh, Rakhi ^a   Horn, Bruce W ^b   Carbone, Ignazio ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b NATIONAL PEANUT RESEARCH LABORATORY   (United States)

Author keywords

Ancestral recombination graph; Balancing selection; Coalescent; Linkage disequilibrium

Indexed keywords

AFLATOXIN; FUNGAL DNA;

ARTICLE; ASPERGILLUS FLAVUS; DNA BASE COMPOSITION; DNA SEQUENCE; FUNGAL GENOME; GENE LINKAGE DISEQUILIBRIUM; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; MOLECULAR EVOLUTION; MULTIGENE FAMILY; POPULATION GENETICS; SEQUENCE ALIGNMENT; TELOMERE;

AFLATOXINS; ASPERGILLUS FLAVUS; BASE COMPOSITION; DNA, FUNGAL; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENETICS, POPULATION; GENOME, FUNGAL; LINKAGE DISEQUILIBRIUM; MULTIGENE FAMILY; RECOMBINATION, GENETIC; SELECTION, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TELOMERE;

ASPERGILLUS FLAVUS;

EID: 70449728010     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04414.x     Document Type: Article

References (67)

1. Aylor DL, Price EW, Carbone I (2006) snap: combine and map modules for multilocus population genetic analysis. Bioinformatics, 22, 1399 1401.
2. Baudat F, Nicolas A (1997) Clustering of meiotic double-strand breaks on yeast chromosome III. Proceedings of the National Academy of Sciences, USA, 94, 5213 5218.
3. Bayman P, Cotty PJ (1993) Genetic diversity in Aspergillus flavus: association with aflatoxin production and morphology. Canadian Journal of Botany, 71, 23 31.
4. Bowden LC, Price EW, Carbone I (2008) snap Clade and Matrix, Version 2. Distributed Over the Internet. Department of Plant Pathology, North Carolina State University. Available at: http://www.cals.ncsu.edu/plantpath/faculty/ carbone/home.html (last accessed October 2009)
5. Brown RL, Cleveland TE, Cotty PJ, Mellon JE (1992) Spread of Aspergillus flavus in cotton bolls, decay of intercarpellary membranes, and production of fungal pectinases. Phytopathology, 82, 462 467.
6. Burdock GA, Flamm WG (2000) Safety assessment of the mycotoxin cyclopiazonic acid. International Journal of Toxicology, 19, 195 218.
7. Carbone I, Jakobek JL, Ramirez-Prado JH, Horn BW (2007a) Recombination, balancing selection and adaptive evolution in the aflatoxin gene cluster of Aspergillus parasiticus. Molecular Ecology, 16, 4401 4417.
8. Carbone I, Ramirez-Prado JH, Jakobek JL, Horn BW (2007b) Gene duplication, modularity and adaptation in the evolution of the aflatoxin gene cluster. BMC Evolutionary Biology, 7, 111.
9. Cary JW, Ehrlich KC, Bland JM, Montalbano BG (2006) The aflatoxin biosynthesis cluster gene, aflX, encodes an oxidoreductase involved in conversion of versicolorin A to demethylsterigmatocystin. Applied and Environmental Microbiology, 72, 1096 1101.
10. Chang P-K, Yu J (2002) Characterization of a partial duplication of the aflatoxin gene cluster in Aspergillus parasiticus ATCC 56775. Applied Microbiology and Biotechnology, 58, 632 636.
11. Chang P-K, Horn BW, Dorner JW (2005) Sequence breakpoints in the aflatoxin biosynthesis gene cluster and flanking regions in nonaflatoxigenic Aspergillus flavus isolates. Fungal Genetics and Biology, 42, 914 923.
12. Chang P-K, Ehrlich KC, Hua SS (2006) Cladal relatedness among Aspergillus oryzae isolates and Aspergillus flavus S and L morphotype isolates. International Journal of Food Microbiology, 108, 172 177.
13. Chang P-K, Horn BW, Dorner JW (2009) Clustered genes involved in cyclopiazonic acid production are next to the aflatoxin biosynthesis gene cluster in Aspergillus flavus. Fungal Genetics and Biology, 46, 176 182.
14. Cole RJ (1986) Etiology of turkey "X" disease in retrospect: a case for the involvement of cyclopiazonic acid. Mycotoxin Research, 2, 3 7.
15. Cole RJ, Sanders TH, Hill RA, Blankenship PD (1985) Mean geocarposphere temperatures that induce preharvest aflatoxin contamination of peanuts under drought stress. Mycopathologia, 91, 41 46.
16. Cotty PJ (1989) Virulence and cultural characteristics of two Aspergillus flavus strains pathogenic on cotton. Phytopathology, 79, 808 814.
17. Cotty PJ (1994) Influence of field application of an atoxigenic strain of Aspergillus flavus on the populations of A. flavus infecting cotton bolls and on the aflatoxin content of cottonseed. Phytopathology, 84, 1270 1277.
18. Cotty PJ, Cleveland TE, Brown RL, Mellon JE (1990) Variation in polygalacturonase production among Aspergillus flavus isolates. Applied and Environmental Microbiology, 56, 3885 3887.
19. Criseo G, Racco C, Romeo O (2008) High genetic variability in non-aflatoxigenic A. flavus strains by using Quadruplex PCR-based assay. International Journal of Food Microbiology, 125, 341 343.
20. Dorner JW (2005) Biological control of aflatoxin crop contamination. In : Aflatoxin and Food Safet (ed. Abbas HK pp. 333 352. Taylor and Francis, Boca Raton, FL.
21. Dorner JW (2009a) Biological control of aflatoxin contamination in corn using a nontoxigenic strain of Aspergillus flavus. Journal of Food Protection, 72, 801 804.
22. Dorner JW (2009b) Development of biocontrol technology to manage aflatoxin contamination in peanuts. Peanut Science, 36, 60 67.
23. Dorner JW, Horn BW (2007) Separate and combined applications of nontoxigenic Aspergillus flavus and A. parasiticus for biocontrol of aflatoxin in peanuts. Mycopathologia, 163, 215 223.
24. Eaton DL, Groopman JD (1994) The Toxicology of Aflatoxins: Human Health, Veterinary, and Agricultural Significance. Academic Press, San Diego.
25. van Edmond HP, Jonker MA (2005) Worldwide regulations on aflatoxins. In : Aflatoxin and Food Safet (ed Abbas HK pp. 77 93. Taylor and Francis, Boca Raton, FL.
26. Ehrlich KC, Cotty PJ (2004) An isolate of Aspergillus flavus used to reduce aflatoxin contamination in cottonseed has a defective polyketide synthase gene. Applied Microbiology and Biotechnology, 65, 473 478.
27. Ehrlich KC, Montalbano B, Boue SM, Bhatnagar D (2005) An aflatoxin biosynthesis cluster gene encodes a novel oxidase required for conversion of versicolorin A to sterigmatocystin. Applied and Environmental Microbiology, 71, 8963 8965.
28. EPA (2003) Aspergillus flavus AF36. 3 July 2003. Biopesticide Registration Action Document. Available at: http://www.epa.gov/pesticides/ biopesticides/ingredients/tech-docs/brad-006456.pdf
29. EPA (2004) Aspergillus flavus NRRL 21882. 24 March 2004. Biopesticide Registration Action Document. http://www.epa.gov/oppbppd1/biopesticides/ ingredients/tech-docs/brad-006500.pdf.
30. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915 925.
31. Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics, 133, 693 709.
32. Geiser DM, Pitt JI, Taylor JW (1998) Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus. Proceedings of the National Academy of Sciences, USA, 95, 388 393.
33. Geiser DM, Dorner JW, Horn BW, Taylor JW (2000) The phylogenetics of mycotoxin and sclerotium production in Aspergillus flavus and Aspergillus oryzae. Fungal Genetics and Biology, 31, 169 179.
34. Griffiths RC, Tavaré S (1994) Ancestral inference in population genetics. Statistical Science, 9, 307 319.
35. Hey J, Wakeley J (1997) A coalescent estimator of the population recombination rate. Genetics, 145, 833 846.
36. Hodges RL, Kelkar HS, Xuei X et al. (2000) Characterization of an echinocandin B-producing strain blocked for sterigmatocystin biosynthesis reveals a translocation in the stcW gene of the aflatoxin biosynthetic pathway. Journal of Industrial Microbiology & Biotechnology, 25, 333 341.
37. Horn BW (2005) Ecology and population biology of aflatoxigenic fungi in soil. In : Aflatoxin and Food Safet (ed. Abbas HK pp. 95 116. CRC Press, Boca Raton, FL.
38. Horn BW (2007) Biodiversity of Aspergillus section Flavi in the United States: a review. Food Additives and Contaminants, 24, 1088 1101.
39. 1 and cyclopiazonic acid by soil isolates of Aspergillus flavus along a transect within the United States. Applied and Environmental Microbiology, 65, 1444 1449.
40. Horn BW, Greene RL (1995) Vegetative compatibility within populations of Aspergillus flavus, Aspergillus parasiticus, and A. tamarii from a peanut field. Mycologia, 87, 324 332.
41. Horn BW, Dorner JW, Greene RL, Blankenship PD, Cole RJ (1994) Effect of Aspergillus parasiticus soil inoculum on invasion of peanut seeds. Mycopathologia, 125, 179 191.
42. Horn BW, Greene RL, Sobolev VS et al. (1996) Association of morphology and mycotoxin production with vegetative compatibility groups in Aspergillus flavus, A. parasiticus, and A. tamarii. Mycologia, 88, 574 587.
43. Horn BW, Moore GG, Carbone I (2009a) Sexual reproduction in Aspergillus flavus. Mycologia, 101, 423 429.
44. Horn BW, Ramirez-Prado JH, Carbone I (2009b) Sexual reproduction and recombination in the aflatoxin-producing fungus Aspergillus parasiticus. Fungal Genetics and Biology, 46, 169 175.
45. Horn BW, Ramirez-Prado JH, Carbone I (2009c) The sexual state of Aspergillus parasiticus. Mycologia, 101, 275 280.
46. Howlett BJ, Idnurm A, Heitman J (2007) Fungal pathogenesis: gene clusters unveiled as secrets within the Ustilago maydis code. Current Biology, 17, R87 R90.
47. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics, 111, 147 164.
48. Kusumoto K, Nogata Y, Ohta H (2000) Directed deletions in the aflatoxin biosynthesis gene homolog cluster of Aspergillus oryzae. Current Genetics, 37, 104 111.
49. Leslie JF (1993) Fungal vegetative compatibility. Annual Review of Phytopathology, 31, 127 150.
50. Lyngsø RB, Song YS, Hein J (2005) Minimum recombination histories by branch and bound. Proceedings of the 5th International Workshop on Algorithms in Bioinformatics Lecture Notes in Bioinformatics, 3692, 239 250.
51. Machida M, Asai K, Sano M et al. (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature, 438, 1157 1161.
52. Myers SR, Griffiths RC (2003) Bounds on the minimum number of recombination events in a sample history. Genetics, 163, 375 394.
53. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.
54. Patron NJ, Waller RF, Cozijnsen AJ et al. (2007) Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evolutionary Biology, 7, 174.
55. Peterson SW (2008) Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia, 100, 205 226.
56. Peterson SW, Ito Y, Horn BW, Goto T (2001) Aspergillus bombycis, a new aflatoxigenic species and genetic variation in its sibling species, A. nomius. Mycologia, 93, 689 703.
57. Powell AJ, Conant GC, Brown DE, Carbone I, Dean RA (2008) Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens. BMC Genomics, 9, 147.
58. Price EW, Carbone I (2005) snap: workbench management tool for evolutionary population genetic analysis. Bioinformatics, 21, 402 404.
59. Ramirez-Prado JH, Moore GG, Horn BW, Carbone I (2008) Characterization and population analysis of the mating-type genes in Aspergillus flavus and Aspergillus parasiticus. Fungal Genetics and Biology, 45, 1292 1299.
60. Shieh MT, Brown RL, Whitehead MP et al. (1997) Molecular genetic evidence for the involvement of a specific polygalacturonase, P2c, in the invasion and spread of Aspergillus flavus in cotton bolls. Applied and Environmental Microbiology, 63, 3548 3552.
61. Smith CA, Woloshuk CP, Robertson D, Payne GA (2007) Silencing of the aflatoxin gene cluster in a diploid strain of Aspergillus flavus is suppressed by ectopic aflR expression. Genetics, 176, 2077 2086.
62. Swofford DL (1998) paup*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0. Sinauer Associates, Sunderland, MA.
63. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585 595.
64. Watterson GA (1975) On the number of segregating sites in genetic models without recombination. Theoretical Population Biology, 7, 256 276.
65. Yin Y, Lou T, Yan L, Michailides TJ, Ma Z (2009) Molecular characterization of toxigenic and atoxigenic Aspergillus flavus isolates, collected from peanut fields in China. Journal of Applied Microbiology doi :.
66. Yu J, Chang P-K, Ehrlich KC et al. (2004) Clustered pathway genes in aflatoxin biosynthesis. Applied and Environmental Microbiology, 70, 1253 1262.
67. Zhang R, Zhang CT (2004) A systematic method to identify genomic islands and its applications in analyzing the genomes of Corynebacterium glutamicum and Vibrio vulnificus CMCP6 chromosome I. Bioinformatics, 20, 612 622.