Recombination, balancing selection and adaptive evolution in the aflatoxin gene cluster of Aspergillus parasiticus

Molecular Ecology

Volumn 16, Issue 20, 2007, Pages 4401-4417

  Carbone, Ignazio ^a   Jakobek, Judy L ^a   Ramirez Prado, Jorge H ^a   Horn, Bruce W ^b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b NATIONAL PEANUT RESEARCH LABORATORY   (United States)

Author keywords

Coalescent; Compatibility; Linkage disequilibrium; Recombination blocks

Indexed keywords

AFLATOXIN; FUNGAL DNA;

ADAPTATION; ARTICLE; ASPERGILLUS; BIOLOGICAL MODEL; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE HOMOLOGY; TIME;

ADAPTATION, PHYSIOLOGICAL; AFLATOXINS; ASPERGILLUS; BASE SEQUENCE; DNA, FUNGAL; EVOLUTION, MOLECULAR; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; RECOMBINATION, GENETIC; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; TIME FACTORS; VARIATION (GENETICS);

ANIMALIA; ASPERGILLUS; ASPERGILLUS PARASITICUS;

EID: 34547995522     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2007.03464.x     Document Type: Article

References (70)

1. 14C in house flies. Journal of Economic Entomology, 65, 375 378.
2. Andersson JO (2005) Lateral gene transfer in eukaryotes. Cellular and Molecular Life Sciences, 62, 1182 1197.
3. Aylor DL, Price EW, Carbone I (2006) snap: combine and map modules for multilocus population genetic analysis. Bioinformatics, 22, 1399 1401.
4. Brown DW, Yu JH, Kelkar HS et al 1996) Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proceedings of the National Academy of Sciences, USA, 93, 1418 1422.
5. Carbone I, Ramirez-Prado JH, Jakobek JL, Horn BW (2007) Gene duplication, modularity and adaptation in the evolution of the aflatoxin gene cluster. BMC Evolutionary Biology, 7, 111.
6. Carbone I, Liu Y, Hillman BI, Milgroom MG (2004) Recombination and migration of Cryphonectria hypovirus 1 as inferred from gene genealogies and the coalescent. Genetics, 166, 1611 1629.
7. Cary JW, Klich MA, Beltz SB (2005) Characterization of aflatoxin-producing fungi outside of Aspergillus section Flavi. Mycologia, 97, 425 432.
8. 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.
9. Cotty PJ, Bhatnagar D (1994) Variability among atoxigenic Aspergillus flavus strains in ability to prevent aflatoxin contamination and production of aflatoxin biosynthetic pathway enzymes. Applied and Environmental Microbiology, 60, 2248 2251.
10. Ehrlich KC, Chang P-K, Yu J, Cotty PJ (2004) Aflatoxin biosynthesis cluster gene cypA is required for G aflatoxin formation. Applied and Environmental Microbiology, 70, 6518 6524.
11. 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.
12. Ehrlich KC, Yu J, Cotty PJ (2005b) Aflatoxin biosynthesis gene clusters and flanking regions. Journal of Applied Microbiology, 99, 518 527.
13. Ehrlich KC, Montalbano BG, Cotty PJ (2003) Sequence comparison of aflR from different Aspergillus species provides evidence for variability in regulation of aflatoxin production. Fungal Genetics and Biology, 38, 63 74.
14. Ehrlich KC, Montalbano BG, Cotty PJ (2005a) Divergent regulation of aflatoxin production at acidic pH by two Aspergillus strains. Mycopathologia, 159, 579 581.
15. Fearnhead P (2003) Consistency of estimators of the population-scaled recombination rate. Theoretical Population Biology, 64, 67 79.
16. Fearnhead P, Donnelly P (2001) Estimating recombination rates from population genetic data. Genetics, 159, 1299 1318.
17. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915 925.
18. Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics, 133, 693 709.
19. Galagan JE, Calvo SE, Cuomo C et al 2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature, 438, 1105 1115.
20. 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.
21. Hartl DL, Clark AG (1997) Principles of Population Genetics, 3rd edn. Sinauer Associates, Sunderland, Massachusetts.
22. Hey J, Wakeley J (1997) A coalescent estimator of the population recombination rate. Genetics, 145, 833 846.
23. 1 biosynthesis. Bioorg Chemistry, 29, 293 307.
24. Horn BW (2005) Ecology and population biology of aflatoxigenic fungi in soil. In : Aflatoxin and Food Safety (ed. Abbas HK pp. 95 116. CRC Taylor & Francis, Boca Raton, Florida.
25. Horn BW, Dorner JW (1998) Soil populations of Aspergillus species from section Flavi along a transect through peanut-growing regions of the United States. Mycologia, 90, 767 776.
26. 1 and cyclopiazonic acid by soil isolates of Aspergillus flavus along a transect within the United States. Applied and Environmental Microbiology, 65, 1444 1449.
27. Horn BW, Greene RL (1995) Vegetative compatibility within populations of Aspergillus flavus, A. parasiticus, and A. tamarii from a peanut field. Mycologia, 87, 324 332.
28. 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.
29. Hudson RR (2001) Two-locus sampling distributions and their application. Genetics, 159, 1805 1817.
30. Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting geographic subdivision. Molecular Biology and Evolution, 9, 138 151.
31. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proceedings of the National Academy of Sciences of the USA, 86, 958 962.
32. Hurst LD, Pal C, Lercher MJ (2004) The evolutionary dynamics of eukaryotic gene order. Nature Reviews Genetics, 5, 299 310.
33. Jarvis JL, Guthrie WD, Lillehoj EB (1984) Aflatoxin and selected biosynthetic precursors: effects on the European corn borer in the laboratory. Journal of Agriculture Entomology, 1, 354 359.
34. Kim JH, Campbell BC, Yu J et al 2005) Examination of fungal stress response genes using Saccharomyces cerevisiae as a model system: targeting genes affecting aflatoxin biosynthesis by Aspergillus flavus Link. Applied Microbiology and Biotechnology, 67, 807 815.
35. Klich MA, Cary JW, Beltz SB, Bennett CA (2003) Phylogenetic and morphological analysis of Aspergillus ochraceoroseus. Mycologia, 95, 1252 1260.
36. Kusumoto K, Nogata Y, Ohta H (2000) Directed deletions in the aflatoxin biosynthesis gene homolog cluster of Aspergillus oryzae. Current Genetics, 37, 104 111.
37. 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.
38. Machida M, Asai K, Sano M et al 2005) Genome sequencing and analysis of Aspergillus oryzae. Nature, 438, 1157 1161.
39. May G, Shaw F, Badrane H, Vekemans X (1999) The signature of balancing selection: fungal mating compatibility gene evolution. Proceedings of the National Academy of Sciences USA, 96, 9172 9177.
40. McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics, 160, 1231 1241.
41. Moore JH, Hammond AM, Llewellyn GC (1978) Chemosterilant and insecticidal activity of mixed aflatoxins against Anthonomus grandis (Coleoptera). Journal of Invertebrate Pathology, 31, 365 367.
42. Myers SR, Griffiths RC (2003) Bounds on the minimum number of recombination events in a sample history. Genetics, 163, 375 394.
43. Navarro A, Barton NH (2002) The effects of multilocus balancing selection on neutral variability. Genetics, 161, 849 863.
44. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.
45. Nierman WC, Pain A, Anderson MJ et al 2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature, 438, 1151 1156.
46. Paoletti M, Rydholm C, Schwier EU et al 2005) Evidence for sexuality in the opportunistic fungal pathogen Aspergillus fumigatus. Current Biology, 15, 1242 1248.
47. Papa KE (1973) The parasexual cycle in Aspergillus flavus. Mycologia, 65, 1201 1205.
48. Papa KE (1978) The parasexual cycle in Aspergillus parasiticus. Mycologia, 70, 766 773.
49. 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.
50. Price EW, Carbone I (2005) snap: workbench management tool for evolutionary population genetic analysis. Bioinformatics, 21, 402 404.
51. Qi X, Bakht S, Leggett M et al 2004) A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proceedings of the National Academy of Sciences, USA, 101, 8233 8238.
52. Rodriguez-Trelles F, Tarrio R, Ayala FJ (2003) Convergent neofunctionalization by positive Darwinian selection after ancient recurrent duplications of the xanthine dehydrogenase gene. Proceedings of the National Academy of Sciences, USA, 100, 13413 13417.
53. Rozas J, Sanchez-De I, Barrio JC, Messeguer X, Rozas R (2003) dnasp, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496 2497.
54. Song YS, Hein J (2003) Parsimonious reconstruction of sequence evolution and haplotype blocks: finding the minimum number of recombination events. In : Algorithms in Bioinformatics (eds Benson G Page RDM pp. 287 302. Proceedings of the Third International Workshop, WABI, Budapest, Hungary.
55. Song YS, Wu Y, Gusfield D (2005) Efficient computation of close lower and upper bounds on the minimum number of recombinations in biological sequence evolution. Bioinformatics, 21 (Suppl. 1 i413 i422.
56. Swofford DL (1998) Paup*. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0. Sinauer Associates, Sunderland, Massachusetts.
57. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585 595.
58. Takahata N (1990) A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proceedings of the National Academy of Sciences, USA, 87, 2419 2423.
59. Trowsdale J (2002) The gentle art of gene arrangement: the meaning of gene clusters. Genome Biology, 3, comment2002.2001-02.2005.
60. Venables WN, Ripley BD (2002) Modern Applied Statistics with S, 4th edn. Springer-Verlag, New York.
61. Walton JD (2000) Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genetics and Biology, 30, 167 171.
62. Ward TJ, Bielawski JP, Kistler HC, Sullivan E, O'Donnell K (2002) Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proceedings of the National Academy of Sciences of the USA, 99, 9278 9283.
63. Watterson GA (1975) On the number of segregating sites in genetic models without recombination. Theoretical Population Biology, 7, 256 276.
64. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In : PCR Protocols: a Guide to Methods and Applications (eds Innis MA Gelfand DH Sninsky JJ White TJ pp. 315 322. Academic Press, San Diego, California.
65. Wilkinson HH, Ramaswamy A, Sim SC, Keller NP (2004) Increased conidiation associated with progression along the sterigmatocystin biosynthetic pathway. Mycologia, 96, 1190 1198.
66. Woloshuk CP, Foutz KR, Brewer JF et al 1994) Molecular characterization of aflR, a regulatory locus for aflatoxin biosynthesis. Applied and Environmental Microbiology, 60, 2408 2414.
67. Wong S, Wolfe KH (2005) Birth of a metabolic gene cluster in yeast by adaptive gene relocation. Nature Genetics, 37, 777 782.
68. Yu J, Bhatnagar D, Cleveland TE (2004a) Completed sequence of aflatoxin pathway gene cluster in Aspergillus parasiticus. FEBS Letters, 564, 126 130.
69. Yu J, Chang P-K, Ehrlich KC et al 2004b) Clustered pathway genes in aflatoxin biosynthesis. Applied and Environmental Microbiology, 70, 1253 1262.
70. Yu JH, Keller N (2005) Regulation of secondary metabolism in filamentous fungi. Annual Review of Phytopathology, 43, 437 458.