Sexuality Generates Diversity in the Aflatoxin Gene Cluster: Evidence on a Global Scale

PLoS Pathogens

Volumn 9, Issue 8, 2013, Pages

  Moore, Geromy G ^a   Elliott, Jacalyn L ^b   Singh, Rakhi ^b   Horn, Bruce W ^c   Dorner, Joe W ^c   Stone, Eric A ^b   Chulze, Sofia N ^d   Barros, German G ^d   Naik, Manjunath K ^e   Wright, Graeme C ^f   Hell, Kerstin ^g   Carbone, Ignazio ^b  

^a SOUTHERN REGIONAL RESEARCH CENTER   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c NATIONAL PEANUT RESEARCH LABORATORY   (United States)

^d DEPARTAMENTO DE QUÍMICA   (Argentina)

^e Parbhani   (India)

^f DEPARTMENT OF AGRICULTURE AND FISHERIES   (Australia)

^g INTERNATIONAL INSTITUTE OF TROPICAL AGRICULTURE   (Benin)

Author keywords

[No Author keywords available]

Indexed keywords

AFLATOXIN; BETA TUBULIN; CALMODULIN; FUNGAL PROTEIN; REPRESSOR PROTEIN;

ARGENTINA; ARTICLE; ASEXUAL REPRODUCTION; ASPERGILLUS; ASPERGILLUS FLAVUS; ASPERGILLUS MINISCLEROTIGENES; ASPERGILLUS PARASITICUS; CLIMATE; DNA ISOLATION; FUNGAL REPRODUCTION; GENE CLUSTER; GENE FREQUENCY; GENETIC RECOMBINATION; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; MULTILOCUS SEQUENCE TYPING; MUTATION RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; UNITED STATES; BIOSYNTHESIS; FUNGAL GENE; GENETICS; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGY; SPECIES DIFFERENCE;

AFLATOXINS; ASPERGILLUS FLAVUS; FUNGAL PROTEINS; GENES, FUNGAL; MULTIGENE FAMILY; REPRESSOR PROTEINS; SPECIES SPECIFICITY;

EID: 84883408841     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003574     Document Type: Article

References (47)

1. Klich MA, (2007) Aspergillus flavus: the major producer of aflatoxin. Molecular Plant Pathology 8: 713-722.
2. Scheidegger K, Payne G, (2003) Unlocking the secrets behind secondary metabolism: A review of Aspergillus flavus from pathogenicity to functional genomics. Journal of Toxicology - Toxin Reviews 22: 423-459.
3. Blankenship PD, Cole RJ, Sanders TH, Hill RA, (1984) Effect of geocarposphere temperature on pre-harvest colonization of drought-stressed peanuts by Aspergillus flavus and subsequent aflatoxin contamination. Mycopathologia 85: 69-74.
4. Cotty PJ, (1989) Virulence and cultural characteristics of two Aspergillus flavus strains pathogenic on cotton. Phytopathology 78: 1250-1253.
5. Horn BW, (2003) Ecology and population biology of aflatoxigenic fungi in soil. Journal of Toxicology-Toxin Reviews 22: 351-379.
6. Cole RJ, (1986) Etiology of Turkey "X" disease in retrospect: A case for the involvement of cyclopiazonic acid. Mycotoxin Research 2: 3-7.
7. Pildain MB, Frisvad JC, Vaamonde G, Cabral D, Varga J, et al. (2008) Two novel aflatoxin-producing Aspergillus species from Argentinean peanuts. Interntaional Journal of Systematic and Evolutionary Microbiology 58: 725-735.
8. Bhatnagar D, McCormick SP, Lee LS, Hill RA, (1987) Identification of O-methylsterigmatocystin as an aflatoxin B1 and G1 precursor in Aspergillus parasiticus. Applied and Environmental Microbiology 53: 1028-1033.
9. Yu J, Chang PK, Ehrlich KC, Cary JW, Bhatnagar D, et al. (2004) Clustered pathway genes in aflatoxin biosynthesis. Appl Environ Microbiol 70: 1253-1262.
10. Yu J, Chang PK, Ehrlich KC, Cary JW, Montalbano B, et al. (1998) 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. Applied and Environmental Microbiology 64: 4834-4841.
11. Ehrlich KC, Chang PK, Yu J, Cotty PJ, (2004) Aflatoxin biosynthesis cluster gene cypA is required for G aflatoxin formation. Applied and Environmental Microbiology 70: 6518-6524.
12. Ehrlich KC, Cotty PJ, (2004) An isolate of Aspergillus flavus used to reduce aflatoxin contamination in cottonseed has a defective polyketide synthase gene. Appl Microbiol Biotechnol 65: 473-478.
13. Chang PK, 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.
14. Moore GG, Singh R, Horn BW, Carbone I, (2009) Recombination and lineage-specific gene loss in the aflatoxin gene cluster of Aspergillus flavus. Molecular Ecology 18: 4870-4887.
15. Horn BW, Moore GG, Carbone I, (2009) Sexual reproduction in Aspergillus flavus. Mycologia 101: 423-429.
16. Horn BW, Ramirez-Prado JH, Carbone I, (2009) Sexual reproduction and recombination in the aflatoxin-producing fungus Aspergillus parasiticus. Fungal Genetics and Biology 46: 169-175.
17. Horn BW, Ramirez-Prado JH, Carbone I, (2009) The sexual state of Aspergillus parasiticus. Mycologia 101: 275-280.
18. Olarte RA, Horn BW, Dorner JW, Monacell JT, Singh R, et al. (2012) Effect of sexual recombination on population diversity in aflatoxin production by Aspergillus flavus and evidence for cryptic heterokaryosis. Molecular Ecology 21: 1453-1476.
19. 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.
20. Papa KE, (1973) The parasexual cycle in Aspergillus flavus. Mycologia 65: 1201-1205.
21. Papa KE, (1978) The parasexual cycle in Aspergillus parasiticus. Mycologia 70: 766-773.
22. Grubisha LC, Cotty PJ, (2009) Genetic isolation among sympatric vegetative compatibility groups of the aflatoxin-producing fungus Aspergillus flavus. Molecular Ecology 19: 269-280.
23. Horn BW, Greene RL, Sobolev VS, Dorner JW, Powell JH, 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.
24. Carbone I, Jakobek JL, Ramirez-Prado JH, Horn BW, (2007) Recombination, balancing selection and adaptive evolution in the aflatoxin gene cluster of Aspergillus parasiticus. Molecular Ecology 16: 4401-4417.
25. 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.
26. Worthington C, J. (2011) Evidence for recombination, heterosis and toxigenesis in experimental hybrid crosses between Aspergillus flavus and Aspergillus parasiticus. Raleigh: North Carolina State University.
27. Leslie JF, Klein KK, (1996) Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics 144: 557-567.
28. 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.
29. Horn BW, Dorner JW, (1999) Regional Differences in Production of Aflatoxin B1 and Cyclopiazonic Acid by Soil Isolates of Aspergillus flavus along a Transect within the United States. Applied and Environmental Microbiology 65: 1444-1449.
30. 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.
31. Moore GG (2010) Global population structure and aflatoxin chemotype diversity in Aspergillus section Flavi. Raleigh: North Carolina State University.
32. Aylor DL, Price EW, Carbone I, (2006) SNAP: Combine and Map modules for multilocus population genetic analysis. Bioinformatics 22: 1399-1401.
33. Bowden LC, Price EW, Carbone I (2008) SNAP Clade and Matrix, Version 2. Distributed over the Internet, http://www.cals.ncsu.edu/plantpath/faculty/carbone/home.html, Department of Plant Pathology, North Carolina State University.
34. Price EW, Carbone I, (2005) SNAP: workbench management tool for evolutionary population genetic analysis. Bioinformatics 21: 402-404.
35. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, et al. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23: 2633-2635.
36. Myers SR, Griffiths RC, (2003) Bounds on the minimum number of recombination events in a sample history. Genetics 163: 375-394.
37. Hey J, Wakeley J, (1997) A coalescent estimator of the population recombination rate. Genetics 145: 833-846.
38. Auton A, McVean G, (2007) Recombination rate estimation in the presence of hotspots. Genome Research 17: 1219-1227.
39. Watterson GA, (1975) On the number of segregating sites in genetical models without recombination. Theoretical Population Biology 7: 256-276.
40. Tajima F, (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
41. Fu YX, Li WH, (1993) Statistical tests of neutrality of mutations. Genetics 133: 693-709.
42. Tsai IJ, Burt A, Koufopanou V, (2010) Conservation of recombination hotspots in yeast. Proceedings of the National Academy of Sciences of the United States of America 107: 7847-7852.
43. Kurtzman CP, Smiley MJ, Robnett CJ, Wicklow DT, (1986) DNA relatedness among wild and domesticated species in the Aspergillus flavus group. Mycologia 78: 955-959.
44. Worthington CJ, Horn BW, Moore GG, Monacell JT, Singh R, et al. (2011) Hybridization between Aspergillus flavus and Aspergillus parasiticus. The 26th Fungal Genetics Conference. Asilomar Conference Center, Pacific Grove, CA.
45. Probst C, Callicott KA, Cotty PJ, (2012) Deadly strains of Kenyan Aspergillus are distinct from other aflatoxin producers. European Journal of Plant Pathology 132: 419-429.
46. Henk DA, Shahar-Golan R, Devi KR, Boyce KJ, Zhan N, et al. (2012) Clonality despite sex: the evolution of host-associated sexual neighborhoods in the pathogenic fungus Penicillium marneffei. PLoS pathogens 8: e1002851.
47. Dorner JW (2005) Biological control of aflatoxin crop contamination. In: Abbas HK, editor. Aflatoxin and Food Safety: CRC Press: Boca Raton, FL. pp. 333-352.