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Research Article

Ecology and Population Biology of Aflatoxigenic Fungi in Soil

Pages 351-379 | Published online: 08 Nov 2003

References

  • Angle J. S., Dunn K. A., Wagner G. H. Effect of cultural practices on the soil population of Aspergillus flavus and Aspergillus parasiticus. Soil Sci. Soc. Am. J. 1982; 46: 301–304
  • Aucamp J. L. The role of mite vectors in the development of aflatoxin in groundnuts. J. Stored Prod. Res. 1969; 5: 245–249
  • Barnes S. E., Dola T. P., Bennett J. W., Bhatnagar D. Synthesis of sterigmatocystin on a chemically defined medium by species of Aspergillus and Chaetomium. Mycopathologia 1994; 125: 173–178
  • Bayman P., Cotty P. J. Vegetative compatibility and genetic diversity in the Aspergillus flavus population of a single field. Can. J. Bot. 1991; 69: 1707–1711
  • Bayman P., Cotty P. J. Genetic diversity in Aspergillus flavus: association with aflatoxin production and morphology. Can. J. Bot. 1993; 71: 23–31
  • Betts W. B., Dart R. K. Initial reactions in degradation of tri‐ and tetrameric lignin‐related compounds by Aspergillus flavus. Mycol. Res. 1989; 92: 177–181
  • Bosland P. W., Williams P. H. An evaluation of Fusarium oxysporum from crucifers based on pathogenicity, isozyme polymorphism, vegetative compatibility, and geographic origin. Can. J. Bot. 1987; 65: 2067–2073
  • Bowen K. L., Mack T. P. Relationship of damage from the lesser cornstalk borer to Aspergillus flavus contamination in peanuts. J. Entomol. Sci. 1993; 28: 29–42
  • Boyd M. L., Cotty P. J. Aspergillus flavus and aflatoxin contamination of leguminous trees of the Sonoran Desert in Arizona. Phytopathology 2001; 91: 913–919
  • Calvert O. H., Lillehoj E. B., Kwolek W. F., Zuber M. S. Aflatoxin B1 and G1 production in developing Zea mays kernels from mixed inocula of Aspergillus flavus and A. parasiticus. Phytopathology 1978; 68: 501–506
  • Cardwell K. F., Cotty P. J. Distribution of Aspergillus section Flavi among field soils from the four agroecological zones of the Republic of Bénin, West Africa. Plant Dis. 2002; 86: 434–439
  • Carter D., Bui T., Walsh S., Tran‐Dinh N. RAPD analysis of Aspergillus parasiticus isolates from peanut growing soils in Queensland, Australia. J. Food Mycol. 1998; 1: 31–39
  • Christensen M., Tuthill D. E. Aspergillus: an overview. Advances in Penicillium and Aspergillus Systematics, R. A. Samson, J. I. Pitt. Plenum Press, New York 1985; 195–209
  • Cole R. J., Cox R. H. Handbook of Toxic Fungal Metabolites. Academic Press, New York 1981, 937 pp.
  • Cole R. J., Hill R. A., Blankenship P. D., Sanders T. H. Color mutants of Aspergillus flavus and Aspergillus parasiticus in a study of preharvest invasion of peanuts. Appl. Environ. Microbiol. 1986; 52: 1128–1131
  • Coley‐Smith J. R., Cooke R. C. Survival and germination of fungal sclerotia. Annu. Rev. Phytopathol. 1971; 9: 65–92
  • Cotty P. J. Virulence and cultural characteristics of two Aspergillus flavus strains pathogenic on cotton. Phytopathology 1989; 79: 808–814
  • Cotty P. J. 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 1994; 84: 1270–1277
  • Cotty P. J. Aflatoxin‐producing potential of communities of Aspergillus section Flavi from cotton producing areas in the United States. Mycol. Res. 1997; 101: 698–704
  • Cotty P. J., Cardwell K. F. Divergence of West African and North American communities of Aspergillus section Flavi. Appl. Environ. Microbiol. 1999; 65: 2264–2266
  • Cotty P. J., Cleveland T. E., Brown R. L., Mellon J. E. Variation in polygalacturonase production among Aspergillus flavus isolates. Appl. Environ. Microbiol. 1990; 56: 3885–3887
  • Davis N. D., Diener U. L., Agnihotri V. P. Production of aflatoxins B1 and G1 in chemically defined medium. Mycopathol. Mycol. Appl. 1967; 31: 251–256
  • Diener U. L., Cole R. J., Sanders T. H., Payne G. A., Lee L. S., Klich M. A. Epidemiology of aflatoxin formation by Aspergillus flavus. Annu. Rev. Phytopathol. 1987; 25: 249–270
  • Diener U. L., Pettit R. E., Cole R. J. Aflatoxins and other mycotoxins in peanuts. Peanut Science and Technology, H. E. Pattee, C. T. Young. American Peanut Research and Education Society, Yoakum, TX 1982; 486–519
  • Dorner J. W., Cole R. J., Blankenship P. D. Effect of inoculum rate of biological control agents on preharvest aflatoxin contamination of peanuts. Biol. Cont. 1998; 12: 171–176
  • Dorner J. W., Cole R. J., Diener U. L. The relationship of Aspergillus flavus and Aspergillus parasiticus with reference to production of aflatoxins and cyclopiazonic acid. Mycopathologia 1984; 87: 13–15
  • Dorner J. W., Cole R. J., Sanders T. H., Blankenship P. D. Interrelationship of kernel water activity, soil temperature, maturity, and phytoalexin production in preharvest aflatoxin contamination of drought‐stressed peanuts. Mycopathologia 1989; 105: 117–128
  • Dorner J. W., Cole R. J., Wicklow D. T. Aflatoxin reduction in corn through field application of competitive fungi. J. Food Prot. 1999; 62: 650–656
  • Doster M. A., Michailides T. J. Development of Aspergillus molds in litter from pistachio trees. Plant Dis. 1994; 78: 393–397
  • Doster M. A., Michailides T. J., Morgan D. P. Aspergillus species and mycotoxins in figs from California orchards. Plant Dis. 1996; 80: 484–489
  • Frank Z. R., Smulevitch Y., Lisker N. Preharvest kernel invasion in groundnut genotypes by Aspergillus flavus and its relation to the pod surface area. Euphytica 1994; 75: 207–213
  • Garber R. K., Cotty P. J. Formation of sclerotia and aflatoxins in developing cotton bolls infected by the S strain of Aspergillus flavus and potential for biocontrol with an atoxigenic strain. Phytopathology 1997; 87: 940–945
  • Geiser D. M., Dorner J. W., Horn B. W., Taylor J. W. The phylogenetics of mycotoxin and sclerotium production in Aspergillus flavus and Aspergillus oryzae. Fungal Genet. Biol. 2000; 31: 169–179
  • Geiser D. M., Pitt J. I., Taylor J. W. Cryptic speciation and recombination in the aflatoxin‐producing fungus Aspergillus flavus. Proc. Natl. Acad. Sci. U.S.A. 1998; 95: 388–393
  • Gordon T. R., Okamoto D. Vegetative compatibility groupings in a local population of Fusarium oxysporum. Can. J. Bot. 1991; 69: 168–172
  • Goto T., Ito Y., Peterson S. W., Wicklow D. T. Mycotoxin producing ability of Aspergillus tamarii. Mycotoxins 1997; 44: 17–20
  • Griffin G. J. Fusarium oxysporum and Aspergillus flavus spore germination in the rhizosphere of peanut. Phytopathology 1969; 59: 1214–1218
  • Griffin G. J. Conidial germination and population of Aspergillus flavus in the geocarposphere of peanut. Phytopathology 1972; 62: 1387–1391
  • Griffin G. J., Garren K. H. Population levels of Aspergillus flavus and the A. niger group in Virginia peanut field soils. Phytopathology 1974; 64: 322–325
  • Griffin G. J., Garren K. H. Colonization of rye green manure and peanut fruit debris by Aspergillus flavus and Aspergillus niger group in field soils. Appl. Environ. Microbiol. 1976; 32: 28–32
  • Griffin G. J., Garren K. H., Taylor J. D. Influence of crop rotation and minimum tillage on the population of Aspergillus flavus group in peanut field soil. Plant Dis. 1981; 65: 898–900
  • Griffin G. J., Smith E. P., Robinson T. J. Population patterns of Aspergillus flavus group and A. niger group in field soils. Soil Biol. Biochem. 2001; 33: 253–257
  • Hale M. G., Griffin G. J. The effect of mechanical injury on exudation from immature and mature peanut fruits under axenic conditions. Soil Biol. Biochem. 1976; 8: 225–227
  • Hesseltine C. W., Sorenson W. G., Smith M. Taxonomic studies of the aflatoxin‐producing strains in the Aspergillus flavus group. Mycologia 1970a; 62: 123–132
  • Hesseltine C. W., Shotwell O. L., Smith M., Ellis J. J., Vandegraft E., Shannon G. Production of various aflatoxins by strains of the Aspergillus flavus series. Toxic Micro‐Organisms, M. Herzberg. U.S. Gov. Printing Off., Washington, DC 1970b; 202–210
  • Hill R. A., Blankenship P. D., Cole R. J., Sanders T. H. Effects of soil moisture and temperature on preharvest invasion of peanuts by the Aspergillus flavus group and subsequent aflatoxin development. Appl. Environ. Microbiol. 1983; 45: 628–633
  • Hill R. A., Wilson D. M., Burg W. R., Shotwell O. L. Viable fungi in corn dust. Appl. Environ. Microbiol. 1984; 47: 84–87
  • Hill R. A., Wilson D. M., McMillian W. W., Widstrom N. W., Cole R. J., Sanders T. H., Blankenship P. D. Ecology of the Aspergillus flavus group and aflatoxin formation in maize and groundnut. Trichothecenes and Other Mycotoxins, J. Lacey. John Wiley, ChichesterUnited Kingdom 1985; 79–95
  • Horn B. W., Dorner J. W. Soil populations of Aspergillus species from section Flavi along a transect through peanut‐growing regions of the United States. Mycologia 1998; 90: 767–776
  • Horn B. W., Dorner J. W. Regional differences in production of aflatoxin B1 and cyclopiazonic acid by soil isolates of Aspergillus flavus along a transect within the United States. Appl. Environ. Microbiol. 1999; 65: 1444–1449
  • Horn B. W., Dorner J. W. Effect of competition and adverse culture conditions on aflatoxin production by Aspergillus flavus through successive generations. Mycologia 2002; 94: 741–751
  • Horn B. W., Dorner J. W., Greene R. L., Blankenship P. D., Cole R. J. Effect of Aspergillus parasiticus soil inoculum on invasion of peanut seeds. Mycopathologia 1994; 125: 179–191
  • Horn B. W., Greene R. L. Vegetative compatibility within populations of Aspergillus flavus, A. parasiticus, and A. tamarii from a peanut field. Mycologia 1995; 87: 324–332
  • Horn B. W., Greene R. L., Dorner J. W. Effect of corn and peanut cultivation on soil populations of Aspergillus flavus and A. parasiticus in southwestern Georgia. Appl. Environ. Microbiol. 1995; 61: 2472–2475
  • Horn B. W., Greene R. L., Sobolev V. S., Dorner J. W., Powell J. H., Layton R. C. Association of morphology and mycotoxin production with vegetative compatibility groups in Aspergillus flavus, A. parasiticus, and A. tamarii. Mycologia 1996; 88: 574–587
  • Horn B. W., Greene R. L., Sorensen R. B., Blankenship P. D., Dorner J. W. Conidial movement of nontoxigenic Aspergillus flavus and A. parasiticus in peanut fields following application to soil. Mycopathologia 2001; 151: 81–92
  • Hussein H. S., Brasel J. M. Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology 2001; 167: 101–134
  • Ito Y., Peterson S. W., Wicklow D. T., Goto T. Aspergillus pseudotamarii, a new aflatoxin producing species in Aspergillus section Flavi. Mycol. Res. 2001; 105: 233–239
  • Joffe A. Z. Aflatoxin produced by 1,626 isolates of Aspergillus flavus from groundnut kernels and soils in Israel. Nature 1969; 221: 492
  • Johnson S. J., Smith J. W. Ecology of Elasmopalpus lignosellus parasite complex on peanuts in Texas. Ann. Entomol. Soc. Am. 1981; 74: 467–471
  • Jones D., Bass M. H. Evaluation of pitfall traps for sampling lesser cornstalk borer larvae in peanuts. J. Econ. Entomol. 1979; 72: 289–290
  • Jones R. K., Duncan H. E., Hamilton P. B. Planting date, harvest date, and irrigation effects on infection and aflatoxin production by Aspergillus flavus in field corn. Phytopathology 1981; 71: 810–816
  • Klich M. A. Relation of plant water potential at flowering to subsequent cottonseed infection by Aspergillus flavus. Phytopathology 1987; 77: 739–741
  • Klich M. A. Biogeography of Aspergillus species in soil and litter. Mycologia 2002a; 94: 21–27
  • Klich M. A. Identification of Common Aspergillus Species. Centraalbureau voor Schimmelcultures, UtrechtThe Netherlands 2002b, 116 pp.
  • Klich M. A., Mullaney E. J., Daly C. B., Cary J. W. Molecular and physiological aspects of aflatoxin and sterigmatocystin biosynthesis by Aspergillus tamarii and A. ochraceoroseus. Appl. Microbiol. Biotechnol. 2000; 53: 605–609
  • Klich M. A., Pitt J. I. Differentiation of Aspergillus flavus from A. parasiticus and other closely related species. Trans. Br. Mycol. Soc. 1988; 91: 99–108
  • Klich M. A., Tiffany L. H., Knaphus G. Ecology of the aspergilli of soils and litter. Aspergillus: Biology and Industrial Applications, J. W. Bennett, M. A. Klich. Butterworth‐Heinemann, Boston 1992; 329–353
  • Kloepper J. W., Bowen K. L. Quantification of the geocarposphere and rhizosphere effect of peanut (Arachis hypogaea L.). Plant Soil 1991; 136: 103–109
  • Kurtzman C. P., Horn B. W., Hesseltine C. W. Aspergillus nomius, a new aflatoxin‐producing species related to Aspergillus flavus and Aspergillus tamarii. Antonie van Leeuwenhoek 1987; 53: 147–158
  • Lamb M. C., Sternitzke D. A. Cost of aflatoxin to the farmer, buying point, and sheller segments of the Southeast United States peanut industry. Peanut Sci. 2001; 28: 59–63
  • Larkin R. P., Hopkins D. L., Martin F. N. Vegetative compatibility within Fusarium oxysporum f.sp. niveum and its relationship to virulence, aggressiveness, and race. Can. J. Microbiol. 1990; 36: 352–358
  • Lee L. S., Lee L. V., Jr., Russell T. E. Aflatoxin in Arizona cottonseed: field inoculation of bolls by Aspergillus flavus spores in wind‐driven soil. JAOCS 1986; 63: 530–532
  • Leslie J. F. Fungal vegetative compatibility. Annu. Rev. Phytopathol. 1993; 31: 127–150
  • Lillehoj E. B., McMillian W. W., Guthrie W. D., Barry D. Aflatoxin‐producing fungi in preharvest corn: inoculum source in insects and soils. J. Environ. Qual. 1980; 9: 691–694
  • Long K., Ghazali H. M., Ariff A., Man Y. C., Bucke C. Substrate preference of mycelium‐bound lipase from a strain of Aspergillus flavus link. Biotechnol. Lett. 1998; 20: 369–372
  • Lussenhop J., Wicklow D. T. Nitidulid beetles (Nitidulidae: Coleoptera) as vectors of Aspergillus flavus in pre‐harvest maize. Trans. Mycol. Soc. Jpn 1990; 31: 63–74
  • Lynch R. E., Ouedraogo A. P., Dicko I. Insect damage to groundnut in semi‐arid tropical Africa. Agrometeorology of Groundnut, Proceedings of an International Symposium. ICRISAT, Andhra PradeshIndia 1986; 175–183
  • Lynch R. E., Wightman J. A., Ranga Rao G. V. Insects and arthropods. Compendium of Peanut Diseases2nd ed., N. Kokalis‐Burelle, D. M. Porter, R. Rodríguez‐Kábana, D. H. Smith, P. Subrahmanyam. APS Press, St. Paul, Minnesota 1997; 65–69
  • Lynch R. E., Wilson D. M. Enhanced infection of peanut, Arachis hypogaea L., seeds with Aspergillus flavus group fungi due to scarification of peanut pods by the lesser cornstalk borer, Elasmopalpus lignosellus (Zeller). Peanut Sci. 1991; 18: 110–116
  • Maggi O., Persiani A. M. Mycological studies of the soil. Comparative Studies on Microfungi in Tropical Ecosystems, Mycological Studies in South Western Ivory Coast Forest, A. Rambelli, A. M. Persiani, O. Maggi, D. Lunghini, S. Onofri, S. Riess, G. Dowgiallo, G. Puppi. MAB, UNESCO, Rome 1983; 69–94
  • Manabe M., Tsuruta O. Geographical distribution of aflatoxin‐producing fungi inhabiting in Southeast Asia. Jpn. Agric. Res. Quart. 1978; 12: 224–227
  • Manabe M., Tsuruta O., Tanaka K., Matsuura S. Distribution of aflatoxin‐producing fungi in soil in Japan. Trans. Mycol. Soc. Jpn. 1976; 17: 436–444
  • McAlpin C. E., Wicklow D. T., Platis C. E. Genotypic diversity of Aspergillus parasiticus in an Illinois corn field. Plant Dis. 1998; 82: 1132–1136
  • McAlpin C. E., Wicklow D. T., Horn B. W. DNA fingerprinting analysis of vegetative compatibility groups in Aspergillus flavus from a peanut field in Georgia. Plant Dis. 2002; 86: 254–258
  • McDonald D. The influence of the developing groundnut fruit on soil mycoflora. Trans. Br. Mycol. Soc. 1969; 53: 393–406
  • McGee D. C., Olanya O. M., Hoyos G. M., Tiffany L. H. Populations of Aspergillus flavus in the Iowa cornfield ecosystem in years not favorable for aflatoxin contamination of corn grain. Plant Dis. 1996; 80: 742–746
  • Novas M. V., Cabral D. Association of mycotoxin and sclerotia production with compatibility groups in Aspergillus flavus from peanut in Argentina. Plant Dis. 2002; 86: 215–219
  • Olanya O. M., Hoyos G. M., Tiffany L. H., McGee D. C. Waste corn as point source of inoculum for Aspergillus flavus in the corn agroecosystem. Plant Dis. 1997; 81: 576–581
  • Olutiola P. O. Cellulase enzymes in culture filtrates of Aspergillus flavus. Trans. Br. Mycol. Soc. 1976; 67: 265–268
  • Orum T. V., Bigelow D. M., Nelson M. R., Howell D. R., Cotty P. J. Spatial and temporal patterns of Aspergillus flavus strain composition and propagule density in Yuma County, Arizona, soils. Plant Dis. 1997; 81: 911–916
  • Orum T. V., Bigelow D. M., Cotty P. J., Nelson M. R. Using predictions based on geostatistics to monitor trends in Aspergillus flavus strain composition. Phytopathology 1999; 89: 761–769
  • Papa K. E. The parasexual cycle in Aspergillus flavus. Mycologia 1973; 65: 1201–1205
  • Papa K. E. The parasexual cycle in Aspergillus parasiticus. Mycologia 1978; 70: 766–773
  • Papa K. E. Heterokaryon incompatibility in Aspergillus flavus. Mycologia 1986; 78: 98–101
  • Payne G. A. Process of contamination by aflatoxin‐producing fungi and their impact on crops. Mycotoxins in Agriculture and Food Safety, K. K. Sinha, D. Bhatnagar. Marcel Dekker, New York 1998; 279–306
  • Peraica M., Radić B., Lucić A., Pavlović M. Toxic effects of mycotoxins in humans. Bull. World Health Organ. 1999; 77: 754–766
  • Peterson S. W., Ito Y., Horn B. W., Goto T. Aspergillus bombycis, a new aflatoxigenic species and genetic variation in its sibling species, A. nomius. Mycologia 2001; 93: 689–703
  • Pettit R. E., Taber R. A., Schroeder H. W. Prevalence of Aspergillus flavus in peanut soils. J. Am. Peanut Res. Assoc. 1973; 5: 195
  • Raper K. B., Fennell D. I. The Genus Aspergillus. Williams and Wilkins, Baltimore, MD 1965, 686 pp.
  • Saito M., Tsuruta O. A new variety of Aspergillus flavus from tropical soil in Thailand and its aflatoxin productivity. Proc. Jpn. Assoc. Mycotoxicol. 1993; 37: 31–36
  • Schroeder H. W., Boller R. A. Aflatoxin production of species and strains of Aspergillus flavus group isolated from field crops. Appl. Microbiol. 1973; 25: 885–889
  • Shearer J. F., Sweets L. E., Baker N. K., Tiffany L. H. A study of Aspergillus flavus/parasiticus in Iowa crop fields: 1988–1990. Plant Dis. 1992; 76: 19–22
  • Siriacha P., Kawashima K., Kawasugi S., Saito M., Tonboon‐Ek P. Postharvest contamination of Thai corn with Aspergillus flavus. Cereal Chem. 1989; 66: 445–448
  • Stack J. P., Pettit P. E. Germination of Aspergillus flavus sclerotia in soil. Phytopathology 1984a; 74: 799
  • Stack J. P., Pettit P. E. Colonization of organic matter substrates in soil by Aspergillus flavus. Proc. Am. Peanut Res. Educ. Soc. 1984b; 16: 45
  • Subrahmanyam P., Rao A. S. Rhizosphere and geocarposphere mycoflora of groundnut (Arachis hypogaea Linn.). Proc. Indian Acad. Sci. 1977; 85B: 420–431
  • Tran‐Dinh N., Pitt J. I., Carter D. A. Molecular genotype analysis of natural toxigenic and nontoxigenic isolates of Aspergillus flavus and A. parasiticus. Mycol. Res. 1999; 103: 1485–1490
  • Umeh V. C., Waliyar F., Traoré A. Aspergillus species colonization of termite‐damaged peanuts in parts of West Africa and its control prospects. Peanut Sci. 2000; 27: 1–6
  • White J. P., Johnson G. T. Aflatoxin production correlated with nitrification in Aspergillus flavus group species. Mycologia 1982; 74: 718–723
  • Wicklow D. T. Survival of Aspergillus flavus sclerotia in soil. Trans. Br. Mycol. Soc. 1987; 89: 131–134
  • Wicklow D. T., Donahue J. E. Sporogenic germination of sclerotia in Aspergillus flavus and A. parasiticus. Trans. Br. Mycol. Soc. 1984; 82: 621–624
  • Wicklow D. T., Horn B. W., Burg W. R., Cole R. J. Sclerotium dispersal of Aspergillus flavus and Eupenicillium ochrosalmoneum from maize during harvest. Trans. Br. Mycol. Soc. 1984; 83: 299–303
  • Wicklow D. T., McAlpin C. E., Platis C. E. Characterization of the Aspergillus flavus population within an Illinois corn field. Mycol. Res. 1998; 102: 263–268
  • Wicklow D. T., Wilson D. M. Germination of Aspergillus flavus sclerotia in a Georgia maize field. Trans. Br. Mycol. Soc. 1986; 87: 651–653
  • Wicklow D. T., Wilson D. M., Nelsen T. C. Survival of Aspergillus flavus sclerotia and conidia buried in soil in Illinois or Georgia. Phytopathology 1993; 83: 1141–1147
  • Wilson D. M., Holbrook C. C., Matheron M. E. Aspergillus flavus and A. parasiticus used as peanut plot inoculum to study preharvest aflatoxin contamination. Proc. Am. Peanut Res. Educ. Soc. 1996; 28: 30
  • Wilson D. M., McMillian W. W., Widstrom N. Use of Aspergillus flavus and A. parasiticus color mutants to study aflatoxin contamination of corn. Biodeterioration 6, S. Barry, D. R. Houghton, G. C. Llewellyn, C. E. O'Rear. CAB International, SloughUnited Kingdom 1986; 284–288
  • Xu H., Annis S., Linz J., Trail F. Infection and colonization of peanut pods by Aspergillus parasiticus and the expression of the aflatoxin biosynthetic gene, nor‐1, in infection hyphae. Physiol. Mol. Plant Pathol. 2000; 56: 185–196
  • Zummo N., Scott G. E. Relative aggressiveness of Aspergillus flavus and A. parasiticus on maize in Mississippi. Plant Dis. 1990; 74: 978–981

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