Seeds of aflatoxin-resistant and aflatoxin-susceptible maize lines were inoculated with conidia of aflatoxin-producing Aspergillus flavus or A. parasiticus isolates or isogenic non-producing mutants. Conidia were recovered from resistant maize seed after seven days in significantly lower amounts for aflatoxin-producing A. flavus and A. parasiticus strains than for isogenic mutants incapable of aflatoxin production. This result helps to explain why, in currently used biocontrol strategies for aflatoxin elimination, non-aflatoxigenic isolates are able to out-compete aflatoxin-producing isolates for invasion of the seed.
KeywordsSporesGene DisruptionBiocontrolFungi
K. Ehrlich, “Effect on Aflatoxin Production of Competition between Wild-Type and Mutant Strains of Aspergillus Parasiticus,” Mycopathologia, Vol. 97, No. 2, 1987, pp. 93-96. doi:10.1007/BF00436844
P. J. Cotty and P. Bayman, “Competitive Exclusion of a Toxigenic Strain of Aspergillus Flavus by an Atoxigenic Strain,” Phytopathology, Vol. 83, No. 12, 1993, pp. 1283-1287. doi:10.1094/Phyto-83-1283
D. T. Wicklow, J. R. Bobell and D. E. Palmquist, “Effect of Intraspecific Competition by Aspergillus Flavus on Aflatoxin Formation in Suspended Disc Culture,” Mycological Research, Vol. 107, No. Pt 5, 2003, pp. 617-623.
J. J. Pan and G. May, “Fungal-Fungal Associations Affect the Assembly of Endophyte Communities in Maize (Zea Mays),” Microbial Ecology, Vol. 58, No. 3, 2009, pp. 668-678. doi:10.1007/s00248-009-9543-7
C. Mille-Lindblom, H. Fischer and L. J. Tranvik, “Antagonism between Bacteria and Fungi: Substrate Competition and a Possible Tradeoff between Fungal Growth and Tolerance towards Bacteria,” Oikos, Vol. 113, No. 2, 2006, pp. 233-242. doi:10.1111/j.2006.0030-1299.14337.x
L. Losada, O. Ajayi, J. C. Frisvad, J. Yu and W. C. Nierman, “Effect of Competition on the Production and Activity of Secondary Metabolites in Aspergillus Species,” Medical Mycology, Vol. 47 Suppl 1, 2009, pp. S88-96. doi:10.1080/13693780802409542
K. Ehrlich, A. Ciegler, M. A. Klich and L. Lee, “Fungal Competition and Mycotoxin Production on Corn,” Experientia, Vol. 41, 1985, pp. 691-693. doi:10.1007/BF02007725
A. Velluti, S. Marin, L. Bettucci, A. J. Ramos and V. Sanchis, “The Effect of Fungal Competition on Colonization of Maize Grain by Fusarium Moniliforme, F. Proliferatum and F. Graminearum and on Fumonisin B-1 and Zearalenone Formation,” International Journal of Food Microbiology, Vol. 59, No. 1-2, 2000, pp. 59-66. doi:10.1016/S0168-1605(00)00289-0
N. Ramakrishna, J. Lacey and J. E. Smith, “The Effects of Fungal Competition on Colonization of Barley Grain by Fusarium Sporotrichioides on T-2 Toxin Formation,” Food Additives and Contaminants, Vol. 13, No. 8, 1996, pp. 939-948.
D. Bhatnagar, R. Brown, K. Ehrlich and T. E. Cleveland, “Mycotoxins Contaminating Cereal Grain Crops: Their Occurrence and Toxicity,” In: G. G. Khachatourians and D. K. Arora, Eds., Applied Mycology and Biotechnology, Vol. 2, Elsevier B.V., New York, 2002, pp. 171-196.
C. Probst, F. Schulthess and P. J. Cotty, “Impact of Aspergillus Section Flavi Community Structure on the Development of Lethal Levels of Aflatoxins in Kenyan Maize (Zea Mays),” Journal of Applied Microbiology, Vol. 108, No. 2, 2010, pp. 600-610. doi:10.1111/j.1365-2672.2009.04458.x
J. Atehrikeng, P. S. Ojiambo, M. Donner, T. Ikotun, R. A. Sikora, P. J. Cotty and R. Bandyopadhyay, “Distribution and Toxigenicity of Aspergillus Species Isolated from Maize Kernels from Three Agro-Ecological Zones in Nigeria,” International Journal of Food Microbiology, Vol. 122, No. 1-2, 2008, pp. 74-84. doi:10.1016/j.ijfoodmicro.2007.11.062
P. J. Cotty, “Biocompetitive Exclusion of Toxigenic Fungi,” In: D. Barug, Ed., The Mycotoxin Factbook, 2006, pp. 179-197.
K. R. N. Reddy, H. K. Abbas, C. A. Abel, W. T. Shier, C. A. F. Oliveira and C. R. Raghavender, “Mycotoxin Contamination of Commercially Important Agricultural Commodities,” Toxin Reviews, Vol. 28, No. 2-3, 2009, pp. 154-168. doi:10.1080/15569540903092050
H. K. Abbas, J. R. Wilkinson, R. M. Zablotowicz, C. Accinelli, C. A. Abel, H. A. Bruns and M. A. Weaver, “Ecology of Aspergillus Flavus, Regulation of Aflatoxin Production, and Management Strategies to Reduce Aflatoxin Contamination of Corn,” Toxin Reviews, Vol. 28, No. 2-3, 2009, pp. 142-153. doi:10.1080/15569540903081590
J. W. Dorner and B. W. Horn, “Separate and Combined Applications of Nontoxigenic Aspergillus Flavus and A. Parasiticus for Biocontrol of Aflatoxin in Peanuts,” Mycopathologia, Vol. 163, No. 4, 2007, pp. 215-223. doi:10.1007/s11046-007-9004-0
J. W. Dorner, “Efficacy of a Biopesticide for Control of Aflatoxins in Corn,” Journal of Food Protection, Vol. 73, No. 3, 2010, pp. 495-499.
R. Jaime-Garcia and P. J. Cotty, “Formulations of Aspergillus Flavus AF36 to Improve in-Field Residence and Sporulation,” Phytopathology, Vol. 98, No. 6, 2008, pp. S73-S73.
B. W. Horn, “Ecology and Population Biology of Aflatoxigenic Fungi in Soil,” Journal of Toxicology—Toxin Reviews, Vol. 22, No. 2-3, 2003, pp. 351-379.
B. W. Horn and J. W. Dorner, “Effect of Nontoxigenic Aspergillus Flavus and A. Parasiticus on Aflatoxin Contamination of Wounded Peanut Seeds Inoculated with Agricultural Soil Containing Natural Fungal Populations,” Biocontrol Science and Technology, Vol. 19, No. 3, 2009, pp. 249-262. doi:10.1080/09583150802696541
K. C. Ehrlich, P.-K. Chang, J. Yu and P. J. Cotty, “Aflatoxin Biosynthesis Cluster Gene cypA Is Required for G Aflatoxin Formation,” Applied and Environmental Microbiology, Vol. 70, No. 11, 2004, pp. 6518-6524. doi:10.1128/AEM.70.11.6518-6524.2004
K. C. Ehrlich, Q. Wei and D. Bhatnagar, “Increased Sensitivity of Aspergillus Flavus and A. Parasiticus Polyketide Synthase Mutants to UVB Light,” World Mycotoxin Journal, Vol. 3, No. 2010, pp. 263-270.
P. K. Chang, K. C. Ehrlich, J. E. Linz, D. Bhatnagar, T. E. Cleveland and J. W. Bennett, “Characterization of the Aspergillus Parasiticus niaD and niiA Gene Cluster,” Current Genetics, Vol. 30, No. 1, 1996, pp. 68-75. doi:10.1007/s002940050102
K. W. Campbell and D. G. White, “Evaluation of Corn Genotypes for Resistance to Aspergillus Ear Rot, Kernal Infection, and Aflatoxin Production,” Plant Disease, Vol. 79, No. 1995, pp. 1039-1045.
R. L. Brown, T. E. Cleveland, G. A. Payne, C. P. Woloshuk, K. W. Campbell and D. G. White, “Determination of Resistance to Aflatoxin Production in Maize Kernels and Detection of Fungal Colonization using an Aspergillus Flavus Transformant Expressing Escherichia Coli β-Glucuronidase,” Phytopathology, Vol. 85, No. 9, 1995, pp. 983-990. doi:10.1094/Phyto-85-983
R. L. Brown, C. S. Brown-Jenco, D. Bhatnagar and G. A. Payne, “Construction and Preliminary Evaluation of an Aspergillus Flavus Reporter Gene Construct as a Potential Tool for Screening Aflatoxin Resistance,” Journal of Food Protection, Vol. 66, No. 10, 2003, pp. 1927-1931.
Z. Y. Chen, R. L. Brown, T. E. Cleveland, K. F. Damann and J. S. Russin, “Comparison of Constitutive and Inducible Maize Kernel Proteins of Genotypes Resistant or Susceptible to Aflatoxin Production,” Journal of Food Protection, Vol. 64, No. 11, 2001, pp. 1785-1792.
H. Wilkinson, A. Ramaswamy, S. C. Sim and N. P. Keller, “Increased Conidiation Associated with Progression along the Sterigmatocystin Biosynthetic Pathway,” Mycologia, Vol. 96, 2004, pp. 1190-1198. doi:10.2307/3762134
O. Bayram, S. Krappmann, M. Ni, J. W. Bok, K. Helmstaedt, O. Valerius, S. Braus-Stromeyer, N. J. Kwon, N. P. Keller, J. H. Yu and G. H. Braus, “VelB/VeA/LaeA Complex Coordinates Light Signal with Fungal Development and Secondary Metabolism,” Science, Vol. 320, No. 5882, 2008, pp. 1504-1506. doi:10.1126/science.1155888
A. M. Calvo, R. A. Wilson, J. W. Bok and N. P. Keller, “Relationship between Secondary Metabolism and Fungal Development,” Microbiology and Molecular Biology Reviews, Vol. 66, No. 3, 2002, pp. 447-459. doi:10.1128/MMBR.66.3.447-459.2002
J. K. Hicks, J. H. Yu, N. P. Keller and T. H. Adams, “Aspergillus Sporulation and Mycotoxin Production both Require Inactivation of the FadA G Alpha Protein-Dependent Signaling Pathway,” The EMBO Journal, Vol. 16, No. 16, 1997, pp. 4916-4923. doi:10.1093/emboj/16.16.4916
S. N. Khan and T. A. Venkitasubramanian, “Cyclic AMP Pool and Aflatoxin Production in Aspergillus Parasiticus NRRL 3240 and Aspergillus Flavus NRRL 3537,” Indian Journal of Biochemistry and Biophysics, Vol. 24, No. 6, 1987, pp. 308-313.
T. A. Venkitasubramanian, R. K. Bhatnagar, S. Saraswathy, V. B. Rao and J. Sivaswami, “Intermediary Metabolism of Aspergillus Parasiticus in Relation to Aflatoxin Biosynthesis in Fungi,” Federation of European Microbiological Societies Symposium, No. 13, 1982, pp. 153-165.
R. L. Buchanan, S. B. Jones, W. V. Gerasimowicz, L. L. Zaika, H. G. Stahl and L. A. Ocker, “Regulation of Aflatoxin Biosynthesis: Assessment of the Role of Cellular Energy Status as a Regulator of the Induction of Aflatoxin Production,” Applied and Environmental Microbiology, Vol. 53, No. 6, 1987, pp. 1224-1231.