Aflatoxin contamination of maize grain is a huge economic and health problem, causing death and increased disease burden in much of the developing world and income loss in the developed world. Despite the gravity of the problem, deployable solutions are still being sought. In the past 15 years, much progress has been made in creating resistant maize inbred lines; mapping of genetic factors associated with resistance; and identifying possible resistance mechanisms. This review highlights this progress, most of which has occurred since the last time a review was published on this topic. Many of the needs highlighted in the last reviews have been addressed, and several solutions, taken together, can now greatly reduce the aflatoxin problem in maize grain. Continued research will soon lead to further solutions, which promise to further reduce and even eliminate the problem completely. 1. Introduction to the Problem Although the detrimental health effects of aflatoxins and grain contamination have been known for over 50 years [1–5], a satisfactory solution has yet to be attained, from either a health or economic point of view. Since the publication of earlier reviews [6–11], encouraging advances have been achieved, but much remains to be done. The more recent reviews by Gorman and Kang [7]; Brown et al. [10]; and Moreno and Kang [11] highlighted the need for new sources of resistant germplasm, which have since been identified. QTL mapping was also called for, and several mapping studies and one meta-analysis have now presented the genetic architecture of aflatoxin resistance in maize in many of the most resistant lines. The suggestion of the use of nontoxigenic A. flavus in the review of Moreno and Kang [11] has been implemented with considerable success in some countries. Other suggestions as to specific genetic mechanisms of resistance, tools to study the problem including laboratory assays and simpler inoculation procedures, nixtamalization and chemical remediation treatments, have not yet contributed to appreciable progress outside of a limited scope. However, all information, taken together, and added to new proteomic, genomic, and genetic studies, is beginning to fill in the larger picture of this very complicated disease problem of maize and other oil-seed crops. 2. Aflatoxins Aflatoxins are hepatotoxic, carcinogenic secondary metabolites produced by some species of the fungal genus Aspergillus. Aflatoxin is one of the most toxic compounds found in nature, and it can be lethal to humans and other animals in amounts measured in parts per billion. In
References
[1]
J. E. Burnside, W. L. Sippel, W. T. Carll, and E. R. Doll, “A disease of swine and cattle caused by eating moldy corn. II. Experimental production with pure cultures of molds,” American Journal of Veterinary Research, vol. 18, no. 69, pp. 817–824, 1957.
[2]
W. P. Blount, “A new turkey disease problem in England characterised by heavy mortality,” British Oil & Cake Mills, vol. 27, pp. 1–3, 1960.
[3]
H. de Iongh, R. K. Beerthuis, R. O. Vles, C. B. Barrett, and W. O. Ord, “Investigation of the factor in groundnut meal responsible for ‘Turkey X disease’,” Biochimica et Biophysica Acta, vol. 65, no. 3, pp. 549–551, 1962.
[4]
W. H. Butler, “Acute toxicity of aflatoxin B1 in rats,” British Journal of Cancer, vol. 18, pp. 756–762, 1964.
[5]
A. Ciegler, E. B. Lillehoj, R. E. Peterson, and H. H. Hall, “Microbial detoxification of aflatoxin,” Applied Microbiology, vol. 14, no. 6, pp. 934–939, 1966.
[6]
M. S. Zuber and E. B. Lillehoj, “Status of the aflatoxin problem in corn,” Journal of Environmental Quality, vol. 8, no. 1, pp. 1–5, 1979.
[7]
D. P. Gorman and M. S. Kang, “Preharvest aflatoxin contamination in maize: resistance and genetics,” Plant Breeding, vol. 107, no. 1, pp. 1–10, 1991.
[8]
G. A. Payne and N. W. Widstrom, “Aflatoxin in maize,” Critical Reviews in Plant Sciences, vol. 10, pp. 423–440, 1992.
[9]
N. W. Widstrom, “The aflatoxin problem with corn grain,” Advances in Agronomy, vol. 56, pp. 219–280, 1996.
[10]
R. L. Brown, Z. Chen, T. E. Cleveland, and J. S. Russin, “Advances in the development of host resistance in corn to aflatoxin contamination by Aspergillus flavus,” Phytopathology, vol. 89, no. 2, pp. 113–117, 1999.
[11]
O. J. Moreno and M. S. Kang, “Aflatoxins in maize: the problem and genetic solutions,” Plant Breeding, vol. 118, no. 1, pp. 1–16, 1999.
[12]
D. L. Eaton and J. D. Groopman, The Toxicology of Aflatoxins: Human Health, Veterinary and Agricultural Significance, Academic Press, 1993.
[13]
J. H. Williams, T. D. Phillips, P. E. Jolly, J. K. Stiles, C. M. Jolly, and D. Aggarwal, “Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions,” The American Journal of Clinical Nutrition, vol. 80, no. 5, pp. 1106–1122, 2004.
[14]
J. H. Williams, D. Aggarwal, P. E. Jolly, T. D. Phillips, and J. S. Wang, “Connecting the dots: logical and statistical connections between aflatoxin exposure and HIV/AIDS,” Peanut Collaborative Research Support Program, 2005.
[15]
M. S. Zuber, L. L. Darrah, E. B. Lillehoj, et al., “Comparison of open pollinated maize varieties and hybrids for preharvest aflatoxin contamination in the southern United States,” Plant Disease, vol. 67, pp. 185–187, 1983.
[16]
N. W. Widstrom, D. M. Wilson, and W. W. McMillian, “Ear resistance of maize inbreds to field aflatoxin contamination,” Crop Science, vol. 24, pp. 1155–1157, 1984.
[17]
N. W. Widstrom, D. M. Wilson, and W. W. McMillian, “Differentiation of maize genotypes for aflatoxin concentration in developing kernels,” Crop Science, vol. 26, pp. 935–937, 1986.
[18]
G. E. Scott and N. Zummo, “Sources of resistance in maize to kernel infection by Aspergillus flavus in the field,” Crop Science, no. 28, pp. 504–507, 1988.
[19]
A. M. Hamblin and D. G. White, “Inheritance of resistance to aspergillus ear rot and aflatoxin production of corn from Tex6,” Phytopathology, vol. 90, no. 3, pp. 292–296, 2000.
[20]
F. J. Betrán, T. Isakeit, and G. Odvody, “Aflatoxin accumulation of white and yellow maize inbreds in diallel crosses,” Crop Science, vol. 42, no. 6, pp. 1894–1901, 2002.
[21]
G. Naidoo, A. M. Forbes, C. Paul, D. G. White, and T. R. Rocheford, “Resistance to Aspergillus ear rot and aflatoxin accumulation in maize F1 hybrids,” Crop Science, vol. 42, no. 2, pp. 360–364, 2002.
[22]
W. P. Williams, G. L. Windham, and P. M. Buckley, “Diallel analysis of aflatoxin accumulation in maize,” Crop Science, vol. 48, no. 1, pp. 134–138, 2008.
[23]
W. P. Williams, M. D. Krakowsky, G. L. Windham, P. Balint-Kurti, L. K. Hawkins, and W. B. Henry, “Identifying maize germplasm with resistance to aflatoxin accumulation,” Toxin Reviews, vol. 27, pp. 319–345, 2008.
[24]
R. D. Walker and D. G. White, “Inheritance of resistance to Aspergillus ear rot and aflatoxin production of corn from CI2,” Plant Disease, vol. 85, no. 3, pp. 322–327, 2001.
[25]
W. W. McMillian, N. W. Widstrom, and D. M. Wilson, “Registration of GT-MAS:gk maize germplasm,” Crop Science, vol. 33, p. 882, 1993.
[26]
W. P. Williams and G. L. Windham, “Registration of maize germplasm line Mp715,” Crop Science, vol. 41, p. 1375, 2001.
[27]
W. P. Williams and G. L. Windham, “Registration of maize germplasm line Mp717,” Crop Science, vol. 46, pp. 1407–1408, 2006.
[28]
B. Z. Guo, R. G. Li, N. W. Widstrom, R. E. Lynch, and T. E. Cleveland, “Genetic variation within maize population GT-MAS:gk and the relationship with resistance to Aspergiilus flavus and aflatoxin production,” Theoretical and Applied Genetics, vol. 103, no. 4, pp. 533–539, 2001.
[29]
W. P. Williams and G. L. Windham, “Registration of Mp718 and Mp719 germplasm lines of maize,” Journal of Plant Registrations, vol. 6, no. 2, pp. 200–202, 2012.
[30]
K. Mayfield, F. J. Betrán, T. Isakeit et al., “Registration of maize germplasm lines Tx736, Tx739, and Tx740 for reducing preharvest aflatoxin accumulation,” Journal of Plant Registrations, vol. 6, no. 1, pp. 88–94, 2012.
[31]
R. Li, M. S. Kang, O. J. Moreno, and L. M. Pollak, “Field resistance to Aspergillus flavus from exotic maize (Zea mays L.) germplasm,” Plant Genetic Resources News, vol. 130, pp. 11–15, 2002.
[32]
W. B. Henry, G. L. Windham, D. E. Rowe, M. H. Blanco, S. C. Murray, and W. P. Williams, “Diallel analysis of diverse maize germplasm lines for resistance to aflatoxin accumulation,” Crop Science, vol. 53, no. 2, pp. 394–402, 2013.
[33]
M. L. Warburton, W. P. Williams, G. Windham et al., “Phenotypic and genetic characterization of a maize association mapping panel developed for the identification of new sources of resistance to Aspergillus flavus and aflatoxin accumulation,” Crop Science, vol. 53, pp. 2374–2383, 2013.
[34]
M. L. Warburton, “Identification and validation of genetic factors associated with aflatoxin accumulation and A. flavus resistance in maize,” in Proceedings of the American Seed Trade Association Annual Meetings, Chicago, Ill, USA, December 2013.
[35]
C. A. Paul, G. A. Naidoo, A. A. Forbes, V. A. Mikkilineni, D. A. White, and T. P. Rocheford, “Quantitative trait loci for low aflatoxin production in two related maize populations,” Theoretical and Applied Genetics, vol. 107, no. 2, pp. 263–270, 2003.
[36]
T. D. Brooks, W. P. Williams, G. L. Windham, M. C. Willcox, and H. K. Abbas, “Quantitative trait loci contributing resistance to aflatoxin accumulation in the maize inbred Mp313E,” Crop Science, vol. 45, no. 1, pp. 171–174, 2005.
[37]
M. L. Warburton, T. D. Brooks, M. D. Krakowsky, X. Shan, G. L. Windham, and W. P. Williams, “Identification and mapping of new sources of resistance to AFL atoxin accumulation in maize,” Crop Science, vol. 49, no. 4, pp. 1403–1408, 2009.
[38]
M. L. Warburton, T. D. Brooks, G. L. Windham, and W. P. Williams, “Identification of novel QTL contributing resistance to aflatoxin accumulation in maize,” Molecular Breeding, vol. 27, no. 4, pp. 491–499, 2011.
[39]
K. L. Mayfield, S. C. Murray, W. L. Rooney, T. Isakeit, and G. A. Odvody, “Confirmation of QTL reducing aflatoxin in maize testcrosses,” Crop Science, vol. 51, no. 6, pp. 2489–2498, 2011.
[40]
M. C. Willcox, G. L. Davis, M. L. Warburton et al., “Confirming quantitative trait loci for aflatoxin resistance from Mp313E in different genetic backgrounds,” Molecular Breeding, vol. 32, no. 1, pp. 15–26, 2013.
[41]
Z. Yin, Y. Wang, F. Wu, X. Gu, Y. Bian, and D. Deng, “Quantitative trait locus mapping of resistance to Aspergillus flavus infection using a recombinant inbred line population in maize,” Molecular Breeding, vol. 33, no. 1, pp. 39–49, 2014.
[42]
S. X. Mideros, M. L. Warburton, T. M. Jamann, G. L. Windham, W. P. Williams, and R. J. Nelson, “Quantitative trait loci influencing mycotoxin contamination of maize: analysis by linkage mapping, characterization of near-isogenic lines and meta-analysis,” Crop Science, vol. 54, no. 1, pp. 127–142, 2014.
[43]
K. N. Busboom and D. G. White, “Inheritance of resistance to aflatoxin production and aspergillus ear rot of corn from the cross of inbreds B73 and Oh516,” Phytopathology, vol. 94, no. 10, pp. 1107–1115, 2004.
[44]
R. J. Wisser, P. J. Balint-Kurti, and R. J. Nelson, “The genetic architecture of disease resistance in maize: a synthesis of published studies,” Phytopathology, vol. 96, no. 2, pp. 120–129, 2006.
[45]
Z. Huang, D. G. White, and G. A. Payne, “Corn seed proteins inhibitory to Aspergillus flavus and aflatoxin biosynthesis,” Phytopathology, vol. 87, no. 6, pp. 622–627, 1997.
[46]
R. Y. Kelley, W. P. Williams, J. E. Mylroie et al., “Genomic profile of maize response to Aspergillus flavus infection,” Toxin Reviews, vol. 28, no. 2-3, pp. 129–141, 2009.
[47]
R. Y. Kelley, W. P. Williams, J. E. Mylroie et al., “Identification of maize genes associated with host plant resistance or susceptibility to aspergillus flavus infection and aflatoxin accumulation,” PLoS ONE, vol. 7, no. 5, Article ID e36892, 2012.
[48]
O. Pechanova, T. Pechan, W. P. Williams, and D. S. Luthe, “Proteomic analysis of the maize rachis: potential roles of constitutive and induced proteins in resistance to Aspergillus flavus infection and aflatoxin accumulation,” Proteomics, vol. 11, no. 1, pp. 114–127, 2011.
[49]
Z. Y. Chen, R. L. Brown, K. E. Damann, and T. E. Cleveland, “Identification of unique or elevated levels of kernel proteins in aflatoxin-resistant maize genotypes through proteome analysis,” Phytopathology, vol. 92, no. 10, pp. 1084–1094, 2002.
[50]
B. Z. Guo, J. S. Russin, T. E. Cleveland, R. L. Brown, and N. W. Widstrom, “Wax and cutin layers in maize kernels associated with resistance to aflatoxin production by Aspergillus flavus,” Journal of Food Protection, vol. 58, no. 3, pp. 296–300, 1995.
[51]
R. J. Elshire, J. C. Glaubitz, Q. Sun et al., “A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species,” PLoS ONE, vol. 6, no. 5, Article ID e19379, 2011.
[52]
I. D. Barrero Farfan, G. N. de la Fuente, S. C. Murray et al., “Whole genome association study for drought, aflatoxin resistance, and important agronomic traits in maize in a sub-tropical environment,” PLoS ONE. In press.
[53]
M. L. Warburton, W. P. Williams, L. Hawkins et al., “A public platform for the verification of the phenotypic effect of candidate genes for resistance to aflatoxin accumulation and Aspergillus flavus infection in maize,” Toxins, vol. 3, no. 7, pp. 754–765, 2011.
[54]
J. E. Mylroie, M. L. Warburton, and J. R. Wilkinson, “Development of a gene-based marker correlated to reduced aflatoxin accumulation in maize,” Euphytica, vol. 194, pp. 431–441, 2013.
[55]
M. L. Warburton, W. P. Williams, L. Hawkins et al., “Ongoing results from a candidate gene pipeline for testing the effect of DNA sequences on aflatoxin accumulation and A. flavus resistance in maize,” in Proceedings of the ASA-CSSA-SSA Annual Meeting, pp. 109–110, Crop Science Society of America, Pittsburgh, Pa, USA, October 2012.
[56]
Z. Y. Chen, M. L. Warburton, L. Hawkins, Q. Wei, R. L. Brown, and D. Bhatnagar, “RNAi silencing of the 14？kDa trypsin inhibitor protein in maize and its effect on host resistance against Aspergillus flavus infection/aflatoxin production,” . In press.
[57]
Z. Chen, R. L. Brown, K. E. Damann, and T. E. Cleveland, “PR10 expression in maize and its effect on host resistance against Aspergillus flavus infection and aflatoxin production,” Molecular Plant Pathology, vol. 11, no. 1, pp. 69–81, 2010.
[58]
S. A. Christensen, A. Nemchenko, E. Borrego et al., “The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack,” Plant Journal, vol. 74, no. 1, pp. 59–73, 2013.
[59]
X. Gao, W. B. Shim, C. G？bel et al., “Disruption of a maize 9-lipoxygenase results in increased resistance to fungal pathogens and reduced levels of contamination with mycotoxin fumonisin,” Molecular Plant-Microbe Interactions, vol. 20, no. 8, pp. 922–933, 2007.
[60]
M. C. Asters, W. P. Williams, A. D. Perkins, J. E. Mylroie, G. L. Windham, and X. Shan, “Relating significance and relations of differentially expressed genes in response to Aspergillus flavus infection in maize,” Scientific Reports, vol. 4, article 4815, 2014.
[61]
S. V. Gembeh, R. L. Brown, C. Grimm, and T. E. Cleveland, “Identification of chemical components of corn kernel pericarp wax associated with resistance to Aspergillus flavus infection and aflatoxin production,” Journal of Agricultural and Food Chemistry, vol. 49, no. 10, pp. 4635–4641, 2001.
[62]
Z.-. Chen, R. L. Brown, K. Rajasekaran, K. E. Damann, and T. E. Cleveland, “Identification of a maize kernel pathogenesis-related protein and evidence for its involvement in resistance to Aspergillus flavus infection and aflatoxin production,” Phytopathology, vol. 96, no. 1, pp. 87–95, 2006.
[63]
V. V. Lozovaya, A. Waranyuwat, and J. M. Widholm, “β-1,3-Glucanase and resistance to Aspergillus flavus infection in maize,” Crop Science, vol. 38, no. 5, pp. 1255–1260, 1998.
[64]
B. Peethambaran, L. Hawkins, G. L. Windham, W. P. Williams, and D. S. Luthe, “Anti-fungal activity of maize silk proteins and role of chitinases in Aspergillus flavus resistance,” Toxin Reviews, vol. 29, no. 1, pp. 27–39, 2010.
[65]
K. Nielsen, G. A. Payne, and R. S. Boston, “Maize ribosome-inactivating protein inhibits normal development of Aspergillus nidulans and Aspergillus flavus,” Molecular Plant-Microbe Interactions, vol. 14, no. 2, pp. 164–172, 2001.
[66]
R. Y. Kelley, C. Gresham, J. Harper et al., “Integrated database for identifying candidate genes for Aspergillus flavus resistance in maize,” BMC Bioinformatics, vol. 11, no. 6, article 25, 2010.
[67]
N. W. Widstrom, A. Butron, B. Z. Guo et al., “Control of preharvest aflatoxin contamination in maize by pyramiding QTL involved in resistance to ear-feeding insects and invasion by Aspergillus spp.,” European Journal of Agronomy, vol. 19, no. 4, pp. 563–572, 2003.
[68]
W. P. Williams, G. L. Windham, P. M. Buckley, and J. M. Perkins, “Southwestern corn borer damage and aflatoxin accumulation in conventional and transgenic corn hybrids,” Field Crops Research, vol. 91, no. 2-3, pp. 329–336, 2005.
[69]
G. L. Windham, W. P. Williams, and F. M. Davis, “Effects of the southwestern corn borer on Aspergillus flavus kernel infection and aflatoxin accumulation in maize hybrids,” Plant Disease, vol. 83, no. 6, pp. 535–540, 1999.
[70]
M. Sétamou, K. F. Cardwell, F. Schulthess, and K. Hell, “Effect of insect damage to maize ears, with special reference to Mussidia nigrivenella (Lepidoptera: Pyralidae), on Aspergillus flavus (Deuteromycetes: Monoliales) infection and aflatoxin production in maize before harvest in the Republic of Benin,” Journal of Economic Entomology, vol. 91, no. 2, pp. 433–438, 1998.
[71]
W. W. McMillian, N. W. Widstrom, D. M. Wilson, and R. A. Hill, “Transmission by maize weevils of Aspergillus flavus and its survival on selected corn hybrids,” Journal of Economic Entomology, vol. 73, no. 6, pp. 793–794, 1980.
[72]
N. W. Widstrom, “The role of insects and other plant pests in aflatoxin contamination of corn, cotton, and peanuts—a review,” Journal of Environmental Quality, vol. 8, no. 1, pp. 5–11, 1979.
[73]
S. F. Marsh and G. A. Payne, “Preharvest infection of corn silks and kernels by Aspergillus flavus,” Phytopath, vol. 74, pp. 1284–1289, 1984.
[74]
G. A. Payne, D. L. Thompson, E. B. Lillehoj, M. S. Zuber, and C. R. Adkins, “Effect of temperature on the preharvest infection of maize kernels by Aspergillus flavus,” PhytoPath, vol. 78, pp. 1376–1380, 1988.
[75]
S. X. Mideros, G. L. Windham, W. P. Williams, and R. J. Nelson, “Tissue-specific components of resistance to aspergillus ear rot of maize,” Phytopathology, vol. 102, no. 8, pp. 787–793, 2012.
[76]
D. Barry, E. B. Lillehoj, N. W. Widstrom et al., “Effect of husk tightness and insect (Lepidoptera) infestation on aflatoxin contamination of preharvest maize,” Environmental Entomology, vol. 15, no. 6, pp. 1116–1118, 1986.
[77]
E. B. Lillehoj, M. S. Zuber, L. L. Darrah, et al., “Aflatoxin occurrence and levels in preharvest corn kernels with varied endosperm characteristics grown at diverse locations,” Crop Science, vol. 23, no. 6, pp. 1181–1184, 1983.
[78]
B. Guo, Z. Chen, R. D. Lee, and B. T. Scully, “Drought stress and preharvest aflatoxin contamination in agricultural commodity: genetics, genomics and proteomics,” Journal of Integrative Plant Biology, vol. 50, no. 10, pp. 1281–1291, 2008.
[79]
K. G. Moore, M. S. Price, R. S. Boston, A. K. Weissinger, and G. A. Payne, “A chitinase from Tex6 maize kernels inhibits growth of Aspergillus flavus,” Phytopathology, vol. 94, no. 1, pp. 82–87, 2004.
[80]
C. Ji, R. A. Norton, D. T. Wicklow, and P. F. Dowd, “Isoform patterns of chitinase and β-1,3-glucanase in maturing corn kernels (Zea mays L.) associated with Aspergillus fiavus milk stage infection,” Journal of Agricultural and Food Chemistry, vol. 48, no. 2, pp. 507–511, 2000.
[81]
C. P. Woloshuk, J. R. Cavaletto, and T. E. Cleveland, “Inducers of aflatoxin biosynthesis from colonized maize kernels are generated by an amylase activity from Aspergillus flavus,” Phytopathology, vol. 87, no. 2, pp. 164–169, 1997.
[82]
Z.-. Chen, R. L. Brown, J. S. Russin, A. R. Lax, and T. E. Cleveland, “A corn trypsin inhibitor with antifungal activity inhibits Aspergillus flavusα-amylase,” Phytopathology, vol. 89, no. 10, pp. 902–907, 1999.
[83]
S. A. Christensen and M. V. Kolomiets, “The lipid language of plant-fungal interactions,” Fungal Genetics and Biology, vol. 48, no. 1, pp. 4–14, 2011.
[84]
E. J. Borrego and M. V. Kolomeits, “Lipid-mediated signaling between fungi and plants,” in Biocommunications of Fungi, G. Witzany, Ed., pp. 249–260, Springer, Amsterdam, The Netherlands, 2012.
[85]
R. A. Holmes, R. S. Boston, and G. A. Payne, “Diverse inhibitors of aflatoxin biosynthesis,” Applied Microbiology and Biotechnology, vol. 78, no. 4, pp. 559–572, 2008.
[86]
J. E. Mellon and R. A. Moreau, “Inhibition of aflatoxin biosynthesis in Aspergillus flavus by diferuloylputrescine and p-coumaroylferuloylputrescine,” Journal of Agricultural and Food Chemistry, vol. 52, no. 21, pp. 6660–6663, 2004.
[87]
H. J. Zeringue Jr., “Effects of methyl jasmonate on phytoalexin production and aflatoxin control in the developing cotton boll,” Biochemical Systematics and Ecology, vol. 30, no. 6, pp. 497–503, 2002.
[88]
V. S. Sobolev, “Localized production of phytoalexins by peanut (Arachis hypogaea) kernels in response to invasion by Aspergillus species,” Journal of Agricultural and Food Chemistry, vol. 56, no. 6, pp. 1949–1954, 2008.
[89]
A. Huffaker, F. Kaplan, M. M. Vaughan et al., “Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize,” Plant Physiology, vol. 156, no. 4, pp. 2082–2097, 2011.
[90]
J. S. Russin, B. Z. Guo, K. M. Tubajika, R. L. Brown, T. E. Cleveland, and N. W. Widstrom, “Comparison of kernel wax from corn genotypes resistant or susceptible to Aspergillus flavus,” Phytopathology, vol. 87, no. 5, pp. 529–533, 1997.
[91]
U. L. Diener, R. J. Cole, T. H. Sanders, G. A. Payne, L. S. Lee, and M. A. Klich, “Epidemiology of aflatoxin formation by Aspergillus flavus,” Annual Review of Phytopathology, vol. 25, pp. 249–270, 1987.
[92]
A. L. Dolezal, G. R. Obrian, D. M. Nielsen, C. P. Woloshuk, R. S. Boston, and G. A. Payne, “Localization, morphology and transcriptional profile of Aspergillus flavus during seed colonization,” Molecular Plant Pathology, vol. 14, no. 9, pp. 898–909, 2013.
[93]
S. Leclere, E. A. Schmelz, and P. S. Chourey, “Cell wall invertase-deficient miniature1 kernels have altered phytohormone levels,” Phytochemistry, vol. 69, no. 3, pp. 692–699, 2008.
[94]
T. Roitsch, M. E. Balibrea, M. Hofmann, R. Proels, and A. K. Sinha, “Extracellular invertase: key metabolic enzyme and PR protein,” Journal of Experimental Botany, vol. 54, no. 382, pp. 513–524, 2003.
[95]
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 coliβ-glucuronidase,” Phytopathology, vol. 85, no. 9, pp. 983–989, 1995.
[96]
D. R. Georgianna and G. A. Payne, “Genetic regulation of aflatoxin biosynthesis: from gene to genome,” Fungal Genetics and Biology, vol. 46, no. 2, pp. 113–125, 2009.
[97]
W. D. Beavis, “QTL analyses: power, precision, and accuracy,” in Molecular Dissection of Complex Traits, A. H. Patterson, Ed., pp. 145–162, CRC Press, New York, NY, USA, 1998.
[98]
R. L. Brown, Z. Chen, M. Warburton et al., “Discovery and characterization of proteins associated with aflatoxin-resistance: evaluating their potential as breeding markers,” Toxins, vol. 2, no. 4, pp. 919–933, 2010.
[99]
Z. Y. Chen, R. L. Brown, K. E. Damann, and T. E. Cleveland, “Identification of Maize Kernel endosperm proteins associated with resistance to aflatoxin contamination by Aspergillus flavus,” Phytopathology, vol. 97, no. 9, pp. 1094–1103, 2007.
[100]
W. M. Snelling, R. A. Cushman, J. W. Keele et al., “Breeding and Genetics Symposium: networks and pathways to guide genomic selection1,” Journal of Animal Science, vol. 91, no. 2, pp. 537–552, 2013.
[101]
J. Yan, C. B. Kandianis, C. E. Harjes et al., “Rare genetic variation at Zea mays crtRB1 increases Β-carotene in maize grain,” Nature Genetics, vol. 42, no. 4, pp. 322–327, 2010.
[102]
C. E. Harjes, T. R. Rocheford, L. Bai et al., “Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification,” Science, vol. 319, no. 5861, pp. 330–333, 2008.
[103]
R. P. Singh, J. Huerta-Espino, S. Rajaram, B. Barna, and Z. Kiraly, “Achieving near-immunity to leaf and stripe rusts in wheat by combining slow rusting resistance genes,” in Proceedings of the 10th Cereal Rusts and Powdery Mildews Conference, 35139, pp. 2000–35133, Budapest, Hungary, August-September 2000.
[104]
C. L. Niblett and A. M. Bailey, Using RNAi Technology against Mycotoxin-Producing Aspergillus and Fusarium Species, International Aflatoxin-in-Maize Working Group, New Orleans, La, USA, 2013.
[105]
K. Rajasekaran, J. W. Cary, R. J. Sayler, J. M. Jaynes, D. Bhatnagar, and T. E. Cleveland, “Synthetic peptides to control the pesky, atypical fungus, Aspergillus flavus,” International Aflatoxin-in-Maize Working Group, New Orleans, La, USA, May 2013.
