Abstract
Aflatoxin produced by Aspergillus flavus in corn poses significant health risks to both humans and livestock. Exploitation of host-plant resistance in breeding programs is a sustainable way to minimize aflatoxin contamination. Identification of quantitative trait loci (QTL) associated with resistance to aflatoxin accumulation in kernels can accelerate development of aflatoxin-resistant corn using marker-assisted selection. An F2:3 mapping population, developed from a cross involving a resistant inbred Mp715 and a susceptible inbred B73, was evaluated in replicated field trials with developing ears artificially inoculated with A. flavus for 2 years to identify QTL for reduced aflatoxin accumulation. Using composite interval mapping, 6 to 7 QTL for aflatoxin content were identified in both years with contribution of individual QTL ranging from <1 to 10% of phenotypic variation. More QTL were detected for husk coverage with phenotypic variance range of <1 to 16% explained by individual QTL. Both B73 and Mp715 alleles at these QTL loci contributed toward resistance. Husk coverage and aflatoxin levels were significantly correlated in both years. Our findings were further supported by overlapping of QTL for husk coverage ratings in four genomic regions on chromosomes 4, 8, and 10, where aflatoxin resistance QTL were reported in previous studies. Since most of the QTL were of low to moderate effects, pyramiding of these QTL may lead to enhanced resistance to aflatoxin accumulation in corn.
Similar content being viewed by others
References
Abbas HK, Williams WP, Windham GL, Pringle HC III, Xie W, Shier WT (2002) Aflatoxin and fumonisin contamination of commercial corn hybrids in Mississippi. J Agric Food Chem 50:5246–5254
Balconi C, Motto M, Mazzinelli G, Berardo N (2010) Ear secondary traits related to aflatoxin accumulation in commercial maize hybrids under artificial field inoculation. World Mycotox J 3:239–250
Barry D, Lillehoj EB, Widstrom NW, McMillan WW, Zuber MS, Kwolek WF, Guthrie WD (1986) Effect of husk tightness and insect (Lepidoptera) infestation on aflatoxin contamination of preharvest maize. Environ Entomol 15:1116–1118
Bello HT (2007) Phenotypic and genotypic evaluation of generations and recombinant inbred lines for response to aflatoxin. Dissertation, Texas A&M University, USA
Betrán FJ, Isakeit T (2004) Aflatoxin accumulation in maize hybrids of different maturities. Agron J 96:565–570
Betrán FJ, Isakeit T, Odvody G (2002) Aflatoxin accumulation of white and yellow maize inbreds in diallel crosses. Crop Sci 42:1894–1901
Betrán J, Isakeit T, Odvody G, Mayfield K (2005) Breeding corn to reduce preharvest aflatoxin contamination. In: Abbas HK (ed) Aflatoxin and food safety. CRC Press, Boca Raton, FL, pp. 353–378
Betrán FJ, Bhatnagar S, Isakeit T, Odvody G, Mayfield K (2006) Aflatoxin accumulation and associated traits in QPM maize inbreds and their testcrosses. Euphytica 152:247–257
Bhatnagar S, Betrán FJ, Transue D (2003) Aflatoxin resistance of subtropical/tropical quality protein maize hybrids in Texas. Maydica 48:113–124
Brooks TD, Williams WP, Windham GL, Willcox MC, Abbas HK (2005) Quantitative trait loci contributing resistance to aflatoxin accumulation in the maize inbred Mp313E. Crop Sci 45:171–174
Brown RL, Chen ZY, Cleveland TE, Russin JS (1999) Advances in the development of host resistance to aflatoxin contamination by Aspergillus flavus. Phytopathol 89:113–117
Campbell KW, White DG (1995) Evaluation of corn genotypes for resistance to Aspergillus ear rot, kernel infection, and aflatoxin production. Plant Dis 79:1039–1045
Castegnaro M, McGregor D (1998) Carcinogenic risk assessment of mycotoxins. Rev Med Vet 149:671–678
Chiuraise N, Derera J, Yobo KS, Magorokosho C, Nunkumar A, Qwabe NFP (2016) Progress in stacking aflatoxin and fumonisin contamination resistance genes in maize hybrids. Euphytica 207:49–67
CIMMYT (1985) Managing trials and reporting data for CIMMYT’s international maize testing program. Mexico, DF
Farfan IDB, De La Funte GN, Murray SC, Isakeit T, Huang PC, Warburton ML et al (2015) Genome wide association study for drought, aflatoxin resistance and important agronomic traits of maize hybrids in sub-tropics. PLoS One 10(2):e0117737
Guo BZ, Widstrom NW, Holbrook CC, Lee RD, Lynch RE (2001) Molecular genetic analysis of resistance mechanisms to aflatoxin formation in maize and peanut. Mycopathol 155:78
Hallauer AR, Miranda JB (1981) Quantitative genetics in maize breeding. Iowa Stat. Univ. Press, Ames, IA
Hamblin AM, White DG (2000) Inheritance of resistance to Aspergillus ear rot and aflatoxin production of corn from Tex6. Phytopathol 90:292–296
Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugenics 12:172–175
Lander ES, Green P, Abrahamson J, Barlow A, Daly AJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural population. Genomics 1:174–181
Lawrence CJ, Harper LC, Schaeffer ML, Sen TZ, Seigfried TE, Campbell DA (2008) Maize GDB: the maize model organism database for basic, translational, and the applied research. Int J Plant Genom 2008:496957
Lillehoj EB, Zuber MS, Darrah LL (1983) Aflatoxin occurrence and levels in preharvest corn kernels with varied endosperm characteristics grown at diverse locations. Crop Sci 15:1181–1186
Mayfield KL, Murray SC, Rooney WL, Isakeit T, Odvody GA (2011) Confirmation of QTL reducing aflatoxin in maize testcrosses. Crop Sci 51:2489–2498
Mideros SX, Warburton WL, Jamann TM, Windham WL, Williams WP, Nelson RJ (2013) Quantitative trait loci influencing mycotoxin contamination of maize: analysis by linkage mapping, characterization of near-isogenic lines, and meta-analysis. Crop Sci 54:127–142
Naidoo G, Forbes AM, Paul C, White DG, Rocheford TR (2002) Resistance to Aspergillus ear rot and aflatoxin accumulation in maize F1 hybrids. Crop Sci 42:360–364
Nichols TE (1983) Economic impact of aflatoxin in corn. South Coop Ser Bulletin 279:67–71
Odvody GN, Spencer N, Remmers J (1997) A description of silk cut, a stress-related loss of kernel integrity in preharvest maize. Plant Dis 81:439–444
Park DL, Liang B (1993) Perspectives on aflatoxin control for human food and animal feed. Trends Food Sci Technol 4:334–342
Paul CG, Naidoo A, Mikkilineni FV, White D, Rocheford T (2003) Quantitative trait loci for low aflatoxin production in two related maize populations. Theor Appl Genet 107:263–270
Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal spacer length polymorphism in barley: Mendelian inheritance, chromosomal location and population dynamics. Proc Natl Acad Sci 81:8014–8018
SAS Institute (2011) SAS® 9.3 system options: Reference, 2nd edn. SAS Institute Inc., Cary, NC
Scott GE, Zummo N (1990) Registration of Mp313E parental line of maize. Crop Sci 30:1378
Scott GE, Zummo N (1992) Registration of Mp420 germplasm line of maize. Crop Sci 32:1296
Walker RD, White DG (2001) Inheritance of resistance to Aspergillus ear rot and aflatoxin production of corn for CI2. Plant Dis 85:322–327
Wang S, Basten CJ, Zeng ZB (2012) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC
Warburton ML, Brooks TD, Krakowasky MW, Shan X, Windham GL, Williams WP (2009) Identification and mapping of new sources of resistance to aflatoxin accumulation in maize. Crop Sci 49:1403–1408
Warburton ML, Brooks TD, Windham GL, Williams WP (2011) Identification of novel QTL contributing resistance to aflatoxin accumulation in maize. Mol Breed 27:491–499
Warburton ML, Tang JD, Windham GL, Hawkins LK, Murray SC, Xu W, Boykin D, Perkins A, Williams WP (2015) Genome-wide association mapping of Aspergillus flavus and aflatoxin accumulation resistance in maize. Crop Sci 55:1857–1867
Widstrom NW (1996) The aflatoxin problem with corn grain. Adv Agron 56:219–280
Willcox MC, Davis GL, Warburton ML, Windham GL, Abbas HK, Betrán J et al (2013) Confirming quantitative trait loci for aflatoxin resistance from Mp313E in different genetic backgrounds. Mol Breed 32:15–26
Williams WP, Windham GL (2001) Registration of maize germplasm line Mp715. Crop Sci 41:1374–1375
Williams WP, Windham GL (2012) Registration of Mp718 and Mp719 germplasm lines of maize. J Plant Regis 6:200–202
Williams WP, Davis FM, Windham GL, Buckley PM (2002) Southwestern corn borer damage and aflatoxin accumulation in a diallel cross of maize. J Genet Breed 56:165–169
Williams WP, Windham GL, Buckley PM (2008) Diallel analysis of aflatoxin accumulation in maize. Crop Sci 45:143–138
Windham WP, Williams W (1998) Aspergillus flavus infection and aflatoxin accumulation in resistant and susceptible maize hybrids. Plant Dis 82:281–284
Windham GL, Williams WP, Davis FM (1999) Effects of the southeastern corn borer on Aspergillus flavus kernel infection and aflatoxin accumulation in maize hybrids. Plant Dis 83:535–540
Windham GL, Williams WP, Buckley PM, Abbas HK (2003) Inoculation techniques used to quantify aflatoxin resistance in corn. J Toxicol Toxin Rev 22:313–325
Yin Z, Wang Y, Wu F, Gu X, Bian Y, Wang Y, Deng D (2014) Quantitative trait locus mapping of resistance to Aspergillus flavus infection using a recombinant inbred line population in maize. Mol Breed 33:39–49
Zummo N, Scott GE (1989) Evaluation of field inoculation technique for screening maize genotypes against kernel infection by Aspergillus flavus in Mississippi. Plant Dis 73:313–316
Acknowledgements
This material is based upon work that is supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture, under award number 2010-85117-20559, and the National Corn Growers Association. The manuscript is approved for publication by the Director of Louisiana Agricultural Experiment Station, USA, as manuscript number 2016-306-26061.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Fig. S1
Frequency distributions of the original aflatoxin concentration (ng g-1) in an F2:3 mapping population derived from the cross B73 x Mp715 at the LSU Agricultural Center Central Research Farm in 2012 (A) and 2013 (B). Arrows indicate mean values for hybrid (F1) and parents, B73 and Mp715 (GIF 32 kb)
Fig. S2
Frequency distributions of the husk coverage rating in an F2:3 mapping population derived from the cross B73 x Mp715 at the LSU Agricultural Center Central Research Farm in 2012 (A) and 2013 (B). Arrows indicate mean values for hybrid (F1) and parents, B73 and Mp715 (GIF 27 kb)
Fig. S3
Relationship between aflatoxin content (ppb) and husk coverage rating (HC) in F2:3 mapping population (B73 x Mp715) inoculated with A. flavus at Central Research Station, LSU AgCenter, Baton Rouge (Combined analysis) (GIF 73 kb)
Table S1
(DOCX 15 kb)
Table S2
(DOCX 15 kb)
Table S3
(DOCX 14 kb)
Table S4
(DOCX 14 kb)
Rights and permissions
About this article
Cite this article
Dhakal, R., Windham, G.L., Williams, W.P. et al. Quantitative trait loci (QTL) for reducing aflatoxin accumulation in corn. Mol Breeding 36, 164 (2016). https://doi.org/10.1007/s11032-016-0590-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-016-0590-8