Genomics-assisted breeding for ear rot resistances and reduced mycotoxin contamination in maize: methods, advances and prospects

Theoretical and Applied Genetics - Tập 132 - Trang 2721-2739 - 2019
David Sewordor Gaikpa1, Thomas Miedaner1
1State Plant Breeding Institute, University of Hohenheim, Stuttgart, Germany

Tóm tắt

Genetic mapping, genomic profiling and bioinformatic approaches were used to identify putative resistance genes for ear rots and low mycotoxin contamination in maize. Genomic selection seems to have good perspectives. Maize is globally an indispensable crop for humans and livestock. About 30% of yield is lost by fungal diseases with Gibberella, Fusarium and Aspergillus ear rots (ERs) having a high economic impact in most maize-growing regions of the world. They reduce not only yield, but also contaminate grains with mycotoxins like deoxynivalenol, zearalenone, fumonisins and aflatoxins, respectively. These mycotoxins pose serious health problems to humans and animals. A number of studies have been conducted to dissect the genetic architecture of resistance to these three major ear rots over the past decade. The review concentrates on studies carried out to locate quantitative trait loci (QTL) and candidate genes (CG) on the maize genome as well as the application of genomic selection in maize for resistance against Fusarium graminearum, Fusarium verticillioides and Aspergillus flavus. QTL studies by linkage or genome-wide association mapping, omic technologies (genomics, proteomics, transcriptomics and metabolomics) and bioinformatics are the methods used in the current studies to propose resistance genes against ear rot pathogens. Though a number of QTL and CG are reported, only a few specific genes were found to directly confer ER resistance in maize. A combination of two or more gene identification methods would provide a more powerful and reliable tool. Genomic selection seems to be promising for ER resistance breeding, but there are only a limited number of studies in this area. A strategy that can accurately validate and predict genotypes with major effect QTL and CG for selection will be worthwhile for practical breeding against ERs and mycotoxin contamination in maize.

Tài liệu tham khảo

Abdel-Rahman MM, Bayoumi SR, Barakat MN (2016) Identification of molecular markers linked to Fusarium ear rot genes in maize plants Zea mays L. Biotechnol Biotechnol Equip 30:692–699. https://doi.org/10.1080/13102818.2016.1181987 Agbetiameh D, Ortega-Beltran A, Awuah RT et al (2018) Prevalence of aflatoxin contamination in maize and groundnut in Ghana: population structure, distribution, and toxigenicity of the causal agents. Plant Dis 102:764–772. https://doi.org/10.1094/PDIS-05-17-0749-RE Al Masri A, Hau B, Dehne HW et al (2017) Impact of primary infection site of Fusarium species on head blight development in wheat ears evaluated by IR-thermography. Europ J Plant Pathol 147:855–868. https://doi.org/10.1007/s10658-016-1051-2 Bernardo R, Yu J (2007) Prospects for genomewide selection for quantitative traits in maize. Crop Sci 47:1082–1090. https://doi.org/10.2135/cropsci2006.11.0690 Bian Y, Holland JB (2017) Enhancing genomic prediction with genome-wide association studies in multiparental maize populations. Hered (Edinb) 118:585–593. https://doi.org/10.1038/hdy.2017.4 Bolduan C, Miedaner T, Schipprack W et al (2009) Genetic variation for resistance to ear rots and mycotoxins contamination in early European maize inbred lines. Crop Sci 49:2019–2028. https://doi.org/10.2135/cropsci2008.12.0701 Brauner PC, Melchinger AE, Schrag TA et al (2017) Low validation rate of quantitative trait loci for Gibberella ear rot resistance in European maize. Theor Appl Genet 130:175–186. https://doi.org/10.1007/s00122-016-2802-3 Busboom KN, White DG (2004) Inheritance of resistance to aflatoxin production and Aspergillus ear rot of corn from the cross of inbreds B73 and Oh516. Phytopathology 94:1107–1115. https://doi.org/10.1094/PHYTO.2004.94.10.1107 Butrón A, Reid LM, Santiago R et al (2015) Inheritance of maize resistance to Gibberella and Fusarium ear rots and kernel contamination with deoxynivalenol and fumonisins. Plant Pathol 64:1053–1060. https://doi.org/10.1111/ppa.12351 Butrón A, Santiago R, Cao A, Samayoa LF, Malvar RA (2019) QTLs for resistance to Fusarium ear rot in a multi-parent advanced generation inter-cross (MAGIC) maize population. Plant Dis 103:897–904. https://doi.org/10.1094/PDIS-09-18-1669-RE Campos-Bermudez VA, Fauguel CM, Tronconi MA et al (2013) Transcriptional and metabolic changes associated to the infection by Fusarium verticillioides in maize inbreds with contrasting ear rot resistance. PLoS ONE 8:e61580. https://doi.org/10.1371/journal.pone.0061580 Chaudhary HK, Kaila V, Rather SA (2014) Maize. In: Pratap A, Kumar J (eds) Alien gene transfer in crop plants: achievemnets and impacts. Springer, New York, pp 27–51 Chauhan NM, Washe AP, Minota T (2016) Fungal infection and aflatoxin contamination in maize collected from Gedeo zone, Ethiopia. Springerplus 5:1–8. https://doi.org/10.1186/s40064-016-2485-x Chen J, Shrestha R, Ding J et al (2016) Genome-wide association study and QTL mapping reveal genomic loci associated with Fusarium ear rot resistance in tropical maize germplasm. G3:genes. Genomes Genet 6:3803–3815. https://doi.org/10.1534/g3.116.034561 Chilaka AC, De Boevre M, Atanda OO, De Saeger S (2016) Occurrence of Fusarium mycotoxins in cereal crops and processed products (Ogi) from Nigeria. Toxins (Basel) 8:1–18. https://doi.org/10.3390/toxins8110342 Chungu C, Mather D, Reid L, Hamilton R (1996) Inheritance of kernel resistance to Fusarium graminearum in maize. J Hered 87:382–385. https://doi.org/10.1093/oxfordjournals.jhered.a023019 Coan MMD, Senhorinho HJC, Pinto RJB et al (2018) Genome-wide association study of resistance to ear rot by Fusarium verticillioides in a tropical field maize and popcorn core collection. Crop Sci 58:564–578. https://doi.org/10.2135/cropsci2017.05.0322 Cobb JN, DeClerck G, Greenberg A et al (2013) Next-generation phenotyping: requirements and strategies for enhancing our understanding of genotype-phenotype relationships and its relevance to crop improvement. Theor Appl Genet 126:867–887. https://doi.org/10.1007/s00122-013-2066-0 de Jong G, Pamplona AKA, Von Pinho RG, Balestre M (2017) Genome-wide association analysis of ear rot resistance caused by Fusarium verticillioides in maize. Genomics 10:291–303. https://doi.org/10.1016/j.ygeno.2017.12.001 Dhakal R, Chai C, Karan R et al (2017) Expression profiling coupled with in silico mapping identifies candidate genes for reducing aflatoxin accumulation in maize. Front Plant Sci 8:1–15. https://doi.org/10.3389/fpls.2017.00503 Dhokane D, Karre S, Kushalappa AC, McCartney C (2016) Integrated metabolo-transcriptomics reveals Fusarium head blight candidate resistance genes in wheat QTL-Fhb2. PLoS ONE 11:e0155851. https://doi.org/10.1371/journal.pone.0155851 dos Santos JPR, Pires LPM, de Castro Vasconcellos RC et al (2016) Genomic selection to resistance to Stenocarpella maydis in maize lines using DArTseq markers. BMC Genet 17:1–10. https://doi.org/10.1186/s12863-016-0392-3 Dowd PF, Naumann TA, Price NPJ, Johnson ET (2018a) Identification of a maize (Zea mays) chitinase allele sequence suitable for a role in ear rot fungal resistance. Agric Genet 7:15–22. https://doi.org/10.1016/j.aggene.2017.10.001 Dowd PF, Zilkowski BW, Johnson ET et al (2018b) Transgenic expression of a maize geranyl geranyl transferase gene sequence in maize callus increases resistance to ear rot pathogens. Agric Genet 7:52–58. https://doi.org/10.1016/j.aggene.2018.01.001 FAO [Food and Agriculture Organization of the United Nations] (2018) FAOSTAT Database. Rome, Italy Farfan IDB, De La Fuente GN, Murray SC et al (2015) Genome wide association study for drought, aflatoxin resistance, and important agronomic traits of maize hybrids in the sub-tropics. PLoS ONE 10:e0117737. https://doi.org/10.1371/journal.pone.0117737 Folcher L, Jarry M, Weissenberger A et al (2009) Comparative activity of agrochemical treatments on mycotoxins levels with regard to corn borers and Fusarium microflora in maize (Zea mays L.) fields. Crop Prot 28:302–308 Gelderblom WCA, Cawood ME, Snymann SD et al (1993) Structure-activity relationships of fumonisins in short-term carcinogenesis and cytotoxicity assays. Food Chem Toxicol 31:407–414. https://doi.org/10.1016/0278-6915(93)90155-R Giomi GM, Kreff ED, Iglesias J et al (2016) Quantitative trait loci for Fusarium and Gibberella ear rot resistance in Argentinian maize germplasm. Euphytica 211:287. https://doi.org/10.1007/s10681-016-1725-z Giorni P, Magan N, Pietri A, Bertuzzi T, Battilani P (2007) Studies on Aspergillus section Flavi isolated in northern Italy from maize. Int J Food Microbiol 113:330–338. https://doi.org/10.1016/j.ijfoodmicro.2006.09.007 Goddard ME, Hayes BJ (2007) Genomic selection. J Anim Breed Genet 124:323–330. https://doi.org/10.1111/j.1439-0388.2007.00702.x Gong YY, Egal S, Hounsa A et al (2003) Determinants of aflatoxin exposure in young children from Benin and Togo, West Africa: the critical role of weaning. Int J Epidemiol 32:556–562. https://doi.org/10.1093/ije/dyg109 Gowda M, Das B, Makumbi D et al (2015) Genome-wide association and genomic prediction of resistance to maize lethal necrosis disease in tropical maize germplasm. Theor Appl Genet 128:1957–1968. https://doi.org/10.1007/s00122-015-2559-0 Guo B, Ji X, Ni X et al (2017) Evaluation of maize inbred lines for resistance to pre-harvest aflatoxin and fumonisin contamination in the field. Crop J 5:259–264. https://doi.org/10.1016/j.cj.2016.10.005 Han S, Utz HF, Liu W et al (2016) Choice of models for QTL mapping with multiple families and design of the training set for prediction of Fusarium resistance traits in maize. Theor Appl Genet 129:431–444. https://doi.org/10.1007/s00122-015-2637-3 Han S, Miedaner T, Utz HF et al (2018) Genomic prediction and GWAS of Gibberella ear rot resistance traits in dent and flint lines of a public maize breeding program. Euphytica 214:1–20. https://doi.org/10.1007/s10681-017-2090-2 Harris LJ, Balcerzak M, Johnston A et al (2016) Host-preferential Fusarium graminearum gene expression during infection of wheat, barley, and maize. Fungal Biol 120:111–123. https://doi.org/10.1016/j.funbio.2015.10.010 Hawkins LK, Mylroie JE, Oliveira DA et al (2015) Characterization of the maize chitinase genes and their effect on Aspergillus flavus and aflatoxin accumulation resistance. PLoS ONE 10:e0126185. https://doi.org/10.1371/journal.pone.0126185 Hawkins LK, Warburton ML, Tang J et al (2018) Survey of candidate genes for maize resistance to infection by Aspergillus flavus and/or aflatoxin contamination. Toxins (Basel). https://doi.org/10.3390/toxins10020061 Hefny M, Attaa S, Bayoumi T et al (2012) Breeding maize for resistance to ear rot caused by Fusarium moniliforme. Pak J Biol Sci 15:78–84. https://doi.org/10.3923/pjbs.2012.78.84 Hung H, Holland BJ (2012) Diallel analysis of resistance to Fusarium ear rot and fumonisin contamination in maize. Crop Sci 52:2173–2181. https://doi.org/10.2135/cropsci2012.03.0154 Ju M, Zhou Z, Mu C et al (2017) Dissecting the genetic architecture of Fusarium verticillioides seed rot resistance in maize by combining QTL mapping and genome-wide association analysis. Nat Publ Gr. https://doi.org/10.1038/srep46446 Kage U, Yogendra KN, Kushalappa AC (2017) TaWRKY70 transcription factor in wheat QTL-2DL regulates downstream metabolite biosynthetic genes to resist Fusarium graminearum infection spread within spike. Sci Rep 7:13–16. https://doi.org/10.1038/srep42596 Kebede AZ, Woldemariam T, Reid LM, Harris LJ (2016) Quantitative trait loci mapping for Gibberella ear rot resistance and associated agronomic traits using genotyping-by-sequencing in maize. Theor Appl Genet. https://doi.org/10.1007/s00122-015-2600-3 Kebede AZ, Johnston A, Schneiderman D et al (2018) Transcriptome profiling of two maize inbreds with distinct responses to Gibberella ear rot disease to identify candidate resistance genes. BMC Genom 19:131. https://doi.org/10.1186/s12864-018-4513-4 Kimanya ME, De Meulenaer B, Tiisekwa B et al (2008) Co-occurrence of fumonisins with aflatoxins in home-stored maize for human consumption in rural villages of Tanzania. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 25:1353–1364. https://doi.org/10.1080/02652030802112601 Kuska MT, Mahlein AK (2018) Aiming at decision making in plant disease protection and phenotyping by the use of optical sensors. Eur J Plant Pathol 152(4):987–992. https://doi.org/10.1007/s10658-018-1464-1 Lanubile A, Pasini L, Lo Pinto M, Battilani P, Prandini A, Marocco A (2010a) Evaluation of broad spectrum sources of resistance to Fusarium verticillioides and advanced maize breeding lines. World Mycotoxin J 4:43–51. https://doi.org/10.3920/WM2010.1206 Lanubile A, Pasini L, Marroco A (2010b) Differential gene expression in kernels and silks of maize lines with contrasting levels of ear rot resistance after Fusarium verticillioides infection. J Plant Physiol 167:1398–1406. https://doi.org/10.1016/j.jplph.2010.05.015 Lanubile A, Ferrarini A, Maschietto V et al (2014) Functional genomic analysis of constitutive and inducible defense responses to Fusarium verticillioides infection in maize genotypes with contrasting ear rot resistance. BMC Genom 15:1–16. https://doi.org/10.1186/1471-2164-15-710 Lanubile A, Maschietto V, De Leonardis S, Battilani P, Paciolla C, Marocco A (2015) Defense responses to mycotoxin-producing fungi Fusarium proliferatum, F. subglutinans, and Aspergillus flavus in kernels of susceptible and resistant maize genotypes. Mol Plant Microbe Interact 28:546–557. https://doi.org/10.1094/MPMI-09-14-0269-R Lanubile A, Maschietto V, Borrelli VM et al (2017) Molecular basis of resistance to Fusarium ear rot in maize. Front Plant Sci 8:1–13. https://doi.org/10.3389/fpls.2017.01774 Leng P-F, Lübberstedt T, Xu M-L (2017) Genomics-assisted breeding—a revolutionary strategy for crop improvement. J Integr Agric 16:2674–2685. https://doi.org/10.1016/S2095-3119(17)61813-6 Li X, Quigg RJ, Zhou J et al (2006) A critical evaluation of the effect of population size and phenotypic measurement on QTL detection and localization using a large F2 murine mapping population. Genet Mol Biol 29:166–173. https://doi.org/10.1590/S1415-47572006000100030 Löffler M, Kessel B, Ouzunova M, Miedaner T (2011) Covariation between line and testcross performance for reduced mycotoxin concentrations in European maize after silk channel inoculation of two Fusarium species. Theor Appl Genet 122:925–934. https://doi.org/10.1007/s00122-010-1499-y Logrieco A, Mulè G, Moretti A, Bottalico A (2002) Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. Eur J Plant Pathol 108:597–609. https://doi.org/10.1023/A:1020679029993 Lombard MJ (2014) Mycotoxin exposure and infant and young child growth in Africa: What do we know? Ann Nutr Metab 64:42–52. https://doi.org/10.1159/000365126 Long A (2001) Candidate gene. Encycl Genet 1:263–264 Mackay TFC (2009) Q&A: genetic analysis of quantitative traits. J Biol 8:23. https://doi.org/10.1186/jbiol133 Martin CJ (2011) Development of sequence-specific molecular markers based on phenylpropanoid pathway genes for resistance to Fusarium graminearum (Schwabe) in Zea mays (L.). M.Sc dissertation, University of Guelph, Ontario, Canada Martin M, Miedaner T, Dhillon BS, Ufermann U, Kessel B, Ouzunova M, Schipprack W, Melchinger AE (2011) Colocalization of QTL for Gibberella ear rot resistance and low mycotoxin contamination in early European maize. Crop Sci 51:1935–1945. https://doi.org/10.2135/cropsci2010.11.0664 Martin M, Dhillon BS, Miedaner T, Melchinger AE (2012a) Inheritance of resistance to Gibberella ear rot and deoxynivalenol contamination in five flint maize crosses. Plant Breed 131:28–32. https://doi.org/10.1111/j.1439-0523.2011.01908.x Martin M, Miedaner T, Schwegler DD et al (2012b) Comparative quantitative trait loci mapping for Gibberella ear rot resistance and reduced deoxynivalenol contamination across connected maize populations. Crop Sci 52:32–43. https://doi.org/10.2135/cropsci2011.04.0214 Maschietto V, Colombi C, Pirona R et al (2017) QTL mapping and candidate genes for resistance to Fusarium ear rot and fumonisin contamination in maize. BMC Plant Biol 17:1–21. https://doi.org/10.1186/s12870-017-0970-1 Mesterházy Á, Lemmens M, Reid LM (2012) Breeding for resistance to ear rots caused by Fusarium spp. in maize - A review. Plant Breed 131:1–19. https://doi.org/10.1111/j.1439-0523.2011.01936.x Mideros SX, Warburton ML, Jamann TM et al (2014) 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. https://doi.org/10.2135/cropsci2013.04.0249 Miedaner T, Korzun V (2012) Marker-assisted selection for disease resistance in wheat and barley breeding. Phytopathology 102:560–566. https://doi.org/10.1094/PHYTO-05-11-0157 Mohammadi M, Anoop V, Gleddie S, Harris LJ (2011) Proteomic profiling of two maize inbreds during early Gibberella ear rot infection. Proteomics 11:3675–3684. https://doi.org/10.1002/pmic.201100177 Mouton M (2014) Resistance in South African maize inbred lines to the major ear rot diseases and associated mycotoxin contamination. M.Sc dissertation, Faculty of AgriSciences, University of Stellenbosch, South Africa. pp 60–76 Munkvold GP, Desjardins AE (1997) Fumonisins in maize: Can we reduce their occurrence? Plant Dis 81:556–565. https://doi.org/10.1094/PDIS.1997.81.6.556 Mutka AM, Bart RS (2015) Image-based phenotyping of plant disease symptoms. Front Plant Sci 5:1–8. https://doi.org/10.3389/fpls.2014.00734 Newell M, Jannink J (2014) Genomic selection in plant breeding. In: Fleury D, Whitford R (eds) Crop breeding methods in molecular biology (Methods and Protocols), 1145th edn. Humana Press, New York, pp 117–130 Nutz S (2010) Colonization of maize with Fusarium spp. and mycotoxin accumulation. Doctoral dissertation, Faculty of Agriculture, Georg-August-University, Göttingen. https://ediss.uni-goettingen.de/bitstream/handle/11858/00-1735-0000-000D-F1E4-1/nutz.pdf?sequence=1. Accessed 15 Mar 2018 Okoth S, Rose L, Ouko A et al (2017) Assessing genotype-by-environment interactions in Aspergillus ear rot and pre-harvest aflatoxin accumulation in maize inbred lines. Agronomy 7:86. https://doi.org/10.3390/agronomy7040086 Pè ME, Gianfranceschi L, Taramino G et al (1993) Mapping quantitative trait loci (QTLs) for resistance to Gibberella zeae infection in maize. Mol Gen Genet 241:11. https://doi.org/10.1007/BF00280195 Pereira GS, Pinho RGV, Pinho EVRV et al (2017) Selection of maize inbred lines and gene expression for resistance to ear rot. Genet Mol Res 16:1–21. https://doi.org/10.4238/gmr16039415 Piepho HP, Möhring J (2007) Computing heritability and selection response from unbalanced plant breeding trials. Genetics 177:1881–1888. https://doi.org/10.1534/genetics.107.074229 Pierron A, Alassane-Kpembi I, Oswald IP (2016) Impact of two mycotoxins deoxynivalenol and fumonisin on pig intestinal health. Porcine Health Manag 2:21. https://doi.org/10.1186/s40813-016-0041-2 Pinton P, Oswald I (2014) Effect of deoxynivalenol and other type B trichothecenes on the intestine: a review. Toxins (Basel) 6:1615–1643. https://doi.org/10.3390/toxins6051615 Rawat N (2016) Approaches for disease resistant candidate genes identification in plants: recent techniques and trends. Austin Food Sci 1:1010 Reid LM, Nicol RW, Quellet T et al (1999) Interaction of Fusarium graminearum and F. moniliforme in maize ears: disease progress, fungal biomass, and mycotoxin accumulation. Phytopathology 89:1028–1037. https://doi.org/10.1094/PHYTO.1999.89.11.1028 Reid LM, Woldemariam T, Zhu X, Stewart DW, Schaafsma AW (2002) Effect of inoculation time and point of entry on disease severity in Fusarium graminearum, Fusarium verticillioides, or Fusarium subglutinans inoculated maize ears. Can J Plant Pathol 24:162–167. https://doi.org/10.1080/07060660309506991 Riedelsheimer C, Endelman JB, Stange M et al (2013) Genomic predictability of interconnected biparental maize populations. Genetics 194:493–503. https://doi.org/10.1534/genetics.113.150227 Robertson-Hoyt LA, Betrán J, Payne GA et al (2007) Relationships among resistances to Fusarium and Aspergillus ear rots and contamination by fumonisin and aflatoxin in maize. Phytopathology 97:311–317. https://doi.org/10.1094/PHYTO-97-3-0311 Rodrigues FA, Defourny P, Gérard B et al (2017) Use of remote sensing technology in the assessment of resistance of maize to tar spot complex. Adv Anim Biosci 8:259–263. https://doi.org/10.1017/S2040470017001212 Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115. https://doi.org/10.1126/science.1178534 Septiani P, Lanubile A, Stagnati L, Busconi M, Nelissen H, Pè ME, Dell’Acqua M, Marocco A (2019) Unravelling the genetic basis of Fusarium seedling rot resistance in the MAGIC maize population: novel targets for breeding. Sci Rep 9:5665. https://doi.org/10.1038/s41598-019-42248-0 Shikha M, Kanika A, Rao AR et al (2017) Genomic selection for drought tolerance using genome-wide SNPs in maize. Front Plant Sci 8:1–12. https://doi.org/10.3389/fpls.2017.00550 Shuaib FMB, Jolly PE, Ehiri JE et al (2010) Association between birth outcomes and aflatoxin B1 biomarker blood levels in pregnant women in Kumasi, Ghana. Trop Med Int Health 15:160–167. https://doi.org/10.1111/j.1365-3156.2009.02435.x Smith LE, Prendergast AJ, Turner PC et al (2015) The potential role of mycotoxins as a contributor to stunting in the SHINE Trial. Clin Infect Dis 61:S733–S737. https://doi.org/10.1093/cid/civ849 Stagnati L, Lanubile A, Samayoa LF, Bragalanti M, Giorni P, Busconi M, Holland JB, Marocco A (2019) A genome wide association study reveals markers and genes associated with resistance to Fusarium verticillioides infection of seedlings in a maize diversity panel. G3: genes. Genom Genet 9:571–579. https://doi.org/10.1534/g3.118.200916 Su CF, Wang W, Gong SL et al (2016) Factors influencing QTL mapping accuracy under complicated genetic models by computer simulation. Genet Mol Res. https://doi.org/10.4238/gmr15049153 Szabo B, Toth B, Toth Toldine E et al (2018) A new concept to secure food safety standards against Fusarium species and Aspergillus flavus and their toxins in maize. Toxins 10:372. https://doi.org/10.3390/toxins10090372 Talas F, McDonald B (2015) Significant variation in sensitivity to DMI fungicide in field populations of Fusarium graminearum. Plant Pathol 64:664–670. https://doi.org/10.1111/ppa.12280 Tang JD, Perkins A, Williams WP, Warburton ML (2015) Using genome-wide associations to identify metabolic pathways involved in maize aflatoxin accumulation resistance. BMC Genom 16:673. https://doi.org/10.1186/s12864-015-1874-9 Technow F, Bürger A, Melchinger AE (2013) Genomic prediction of Northern corn leaf blight resistance in maize with combined or separated training sets for heterotic groups. G3:genes. Genom Genet 3:197–203. https://doi.org/10.1534/g3.112.004630 van den Berg I, Fritz S, Boichard D (2013) QTL fine mapping with Bayes C(pi): a simulation study. Genet Sel Evol 45:19. https://doi.org/10.1186/1297-9686-45-19 Velluti A, Marín S, Bettucci L et al (2000) The effect of fungal competition on colonization of maize grain by Fusarium moniliforme, F. proliferatum and F. graminearum and on fumonisin B1and zearalenone formation. Int J Food Microbiol 59:59–66. https://doi.org/10.1016/S0168-1605(00)00289-0 Walker R, White DG (2001) Inheritance of resistance to Aspergillus ear rot and aflatoxin production of corn from CI2. Plant Dis 85:322–327. https://doi.org/10.1094/PDIS.2001.85.3.322 Wallace JG, Larsson SJ, Buckler ES (2014) Entering the second century of maize quantitative genetics. Hered (Edinb) 112:30–38. https://doi.org/10.1038/hdy.2013.6 Wang Y, Zhou Z, Gao J et al (2016) The mechanisms of maize resistance to Fusarium verticillioides by comprehensive analysis of RNA-seq data. Front Plant Sci 7:1–14. https://doi.org/10.3389/fpls.2016.01654 Warburton ML, Williams WP (2014) Aflatoxin resistance in maize: what have we learned lately? Adv Bot 2014:10. https://doi.org/10.1155/2014/352831 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. https://doi.org/10.1007/s11032-010-9446-9 Warburton ML, Tang JD, Windham GL et al (2015) Genome-wide association mapping of Aspergillus flavus and aflatoxin accumulation resistance in maize. Crop Sci 55:1857–1867. https://doi.org/10.2135/cropsci2014.06.0424 Willcox MC, Davis GL, Warburton ML et al (2013) Confirming quantitative trait loci for aflatoxin resistance from Mp313E in different genetic backgrounds. Mol Breed 32:15–26. https://doi.org/10.1007/s11032-012-9821-9 Wise K, Allen T, Chilvers M, et al (2016) Corn disease management CPN-2001: ear rots. Crop protection network, United State Department of Agriculture, National Institute of Food and Agriculture. https://crop-protection-network.s3.amazonaws.com/publications/cpn-2001-ear-rots.pdf. Accessed 13 Mar 2018 Würschum T (2012) Mapping QTL for agronomic traits in breeding populations. Theor Appl Genet 125:201–210. https://doi.org/10.1007/s00122-012-1887-6 Xiang K, Reid LM, Zhang Z et al (2010) A meta-analysis of QTL associated with ear rot resistance in maize. Maydica 55:281–290 Yin Z, Wang Y, Wu F et al (2014) Quantitative trait locus mapping of resistance to Aspergillus flavus infection using a recombinant inbred line population in maize. Mol Breed 33:39–49. https://doi.org/10.1007/s11032-013-9932-y Zhang Y, Cui M, Zhang J et al (2016) Confirmation and fine mapping of a major QTL for aflatoxin resistance in maize using a combination of linkage and association mapping. Toxins (Basel) 8:1–15. https://doi.org/10.3390/toxins8090258 Zhou M, Yang L, Shao M et al (2018) Effects of zearalenone exposure on the TGF-β1/Smad3 signaling pathway and the expression of proliferation or apoptosis related genes of post-weaning gilts. Toxins (Basel) 10:1–13. https://doi.org/10.3390/toxins10020049 Zila CT, Samayoa LF, Santiago R et al (2013) A genome-wide association study reveals genes associated with Fusarium ear rot resistance in a maize core diversity panel. G3: genes. Genom Genet 3:2095–2104. https://doi.org/10.1534/g3.113.007328 Zila CT, Ogut F, Romay MC et al (2014) Genome-wide association study of Fusarium ear rot disease in the U.S.A. Maize inbred line collection. BMC Plant Biol 14:1–15. https://doi.org/10.1186/s12870-014-0372-6 Zummo N, Scott GE (1992) Interaction of Fusarium moniliforme and Aspergillus flavus on kernel infection and aflatoxin contamination in maize ears. Plant Dis 76:771–773. https://doi.org/10.1094/PD-76-0771