Abstract
Fusarium ear rot (FER) and fumonisin accumulation in maize, caused by Fusarium verticillioides, can lead to lower grain quality, crop yield reduction and mycotoxicosis of humans and livestock. The best approach to control this fungus is through the development of resistant maize varieties, however, no immune cultivars are available with commercial cultivars ranging from susceptible to moderately resistant. Therefore, this study evaluated F1 maize hybrids, generated from inbred lines resistant to FER/fumonisins and Aspergillus flavus/aflatoxins, for improved resistance to F. verticillioides infection and fumonisin contamination. Diallel analysis was performed to understand the inheritance of resistance to F. verticillioides/fumonisins. Consequently, maize inbred lines resistant to F. verticillioides/fumonisins under South African conditions and lines resistant to Aspergillus flavus under Kenyan conditions were crossed to produce 18 hybrids. Hybrids and parental lines were planted in replicated field trials at three localities in South Africa. Artificially inoculated trials were conducted with disease severity, F. verticillioides target DNA and total fumonisin concentrations determined by visual assessment, quantitative PCR and liquid chromatography tandem mass spectrometry, respectively. Hybrids R119W × CKL05015, CML 495 × CKL05015 and CKL05015 × R119W were the most resistant to FER severity, F. verticillioides colonisation and fumonisin contamination, respectively. The resistance levels of hybrids did not differ significantly from their parental inbred lines, except for specific hybrids in certain test environments. General combining ability and specific combining ability were significant (P ≤ 0.05) for all three parameters evaluated. Kenyan inbred lines CKL05015 and CML 495 were good general combiners for resistance to fumonisin contamination. Specific combinability estimates showed that CKL05015 × R119W was the best hybrid combination for resistance to FER severity, F. verticillioides colonisation and fumonisin contamination. Additive gene effects were predominant in the inheritance of resistance in this set of hybrids. Parental inbred line performance was indicative of F1 hybrids performance. This study provided fundamental information on the maize lines evaluated that would be useful to breeders in the development of F. verticillioides/fumonisin-resistant cultivars.
Similar content being viewed by others
References
Afolabi CG, Ojiambo PS, Ekpo EJA, Menkir A, Bandyopadhyay R (2007) Evaluation of maize inbred lines for resistance to Fusarium ear rot and fumonisin accumulation in grain in tropical Africa. Plant Dis 91:279–286
Baker RJ (1978) Issues in diallel analysis. Crop Sci 18:533–536
Bhullar GS, Gill KS, Khehra AS (1979) Combining ability analysis over F1-F5 generations in diallel crosses of bread wheat. Theor Appl Genet 55:77–80
Bolger M, Coker RD, DiNovi M, Gaylor D, Gelderblom W, Olsen M, Paster N, Riley RT, Shephard G, Speijers GJA (2001) Fumonisins. In: Safety evaluation of certain mycotoxins in food. WHO Food Additives Series 47, FAO Food and Nutrition Paper 74. Prepared by the 56th Meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA). WHO, Geneva, Switzerland, pp 103–279
Bookmyer JM, Bonos SA, Meyer WA (2009) Inheritance characteristics of brown patch resistance in tall fescue. Crop Sci 49:2302–2308
Bottalico A (1998) Fusarium diseases of cereals: species complex and related mycotoxin profiles in Europe. J Plant Pathol 80:85–103
Boutigny A-L, Beukes I, Small I, Zühlke S, Spiteller M, Van Rensburg BJ, Flett BC, Viljoen A (2012) Quantitative detection of Fusarium pathogens and their mycotoxins in South African maize. Plant Pathol 61:522–531
Cairns JE, Crossa J, Zaidi PH, Grudloyma P, Sanchez C, Araus JL, Thaitad S, Makumbi D, Magorokosho C, Bänziger M, Menkir A , Hearne S, Atlin, GN (2013) Identification of drought, heat and combined drought and heat tolerant donors in maize (Zea mays L). Crop Sci 53:1335–1346
Cao A, Santiago R, Ramos AJ, Souto XC, Aquin O, Malvar RA, Butron A (2014) Critical environmental and genotypic factors for Fusarium verticillioides infection, fungal growth and fumonisin contamination in maize grown in northwestern Spain. Int J Food Microbiol 177:63–71
Clements MJ, Kleinschmidt CE, Maragos CM, Pataky JK, White DG (2003) Evaluation of inoculation techniques for Fusarium ear rot and fumonisin contamination of corn. Plant Dis 87:147–153
Clements MJ, Maragos CA, Pataky JK, White DG (2004) Sources of resistance to fumonisin accumulation in grain and Fusarium ear and kernel rot of corn. Phytopathology 94:251–260
Crossa J (1990) Statistical analysis of multilocation trials. Adv Agron 44:55–85
DAFF. Department of Agriculture, Forestry and Fisheries (2013) Trends in the agricultural sector. http://www.nda.agric.za/docs/statsinfo/Trends13.pdf. Accessed 16 Sept 2016
de la Campa R, Hooker DC, Miller JD, Schaafsma AW, Hammond BG (2005) Modeling effects of environment, insect damage, and Bt genotypes on fumonisin accumulation in maize in Argentina and the Philippines. Mycopathologia 159:539–552
FAO. Food and Agriculture Organization of the United Nations (2018) FAOSTAT statistics database collections. Rome. http://www.fao.org/faostat/en/#data/QC. Accessed 7 May 2018
Gauch HG (2006) Statistical analysis of yield trials by AMMI and GGE. Crop Sci 46:1488–1500
Gauch HG, Zobel RW (1996) AMMI analysis of yield trials. In: Kang MS, Gauch HG (eds) Genotype-by-environment interaction. CRC Press, Boca Raton, pp 85–122
Government Gazette of South Africa (2016) Online publication: https://www.greengazette.co.za/documents/national-gazette-40250-of-05-september-2016-vol-615_20160905-GGN-40250.pdf. Accessed 7 Dec 2016
Grain SA (2014) Crop Estimates Committee. http://www.grainsa.co.za/upload/report_files/Media-Feb-2014.pdf. Accessed 16 Sept 2016
Griffing B (1956) Concept of general and specific combining ability in relation to diallel crossing system. Australian Journal of Biological Sciences 9:463–493
Hallauer AR, Carena MJ, Filho JBM (2010) Quantitative genetics in maize breeding. Springer, New York
Harrison LR, Colvin BM, Green JT, Newman LE, Cole JR (1990) Pulmonary oedema and hydrothorax in swine produced by fumonisin B1, a toxic metabolite of Fusarium moniliforme. J Vet Diagn Investig 2:217–221
Headrick JM, Pataky JK (1991) Resistance to kernel infection by Fusarium moniliforme in sweet corn inbred lines and the effect of infection on emergence. Plant Dis 73:887–892
Hung HY, Holland JB (2012) Diallel analysis of resistance to Fusarium ear rot and fumonisin contamination in maize. Crop Sci 52:2173–2181
IARC International Agency for Research on Cancer (2002) IARC monographs on the evaluation of carcinogenic risks to humans. In: Some traditional herbal medicines, mycotoxins, naphthalene and styrene, vol. 82, p 590. https://monographs.iarc.fr/wp-content/uploads/2018/06/mono82.pdf. Accessed 19 Apr 2016
Janse van Rensburg BJ, Mclaren NW, Flett BC, Schoeman A (2015) Fumonisin producing Fusarium spp. and fumonisin contamination in commercial South African maize. Eur J Plant Pathol 141:491–504
Kellerman TS, Marasas WFO, Thiel PG, Gelderblom WC, Cawood M, Coetzer JA (1990) Leukoencephalomalacia in 2 horses induced by oral dosing of fumonisin B1. Onderstepoort J Vet Res 57:269–275
King SB, Scott GE (1981) Genotypic differences in maize to kernel infection by Fusarium moniliforme. Phytopathology 71:1245–1247
Lanubile A, Maschietto V, Borrelli VM, Stagnati L, Logrieco AF, Marocco A (2017) Molecular basis of resistance to fusarium ear rot in maize. Front Plant Sci 8:1774
Marasas WFO, Riley RT, Hendricks KA, Stevens VL, Sadler TW, Gelineau-van Waes J, Missmer SA, Cabrera J, Torres O, Gelderblom WCA, Allegood J, Martinez C, Maddox J, Miller JD, Starr L, Sullards MC, Roman A, Voss KA, Wang E, Merrill AH Jr (2004) Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr 134:711–716
Marijanovic DR, Holt P, Norred WP, Bacon CW, Voss KA, Stancel PC (1991) Immunosuppressive effects of Fusarium moniliforme corn cultures in chicken. Poult Sci 70:1895–1901
Marín S, Magan N, Belli N, Ramos AJ, Canela R, Sanchis V (1999) Two-dimensional profiles of fumonisin B1 production by Fusarium moniliforme and Fusarium proliferatum in relation to environmental factors and potential for modelling toxin formation in maize grain. Int J Food Microbiol 51:159–167
Maschietto V, Cinzia Colombi C, Pirona R, Pea G, Strozzi F, Marocco A, Rossini L, Lanubile A (2017) QTL mapping and candidate genes for resistance to Fusarium ear rot and fumonisin contamination in maize. BMC Plant Biol 17:20–41
Miller JD (1994) Epidemiology of Fusarium diseases of cereals. In: Miller JD, Trenholm HL (eds) Mycotoxins in grain: compounds other than aflatoxin. Eagan Press, St. Paul, pp 19–36
Munkvold GP (2003) Epidemiology of Fusarium diseases and their mycotoxins in maize ears. Eur J Plant Pathol 109:705–713
Munkvold GP, Desjardins AE (1997) Fumonisins in maize: can we reduce their occurrence? Plant Dis 81:556–565
Nankam C, Pataky JK (1996) Resistance to kernel infection by Fusarium moniliforme in the sweet corn inbred IL125b. Plant Dis 80:593
Ncube E, Flett BC, Waalwijk C, Viljoen A (2011) Fusarium spp. and levels of fumonisins in maize produced by subsistence farmers in South Africa. S Afr J Sci 107:1–7
NGFA. National Frain and Feed Association (2011) FDA mycotoxin regulatory guidance: A guide for grain elevators, feed manufacturers, grain processors and exporters, p 5. https://www.ngfa.org/wpcontent/uploads/NGFAComplianceGuide-FDARegulatoryGuidanceforMycotoxins8-2011.pdf. Accessed 24 Mar 2016
Nicolaisen M, Suproniene S, Nielsen LK, Lazzaro I, Spliid NH, Justesen AF (2009) Real-time PCR for quantification of eleven individual Fusarium species in cereals. J Microbiol Methods 76:234–240
Okoth S, Rose LJ, Ouko A, Beukes I, Mouton M, Flett BC, Makumbi D, Viljoen A (2017a) Field evaluation of resistance to aflatoxin accumulation in maize inbred lines in Kenya and South Africa. J Crop Improv 31:862–878
Okoth S, Rose LJ, Ouko A, Nakisani NEI, Sila H, Viljoen A (2017b) Assessing genotype by environment interactions in Aspergillus ear rot and preharvest aflatoxin accumulation in maize inbred lines. Agronomy 7:86. https://doi.org/10.3390/agronomy7040086
Picot A, Barreau C, Pinson-Gadais L, Caron D, Lannou C, Richard-Forget F (2010) Factors of the Fusarium verticillioides-maize environment modulating fumonisin production. Crit Rev Microbiol 36:221–231
Purchase JL, Hatting H, Van Deventer CS (2000) Genotype × environment interaction of winter wheat (T. aestivum) in South Africa: stability analysis of yield performance. S Afr J Plant Soil 17:101–107
Qureshi MA, Hagler WM (1992) Effect of fumonisin-B1 exposure on chicken macrophage functions in vitro. Poult Sci 71:104–112
Reid LM, Nicol RW, Ouellet T, Savard M, Miller JD, Young JC, Stewart DW, Schaafsma AW (1999) Interaction of Fusarium graminearum and F. moniliforme in maize ears: disease progress, fungal biomass, and mycotoxin accumulation. Phytopathology 89:1028–1037
Rheeder JP, Marasas WFO, Thiel PG, Sydenham EW, Shepard GS, van Schalkwyk DJ (1992) Fusarium moniliforme and fumonisins in corn in relation to human esophageal cancer in Transkei. Phytopathology 82:353–357
Robertson LA, Kleinschmidt CE, White DG, Payne GA, Maragos CM, Holland JB (2006) Heritabilities and correlations of Fusarium ear rot resistance and fumonisin contamination resistance in two maize populations. Crop Sci 46:353–361
Robertson-Hoyt LA, Betrán J, Paye GA, White DG, Isakeit T, Maragos CM, Molnár TL, Holland JB (2007) Relationships among resistances to Fusarium and Aspergillus ear rots and contamination by fumonisin and aflatoxin in maize. Phytopathology 97:311–317
Rose LJ, Mouton M, Beukes I, Flett BC, Vyver CVD, Viljoen A (2016) Multi-environment evaluation of maize inbred lines for resistance to Fusarium ear rot and fumonisins. Plant Dis 100:2134–2144
Rose LJ, Okoth S, Beukes I, Mouton M, Flett BC, Makumbi D, Viljoen A (2017) Determining resistance to Fusarium verticillioides and fumonisin accumulation in maize inbred lines resistant to Aspergillus flavus and aflatoxins. Euphytica 213:93
Santiago R, Reid LM, Zhu X, Butrón A, Malvar RA (2009) Gibberella stalk rot (Fusarium graminearum) resistance of maize inbreds and their F1 hybrids and their potential for use in resistance breeding programs. Plant Breeding 129:454–456
Schjøth JE, Tronsmo AM, Sundheim L (2008) Resistance to Fusarium verticillioides in 20 Zambian maize hybrids. Phytopathology 156:470–479
Scott GE, King SB (1984) Site of action of factors for resistance to Fusarium moniliforme in maize. Plant Dis 68:804
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611
Shephard GS (2008) Impact of mycotoxins on human health in developing countries. Food Addit Contam 25:146–151
Shephard GS, Marasas WFO, Burger HM (2007) Exposure assessment for fumonisins in the former Transkei region of South Africa. Food Addit Contam 24:621–629
Small IM, Flett BC, Marasas WFO, McLeod A, Stander MA, Viljoen A (2012) Resistance in maize inbred lines to Fusarium verticillioides and fumonisin accumulation in South Africa. Plant Dis 96:881–888
Sprague GF, Tatum LA (1942) General versus specific combining ability in single crosses of corn. J Am Soc Agron 34:923–932
White D (1999) Fusarium kernel or ear rot. Compendium of corn diseases. American Phytopathological Society Press, St. Paul
Williams PW, Windham GL, Buckley PM (2008) Diallel analysis of aflatoxin accumulation in maize. Crop Sci 48:134–138
Yan W (2002) Singular-value partitioning in biplot analysis of multi-environmental trial data. Agron J 94:990–996
Yan W, Kang MS (2003) GGE biplot analysis: a graphical tool for breeders, geneticists, and agronomists. CRC Press, Boca Raton, pp 57–79
Yan W, Hunt LA, Sheng Q, Szlavnics Z (2000) Cultivar evaluation and mega-environment investigation based on the GGE Biplot. Crop Sci 40:597–605
Yan W, Cornelius PL, Crossa J, Hunt LA (2001) Two types of GGE biplots for analyzing multi-environment trial data. Crop Sci 41:656–663
Zhang D, Rossel G, Kriegner A, Hijmans R (2004) AFLP assessment of diversity in sweet potato from Latin America and the Pacific region: its implications on the dispersal of the crop. Genet Resour Crop Evolut 51:115–120
Acknowledgements
The South African Maize Trust and the South African National Research Foundation (NRF): Technology and Human Resources for Industry Programme (THRIP) of South Africa are acknowledged for funding of this research. We also thank Ms M. van der Rijst and Dr M. Booyse from ARC-Infruitec for statistical analyses.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Netshifhefhe, N.E.I., Flett, B.C., Viljoen, A. et al. Inheritance and genotype by environment analyses of resistance to Fusarium verticillioides and fumonisin contamination in maize F1 hybrids. Euphytica 214, 235 (2018). https://doi.org/10.1007/s10681-018-2310-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10681-018-2310-4