Low aflatoxin levels in Aspergillus flavus-resistant maize are correlated with increased corn earworm damage and enhanced seed fumonisin

Authors: CHALIVENDRA, SUBBAIAH - Louisiana State University Agcenter; HUANG, FANGNENG - Louisiana State University Agcenter; Busman, Mark; Williams, William; HAM, JONG - Louisiana State University Agcenter

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/19/2020
Publication Date: 9/23/2020
Citation: Chalivendra, S., Huang, F., Busman, M., Williams, W.P., Ham, J. 2020. Low aflatoxin levels in Aspergillus flavus-resistant maize are correlated with increased corn earworm damage and enhanced seed fumonisin. Frontiers in Plant Science. 11. Article 565323. https://doi.org/10.3389/fpls.2020.565323.
DOI: https://doi.org/10.3389/fpls.2020.565323

Interpretive Summary: Both Aspergillus and Fusarium ear rots of corn not only lead to crop loss, but also contaminate the grain with carcinogenic mycotoxins. Incorporation of genetic resistance to fungal contamination into corn breeding lines is an ideal solution for combating ear rot and mycotoxin contamination. However, the goal is fraught by a major problem. Resistance for aflatoxin or fumonisin accumulation is quantitative and contributed by several loci with small effects. Our work reveals that host phenology (flowering time) and insect vector-mycotoxin interactions can further confound the breeding efforts. Incorporation of resistance to production of a single mycotoxin and not pairing it with insect resistance may not adequately ensure food safety. The Aspergillus flavus resistant corn varieties were found to have much higher levels of corn earworm infestation, as compared to the susceptible hybrid; and corn earworm infested ears had significantly higher fumonisin levels in the seed. Transgenic approaches such as host-induced gene silencing and developing broad-spectrum biocontrol systems need to be part of mycotoxin mitigation strategies. This information should be of assistance to crop breeders seeking to improve the quality and safety of the US corn supply.

Technical Abstract: A preference in the natural infestation of corn earworm (CEW: Helicoverpa zea Boddie) to specific host genotypes was observed in field trials to assess the pathogenicity of Aspergillus flavus strains in maize (Zea mays L.), using two hybrids and two inbreds with contrasting levels of resistance to aflatoxin accumulation. The resistant hybrid (Mp313E × Mp717) had greater than 14-fold infested ears than the susceptible hybrid (GA209 × T173). Similarly, the resistant inbred (CML322) showed >7-fold greater CEW infestation than the susceptible inbred (B73). Seed aflatoxin B1 (AF) levels either in mock-inoculated or A. flavus inoculated ears were consistent with the A. flavus resistance of a genotype and not affected by CEW damage. Although no manual inoculation with Fusarium verticilloides was carried out, the CEW-infested ears showed a significantly greater seed fumonisin B1 (FUM) content compared to uninfested ears, indicating that the insect may have vectored the fungus. In spite of its demonstrably superior resistance to FUM accumulation, Mp313E × Mp717 had greater levels of FUM than GA209 × T173 correlating with the level of CEW infestation. In accordance with their tropical origin, the two maize lines with heavy infestation were delayed in flowering. The availability of young silk for egg-laying could have been a factor in the pervasive CEW damage observed in these lines. At the same time, H. zea larvae reared on AF or FUM showed that the larval mass decreased with increasing AF in the diet (>90% of mass reduction and >30% lethality at or above 250 ppb). On the contrary, the pest was very tolerant to FUM with no significant loss in mass even up to 100 ppm. These results suggest that the low seed AF content may be a compelling reason for the prevalence of CEW infestation and the resultant FUM contamination in the A. flavus resistant lines. These results highlight the need for integrated strategies that target mycotoxigenic fungi and their insect vectors are needed to enhance the safety of crop commodities.