Genomics and Pathways Involved in Maize Resistance to Fusarium Ear Rot and Kernel Contamination With Fumonisins

Abstract

Fusarium verticillioides is a causal agent of maize ear rot and produces fumonisins, which are mycotoxins that are toxic to animals and humans. In this study, quantitative trait loci (QTLs) and bulk-segregant RNA-seq approaches were used to uncover genomic regions and pathways involved in resistance to Fusarium ear rot (FER) and to fumonisin accumulation in maize kernels. Genomic regions at bins 4.07–4.1, 6–6.01, 6.04–6.05, and 8.05–8.08 were related to FER resistance and/or reduced fumonisin levels in kernels. A comparison of transcriptomes between resistant and susceptible inbred bulks 10 days after inoculation with F. verticillioides revealed 364 differentially expressed genes (DEGs). In the resistant inbred bulks, genes involved in sink metabolic processes such as fatty acid and starch biosynthesis were downregulated, as well as those involved in phytosulfokine signaling and many other genes involved in cell division; while genes involved in secondary metabolism and compounds/processes related to resistance were upregulated, especially those related to cell wall biosynthesis/rearrangement and flavonoid biosynthesis. These trends are indicative of a growth–defense trade-off. Among the DEGs, Zm00001d053603, Zm00001d035562, Zm00001d037810, Zm00001d037921, and Zm00001d010840 were polymorphic between resistant and susceptible bulks, were located in the confidence intervals of detected QTLs, and showed large differences in transcript levels between the resistant and susceptible bulks. Thus, they were identified as candidate genes involved in resistance to FER and/or reduced fumonisin accumulation.

Meta-analysis and co-expression analysis revealed stable QTL and candidate genes conferring resistances to Fusarium and Gibberella ear rots while reducing mycotoxin contamination in maize

“…(2015) observed strong correlations (r = 0.97) between disease severity and FUM. Similarly, Cao et al. (2022) found strong genotypic correlation (r g = 0.85) between FUM and FER severity after kernel inoculation.…”

“…For FER, Butrón et al (2015) observed strong correlations (r = 0.97) between disease severity and FUM. Similarly, Cao et al (2022) found strong genotypic correlation (r g = 0.85) between FUM and FER severity after kernel inoculation. Based on this, selection for FER-resistant lines would indirectly reduce fumonisins accumulation (Maschietto et al, 2017;Galićet al, 2019).…”

Maize kernel metabolome involved in resistance to fusarium ear rot and fumonisin contamination

“…Eight RILs of maize were selected from a set of 144 RILs derived from the cross between the European flint inbred line EP42 (susceptible to FER and kernel contamination with fumonisins) and the American dent inbred line A637 (resistant), and previously genotyped and phenotyped for FER and kernel fumonisin content under inoculation with F. verticillioides ( Santiago et al, 2013 ; Samayoa et al, 2014 ; Cao et al, 2022 ). The four RILs with the lowest values (resistant) for fumonisin content (10-15 µg/g) and FER (~ 2 in a visual scale from 1 to 7) along with the four RILs with the highest values (susceptible) for fumonisin content (55-75 µg/g) and FER (~ 4) were selected based on previous evaluations ( Supplementary Table 1 ) ( Cao et al., 2022 ). In 2018, 15 seeds from each RIL were sown in a single row of 3.5 m; distance between adjacent rows being 0.8 m. RILs were arranged in four pairs, each pair formed with one resistant and one susceptible RIL.…”

“…RILs within each pair were planted in adjacent rows in order to minimize the contribution of field heterogeneity to differential metabolite content between resistant and susceptible inbreds. We self-crossed at least six plants per RIL, and 15 days later the main ear of each plant was inoculated, using a kernel inoculation technique ( Cao et al., 2014 ), with a spore suspension of F. verticillioides as previously described ( Cao et al, 2022 ). Ears were individually collected at 3 or 10 days after inoculation treatment (dat) (18 and 25 days after pollination, respectively).…”

“…Finally, we used the Pathview platform ( Luo and Brouwer, 2013 ; Luo et al, 2017 ) to integrate and visualize previous transcriptomic data ( Cao et al, 2022 ) and the current untargeted metabolomic data. Target pathways for visualization were: phenylpropanoid biosynthesis, and glutathione and glycerophospholipid metabolisms.…”