Genotypic variation in field-grown maize eliminates trade-offs between resistance, tolerance and growth in response to high pressure from the Asian corn borer

Insect herbivory challenges plant survival, and coordination of the interactions between growth, herbivore resistance/tolerance is a key problem faced by plants. Based on field experiments into resistance to the Asian corn borer (ACB, Ostrinia furnacalis), we selected 10 inbred maize lines, of which five were resistant and five were susceptible to ACB. We conducted ACB larval bioassays, analysed defensive chemicals, phytohormones, and relative gene expression using RNA-seq and qPCR as well as agronomic traits, and found resistant lines had weaker inducibility, but were more resistant after ACB attack than susceptible lines. Resistance was related to high levels of major benzoxazinoids, but was not related to induced levels of JA or JA-Ile. Following combination analyses of transcriptome, metabolome and larval performance data, we discovered three benzoxazinoids biosynthesis-related transcription factors, NAC60, WRKY1 and WRKY46. Protoplast transformation analysis suggested that these may regulate maize defence-growth trade-offs by increasing levels of benzoxazinoids, JA and SA but decreasing IAA. Moreover, the resistance/tolerance-growth trade-offs were not observed in the 10 lines, and genotype-specific metabolic and genetic features probably eliminated the trade-offs. This study highlights the possibility of breeding maize varieties simultaneously with improved defences and higher yield under complex field conditions.

Automated summary

Insect herbivory poses a challenge to plant survival, and plants need to coordinate the interactions between growth and herbivore resistance/tolerance. This study conducted field experiments on resistance to the Asian corn borer (ACB) and found that resistant maize lines had weaker inducibility but higher resistance after ACB attack compared to susceptible lines. The resistance was related to high levels of benzoxazinoids. Through combination analyses of transcriptome, metabolome, and larval performance data, the study identified three transcription factors related to benzoxazinoid biosynthesis. This study highlights the possibility of breeding maize varieties with improved defenses and higher yield under complex field conditions.