Concerted cis and trans effects underpin heightened defense gene expression in multi‐herbivore‐resistant maize lines. (5th June 2022)

• Record Type: Journal Article
• Authors: Ji, Meiyuan; Bui, Huyen; Ramirez, Ricardo A.; Clark, Richard M.
• Is Part Of: Plant journal. Volume 111:Number 2(2022)
• Page Start: 508
• Page End: 528
• Publication Date: 2022-06-05
• Subjects: Zea mays ssp. mays -- Tetranychus urticae -- two‐spotted spider mite -- benzoxazinoid -- BX1 -- AOS2 -- European corn borer -- Ostrinia nubilalis; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.15812
• Languages: English
• ISSNs: 0960-7412

Abstract

SUMMARY: In maize ( Zea mays ssp. mays ), agriculturally damaging herbivores include lepidopteran insects, such as the European corn borer ( Ostrinia nubilalis ), and distantly related arthropods, like the two‐spotted spider mite ( Tetranychus urticae ). A small number of maize lines, including B96 and B75, are highly resistant to both herbivores, and B96 is also resistant to thrips. Using T. urticae as a representative pest that causes significant leaf tissue damage, we examined the gene expression responses of these lines to herbivory in comparison with each other and with the susceptible line B73. Upon herbivory, the most resistant line, B96, showed the strongest gene expression response, with a dramatic upregulation of genes associated with jasmonic acid biosynthesis and signaling, as well as the biosynthesis of specialized herbivore deterrent compounds, such as death acids and benzoxazinoids. Extending this work with allele‐specific expression analyses in F1 hybrids, we inferred that the concerted upregulation of many defense genes, including the majority of benzoxazinoid biosynthetic genes in B96, as compared with B73, for the herbivore treatment, resulted from an assemblage of trans control and multiple cis effects acting with similar directionality on gene expression. Further, at the level of individual and potentially rate limiting genes in several major defense pathways, cis and trans effects acted in a reinforcing manner to result in exceptionally high expression in B96. Our study provides a comprehensive resource of cis elements for maize lines important in breeding efforts for herbivore resistance, and reveals potential genetic underpinnings of the origins of multi‐herbivore resistance in plant populations. Significance Statement: Upon herbivory by a generalist spider mite, transcriptome reprogramming varied among maize lines, with differences in the expression of genes involved in jasmonic acid synthesis and signaling and specialized compound production. As assessed using allelic expression, cis + trans reinforcing regulation led to the very high expression of key defense genes in the most herbivore‐resistant line.