Concerted cis and trans effects underpin heightened defense gene expression in multi‐herbivore‐resistant maize lines

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.

Abundant trans-driven variation in detoxification gene expression in the extreme generalist herbivore Tetranychus urticae

“…In all pairwise comparisons, we found that trans effects on expression variation were more common than cis, even though the latter became more frequent when expression differences between parents were large, as reported in some earlier studies [21,76]. Support for our finding of a higher prevalence of trans effects comes as well from inferred modes of inheritance -that is, trans effects have been strongly associated with dominance in gene expression ( [21], and references therein), and in our study the higher frequency of genes with dominant versus additive inheritance closely mirrored the higher frequency of trans versus cis effects (this was true among comparisons as well; for instance, for the ROS-ITi x SOL-BEi contrast, relatively fewer trans effects and dominance were detected as compared to the other three, compare . The proportion of trans versus cis effects has been a focus of many studies, although caution is needed in comparing across studies owing to differences in experimental designs and statistical methods.…”

“…Albeit in a different system, Ji et al [21] reached a similar conclusion based on their finding that reinforc-ing cis and trans effects explained the very high expression of several key and potentially rate-limiting genes in defense pathways in maize lines subjected to intense selection for herbivore resistance.…”

“…One widely used approach to understand the genetic control of gene expression variation, as well as its associated inheritance, involves comparing expression between parents and F1 offspring [9,[12][13][14][15][16][17][18][19][20][21].…”

“…However, if expression differences between parents are not observed in F1 ASE (or parental and ASE patterns contrast), trans effects contribute to regulatory variation [9]. This type of parental/F1 design also enables the degree of dominance -an important factor in understanding responses to selection -to be inferred [14,[19][20][21]. A number of studies in diploid organisms, often using genetic models selected in part because of their extensive genomic resources, have revealed trends about the frequency of cis and trans effects, their interactions, as well as associations with inheritance type.…”

“…For example, in many instances, expression variation more often results from trans versus cis regulation in intraspecific comparisons, with the opposite pattern observed for interspecific ones ( [22], and references therein). Further, while trans regulation is associated with dominance or non-additivity in gene expression inheritance, genes with cis effects are enriched for additive inheritance [14,16,[19][20][21].…”