Bivariate GWA mapping reveals associations between aliphatic glucosinolates and plant responses to thrips and heat stress.

ABSTRACT

Although plants harbor a huge phytochemical diversity, only a fraction of plant metabolites is functionally characterized. In this work, we aimed to identify the genetic basis of metabolite functions during harsh environmental conditions in Arabidopsis thaliana. With machine learning algorithms we predicted stress-specific metabolomes for 23 (a)biotic stress phenotypes of 300 natural Arabidopsis accessions. The prediction models identified several aliphatic glucosinolates (GLSs) and their breakdown products to be implicated in responses to heat stress in siliques and herbivory by Western flower thrips, Frankliniella occidentalis. Bivariate GWA mapping of the metabolome predictions and their respective (a)biotic stress phenotype revealed genetic associations with MAM, AOP, and GS-OH, all three involved in aliphatic GSL biosynthesis. We, therefore, investigated thrips herbivory on AOP, MAM, and GS-OH loss-of-function and/or overexpression lines. Arabidopsis accessions with a combination of MAM2 and AOP3, leading to 3-hydroxypropyl dominance, suffered less from thrips feeding damage. The requirement of MAM2 for this effect could, however, not be confirmed with an introgression line of ecotypes Cvi and Ler, most likely due to other, unknown susceptibility factors in the Ler background. However, AOP2 and GS-OH, adding alkenyl or hydroxy-butenyl groups, respectively, did not have major effects on thrips feeding. Overall, this study illustrates the complex implications of aliphatic GSL diversity in plant responses to heat stress and a cell-content-feeding herbivore.