Abstract
Recently, increasing attempts have been made to understand how plant genes function in natura. In this context, transcriptional profiles represent plant physiological status in response to environmental stimuli. Herein, we combined high-throughput RNA-Seq with insect survey data on 19 accessions of Arabidopsis thaliana grown at a field site in Switzerland. We found that genes with the gene ontology (GO) annotations of “glucosinolate biosynthetic process” and “response to insects” were most significantly enriched, and the expression of these genes was highly variable among plant accessions. Nearly half of the total expression variation in the glucosinolate biosynthetic genes (AOPs, ESM1, ESP, and TGG1) was explained by among-accession variation. Of these genes, the expression level of AOP3 differed among Col-0 accession individuals depending on the abundance of the mustard aphid (Lipaphis erysimi). We also found that the expression of the major cis-jasmone activated gene CYP81D11 was positively correlated with the number of flea beetles (Phyllotreta striolata and Phyllotreta atra). Combined with the field RNA-Seq data, bioassays confirmed that AOP3 was up-regulated in response to attack by mustard aphids. The combined results from RNA-Seq and our ecological survey illustrate the feasibility of using field transcriptomics to detect an inducible defense, providing a first step towards an in natura understanding of biotic interactions involving phenotypic plasticity.
Highlights
As sessile organisms, plants are exposed to multiple stresses under naturally fluctuating environments (Wilczek et al, 2009; Carrera et al, 2017; Mishra et al, 2017)
L. erysimi, P. xylostella, P. striolata, and P. atra are specialists of Brassicaceae (Ahuja et al, 2010), whereas F. occidentalis is a generalist that feeds on various plant families (Escobar-Bravo et al, 2018) (Figure 1B)
Nearly half of the expression variation in alkenyl hydroxalkyl producing (AOP), EPITHIOSPECIFIER MODIFIER1 (ESM1), and TGG1 was explained by plant accessions (Figure 2), showing a comparable magnitude of variation with the heritability reported by a laboratory eQTL study (Wentzell et al, 2007)
Summary
Plants are exposed to multiple stresses under naturally fluctuating environments (Wilczek et al, 2009; Carrera et al, 2017; Mishra et al, 2017). Increased efforts have been made to understand how plants cope with complex field conditions (Kerwin et al, 2015; Carrera et al, 2017; Kono et al, 2017; Sugiyama et al, 2017; Taylor et al, 2017; Hiraki et al, 2018). Such in natura studies are important to gain a comprehensive understanding of gene functions from the laboratory to the field (Shimizu et al, 2011; Kudoh, 2016; Yamasaki et al, 2018; Zaidem et al, 2019; Nagano et al, 2019). Spatiotemporal variation in herbivory and insect abundance in the field could modulate defense metabolism through phenotypic plasticity or gene-by-environment interactions (Agrawal, 2001; Kerwin et al, 2015; Kerwin et al, 2017)
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