Differential phenotypic and genetic expression of defence compounds in a plant-herbivore interaction along elevation.

Ana L Salgado,Loïc Pellissier,Nadir Alvarez,Anne-Lyse Ducrest,Tomasz Suchan,Sergio Rasmann

doi:10.1098/rsos.160226

Abstract

Elevation gradients impose large differences in abiotic and biotic conditions over short distances, in turn, likely driving differences in gene expression more than would genetic variation per se, as natural selection and drift are less likely to fix alleles at such a narrow spatial scale. As elevation increases, the pressure exerted on plants by herbivores and on arthropod herbivores by predators decreases, and organisms spanning the elevation gradient are thus expected to show lower levels of defence at high elevation. The alternative hypothesis, based on the optimal defence theory, is that defence allocation should be higher in low-resource habitats such as those at high elevation, due to higher costs associated with tissue replacement. In this study, we analyse variation with elevation in (i) defence compound content in the plant Lotus corniculatus and (ii) gene expression associated with defence against predators in the specific phytophagous moth, Zygaena filipendulae. Both species produce cyanogenic glycosides (CNglcs) such as lotaustralin and linamarin as defence mechanisms, with the moth, in addition, being able to sequester CNglcs from its host plant. Specifically, we tested the assumption that the defence-associated phenotype in plants and the gene expression in the insect herbivore should covary between low- and high-elevation environments. We found that L. corniculatus accumulated more CNglcs at high elevation, a result in agreement with the optimal defence theory. By contrast, we found that the levels of expression in the defence genes of Z. filipendulae larvae were not related to the CNglc content of their host plant. Overall, expression levels were not correlated with elevation either, with the exception of the UGT33A1 gene, which showed a marginally significant trend towards higher expression at high elevation when using a simple statistical framework. These results suggest that the defence phenotype of plants against herbivores, and subsequent herbivore sequestration machineries and de novo production, are based on a complex network of interactions.

Highlights

Phenotypes are the result of variation in gene sequence, gene expression and subsequent molecular modifications within a metabolic scheme that varies across populations under distinct environmental pressures [1,2]
We focused on the six-spotted burnet moth Z. filipendulae (Lepidoptera) and its preferred host plant, the bird’s-foot trefoil L. corniculatus (Fabaceae) to examine if defence mechanisms vary along the elevation gradient
Genes involved in the biosynthesis of CNglcs in Z. filipendulae include CYP405A2, CYP332A3 and UGT33A1; the first two genes are part of the cytochrome P450s family (CYP) whose principal role is the assimilation of xenobiotics, and the third gene is part of the UDP glucuronosyltransferase (UGT) enzyme family, which have a role in detoxification of the compounds produced by the P450 enzymes

Summary

Introduction

Phenotypes are the result of variation in gene sequence, gene expression and subsequent molecular modifications within a metabolic scheme that varies across populations under distinct environmental pressures [1,2]. Adaptation along the dimensions of the ecological niche [3] can be caused by molecular changes occurring at the genetic [4], epigenetic [5] or transcription [6] levels, the latter being considered as the predominant driver of phenotypic plasticity [7,8]. Fixation of adaptive alleles and epigenetic polymorphisms occurs in populations if natural selection is not counterbalanced by gene flow [9]. An increasing number of studies have documented differential gene expression along environmental gradients. Phenotypic differences and associated differential gene expression have been observed for genes dealing with cold and hypoxia stress, and haemoglobin polymorphisms [10,11,12]. Few studies have investigated traits that are directly related to interactions among organisms along environmental clines [13,14]

Methods

Results

Conclusion