Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae).

Tobias Züst,Caroline Müller,Pavan Kumar,Cynthia K Holland,J Chris Pires,Francisco Perfectti,Hong An,Thomas York,Georg Jander,José-María Gómez,Mahdieh Mirzaei,Makenzie E Mabry,Adrian F Powell,Matthias Erb,Susan R Strickler,Georg Petschenka,Lukas A Mueller

doi:10.7554/elife.51712

Abstract

Phytochemical diversity is thought to result from coevolutionary cycles as specialization in herbivores imposes diversifying selection on plant chemical defenses. Plants in the speciose genus Erysimum (Brassicaceae) produce both ancestral glucosinolates and evolutionarily novel cardenolides as defenses. Here we test macroevolutionary hypotheses on co-expression, co-regulation, and diversification of these potentially redundant defenses across this genus. We sequenced and assembled the genome of E. cheiranthoides and foliar transcriptomes of 47 additional Erysimum species to construct a phylogeny from 9868 orthologous genes, revealing several geographic clades but also high levels of gene discordance. Concentrations, inducibility, and diversity of the two defenses varied independently among species, with no evidence for trade-offs. Closely related, geographically co-occurring species shared similar cardenolide traits, but not glucosinolate traits, likely as a result of specific selective pressures acting on each defense. Ancestral and novel chemical defenses in Erysimum thus appear to provide complementary rather than redundant functions.

Highlights

Plant chemical defenses play a central role in the coevolutionary arms race with herbivorous insects
After grouping species into nine chemotypes defined by chemical dissimilarity and the production of characteristic glucosinolate compounds (Figure 7C), we found that myrosinase activity significantly differed among these chemotypes (Figure 8, F8,33 = 8.31, p
The evolutionarily recent gain of novel cardenolides has resulted in a system in which no known specific adaptations to cardenolides have yet evolved de novo in insect herbivores, general adaptations to toxic food may still allow herbivores to consume the plants

Summary

Introduction

Plant chemical defenses play a central role in the coevolutionary arms race with herbivorous insects. In response to diverse environmental challenges, plants have evolved a plethora of structurally diverse organic compounds with repellent, antinutritive, or toxic properties (Fraenkel, 1959; Mithofer and Boland, 2012). Chemical diversity is likely evolving in response to a multitude of plant-herbivore interactions (Salazar et al, 2018), and community-level phytochemical diversity may be a key driver of niche segregation and insect community dynamics (Richards et al, 2015; Sedio et al, 2017).

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Discussion

Conclusion