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

Author:

Züst Tobias1ORCID,Strickler Susan R2,Powell Adrian F2,Mabry Makenzie E3,An Hong3,Mirzaei Mahdieh2,York Thomas2,Holland Cynthia K2,Kumar Pavan2ORCID,Erb Matthias1ORCID,Petschenka Georg4ORCID,Gómez José-María5,Perfectti Francisco6ORCID,Müller Caroline7,Pires J Chris3,Mueller Lukas A2,Jander Georg2ORCID

Affiliation:

1. Institute of Plant Sciences, University of Bern, Bern, Switzerland

2. Boyce Thompson Institute, Ithaca, United States

3. Division of Biological Sciences, University of Missouri, Columbia, United States

4. Institut für Insektenbiotechnologie, Justus-Liebig-Universität Giessen, Giessen, Germany

5. Department of Functional and Evolutionary Ecology, Estación Experimental de Zonas Áridas (EEZA-CSIC), Almería, Spain

6. Research Unit Modeling Nature, Department of Genetics, University of Granada, Granada, Spain

7. Department of Chemical Ecology, Bielefeld University, Bielefeld, Germany

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.

Funder

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

National Science Foundation

Triad Foundation

Deutsche Forschungsgemeinschaft

Agencia Estatal de Investigación

LOEWE Program Insect Biotechnology and Bioresources

Junta de Andalucia Programa Operativo

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference193 articles.

1. Using complementary techniques to distinguish cryptic species: a new Erysimum (Brassicaceae) species from north africa;Abdelaziz;American Journal of Botany,2011

2. Phylogenetic relationships of Erysimum (Brassicaceae) from the baetic mountains (SE iberian peninsula);Abdelaziz;Anales Del Jardín Botánico De Madrid,2014

3. Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores;Agrawal;Evolutionary Ecology Research,2005

4. Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions;Agrawal;New Phytologist,2012

5. Phylogenetic escalation and decline of plant defense strategies;Agrawal;PNAS,2008

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