Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)
- University of Bern, Switzerland
- Boyce Thompson Institute, United States
- University of Missouri, United States
- Justus-Liebig-Universität, Germany
- Estación Experimental de Zonas Áridas, Spain
- Universidad de Granada, Spain
- Bielefeld University, 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 9,869 orthologous genes, revealing several geographic clades but also high levels 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.
Data availability
Sequence data are available under GenBank project ID PRJNA563696 and www.erysimum.org, while all trait data and R code for trait and phylogenetic analyses are available from the Dryad Digital Repository
-
Data from: Rapid and independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)Dryad Digital Repository, doi:10.5061/dryad.7hb5c59.
Article and author information
Author details
Francisco Perfectti
Funding
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (PZ00P3-161472)
- Tobias Züst
National Science Foundation (1811965)
- Cynthia K Holland
Triad Foundation
- Susan R Strickler
- Georg Jander
National Science Foundation (1645256)
- Georg Jander
Deutsche Forschungsgemeinschaft (DFG-PE 2059/3-1)
- Georg Petschenka
Agencia Estata de Investigacion, Spain (CGL2017-86626-C2-2-P)
- Francisco Perfectti
LOEWE Program Insect Biotechnology and Bioresources
- Georg Petschenka
Junta de Andalucia Programa Operativo (FEDER 2014-2020 A-RNM-505-UGR18)
- Francisco Perfectti
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Daniel J Kliebenstein, University of California, Davis, United States
Version history
- Received: September 8, 2019
- Accepted: March 24, 2020
- Accepted Manuscript published: April 7, 2020 (version 1)
- Version of Record published: April 23, 2020 (version 2)
Copyright
© 2020, Züst et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 4,876
- Page views
-
- 648
- Downloads
-
- 42
- Citations
Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)
eLife 9:e51712.
https://doi.org/10.7554/eLife.51712
Further reading
-
- Evolutionary Biology
Biologically-controlled mineralization producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation since the earliest Cambrian. Among them, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to build their shells. One of the most distinct shell structures is the organo-phosphatic cylindrical column exclusive to phosphatic-shelled brachiopods, including both crown and stem groups. However, the complexity, diversity, and biomineralization processes of these microscopic columns are far from clear in brachiopod ancestors. Here, exquisitely well-preserved columnar shell ultrastructures are reported for the first time in the earliest eoobolids Latusobolus xiaoyangbaensis gen. et sp. nov. and Eoobolus acutulus sp. nov. from the Cambrian Series 2 Shuijingtuo Formation of South China. The hierarchical shell architectures, epithelial cell moulds, and the shape and size of cylindrical columns are scrutinised in these new species. Their calcium phosphate-based biomineralized shells are mainly composed of stacked sandwich columnar units. The secretion and construction of the stacked sandwich model of columnar architecture, which played a significant role in the evolution of linguliforms, is highly biologically controlled and organic-matrix mediated. Furthermore, a continuous transformation of anatomic features resulting from the growth of diverse columnar shells is revealed between Eoobolidae, Lingulellotretidae, and Acrotretida, shedding new light on the evolutionary growth and adaptive innovation of biomineralized columnar architecture among early phosphatic-shelled brachiopods during the Cambrian explosion.
-
- Developmental Biology
- Evolutionary Biology
Biomineralization had apparently evolved independently in different phyla, using distinct minerals, organic scaffolds, and gene regulatory networks (GRNs). However, diverse eukaryotes from unicellular organisms, through echinoderms to vertebrates, use the actomyosin network during biomineralization. Specifically, the actomyosin remodeling protein, Rho-associated coiled-coil kinase (ROCK) regulates cell differentiation and gene expression in vertebrates’ biomineralizing cells, yet, little is known on ROCK’s role in invertebrates’ biomineralization. Here, we reveal that ROCK controls the formation, growth, and morphology of the calcite spicules in the sea urchin larva. ROCK expression is elevated in the sea urchin skeletogenic cells downstream of the Vascular Endothelial Growth Factor (VEGF) signaling. ROCK inhibition leads to skeletal loss and disrupts skeletogenic gene expression. ROCK inhibition after spicule formation reduces the spicule elongation rate and induces ectopic spicule branching. Similar skeletogenic phenotypes are observed when ROCK is inhibited in a skeletogenic cell culture, indicating that these phenotypes are due to ROCK activity specifically in the skeletogenic cells. Reduced skeletal growth and enhanced branching are also observed under direct perturbations of the actomyosin network. We propose that ROCK and the actomyosin machinery were employed independently, downstream of distinct GRNs, to regulate biomineral growth and morphology in Eukaryotes.
