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Elife

Title:		"Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)"
Author(s):		Zust T; Strickler SR; Powell AF; Mabry ME; An H; Mirzaei M; York T; Holland CK; Kumar P; Erb M; Petschenka G; Gomez JM; Perfectti F; Muller C; Pires JC; Mueller LA; Jander G;
Address:		"Institute of Plant Sciences, University of Bern, Bern, Switzerland. Boyce Thompson Institute, Ithaca, United States. Division of Biological Sciences, University of Missouri, Columbia, United States. Institut fur Insektenbiotechnologie, Justus-Liebig-Universitat Giessen, Giessen, Germany. Department of Functional and Evolutionary Ecology, Estacion Experimental de Zonas Aridas (EEZA-CSIC), Almeria, Spain. Research Unit Modeling Nature, Department of Genetics, University of Granada, Granada, Spain. Department of Chemical Ecology, Bielefeld University, Bielefeld, Germany"
Journal Title:		Elife
Year:		2020
Volume:		20200407
Issue:
Page Number:		-
DOI:		10.7554/eLife.51712
ISSN/ISBN:		2050-084X (Electronic) 2050-084X (Linking)
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. Plants are often attacked by insects and other herbivores. As a result, they have evolved to defend themselves by producing many different chemicals that are toxic to these pests. As producing each chemical costs energy, individual plants often only produce one type of chemical that is targeted towards their main herbivore. Related species of plants often use the same type of chemical defense so, if a particular herbivore gains the ability to cope with this chemical, it may rapidly become an important pest for the whole plant family. To escape this threat, some plants have gained the ability to produce more than one type of chemical defense. Wallflowers, for example, are a group of plants in the mustard family that produce two types of toxic chemicals: mustard oils, which are common in most plants in this family; and cardenolides, which are an innovation of the wallflowers, and which are otherwise found only in distantly related plants such as foxglove and milkweed. The combination of these two chemical defenses within the same plant may have allowed the wallflowers to escape attacks from their main herbivores and may explain why the number of wallflower species rapidly increased within the last two million years. Zust et al. have now studied the diversity of mustard oils and cardenolides present in many different species of wallflower. This analysis revealed that almost all of the tested wallflower species produced high amounts of both chemical defenses, while only one species lacked the ability to produce cardenolides. The levels of mustard oils had no relation to the levels of cardenolides in the tested species, which suggests that the regulation of these two defenses is not linked. Furthermore, Zust et al. found that closely related wallflower species produced more similar cardenolides, but less similar mustard oils, to each other. This suggests that mustard oils and cardenolides have evolved independently in wallflowers and have distinct roles in the defense against different herbivores. The evolution of insect resistance to pesticides and other toxins is an important concern for agriculture. Applying multiple toxins to crops at the same time is an important strategy to slow the evolution of resistance in the pests. The findings of Zust et al. describe a system in which plants have naturally evolved an equivalent strategy to escape their main herbivores. Understanding how plants produce multiple chemical defenses, and the costs involved, may help efforts to breed crop species that are more resistant to herbivores and require fewer applications of pesticides. eng"
Keywords:		"Erysimum/*chemistry/classification/*genetics Evolution, Molecular *Genome, Plant Geography Phenotype *Phylogeny Phytochemicals/*analysis Plants, Toxic/chemistry/classification/*genetics Erysimum cardenolides evolutionary biology glucosinolates myrosinase;"
Notes:		"MedlineZust, Tobias Strickler, Susan R Powell, Adrian F Mabry, Makenzie E An, Hong Mirzaei, Mahdieh York, Thomas Holland, Cynthia K Kumar, Pavan Erb, Matthias Petschenka, Georg Gomez, Jose-Maria Perfectti, Francisco Muller, Caroline Pires, J Chris Mueller, Lukas A Jander, Georg eng PZ00P3-161472/Schweizerischer Nationalfonds zur Forderung der Wissenschaftlichen Forschung/ 1811965/National Science Foundation/ 1645256/National Science Foundation/ DFG-PE 2059/3-1/Deutsche Forschungsgemeinschaft/ CGL2017-86626-C2-2-P/Agencia Estata de Investigacion, Spain/ FEDER 2014-2020 A-RNM-505-UGR18/Junta de Andalucia Programa Operativo/ CGL2017-86626-C2-2-P/Agencia Estatal de Investigacion/ Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. England 2020/04/08 Elife. 2020 Apr 7; 9:e51712. doi: 10.7554/eLife.51712"