Evolution of Secondary Herbivore Defense Metabolite Biosynthesis from Primary Metabolism in the non-model Crucifer Erysimum (wallflower)

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This action funds an NSF National Plant Genome Initiative Postdoctoral Research Fellowship in Biology for FY 2018. The fellowship supports a research and training plan in a host laboratory for the Fellow who also presents a plan to broaden participation in biology. The title of the research and training plan for this fellowship to Dr. Cynthia Holland is "Evolution of Secondary Herbivore Defense Metabolite Biosynthesis from Primary Metabolism in the non-model Crucifer Erysimum (wallflower)." The host institution for the fellowship is the Boyce Thompson Institute and the sponsoring scientists are Drs. Georg Jander and Lukas Mueller.To protect themselves against insect herbivores, plants have evolved a wide variety of chemical defenses. One class of plant defensive metabolites, known as cardiac glycosides, is found in at least twelve plant families and works by slowing the contractions and increasing the pumping force of the predator's heart. Despite the therapeutic use of these compounds in treating arrhythmias and congestive heart failure, a complete pathway for cardiac glycoside biosynthesis is not known for any plant species. This project will use the cardiac glycoside-producing wormseed wallflower (Erysimum cheiranthoides) to identify the biosynthetic pathway genes for these compounds. These results will contribute to the understanding of the evolution of defensive chemicals in other plant species, including important crops such as maize, soybean, and wheat. Training objectives include metabolomics, genetics, gene expression technologies and bioinformatics. Broader impacts include introducing underrepresented students to genomics and chemical ecology research via mentoring through an NSF-funded REU program, outreach to high school students at an urban high school in Yonkers (NY) and the development of laboratory kits for middle- and high-school teachers in rural New York.As a rapidly-growing, self-pollinating annual, E. cheiranthoides is an excellent model system for investigating the evolution of a new metabolic pathway for the production of cardenolides, a class of cardiac glycosides involved in herbivore defense. Modification of ubiquitous biosynthetic pathways of endogenous plant steroids, e.g. brassinosteroids, has likely been repeatedly selected for in the course of evolution to generate similar anti-herbivore toxins. This research will identify expansion and neofunctionalization of the enzyme families in E. cheiranthoides that normally contribute to primary metabolism in other crucifer species. Erysimum homologs of known cardenolide biosynthetic genes from other species will be identified using genome assemblies and characterized using structure-function-sequence analysis. Missing genes in the cardenolide pathway will be discovered through comparative metabolomics, transcriptomics, genomics, and forward genetic screens. Finally, the ecological "escape from herbivory" hypothesis will be tested by examining the role of cardenolides in host-insect interactions. Results from this research will be shared through publications, presentations at conferences, and inclusion in www.erysimum.org, a wallflower-specific website which will serve as a publicly accessible repository for all data related to this project.Keywords: biosynthesis biochemistry, plant biotic stress, comparative genomicsThis award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.