Collaborative Research: Integration of Glandular Trichome Metabolism and Development by a Flavonoid Pathway Signal

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Trichomes are specialized epidermal cells present in most plants that optimize the production of compounds that provide protection against environmental insults. Broad interest in these epidermal "biofactories" is heightened by the fact that many gland-derived substances are useful for industrial and medicinal purposes. Although significant progress has been made in cataloging the metabolic "parts list" of glandular trichomes, fundamental questions concerning the regulation of metabolism within, and development of, the trichome structure remain to be answered. In keeping with the analogy of the trichome gland as a biochemical factory, this project seeks to address two major questions concerning the operating principles of this highly evolved structure: how are various assembly lines (metabolic pathways) within the factory coordinated, and how do changes in the demand for the assembled products (bioactive compounds) influence the way in which the factory is constructed? The research has potential to transform current views of metabolism by advancing the concept of cross regulation between seemingly disparate metabolic pathways, and defining new roles for well characterized enzymes. Glandular trichomes produce a wide variety of bioactive compounds that protect aerial plant tissues from biotic and abiotic stress. The metabolic activity of trichome glands is often dominated by the production of terpenoids and flavonoids, which comprise two of the most diverse and economically important classes of compounds in nature. Progress in elucidating biosynthetic pathways for these and other secondary metabolites has far outpaced efforts to understand the developmental cell types and structures that are often key to the biological function of defense chemicals. This research project builds on recent studies showing that terpenoid and flavonoid biosynthesis in glandular trichomes of tomato is coupled to gland development and, intriguingly, is coordinately impacted by the action of the flavonoid biosynthesis enzyme chalcone isomerase (CHI). The broad objective of the project is to combine experimental and mathematical modeling approaches to achieve a systems-level understanding of how trichome metabolic and developmental processes are integrated. The experimental approaches are grounded in the use of purified trichome glands (a single cell type) for transcriptomic, proteomic, and metabolomic analyses, as well as powerful genetic tools to manipulate functional processes affecting gland development and metabolism. The research may also reveal new roles for a well-studied metabolic enzyme (CHI) and broaden current views of how small molecules control metabolism. The project provides multi-disciplinary training opportunities for trainees from diverse backgrounds, including participation of undergraduate students in the Plant Genomics REU Summer Research Program. The project will increase access by diverse segments of the public to science through partnerships with the MSU Horticulture Gardens and local industry. Project scientists will partner with the 4-H Children's Garden, local elementary schools, and commercial growers of mint and other aromatic plants to provide children with hands-on learning experiences that illustrate the importance of trichome-derived compounds in plant biology.