RESEARCH-PGR: Combining machine learning and experimental analysis to define trichome and root-specific gene regulatory networks in cultivated tomato and related Solanaceae species

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Plant specialized metabolites are distinct chemicals, only made by certain species, often in specific plant parts. Some specialized metabolites are poisonous to plant pests, while others attract beneficial insects or microbes. Many specialized metabolites are flavorful to humans, for example those in basil, mint, and ginger root, while others have medicinal properties, such as the anti-cancer drug taxol and the antimalarial artemisinin. Tomatoes produce specialized metabolites called acylsugars, which are sticky like fly paper glue and protect against pests. Acylsugars are only made in two parts of the tomato: 1) tiny hair-like structures on the leaf surface called trichomes and 2) roots. Understanding how tomatoes control when and where acylsugars are produced will teach biotechnologists how to modify or even design plants to make specialized metabolites in designated plant parts at certain developmental stages. Our first goal is to combine bench experiments and computational analyses to uncover the DNA sequences and proteins that control acylsugar production in trichomes and roots. Next, we will compare DNA and proteins across tomato relatives to reveal how acylsugar production has evolved in trichomes and roots. Beyond research, our team will lead two activities to engage the public about our scientific approaches and findings: “Code-Like-A-Girl'', designed for elementary and middle school girls to practice computational thinking, and “Why are Plants So Smelly?”, which introduces participants to plant specialized metabolites. Specialized metabolites are synthesized in specific cells or tissues, indicating they are under tight regulatory control. However, the cis-regulatory sequences and DNA-binding transcription factors regulating tissue- and cell type-specific expression of specialized metabolism genes are often unknown. Because tomato acylsugars are synthesized specifically in trichomes and roots, our goals are to utilize the acylsugar pathway as a model to: (1) identify the cis/trans mechanisms regulating spatially-specific expression of metabolic genes and (2) assess the contribution of regulatory evolution to metabolic diversity. These goals will be addressed using Solanaceae species, focusing on the cultivated tomato, Solanum lycopersicum, and its wild relative, S. pennellii. This project will generate trichome and root gene regulatory networks, describing genome-wide connections between transcription factors, the cis-regulatory sequences they bind, and their target genes in each species. Comparison of acylsugar regulatory components across Solanaceae species will reveal the molecular changes underlying trichome- and root-specific expression evolution. These findings will provide new details on how cis/trans regulatory innovations influence spatial expression patterns and ultimately contribute to adaptive functions of specialized metabolites. This project provides a natural platform for interdisciplinary scientific training because it includes experts in biochemistry, computational biology, evolutionary biology, genetics, and genomics. In addition, the project will host undergraduates each summer from the PlantGenomics@MSU REU program, a 10-week research-intensive experience including computational biology training, a weekly STEM career workshop, a weekly seminar engaging students on diverse research themes, professional development opportunities, and oral/poster presentations.This 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.