Steroidal alkaloid biosynthesis is coordinately regulated and differs among tomatoes in the red-fruited clade

Authors: Dzakovich, Michael; FRANCIS, DAVID - The Ohio State University; COOPERSTONE, JESSICA - The Ohio State University

Submitted to: The Plant Genome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/20/2021
Publication Date: 2/20/2022
Citation: Dzakovich, M.P., Francis, D.M., Cooperstone, J.L. 2022. Steroidal alkaloid biosynthesis is coordinately regulated and differs among tomatoes in the red-fruited clade. The Plant Genome. https://doi.org/10.1002/tpg2.20192.
DOI: https://doi.org/10.1002/tpg2.20192

Interpretive Summary: Tomato consumption is associated with many health benefits including lowering the risk of developing diseases, such as prostate cancer. However, it is unknown what chemical components of tomatoes are responsible for these benefits. Recent data suggests that steroidal alkaloids are a chemical component of tomatoes that may contribute to positive health outcomes. However, the quantity, diversity, and production of these compounds is poorly understood. We generated some of the first quantitative data about steroidal alkaloids in a diverse population of tomatoes. Wild ancestors of tomatoes tended to have much higher amounts of steroidal alkaloids in their fruits compared to modern varieties and this outcome is under strong genetic control. We also discovered a genetic region that seems to control the shift from steroidal alkaloids in green unripe tomatoes to steroidal alkaloids found in red, ripe tomatoes. Our findings represent important conclusions for plant metabolism and provide opportunities to better understand the role of tomato steroidal alkaloids in defense, flavor, and human health. The genetic targets we discovered could be used to generate tomato varieties that would allow nutritional questions about tomato consumption to be answered.

Technical Abstract: The tomato clade of Solanaceae features a unique assortment of cholesterol-derived steroidal alkaloids. However, little quantitative data exists reporting the profile and concentration of these alkaloids across diverse fruit germplasm. To address the lack of knowledge regarding the chemical diversity, concentration, and genetic architecture controlling tomato steroidal alkaloids we quantitatively profiled and genotyped two tomato populations representing diversity in the red-fruited clade. We grew 107 genetically diverse fresh market, processing, landrace, and wild tomatoes in multiple environments. Nine steroidal alkaloids were quantified using ultra-high performance liquid chromatography tandem mass spectrometry. The diversity panel and a biparental population segregating for high alpha-tomatine, were genotyped to identify and validate quantitative trait loci (QTL) associated with steroidal alkaloids. Landraces and wild material exhibited higher alkaloid concentrations and more chemical diversity. Average total content of steroidal alkaloids, often dominated by lycoperoside F/G/esculeoside A, ranged from 1.9 to 23.3 mg/100 g fresh weight across accessions. Landrace and wild cherry accessions distinctly clustered based on elevated concentrations of early or late pathway steroidal alkaloids. Significant correlations were observed among alkaloids from the early and late parts of the biosynthetic pathway, in a species-dependent manner. A QTL controlling multiple, early steroidal alkaloid pathway intermediates on chromosome 3 was identified by genome wide association (GWAS) and validated in a backcross population. Tomato steroidal alkaloids are diverse in the red-fruited clade and their biosynthesis is regulated in a coordinated manner.