Steroidal glycoalkaloids contribute to anthracnose resistance in solanum lycopersicum

Authors: FABIAN, MATTHEW - Oak Ridge Institute For Science And Education (ORISE); ZHANG, CHONG - Oak Ridge Institute For Science And Education (ORISE); Sun, Jianghao; Price, Neil; Chen, Pei; Clarke, Christopher; Jones, Richard; Stommel, John

Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/23/2023
Publication Date: 3/24/2023
Citation: Fabian, M.L., Zhang, C., Sun, J., Price, N.P., Chen, P., Clarke, C.R., Jones, R.W., Stommel, J.R. 2023. Steroidal glycoalkaloids contribute to anthracnose resistance in solanum lycopersicum. Journal of Experimental Botany. 74(12):3700-3713. https://doi.org/10.1093/jxb/erad108.
DOI: https://doi.org/10.1093/jxb/erad108

Interpretive Summary: Anthracnose is a widespread plant disease, caused by the fungal pathogen Colletotrichum, that affects a wide range of crops including tomato fruit. Anthracnose infections of tomato fruit are characterized by the formation of necrotic lesions. Previously our laboratory has utilized an anthracnose-resistant, wild tomato line (95L368) in breeding experiments to further understand the inheritance of anthracnose resistance. This work describes our research into the biochemistry and genetic control of anthracnose resistance in 95L368 and discovery of a role for metabolites known as steroidal glycoalkaloids (SGAs) in anthracnose resistance. We determined that the SGA alpha-tomatine, as well as certain derivatives of alpha-tomatine, accumulate to high levels in anthracnose-resistant fruit, and confirmed a role for corresponding genes (GAME genes) that regulate SGA biosynthesis. Furthermore, we tested and affirmed the hypothesis that reducing expression of select GAME genes in anthracnose-susceptible fruit, would result in enhanced anthracnose resistance. This work provides a foundation for new genetic tools for the management of anthracnose in tomato and other crops. The results are valuable for scientists investigating fundamental aspects of plant disease resistance and for plant breeders developing anthracnose resistant tomato cultivars.

Technical Abstract: Anthracnose is a widespread plant disease caused by various species of the fungal pathogen Colletotrichum. In solanaceous plants such as tomato (Solanum lycoperiscum), Colletotrichum infections exhibit a quiescent, asymptomatic state in developing fruit, followed by a transition to necrotrophic infections in ripe fruit. Through analysis of fruit tissue extracts of 95L368, a tomato breeding line that yields fruit with enhanced anthracnose resistance, we identified a role for steroidal glycoalkaloids (SGAs) in anthracnose resistance. The SGA a-tomatine and several of its derivatives accumulated at higher levels, in comparison to fruit of the susceptible tomato cultivar US28, in 95L368 fruit extracts with fungistatic activity against Colletotrichum. Correspondingly, ripe and unripe 95L368 fruit displayed enhanced expression of glycoalkaloid metabolic enzyme (GAME) genes, which encode key enzymes in SGA biosynthesis. Metabolomics analysis incorporating recombinant inbred lines (RILs) generated from 95L368 and US28 yielded strong positive correlations between anthracnose resistance and accumulation of a-tomatine and several derivatives. Lastly, transient silencing of expression of the GAME genes GAME31 and GAME5 in anthracnose-susceptible tomato fruit yielded enhancements to anthracnose resistance. Together, our data support a role for SGAs in anthracnose defense in tomato, with a distinct SGA metabolomic profile conferring resistance to virulent Colletotrichum infections in ripe fruit.