A BAHD-type acyltransferase concludes the biosynthetic pathway of non-bitter glycoalkaloids in ripe tomato fruit

Prashant D. Sonawane (), Sachin A. Gharat, Adam Jozwiak, Ranjit Barbole, Sarah Heinicke, Efrat Almekias-Siegl, Sagit Meir, Ilana Rogachev, Sarah E. O’ Connor, Ashok P. Giri and Asaph Aharoni ()
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Prashant D. Sonawane: Max Planck Institute for Chemical Ecology
Sachin A. Gharat: Weizmann Institute of Science
Adam Jozwiak: Weizmann Institute of Science
Ranjit Barbole: Weizmann Institute of Science
Sarah Heinicke: Max Planck Institute for Chemical Ecology
Efrat Almekias-Siegl: Weizmann Institute of Science
Sagit Meir: Weizmann Institute of Science
Ilana Rogachev: Weizmann Institute of Science
Sarah E. O’ Connor: Max Planck Institute for Chemical Ecology
Ashok P. Giri: Weizmann Institute of Science
Asaph Aharoni: Weizmann Institute of Science

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract Tomato is the highest value fruit and vegetable crop worldwide, yet produces α-tomatine, a renowned toxic and bitter-tasting anti-nutritional steroidal glycoalkaloid (SGA) involved in plant defense. A suite of modifications during tomato fruit maturation and ripening converts α-tomatine to the non-bitter and less toxic Esculeoside A. This important metabolic shift prevents bitterness and toxicity in ripe tomato fruit. While the enzymes catalyzing glycosylation and hydroxylation reactions in the Esculeoside A pathway have been resolved, the proposed acetylating step remains, to date, elusive. Here, we discovered that GAME36 (GLYCOALKALOID METABOLISM36), a BAHD-type acyltransferase catalyzes SGA-acetylation in cultivated and wild tomatoes. This finding completes the elucidation of the core Esculeoside A biosynthetic pathway in ripe tomato, allowing reconstitution of Esculeoside A production in heterologous microbial and plant hosts. The involvement of GAME36 in bitter SGA detoxification pathway points to a key role in the evolution of sweet-tasting tomato as well as in the domestication and breeding of modern cultivated tomato fruit.

Date: 2023
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DOI: 10.1038/s41467-023-40092-5

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