Nature Communications (Jul 2023)

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,
  • Asaph Aharoni

DOI
https://doi.org/10.1038/s41467-023-40092-5
Journal volume & issue
Vol. 14, no. 1
pp. 1 – 15

Abstract

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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.