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

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.

Is bitter actually better? Targeting a soyasaponin acetyltransferase affects soybean seed germination

“… Type‐Ab soyasaponin biosynthesis in soybean and esculeoside A biosynthesis in tomato The biosynthetic pathway of type‐Ab soyasaponins in soybean ( Glycine max ) (A) modified from Yuan et al (2023) and esculeoside A in tomato ( Solanum lycopersicum ) (B) modified from Sonawane et al (2023). In soybean, the accumulation of type‐Ab deacetyl‐soyasaponins inhibits seed germination.…”

“…Most importantly, GmSSAcT1 was identified as a detoxification enzyme, as its absence in soybean triggers the accumulation of toxic non‐acetylated type‐A soyasaponins, thereby inhibiting seed germination. Recently, a BADH‐type acyltransferase was also identified in tomato and shown to catalyze steroidal glycoalkaloid acetylation to produce non‐bitter and less toxic esculeoside A from bitter and toxic α‐tomatine during tomato fruit maturation (Sonawane et al, 2023) (Figure 1). This important metabolic shift prevents bitterness and toxicity in ripe tomato fruit.…”

Current Advances in the Biosynthesis, Metabolism, and Transcriptional Regulation of α-Tomatine in Tomato

“…Subsequently, 23-hydroxytomatine is spontaneously isomerized to neorickiioside B [ 23 ]. Next, neorickiioside B undergoes acetylation at the C-23 hydroxy group by GAME36 to yield lycoperoside C (23-O-acetylated neorickiioside B) [ 24 ]. The lycoperoside C is then hydroxylated at C-27 by C-27 hydroxylase (E8/Sl27DOX) to form prosapogenin A (acetoxy-hydroxytomatine) [ 25 ].…”

Light regulation of the biosynthesis of phenolics, terpenoids, and alkaloids in plants

“…Alkaloids, which are nitrogen-containing compounds, have been studied extensively for their functions in plant defense against pathogens and insects. Different types of alkaloids and nitrogen-containing metabolites, such as terpenoid indole alkaloids (TIA) in Catharanthus roseus (Madagascar periwinkle) 107 , steroidal glycoalkaloids (SGA) in Solanum lycopersicum (tomato) 108 – 110 , and glucosinolates (GSL) in Arabidopsis 111 , have been the focus of research for their roles in plant defense and benefits in human health. While the biosynthesis and regulation of these SM by the phytohormone jasmonate acid (JA) have been a major focus of many studies 112 , recent research has highlighted the regulatory roles of light in the biosynthesis of GSLs 113 , alkaloids including vindoline in C. roseus 114 , camptothecin in Camptotheca acuminata (Chinese Happy Tree) 115 , and SGAs in tomato (Fig.…”

“…The enzymes catalyzing these steps are well characterized and known as GLYCOALKALOID METABOLISM enzymes (GAMEs) (Fig. 5 ) 109 , 110 . SGA biosynthesis is light inducible as most of the GAMEs are upregulated in response to light exposure 126 .…”