Pathways to defense metabolites and evading fruit bitterness in genus Solanum evolved through 2-oxoglutarate-dependent dioxygenases

Pablo D Cárdenas,Tamar Unger,Ilana Rogachev,Saul Burdman,Itai Ofner,Ashok P Giri ,Sayantan Panda,Adam Jóźwiak ,Margarita Pliner,Prashant Sonawane ,Yana Kazachkova,Ester Vilaprinyó ,Amit Gal‐On ,Dalia Wolf,Sagit Meir,Bekele Abebie,Olga Davydov,Tali Scherf,Dani Zamir,Uwe Heinig,Jędrzej Szymański ,Asaph Aharoni

doi:10.1038/s41467-019-13211-4

Abstract

The genus Solanum comprises three food crops (potato, tomato, and eggplant), which are consumed on daily basis worldwide and also producers of notorious anti-nutritional steroidal glycoalkaloids (SGAs). Hydroxylated SGAs (i.e. leptinines) serve as precursors for leptines that act as defenses against Colorado Potato Beetle (Leptinotarsa decemlineata Say), an important pest of potato worldwide. However, SGA hydroxylating enzymes remain unknown. Here, we discover that 2-OXOGLUTARATE-DEPENDENT-DIOXYGENASE (2-ODD) enzymes catalyze SGA-hydroxylation across various Solanum species. In contrast to cultivated potato, Solanum chacoense, a widespread wild potato species, has evolved a 2-ODD enzyme leading to the formation of leptinines. Furthermore, we find a related 2-ODD in tomato that catalyzes the hydroxylation of the bitter α-tomatine to hydroxytomatine, the first committed step in the chemical shift towards downstream ripening-associated non-bitter SGAs (e.g. esculeoside A). This 2-ODD enzyme prevents bitterness in ripe tomato fruit consumed today which otherwise would remain unpleasant in taste and more toxic.

Highlights

The genus Solanum comprises three food crops, which are consumed on daily basis worldwide and producers of notorious anti-nutritional steroidal glycoalkaloids (SGAs)
While several quantitative trait loci (QTL) regions associated with leptinine and leptine biosynthesis were identified in segregating potato populations (S. tuberosum × S. chacoense), none of the genes partaking in leptinine/leptine biosynthesis have been discovered to date[19,20,21,22]
We hypothesized that leptinines formation from α-chaconine and α-solanine in wild potato S. chacoense requires an enzyme similar to the one catalyzing hydroxylation of α-tomatine, the major bitter SGA7 in the green tissues of related tomato species (Fig. 1)

Summary

Introduction

The genus Solanum comprises three food crops (potato, tomato, and eggplant), which are consumed on daily basis worldwide and producers of notorious anti-nutritional steroidal glycoalkaloids (SGAs). During transition from green to red fruit, α-tomatine is converted to esculeoside A, a major non-bitter SGA (Fig. 1, and refer Supplementary Fig. 1 for detailed SGA pathway) This chemical shift during fruit ripening involves several modification steps including hydroxylation, acetylation, and glycosylation[8,9]. In certain wild potato species, such as Solanum chacoense, α-chaconine/α-solanine are hydroxylated to form leptinines (leptinine I and II) which are further acetylated to form leptines (leptine I and II) (Fig. 1) These modified SGAs are known for their insecticidal activity including against the Colorado potato beetle (CPB), a major pest of potato and other Solanum crops comprising pepper, tomato, and eggplant[11,12,13,14,15,16,17,18]. The discovery of SGAs hydroxylating enzymes in important crops such as tomato, potato, and eggplant offers the means to reduce anti-nutritional factors, through

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