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

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.

Genome-wide characterization of 2-oxoglutarate and Fe(II)-dependent dioxygenase family genes in tomato during growth cycle and their roles in metabolism

“…The content of downstream SGAs decreases gradually after the Br period along with the expression of the downstream biosynthesis-related gene GAME31 . These results are consistent with those of a previous study [ 40 ].

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“…7 a). In contrast, GAME31 was mainly expressed at the tomato fruit ripening stage and catalyzes the first important step in the chemical shift after maturation within nonbitter SGA by a hydroxylation reaction [ 39 , 40 ]. Interestingly, we found that the different expression patterns between GAME11 and GAME31 resulted in the appropriate function at the right time.…”

Bitter and sweet make tomato hard to (b)eat

“…The high α‐tomatine levels in immature fruit decrease during ripening by the conversion to esculeoside A (Fig. 1; Mintz‐Oron et al ., 2008; Iijima et al ., 2009; Cárdenas et al ., 2019; Nakayasu et al ., 2020). The antimicrobial activity of α‐tomatine was first demonstrated on the fungal pathogen Fusarium oxysporum f. sp.…”

The biosynthetic pathway of potato solanidanes diverged from that of spirosolanes due to evolution of a dioxygenase

“…Tomato and eggplant, on the other hands, contain only spirosolane glycoalkaloids 3 , 13 . In tomato, α-tomatine 5 and dehydrotomatine 6 are predominant in green tissues, while the non-bitter SGA esculeoside A is the major component in the red mature fruits 14 , 15 . α-Solasonine and α-solamargine are the two major spirosolane glycoalkaloids produced in eggplant 16 .…”