Tomato E8 Encodes a C-27 Hydroxylase in Metabolic Detoxification of α-Tomatine during Fruit Ripening

Plant Cell Physiol. 2021 Oct 1;62(5):775-783. doi: 10.1093/pcp/pcab080.

Abstract

Tomato (Solanum lycopersicum) contains α-tomatine, a steroidal glycoalkaloid that contributes to the plant defense against pathogens and herbivores through its bitter taste and toxicity. It accumulates at high levels in all the plant tissues, especially in leaves and immature green fruits, whereas it decreases during fruit ripening through metabolic conversion to the nontoxic esculeoside A, which accumulates in the mature red fruit. This study aimed to identify the gene encoding a C-27 hydroxylase that is a key enzyme in the metabolic conversion of α-tomatine to esculeoside A. The E8 gene, encoding a 2-oxoglutalate-dependent dioxygenase, is well known as an inducible gene in response to ethylene during fruit ripening. The recombinant E8 was found to catalyze the C-27 hydroxylation of lycoperoside C to produce prosapogenin A and is designated as Sl27DOX. The ripe fruit of E8/Sl27DOX-silenced transgenic tomato plants accumulated lycoperoside C and exhibited decreased esculeoside A levels compared with the wild-type (WT) plants. Furthermore, E8/Sl27DOX deletion in tomato accessions resulted in higher lycoperoside C levels in ripe fruits than in WT plants. Thus, E8/Sl27DOX functions as a C-27 hydroxylase of lycoperoside C in the metabolic detoxification of α-tomatine during tomato fruit ripening, and the efficient detoxification by E8/27DOX may provide an advantage in the domestication of cultivated tomatoes.

Keywords: 2-Oxoglutarate-dependent dioxygenase; E8; Fruit ripening; Sl27DOX; Steroidal glycoalkaloid; Tomato (Solanum lycopersicum); a-Tomatine.

MeSH terms

  • Fruit / growth & development
  • Fruit / metabolism*
  • Mixed Function Oxygenases / genetics
  • Mixed Function Oxygenases / metabolism*
  • Phylogeny
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Plants, Genetically Modified
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Saponins / metabolism
  • Solanum lycopersicum / genetics
  • Solanum lycopersicum / growth & development
  • Solanum lycopersicum / metabolism*
  • Substrate Specificity
  • Tomatine / analogs & derivatives*
  • Tomatine / metabolism

Substances

  • Plant Proteins
  • Recombinant Proteins
  • Saponins
  • alpha-tomatine
  • Tomatine
  • prosapogenin
  • Mixed Function Oxygenases