Green-fruited Solanum habrochaites lacks fruit-specific carotenogenesis due to metabolic and structural blocks

J Exp Bot. 2017 Oct 13;68(17):4803-4819. doi: 10.1093/jxb/erx288.

Abstract

Members of the tomato clade exhibit a wide diversity in fruit color, but the mechanisms governing inter-species diversity of coloration are largely unknown. The carotenoid profiles, carotenogenic gene expression and proteome profiles of green-fruited Solanum habrochaites (SH), orange-fruited S. galapagense, and red-fruited S. pimpinellifolium were compared with cultivated tomato [S. lycopersicum cv. Ailsa Craig (SL)] to decipher the molecular basis of coloration diversity. Green-fruited SH, though it showed normal expression of chromoplast-specific phytoene synthase1 and lycopene β-cyclase genes akin to orange/red-fruited species, failed to accumulate lycopene and β-carotene. The SH phytoene synthase1 cDNA encoded an enzymatically active protein, whereas the lycopene β-cyclase cDNA was barely active. Consistent with its green-fruited nature, SH's fruits retained chloroplast structure and PSII activity, and had impaired chlorophyll degradation with high pheophorbide a levels. Comparison of the fruit proteomes with SL revealed retention of the proteome complement related to photosynthesis in SH. Targeted peptide monitoring revealed a low abundance of key carotenogenic and sequestration proteins in SH compared with tomato. The green-fruitedness of SH appears to stem from blocks at several critical steps regulating fruit-specific carotenogenesis namely the absence of chloroplast to chromoplast transformation, block in carotenoid biosynthesis, and a dearth of carotenoid sequestering proteins.

Keywords: Carotenoid biosynthesis; carotenoid sequestration; fruit color; gene expression; proteome analysis; tomato clade.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carotenoids / metabolism*
  • Color
  • Fruit / physiology*
  • Gene Expression*
  • Pigments, Biological / metabolism
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Proteome*
  • Solanum / genetics
  • Solanum / physiology*

Substances

  • Pigments, Biological
  • Plant Proteins
  • Proteome
  • Carotenoids