Improved fruit α-tocopherol, carotenoid, squalene and phytosterol contents through manipulation of Brassica juncea 3-HYDROXY-3-METHYLGLUTARYL-COA SYNTHASE1 in transgenic tomato

Plant Biotechnol J. 2018 Mar;16(3):784-796. doi: 10.1111/pbi.12828. Epub 2017 Oct 17.

Abstract

3-Hydroxy-3-methylglutaryl-coenzyme A synthase (HMGS) in the mevalonate (MVA) pathway generates isoprenoids including phytosterols. Dietary phytosterols are important because they can lower blood cholesterol levels. Previously, the overexpression of Brassica juncea wild-type (wt) and mutant (S359A) BjHMGS1 in Arabidopsis up-regulated several genes in sterol biosynthesis and increased sterol content. Recombinant S359A had earlier displayed a 10-fold higher in vitro enzyme activity. Furthermore, tobacco HMGS overexpressors (OEs) exhibited improved sterol content, plant growth and seed yield. Increased growth and seed yield in tobacco OE-S359A over OE-wtBjHMGS1 coincided with elevations in NtSQS expression and sterol content. Herein, the overexpression of wt and mutant (S359A) BjHMGS1 in a crop plant, tomato (Solanum lycopersicum), caused an accumulation of MVA-derived squalene and phytosterols, as well as methylerythritol phosphate (MEP)-derived α-tocopherol (vitamin E) and carotenoids, which are important to human health as antioxidants. In tomato HMGS-OE seedlings, genes associated with the biosyntheses of C10, C15 and C20 universal precursors of isoprenoids, phytosterols, brassinosteroids, dolichols, methylerythritol phosphate, carotenoid and vitamin E were up-regulated. In OE-S359A tomato fruits, increased squalene and phytosterol contents over OE-wtBjHMGS1 were attributed to heightened SlHMGR2, SlFPS1, SlSQS and SlCYP710A11 expression. In both tomato OE-wtBjHMGS1 and OE-S359A fruits, the up-regulation of SlGPS and SlGGPPS1 in the MEP pathway that led to α-tocopherol and carotenoid accumulation indicated cross-talk between the MVA and MEP pathways. Taken together, the manipulation of BjHMGS1 represents a promising strategy to simultaneously elevate health-promoting squalene, phytosterols, α-tocopherol and carotenoids in tomato, an edible fruit.

Keywords: 3-hydroxy-3-methylglutaryl-coenzyme A synthase; isoprenoids; mevalonate; phytosterols; squalene; tomato.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carotenoids / metabolism*
  • Fruit / enzymology
  • Fruit / metabolism*
  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / physiology
  • Hydroxymethylglutaryl-CoA Synthase / genetics
  • Hydroxymethylglutaryl-CoA Synthase / metabolism*
  • Mustard Plant / enzymology*
  • Mustard Plant / metabolism*
  • Phytosterols / metabolism*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Solanum lycopersicum / enzymology*
  • Solanum lycopersicum / metabolism*
  • Squalene / metabolism*
  • alpha-Tocopherol / metabolism*

Substances

  • Phytosterols
  • Plant Proteins
  • Carotenoids
  • Squalene
  • Hydroxymethylglutaryl-CoA Synthase
  • alpha-Tocopherol