Application of a JA-Ile Biosynthesis Inhibitor to Methyl Jasmonate-Treated Strawberry Fruit Induces Upregulation of Specific MBW Complex-Related Genes and Accumulation of Proanthocyanidins

Molecules. 2018 Jun 13;23(6):1433. doi: 10.3390/molecules23061433.

Abstract

Fleshy fruits are an important source of anthocyanins and proanthocyanidins (PAs), which protect plants against stress, and their consumption provides beneficial effects for human health. In strawberry fruit, the application of exogenous methyl jasmonate (MeJA) upregulates anthocyanin accumulation, although the relationship between the jasmonate pathway and anthocyanin and PA biosynthesis in fruits remains to be understood. Anthocyanin and PA accumulation is mainly regulated at the transcriptional level through R2R3-MYB and bHLH transcription factors in different plant species and organs. Here, the effect of jarin-1, a specific inhibitor of bioactive JA (jasmonoyl-isoleucine, JA-Ile) biosynthesis, on anthocyanin and PA accumulation was evaluated during strawberry (Fragaria × ananassa) fruit development using an in vitro ripening system for 48 h. Also, we observed the effects of MeJA and the application of jarin-1 to MeJA-treated fruits (MeJA + jarin-1 treatment). We assessed changes of expression levels for the JA-Ile and MeJA biosynthetic (FaJAR1.2 and FaJMT), JA signaling-related (FaMYC2 and FaJAZ1), MYB-bHLH-WD40 (MBW) complex-related (FabHLH3/33, FaMYB9/10/11, and repressor FaMYB1), and anthocyanin and PA biosynthetic (FaANS, FaUFGT, FaANR, and FaLAR) genes. In addition, the promoter region of MBW complex-related MYB genes was isolated and sequenced. We found a higher redness of strawberry fruit skin and anthocyanin content in MeJA-treated fruits with respect to jarin-1-treated ones concomitant with an upregulation of FaANS and FaUFGT genes. Inversely, the PA content was higher in jarin-1- and MeJA + jarin-1-treated than in MeJA-treated fruits. MeJA + jarin-1 treatment resulted in an upregulation of FaANR and associated transcription factors such as FabHLH33 and FaMYB9/11 along with FaJMT and FaJAR1.2. Finally, we found JA-responsive elements in the promoter regions of FaMYB1/9/10/11 genes. It is proposed that PA biosynthesis-related genes can be upregulated by the application of jarin-1 to MeJA-treated fruit, thus increasing PA accumulation in strawberry.

Keywords: Fragaria × ananassa; MYB genes; anthocyanins; jarin-1; jasmonates.

MeSH terms

  • Acetates / pharmacology*
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Cyclopentanes / pharmacology*
  • Enzyme Inhibitors / pharmacology*
  • Fragaria / drug effects
  • Fragaria / growth & development*
  • Fragaria / metabolism
  • Gene Expression Regulation, Plant / drug effects
  • Isoleucine / analogs & derivatives
  • Isoleucine / biosynthesis
  • Nucleotidyltransferases / antagonists & inhibitors
  • Oxylipins / pharmacology*
  • Plant Growth Regulators / pharmacology*
  • Plant Proteins / antagonists & inhibitors
  • Plant Proteins / genetics
  • Proanthocyanidins / biosynthesis
  • Promoter Regions, Genetic
  • Transcription Factors / genetics*
  • Up-Regulation

Substances

  • Acetates
  • Basic Helix-Loop-Helix Transcription Factors
  • Cyclopentanes
  • Enzyme Inhibitors
  • Oxylipins
  • Plant Growth Regulators
  • Plant Proteins
  • Proanthocyanidins
  • Transcription Factors
  • jasmonoyl-isoleucine
  • Isoleucine
  • methyl jasmonate
  • Nucleotidyltransferases