The Influence of Exogenous Jasmonic Acid on the Biosynthesis of Steroids and Triterpenoids in Calendula officinalis Plants and Hairy Root Culture

Int J Mol Sci. 2022 Oct 12;23(20):12173. doi: 10.3390/ijms232012173.

Abstract

The interplay between steroids and triterpenoids, compounds sharing the same biosynthetic pathway but exerting distinctive functions, is an important part of the defense strategy of plants, and includes metabolic modifications triggered by stress hormones such as jasmonic acid. Two experimental models, Calendula officinalis hairy root cultures and greenhouse cultivated plants (pot plants), were applied for the investigation of the effects of exogenously applied jasmonic acid on the biosynthesis and accumulation of steroids and triterpenoids, characterized by targeted GC-MS (gas chromatography-mass spectroscopy) metabolomic profiling. Jasmonic acid elicitation strongly increased triterpenoid saponin production in hairy root cultures (up to 86-fold) and their release to the medium (up to 533-fold), whereas the effect observed in pot plants was less remarkable (two-fold enhancement of saponin biosynthesis after a single foliar application). In both models, the increase of triterpenoid biosynthesis was coupled with hampering the biomass formation and modifying the sterol content, involving stigmasterol-to-sitosterol ratio, and the proportions between ester and glycoside conjugates. The study revealed that various organs in the same plant can react differently to jasmonic acid elicitation; hairy root cultures are a useful in vitro model to track metabolic changes, and enhanced glycosylation (of both triterpenoids and sterols) seems to be important strategy in plant defense response.

Keywords: elicitation; jasmonic acid; metabolic modifications; oleanolic acid; specialized metabolites; sterols; triterpenoids.

MeSH terms

  • Calendula*
  • Esters / metabolism
  • Glycosides / pharmacology
  • Hormones / metabolism
  • Plant Roots / metabolism
  • Saponins* / metabolism
  • Saponins* / pharmacology
  • Sitosterols / metabolism
  • Sitosterols / pharmacology
  • Steroids / metabolism
  • Stigmasterol / metabolism
  • Triterpenes* / metabolism
  • Triterpenes* / pharmacology

Substances

  • jasmonic acid
  • Triterpenes
  • Sitosterols
  • Stigmasterol
  • Saponins
  • Glycosides
  • Steroids
  • Esters
  • Hormones

Grants and funding

The study was partially funded by the Polish Ministry of Education and Science through the Faculty of Biology, University of Warsaw intramural grant DSM 2019 501-D114-01-1140100 obtained by Agata Rogowska. GC-MS analyses were carried out with the use of CePT infrastructure financed by the European Union—the European Regional Development Fund (Agreement POIG.02.02.00-14-024/08-00).