Regulation by biotic stress of tannins biosynthesis in Quercus ilex: Crosstalk between defoliation and Phytophthora cinnamomi infection

Physiol Plant. 2019 Feb;165(2):319-329. doi: 10.1111/ppl.12848. Epub 2018 Nov 15.

Abstract

Sustainability of the Mediterranean forest is threatened by oak decline, a disease of holm oak and other Quercus species that is initiated by infection with the oomycete Phytophthora cinnamomi. Focusing on the role of tannins in the chemical defense of plants, this work investigated whether tannins content in Quercus ilex is regulated by biotic stress. Screening of published genomes allowed the identification of Quercus sequences encoding enzymes for early steps of the biosynthesis of phenolic compounds, like hydrolysable tannins and condensed tannins (CT) among others, plus genes involved in the late steps of CT biosynthesis. Four days after treatment of Q. ilex seedlings by mechanical defoliation, P. cinnamomi infection and both stressors simultaneously, mRNA concentrations for tannins biosynthesis enzymes were measured in leaves. Among the transcript amount for shikimate dehydrogenase (SDH, EC 1.1.1.25), anthocyanidin reductase (EC 1.3.1.77), anthocyanidin synthase (EC 1.14.11.19) and leucoanthocyanidine reductase (EC 1.17.1.3), defoliation induced gene expression for SDH2 isoenzyme. About 4 days after infection of roots by P. cinnamomi, this up-regulation was canceled and SDH enzyme activity decreased. Furthermore, during this late stage of biotrophic interaction the pathogen switched off the correlation engaged by defoliation between the expression of SDH1 and SDH2 encoding genes and chemical defenses corresponding to total tannins, which were down-regulated. Thus, tannins biosynthesis in seedlings of Q. ilex is induced after mechanical defoliation whereas infection by the pathogen interferes with this regulation, potentially increasing the susceptibility of plants to herbivory and aggravating the impact of biotic stress.

MeSH terms

  • Biosynthetic Pathways / genetics
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Isoenzymes / metabolism
  • Linear Models
  • Phylogeny
  • Phytophthora / physiology*
  • Plant Diseases / genetics
  • Plant Diseases / microbiology*
  • Plant Leaves / physiology*
  • Quercus / genetics
  • Quercus / microbiology*
  • Quercus / physiology*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Signal Transduction
  • Stress, Physiological*
  • Succinate Dehydrogenase / metabolism
  • Tannins / biosynthesis*
  • Tannins / chemistry

Substances

  • Isoenzymes
  • RNA, Messenger
  • Tannins
  • Succinate Dehydrogenase