A defensive pathway from NAC and TCP transcription factors activates a BAHD acyltransferase for (Z)-3-hexenyl acetate biosynthesis to resist herbivore in tea plant (Camellia sinensis)

New Phytol. 2025 Feb;245(3):1232-1248. doi: 10.1111/nph.20283. Epub 2024 Nov 17.

Abstract

Numerous herbivore-induced plant volatiles (HIPVs) play important roles in plant defense. In tea plants (Camellia sinensis), (Z)-3-hexenyl acetate (3-HAC) has been characterized as associated with resistance to herbivores. To date, how tea plants biosynthesize and regulate 3-HAC to resist herbivores remain unclear. Based on transcriptomes assembled from Ectropis obliqua-fed leaves, a cDNA encoding BAHD acyltransferase, namely CsCHAT1, was highly induced in leaves fed with E. obliqua. Enzymatic assays showed that CsCHAT1 converted (Z)-3-hexenol into 3-HAC. Further suppression of CsCHAT1 expression reduced the accumulation of 3-HAC and lowered the resistance of tea plants to E. obliqua, while 3-HAC replenishment rescued the reduced resistance of CsCHAT1-silenced tea plants against E. obliqua. Two transcription factors (TFs), CsNAC30 and CsTCP11, were co-expressed with CsCHAT1. An integrative approach of biochemistry, DNA-protein interaction, gene silencing, and metabolic profiling revealed that the two TFs positively regulated the expression of CsCHAT1. The suppression of either one decreased the production of 3-HAC and eliminated the resistance of tea plants to E. obliqua. Notably, the suppression of either one considerably impaired JA-induced 3-HAC biosynthesis in tea plant. The proposed pathway can be targeted for innovative agro-biotechnologies protecting tea plants from damage by E. obliqua.

Keywords: (Z)‐3‐hexenyl acetate; CsCHAT1; NAC transcription factor; TCP transcription factor; herbivore; herbivore‐induced plant volatiles; tea plants.

MeSH terms

  • Acetates* / metabolism
  • Acetates* / pharmacology
  • Acyltransferases* / genetics
  • Acyltransferases* / metabolism
  • Animals
  • Biosynthetic Pathways / genetics
  • Camellia sinensis* / drug effects
  • Camellia sinensis* / enzymology
  • Camellia sinensis* / genetics
  • Camellia sinensis* / metabolism
  • Gene Expression Regulation, Plant*
  • Gene Silencing
  • Herbivory*
  • Plant Defense Against Herbivory
  • Plant Leaves / metabolism
  • Plant Proteins* / genetics
  • Plant Proteins* / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Plant Proteins
  • Transcription Factors
  • Acetates
  • Acyltransferases