Slow food: insect prey and chitin induce phytohormone accumulation and gene expression in carnivorous Nepenthes plants

Ann Bot. 2016 Aug;118(2):369-75. doi: 10.1093/aob/mcw110. Epub 2016 Jun 20.

Abstract

Background and aims: Carnivorous Nepenthes plants use modified leaves forming pitfall traps to capture and digest prey, mainly insects, for additional nutrient supply. These traps, so called pitchers, contain a plant-derived fluid composed of many hydrolytic enzymes and defence-related proteins. In this study, the prey-induced induction of corresponding genes of those proteins and a role for phytohormones in this process was analysed.

Methods: Tissue from insect prey-fed, chitin- and phytohormone-challenged pitchers was harvested and analysed for selected gene expressions by a quantitative PCR technique. Phytohormone levels were determined by LC-MS/MS. Nepenthesin proteolytic activities were measured in the digestive fluid using a fluorescence substrate.

Key results: Insect prey in the pitchers induced the accumulation of phytohormones such as jasmonates as well as the transcription of studied genes encoding a chitinase 3 and a protease (nepenthesin I), whereas a defence-related protein (PR-1) gene was not induced. Treatment with chitin as a component of the insects' exoskeleton triggered the accumulation of jasmonates, the expression of nepenthesin I and chitinase 3 genes similar to jasmonic acid treatment, and induced protease activity in the fluid. All detectable responses were slowly induced.

Conclusions: The results suggest that upon insect prey catch a sequence of signals is initiated: (1) insect-derived chitin, (2) jasmonate as endogenous phytohormone signal, (3) the induction of digestive gene expression and (4) protein expression. This resembles a similar hierarchy of events as described from plant pathogen/herbivore interactions, supporting the idea that carnivory evolved from plant defences.

Keywords: Nepenthes; carnivorous plant; chitin; gene induction; insect prey; jasmonates; nepenthesin; phytohormones.

MeSH terms

  • Animals
  • Carnivory
  • Chitin / metabolism*
  • Cyclopentanes / metabolism*
  • Gene Expression Regulation, Plant*
  • Insecta
  • Magnoliopsida / genetics
  • Magnoliopsida / physiology*
  • Oxylipins / metabolism*
  • Plant Growth Regulators / metabolism*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Signal Transduction

Substances

  • Cyclopentanes
  • Oxylipins
  • Plant Growth Regulators
  • Plant Proteins
  • Chitin
  • jasmonic acid