Insect eggs suppress plant defence against chewing herbivores

Plant J. 2010 Jun 1;62(5):876-85. doi: 10.1111/j.1365-313X.2010.04200.x. Epub 2010 Mar 10.

Abstract

Plants activate direct and indirect defences in response to insect egg deposition. However, whether eggs can manipulate plant defence is unknown. In Arabidopsis thaliana, oviposition by the butterfly Pieris brassicae triggers cellular and molecular changes that are similar to the changes caused by biotrophic pathogens. In the present study, we found that the plant defence signal salicylic acid (SA) accumulates at the site of oviposition. This is unexpected, as the SA pathway controls defence against fungal and bacterial pathogens and negatively interacts with the jasmonic acid (JA) pathway, which is crucial for the defence against herbivores. Application of P. brassicae or Spodoptera littoralis egg extract onto leaves reduced the induction of insect-responsive genes after challenge with caterpillars, suggesting that egg-derived elicitors suppress plant defence. Consequently, larval growth of the generalist herbivore S. littoralis, but not of the specialist P. brassicae, was significantly higher on plants treated with egg extract than on control plants. In contrast, suppression of gene induction and enhanced S. littoralis performance were not seen in the SA-deficient mutant sid2-1, indicating that it is SA that mediates this phenomenon. These data reveal an intriguing facet of the cross-talk between SA and JA signalling pathways, and suggest that insects have evolved a way to suppress the induction of defence genes by laying eggs that release elicitors. We show here that egg-induced SA accumulation negatively interferes with the JA pathway, and provides an advantage for generalist herbivores.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arabidopsis / genetics
  • Arabidopsis / physiology*
  • Butterflies / physiology*
  • Cyclopentanes / metabolism
  • Gene Expression Regulation, Plant
  • Larva / physiology
  • Oviposition*
  • Ovum / chemistry*
  • Oxylipins / metabolism
  • RNA, Plant / genetics
  • Salicylic Acid / metabolism*
  • Spodoptera / physiology

Substances

  • Cyclopentanes
  • Oxylipins
  • RNA, Plant
  • jasmonic acid
  • Salicylic Acid