Ecological trade-offs between jasmonic acid-dependent direct and indirect plant defences in tritrophic interactions.

Jianing Wei,Feng Ge,Le Kang,Chuanyou Li,Lizhong Wang,Jiuhai Zhao

doi:10.1111/j.1469-8137.2010.03491.x

Abstract

Recent studies on plants genetically modified in jasmonic acid (JA) signalling support the hypothesis that the jasmonate family of oxylipins plays an important role in mediating direct and indirect plant defences. However, the interaction of two modes of defence in tritrophic systems is largely unknown.In this study, we examined the preference and performance of a herbivorous leafminer (Liriomyza huidobrensis) and its parasitic wasp (Opius dissitus) on three tomato genotypes: a wild-type (WT) plant, a JA biosynthesis (spr2) mutant, and a JA-overexpression 35S::prosys plant. Their proteinase inhibitor production and volatile emission were used as direct and indirect defence factors to evaluate the responses of leafminers and parasitoids.Here, we show that although spr2 mutant plants are compromised in direct defence against the larval leafminers and in attracting parasitoids, they are less attractive to adult flies compared with WT plants. Moreover, in comparison to other genotypes, the 35S::prosys plant displays greater direct and constitutive indirect defences, but reduced success of parasitism by parasitoids.Taken together, these results suggest that there are distinguished ecological trade-offs between JA-dependent direct and indirect defences in genetically modified plants whose fitness should be assessed in tritrophic systems and under natural conditions.

Highlights

The bottom-up effects of plants against herbivores indicated that plants have evolved a wide range of direct and indirect defensive strategies (Gatehouse, 2002)
Recent studies on plants genetically modified in jasmonic acid (JA) signalling support the hypothesis that the jasmonate family of oxylipins plays an important role in mediating direct and indirect plant defences
In this study, we examined the preference and performance of a herbivorous leafminer (Liriomyza huidobrensis) and its parasitic wasp (Opius dissitus) on three tomato genotypes: a wild-type (WT) plant, a JA biosynthesis mutant, and a JA-overexpression 35S::prosys plant

Summary

Introduction

The bottom-up effects of plants against herbivores indicated that plants have evolved a wide range of direct and indirect defensive strategies (Gatehouse, 2002). Plants defend themselves against insects directly through feeding (e.g. physical barriers or toxins) (Kessler & Baldwin, 2002; Peiffer et al, 2009) and indirectly through attracting natural enemies of herbivores (Turlings et al, 1995; Heil, 2008; Dicke et al, 2009; Kang et al, 2009). Both direct and indirect plant defences are constitutive and inducible, while induced strategies may be favoured over constitutive ones because of the low cost (Kessler & Baldwin, 2002). A recent study revealed that there is no conflict between direct and indirect plant defences in a highly specialized herbivore–natural enemy system involving a brassicaceous plant species (Gols et al, 2008)

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