Foliar herbivory by caterpillars and aphids differentially affects phytohormonal signalling in roots and plant defence to a root herbivore.

Peter N Karssemeijer,Marcel Dicke,Michael Reichelt,Jonathan Gershenzon,Joop Van Loon

doi:10.1111/pce.13707

Peter N Karssemeijer, Marcel Dicke + Show 3 more

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https://doi.org/10.1111/pce.13707

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Abstract

Plant‐mediated interactions are an important force in insect ecology. Through such interactions, herbivores feeding on leaves can affect root feeders. However, the mechanisms regulating the effects of above‐ground herbivory on below‐ground herbivores are poorly understood. Here, we investigated the performance of cabbage root fly larvae (Delia radicum) on cabbage plants (Brassica oleracea) previously exposed to above ground herbivores belonging to two feeding guilds: leaf chewing diamondback moth caterpillars (Plutella xylostella) or phloem‐feeding cabbage aphids (Brevicoryne brassicae). Our study focusses on root‐herbivore performance and defence signalling in primary roots by quantifying phytohormones and gene expression. We show that leaf herbivory by caterpillars, but not by aphids, strongly attenuates root herbivore performance. Above‐ground herbivory causes changes in primary roots in terms of gene transcripts and metabolites involved in plant defence. Feeding by below‐ground herbivores strongly induces the jasmonate pathway in primary roots. Caterpillars feeding on leaves cause a slight induction of the primary root jasmonate pathway and interact with plant defence signalling in response to root herbivores. In conclusion, feeding by a leaf chewer and a phloem feeder differentially affects root‐herbivore performance, root‐herbivore‐induced phytohormonal signalling, and secondary metabolites.

Highlights

We studied how plants respond to D. radicum feeding on the roots, as well as to P. xylostella or B. brassicae on the leaves
salicylic acid (SA) hormone concentrations were not affected by aphids alone, the combination of B. brassicae and D. radicum caused a decrease in this signalling compound relative to control roots (Figure S4)
In leaves of the same cultivar as we use here, the magnitude of jasmonic acid (JA) induction after 24 hr of feeding by several caterpillar species was shown to lie between 4-fold and 11-fold (Bruinsma et al, 2009; Bruinsma et al, 2010), much less compared with the 20-fold increase we find in primary roots responding to root-feeding maggots

Summary

| INTRODUCTION

Caterpillars (Plutella xylostella) and aphids (Brevicoryne brassicae) feeding on leaves of Brassica oleracea differentially affect gene expression, phytohormone concentrations and defence against cabbage root fly larvae (Delia radicum) in the primary root. The type of defence response, and the plant-mediated effect on subsequent herbivores, that is initiated by a feeding herbivore depends largely on the feeding guild (e.g., chewing or phloem feeding) of the inducing insect (Stam et al, 2014). Chewing herbivores on leaves generally negatively impact root-feeding insects (Erb, Robert, & Turlings, 2011; Hunt-Joshi & Blossey, 2005; Johnson et al, 2012), and this has been correlated to changes in secondary metabolites such as tannins or glucosinolates (Huang et al, 2014; Soler et al, 2013). We investigated whether above-ground herbivory modulates the plant response to root herbivory

| MATERIALS AND METHODS

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| DISCUSSION

Findings

| CONCLUSION