Brevicoryne brassicae aphids interfere with transcriptome responses of Arabidopsis thaliana to feeding by Plutella xylostella caterpillars in a density-dependent manner

Anneke Kroes,Sean May,Colette Broekgaarden,Marcos Castellanos Uribe,Marcel Dicke,Joop J A Van Loon

doi:10.1007/s00442-016-3758-3

Anneke Kroes, Sean May + Show 4 more

Open Access

https://doi.org/10.1007/s00442-016-3758-3

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Abstract

Plants are commonly attacked by multiple herbivorous species. Yet, little is known about transcriptional patterns underlying plant responses to multiple insect attackers feeding simultaneously. Here, we assessed transcriptomic responses of Arabidopsis thaliana plants to simultaneous feeding by Plutella xylostella caterpillars and Brevicoryne brassicae aphids in comparison to plants infested by P. xylostella caterpillars alone, using microarray analysis. We particularly investigated how aphid feeding interferes with the transcriptomic response to P. xylostella caterpillars and whether this interference is dependent on aphid density and time since aphid attack. Various JA-responsive genes were up-regulated in response to feeding by P. xylostella caterpillars. The additional presence of aphids, both at low and high densities, clearly affected the transcriptional plant response to caterpillars. Interestingly, some important modulators of plant defense signalling, including WRKY transcription factor genes and ABA-dependent genes, were differentially induced in response to simultaneous aphid feeding at low or high density compared with responses to P. xylostella caterpillars feeding alone. Furthermore, aphids affected the P. xylostella-induced transcriptomic response in a density-dependent manner, which caused an acceleration in plant response against dual insect attack at high aphid density compared to dual insect attack at low aphid density. In conclusion, our study provides evidence that aphids influence the caterpillar-induced transcriptional response of A. thaliana in a density-dependent manner. It highlights the importance of addressing insect density to understand how plant responses to single attackers interfere with responses to other attackers and thus underlines the importance of the dynamics of transcriptional plant responses to multiple herbivory.

Highlights

Throughout the growing season, plants are commonly attacked by multiple herbivorous species
The first component shows a clear separation between transcriptional profiles of dually infested plants at high density (Dual HD) versus the other three treatments, while the second component separated the profiles based on the presence or absence of herbivores
In the present microarray analysis, we found differences in gene expression in A. thaliana plants induced by P. xylostella caterpillars alone compared to infestation by a combination of P. xylostella caterpillars and B. brassicae aphids (Figs. 1, 2)

Summary

Introduction

Throughout the growing season, plants are commonly attacked by multiple herbivorous species. The responses of plants to one specific herbivore may impact the performance of other insects feeding on the same host plant (Rodriguez-Saona et al 2010; Soler et al 2012; Zhang et al 2013; Stam et al 2014). Defenses induced in response to multiple insect feeding (Rodriguez-Saona et al 2010; Tzin et al 2015b; Onkokesung et al 2016), can have positive or negative effects on the performance of one of the attacking herbivores (Soler et al 2012; Ali et al 2014; Li et al 2014; Kroes et al 2015). In dually infested Arabidopsis thaliana plants, the phloemfeeding whitefly Bemisia tabaci suppressed the expression of genes up-regulated by Plutella xylostella caterpillars (Zhang et al 2013)

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