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

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.Electronic supplementary materialThe online version of this article (doi:10.1007/s00442-016-3758-3) contains supplementary material, which is available to authorized users.

Dual herbivore attack and herbivore density affect metabolic profiles of Brassica nigra leaves

“…Research has increasingly shifted from studying the effects of single to multiple herbivore attack on plant defence mechanisms. Increasing the complexity of the studied interactions can have strong and unpredictable consequences for plant–insect interactions (Dicke et al ), and it is clear that our knowledge of how insect species interact individually with a plant is insufficient to predict the effects of combined herbivore attack at the transcriptional level all the way up to the community level, particularly when the herbivores are of different feeding guilds (de Rijk et al ; Kroes et al in press; Mathur et al ; Stam et al ; Voelckel & Baldwin ).…”

“…Studies on the effects of dual attack or herbivore density on global transcriptome changes have recently been initiated (e.g. Davila Coolen et al 2016, Kroes et al 2017), but the effects on metabolome changes are scarce (Jansen et al 2009;Maag et al 2015).…”

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

“…As a study system, we used Brassica oleracea plants and their interaction with several specialist insect herbivores. This system has been previously used to study interactions between folivorous insects (Kroes, van Loon, & Dicke, 2015) and transcriptomic responses to various insects on leaves (Kroes et al, 2017, Sarde et al, 2010. Furthermore, in a closely related plant species, Brassica nigra, Pieris brassicae caterpillars were found to negatively affect the root-chewing herbivore Delia radicum, the cabbage root fly (Soler et al, 2007).…”

Plant defense in response to chewing insects: proteome analysis ofArabidopsis thalianadamaged byPlutella xylostella

“…The A. thaliana-insect interaction is a model system used to demonstrate the defense resistance of plants to leaf chewers, particularly the analysis of cellular changes at gene/proteomic levels (Kliebenstein et al 2002;Collins et al 2010;Truong et al 2015;Kroes et al 2017). Recently, Kroes et al (2017) observed the upregulation of various JAresponsive genes in response to feeding by P. xylostella caterpillar, by a microarray analysis.…”

“…Recently, Kroes et al (2017) observed the upregulation of various JAresponsive genes in response to feeding by P. xylostella caterpillar, by a microarray analysis. The protein expression changes in A. thaliana leaves due to P. xylostella infestation were identified by two-dimensional gel electrophoresis (2-DE) coupled with mass spectrometry in several studies (Collins et al 2010;Liu et al 2010).…”