Transcriptional and metabolic signatures of Arabidopsis responses to chewing damage by an insect herbivore and bacterial infection and the consequences of their interaction.

Heidi M Appel,Guru Jagadeeswaran,Jack C Schultz,Surabhi Raina,Shahina B Maqbool,Leonard Hearnes,A Daniel Jones,Biswa R Acharya,Ramesh Raina,John C Hanley,Kathryn P Miller

doi:10.3389/fpls.2014.00441

Abstract

Plants use multiple interacting signaling systems to identify and respond to biotic stresses. Although it is often assumed that there is specificity in signaling responses to specific pests, this is rarely examined outside of the gene-for-gene relationships of plant-pathogen interactions. In this study, we first compared early events in gene expression and later events in metabolite profiles of Arabidopsis thaliana following attack by either the caterpillar Spodoptera exigua or avirulent (DC3000 avrRpm1) Pseudomonas syringae pv. tomato at three time points. Transcriptional responses of the plant to caterpillar feeding were rapid, occurring within 1 h of feeding, and then decreased at 6 and 24 h. In contrast, plant response to the pathogen was undetectable at 1 h but grew larger and more significant at 6 and 24 h. There was a surprisingly large amount of overlap in jasmonate and salicylate signaling in responses to the insect and pathogen, including levels of gene expression and individual hormones. The caterpillar and pathogen treatments induced different patterns of expression of glucosinolate biosynthesis genes and levels of glucosinolates. This suggests that when specific responses develop, their regulation is complex and best understood by characterizing expression of many genes and metabolites. We then examined the effect of feeding by the caterpillar Spodoptera exigua on Arabidopsis susceptibility to virulent (DC3000) and avirulent (DC3000 avrRpm1) P. syringae pv. tomato, and found that caterpillar feeding enhanced Arabidopsis resistance to the avirulent pathogen and lowered resistance to the virulent strain. We conclude that efforts to improve plant resistance to bacterial pathogens are likely to influence resistance to insects and vice versa. Studies explicitly comparing plant responses to multiple stresses, including the role of elicitors at early time points, are critical to understanding how plants organize responses in natural settings.

Highlights

In the wild, plants experience insect and pathogen attacks at the same time or in close succession and must detect and respond to them in a coordinated way
We examined the effect of feeding by the caterpillar Spodoptera exigua on Arabidopsis response to virulent and avirulent P. syringae pv. tomato
The number of statistically significant changes in the expression of genes in Arabidopsis leaves differed with the treatments and sampling time (Figure 1)

Summary

Introduction

Plants experience insect and pathogen attacks at the same time or in close succession and must detect and respond to them in a coordinated way. When Arabidopsis plants are pre-treated with microbes the effect on insect performance varies with the microbial treatment and the herbivore. Response to herbivore and pathogen when a systemic hypersensitive response (HR) was elicited by avirulent Pseudomonas syringae, caterpillar growth was reduced whereas plants treated with the virulent form of that bacterium supported better caterpillar growth (Cui et al, 2002, 2005; Groen et al, 2013). In Arabidopsis, the reverse effect of herbivore feeding on subsequent pathogen attack is even less well studied. Plants pre-treated with caterpillar herbivory were more resistant to bacterial and viral pathogens, including P. syringae (De Vos et al, 2006). We know that attack by insects or pathogens can affect plant response to the other, but we have little understanding of how or when these interactions occur

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