Disease Interactions in a Shared Host Plant: Effects of Pre-Existing Viral Infection on Cucurbit Plant Defense Responses and Resistance to Bacterial Wilt Disease

Lori R Shapiro,Andrew G Stephenson,Consuelo M De Moraes,Lucie Salvaudon,Hannier Pulido,Kerry E Mauck,Mark C Mescher,Nicolas Desneux

doi:10.1371/journal.pone.0077393

Abstract

Both biotic and abiotic stressors can elicit broad-spectrum plant resistance against subsequent pathogen challenges. However, we currently have little understanding of how such effects influence broader aspects of disease ecology and epidemiology in natural environments where plants interact with multiple antagonists simultaneously. In previous work, we have shown that healthy wild gourd plants (Cucurbita pepo ssp. texana) contract a fatal bacterial wilt infection (caused by Erwinia tracheiphila) at significantly higher rates than plants infected with Zucchini yellow mosaic virus (ZYMV). We recently reported evidence that this pattern is explained, at least in part, by reduced visitation of ZYMV-infected plants by the cucumber beetle vectors of E. tracheiphila. Here we examine whether ZYMV-infection may also directly elicit plant resistance to subsequent E. tracheiphila infection. In laboratory studies, we assayed the induction of key phytohormones (SA and JA) in single and mixed infections of these pathogens, as well as in response to the feeding of A. vittatum cucumber beetles on healthy and infected plants. We also tracked the incidence and progression of wilt disease symptoms in plants with prior ZYMV infections. Our results indicate that ZYMV-infection slightly delays the progression of wilt symptoms, but does not significantly reduce E. tracheiphila infection success. This observation supports the hypothesis that reduced rates of wilt disease in ZYMV-infected plants reflect reduced visitation by beetle vectors. We also documented consistently strong SA responses to ZYMV infection, but limited responses to E. tracheiphila in the absence of ZYMV, suggesting that the latter pathogen may effectively evade or suppress plant defenses, although we observed no evidence of antagonistic cross-talk between SA and JA signaling pathways. We did, however, document effects of E. tracheiphila on induced responses to herbivory that may influence host-plant quality for (and hence pathogen acquisition by) cucumber beetles.

Highlights

Research conducted over the past several decades has shown the signaling networks and molecular mechanisms of induced plant response to biotic and abiotic stressors to be highly complex and tightly regulated; but our understanding of how such responses function in complex ecological environments where plants simultaneously interact with multiple antagonists remains limited, for non-model species [1]
Stronger salicylic acid (SA) responses to Zucchini yellow mosaic virus (ZYMV) compared to healthy plants or those infected by E. tracheiphila alone were again evident in the herbivory experiment (Figure 3A, Table 2) (Contrast “ZYMV” vs, “E. tracheiphila” and “mock” disease treatments F1,66= 39.04, P value < 0.0001), but feeding by A. vittatum did not appear to influence SA levels in any of the treatments
We observed a slight delay in the onset and progression of wilt disease symptoms in plants with prior ZYMV infections compared to mock inoculated controls at two different levels of exposure to the bacterial pathogen (Figures 4,5)

Summary

Introduction

Research conducted over the past several decades has shown the signaling networks and molecular mechanisms of induced plant response to biotic and abiotic stressors to be highly complex and tightly regulated; but our understanding of how such responses function in complex ecological environments where plants simultaneously interact with multiple antagonists remains limited, for non-model species [1]. We explore constitutive and induced plant responses to single and mixed infections of Zucchini yellow mosaic virus (ZYMV) and Erwinia tracheiphila (the causal agent of bacterial wilt disease) and the further influence on these responses of feeding by a key specialist herbivore—the striped cucumber beetle, Acalymma vittatum— that vectors the bacterial pathogen [2] This system is well suited to examining plant defense response in the context of complex ecological interactions, as we have extensive knowledge of co-infection dynamics for these pathogens and of A. vittatum host preferences under field conditions. A. vittatum individuals exhibit a preference for the odors of healthy vs virus-infected flowers in laboratory assays and are much more abundant in healthy than infected flowers in the field [7] This is expected to influence rates of E. tracheiphila infection, as we have shown that this pathogen is efficiently transmitted through floral nectaries [8] and that the incidence of wilt disease in populations of C. pepo ssp. This is expected to influence rates of E. tracheiphila infection, as we have shown that this pathogen is efficiently transmitted through floral nectaries [8] and that the incidence of wilt disease in populations of C. pepo ssp. texana is strongly influenced by the presence and abundance of flowers [3,9]

Methods

Results

Conclusion