Pre-infestation of Tomato Plants by Aphids Modulates Transmission-Acquisition Relationship among Whiteflies, Tomato Yellow Leaf Curl Virus (TYLCV) and Plants.

Xiao L Tan,Ju L Chen,Xue Q Yang,Giovanni Benelli,Nicolas Desneux,Tong X Liu,Feng Ge

doi:10.3389/fpls.2017.01597

Abstract

Herbivory defense systems in plants are largely regulated by jasmonate-(JA) and salicylate-(SA) signaling pathways. Such defense mechanisms may impact insect feeding dynamic, may also affect the transmission-acquisition relationship among virus, plants and vectoring insects. In the context of the tomato – whitefly – Tomato Yellow Leaf Curl Virus (TYLCV) biological model, we tested the impact of pre-infesting plants with a non-vector insect (aphid Myzus persicae) on feeding dynamics of a vector insect (whitefly Bemisia tabaci) as well as virus transmission-acquisition. We showed that an aphid herbivory period of 0–48 h led to a transient systemic increase of virus concentration in the host plant (root, stem, and leaf), with the same pattern observed in whiteflies feeding on aphid-infested plants. We used real-time quantitative PCR to study the expression of key genes of the SA- and JA-signaling pathways, as well as electrical penetration graph (EPG) to characterize the impact of aphid pre-infestation on whitefly feeding during TYLCV transmission (whitefly to tomato) and acquisition (tomato to whitefly). The impact of the duration of aphid pre-infestation (0, 24, or 48 h) on phloem feeding by whitefly (E2) during the transmission phase was similar to that of global whitefly feeding behavior (E1, E2 and probing duration) during the acquisition phase. In addition, we observed that a longer phase of aphid pre-infestation prior to virus transmission by whitefly led to the up-regulation and down-regulation of SA- and JA-signaling pathway genes, respectively. These results demonstrated a significant impact of aphid pre-infestation on the tomato – whitefly – TYLCV system. Transmission and acquisition of TYLCV was positively correlated with feeding activity of B. tabaci, and both were mediated by the SA- and JA-pathways. TYLCV concentration during the transmission phases was modulated by up- and down-regulation of SA- and JA-pathways, respectively. The two pathways were inconsistent during the acquisition phase; SA- related genes were up-regulated, whereas those up- and down-stream of the JA pathway showed a more complex relationship. These findings enhance our understanding of plant – herbivore – virus interactions, which are potentially important for development of ecologically sound pest and pathogen management programs.

Highlights

In recent decades, there have been many studies on the ecological and physiological mechanisms underlying plantmediated interactions among herbivore arthropods and plant pathogens, regarding plant defense responses (Al-Bitar and Luisoni, 1995; Beale et al, 2006; Bleeker et al, 2011; Baldin et al, 2013; Mouttet et al, 2013)
The defense responses induced in plants after incidence of herbivory is central to the longstanding co-evolutionary system of host plant, pathogenic microorganism and herbivore arthropod
This study is the first investigation on impact of herbivore preinfestation on virus transmission and acquisition by subsequent herbivores, in terms of key interactions such as feeding behavior and plant defenses

Summary

INTRODUCTION

There have been many studies on the ecological and physiological mechanisms underlying plantmediated interactions among herbivore arthropods and plant pathogens, regarding plant defense responses (Al-Bitar and Luisoni, 1995; Beale et al, 2006; Bleeker et al, 2011; Baldin et al, 2013; Mouttet et al, 2013). It has been shown that within this defense system, a prior attack by aphid Myzus persicae can influence the feeding strategy and population dynamics of subsequent herbivores (Tan et al, 2014) It is unclear whether TYLCV transmission and acquisition are affected by the feeding behavior of whiteflies, or whether these are influenced by aphid pre-infestation. In order to better understand the interactions in the plant- herbivore-virus system under conditions of sequential herbivory, we tested the hypothesis that pre-infestation by aphid M. persicae affects the expression of hormone-related genes and the SA- and JA-signaling pathways, consequentially impacting feeding behavior of subsequent whiteflies and the transmission and acquisition of TYLCV. We tested if pre-infestation with M. persicae (i) affect the feeding behavior of B. tabaci, (ii) modulate TYLCV transmission and acquisition between host plant and B. tabaci, and (iii) impact the expression of SAand JA-signaling pathway genes (and potential link with vector feeding behavior and virus transmission and acquisition)

MATERIALS AND METHODS

RESULTS

DISCUSSION