Different Plant Viruses Induce Changes in Feeding Behavior of Specialist and Generalist Aphids on Common Bean That Are Likely to Enhance Virus Transmission.

Christopher A Gilligan,Adrienne E Pate,J Musembi Mutuku,Toby J A Bruce,John P Carr,Christine Woodcock,Francis O Wamonje,Ruairí Donnelly,Trisna D Tungadi,Alex M Murphy,John Caulfield,John A Pickett

doi:10.3389/fpls.2019.01811

Abstract

Bean common mosaic virus (BCMV), bean common mosaic necrosis virus (BCMNV), and cucumber mosaic virus (CMV) cause serious epidemics in common bean (Phaseolus vulgaris), a vital food security crop in many low-to-medium income countries, particularly in Sub-Saharan Africa. Aphids transmit these viruses “non-persistently,” i.e., virions attach loosely to the insects' stylets. Viruses may manipulate aphid-host interactions to enhance transmission. We used direct observation and electrical penetration graph measurements to see if the three viruses induced similar or distinct changes in feeding behaviors of two aphid species, Aphis fabae and Myzus persicae. Both aphids vector BCMV, BCMNV, and CMV but A. fabae is a legume specialist (the dominant species in bean fields) while M. persicae is a generalist that feeds on and transmits viruses to diverse plant hosts. Aphids of both species commenced probing epidermal cells (behavior optimal for virus acquisition and inoculation) sooner on virus-infected plants than on mock-inoculated plants. Infection with CMV was especially disruptive of phloem feeding by the bean specialist aphid A. fabae. A. fabae also experienced mechanical stylet difficulty when feeding on virus-infected plants, and this was also exacerbated for M. persicae. Overall, feeding on virus-infected host plants by specialist and generalist aphids was affected in different ways but all three viruses induced similar effects on each aphid type. Specifically, non-specialist (M. persicae) aphids encountered increased stylet difficulties on plants infected with BCMV, BCMNV, or CMV, whereas specialist aphids (A. fabae) showed decreased phloem ingestion on infected plants. Probing and stylet pathway activity (which facilitate virus transmission) were not decreased by any of the viruses for either of the aphid species, except in the case of A. fabae on CMV-infected bean, where these activities were increased. Overall, these virus-induced changes in host-aphid interactions are likely to enhance non-persistent virus transmission, and data from this work will be useful in epidemiological modeling of non-persistent vectoring of viruses by aphids.

Highlights

Aphids, predominantly the bean specialist Aphis fabae, and the generalist Myzus persicae, are implicated in the transmission of viruses in fields of common bean (Phaseolus vulgaris) (Worrall et al, 2015)
We modeled potential E2 index (PEI) using a generalized linear models (GLMs) with Beta-distributed response variable
For A. fabae, the highest proportion of time spent in stylet pathway activity was on cucumber mosaic virus (CMV)-infected plants (80.5%), while for M. persicae, it was highest on mock-inoculated plants (66.3%)

Summary

INTRODUCTION

Predominantly the bean specialist Aphis fabae, and the generalist Myzus persicae, are implicated in the transmission of viruses in fields of common bean (Phaseolus vulgaris) (Worrall et al, 2015). When aphids were moved from CMV-infected plants to healthy plants, their growth rate recovered which was indicative that CMV used feeding deterrence and not host toxicity as the mechanism to render the plants as unsuitable hosts for aphids (Westwood et al, 2013). This is an important scenario because virus-induced changes in feeding habits can affect virus acquisition and inoculation by aphids (Mauck et al, 2012; Mauck et al, 2016; Carr et al, 2018). We investigated how three different viruses of common bean (BCMV, BCMNV, and CMV) influence the behavior of a specialist and non-specialist aphid by examining the effects of virus infection on aphid feeding behavior

MATERIALS AND METHODS

RESULTS

DISCUSSION

DATA AVAILABILITY STATEMENT