Three Aphid-Transmitted Viruses Encourage Vector Migration From Infected Common Bean (Phaseolus vulgaris) Plants Through a Combination of Volatile and Surface Cues.

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

doi:10.3389/fpls.2020.613772

Abstract

Bean common mosaic virus (BCMV), bean common mosaic necrosis virus (BCMNV), and cucumber mosaic virus (CMV) are important pathogens of common bean (Phaseolus vulgaris), a crop vital for food security in sub-Saharan Africa. These viruses are vectored by aphids non-persistently, with virions bound loosely to stylet receptors. These viruses also manipulate aphid-mediated transmission by altering host properties. Virus-induced effects on host-aphid interactions were investigated using choice test (migration) assays, olfactometry, and analysis of insect-perceivable volatile organic compounds (VOCs) using gas chromatography (GC)-coupled mass spectrometry, and GC-coupled electroantennography. When allowed to choose freely between infected and uninfected plants, aphids of the legume specialist species Aphis fabae, and of the generalist species Myzus persicae, were repelled by plants infected with BCMV, BCMNV, or CMV. However, in olfactometer experiments with A. fabae, only the VOCs emitted by BCMNV-infected plants repelled aphids. Although BCMV, BCMNV, and CMV each induced distinctive changes in emission of aphid-perceivable volatiles, all three suppressed emission of an attractant sesquiterpene, α-copaene, suggesting these three different viruses promote migration of virus-bearing aphids in a similar fashion.

Highlights

Two aphid species, Aphis fabae and Myzus persicae have been associated with the spread of viruses in common bean (Phaseolus vulgaris) (Worrall et al, 2015)
We investigated how three different viral pathogens of bean (BCMV, bean common mosaic necrosis virus (BCMNV), and cucumber mosaic virus (CMV)) influence the behavior of specialist and non-specialist aphids by examining the effects of virus infection on aphid host choice, and on emission of aphid-perceivable volatile organic compounds (VOCs)
For A. fabae choosing between CMV-infected and mock-inoculated plants (95% credible interval: 0.26–0.40), for M. persicae choosing between CMV-infected vs. mock-inoculated plants (95% credible interval: 0.36–0.49), and BCMNV vs. mock-inoculated plants (95% credible interval: 0.32–0.44)

Summary

Introduction

Aphis fabae (a bean specialist) and Myzus persicae (a generalist) have been associated with the spread of viruses in common bean (Phaseolus vulgaris) (Worrall et al, 2015). These viruses include the potyviruses bean common mosaic virus (BCMV) and bean common mosaic necrosis virus (BCMNV), and the cucumovirus cucumber mosaic virus (CMV) (Palukaitis and García-Arenal, 2003; Morales, 2006; Jacquemond, 2012). A. fabae feed without difficulty on uninfected plants, whilst M. persicae exhibited feeding difficulties, regardless of plant infection status, making bean an unlikely host plant for long term settlement by this generalist aphid (Wamonje et al, 2020)

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Results

Conclusion