An Innate Preference of Bumblebees for Volatile Organic Compounds Emitted by Phaseolus vulgaris Plants Infected With Three Different Viruses

Netsai Margareth Mhlanga,Nik J. Cunniffe,John C. Caulfield,Beverley J. Glover,John P. Carr,Francis O. Wamonje,Alex M. Murphy

doi:10.3389/fevo.2021.626851

Abstract

Cucumber mosaic virus (CMV)-infected tomato (Solanum lycopersicum L.) plants emit volatile organic compounds (VOCs) attractive to bumblebees (Bombus terrestris L.), which are important tomato pollinators, but which do not transmit CMV. We investigated if this effect was unique to the tomato-CMV pathosystem. In two bean (Phaseolus vulgaris L.) cultivars, infection with the potyviruses bean common mosaic virus (BCMV) or bean common mosaic necrosis virus (BCMNV), or with the cucumovirus CMV induced quantitative changes in VOC emission detectable by coupled gas chromatography–mass spectrometry. In free-choice olfactometry assays bumblebees showed an innate preference for VOC blends emitted by virus-infected non-flowering bean plants and flowering CMV-infected bean plants, over VOCs emitted by non-infected plants. Bumblebees also preferred VOCs of flowering BCMV-infected plants of the Wairimu cultivar over non-infected plants, but the preference was not significant for BCMV-infected plants of the Dubbele witte cultivar. Bumblebees did not show a significant preference for VOCs from BCMNV-infected flowering bean plants but differential conditioning olfactometric assays showed that bumblebees do perceive differences between VOC blends emitted by flowering BCMNV-infected plants over non-infected plants. These results are consistent with the concept that increased pollinator attraction may be a virus-to-host payback, and show that virus-induced changes in bee-attracting VOC emission is not unique to one virus-host combination.

Highlights

Plants emit volatile organic compounds (VOCs) that function as signals in plant-plant communication, defense, and attraction of pollinators, seed dispersers, and other beneficial organisms (Dudareva and Pichersky, 2008)
In this study we investigated whether the innate preference of bumblebees for VOC blends emitted by virus-infected plants is peculiar only to the previously investigated tomato-Cucumber mosaic virus (CMV) pathosystem, or if this can occur in other virus-host combinations, such as bean plants infected with CMV, bean common mosaic virus (BCMV), or bean common mosaic necrosis virus (BCMNV)
This might be expected since all three viruses cause stunting (Supplementary Figure 2) and the VOC emission rate at the tissue-mass level for plants infected with BCMV, BCMNV, and CMV was not significantly different from mockinoculated plants (Figure 1B)

Summary

Introduction

Plants emit volatile organic compounds (VOCs) that function as signals in plant-plant communication, defense, and attraction of pollinators, seed dispersers, and other beneficial organisms (Dudareva and Pichersky, 2008). In particular bees, are the most important group of plant pollinators (Knight et al, 2005; Ghazoul, 2006; Klein et al, 2007). The olfactory cues are important in differentiating between plant species, and in signaling the appropriate phenological stage for pollinator visits (Chen et al, 2009; Hossaert-McKey et al, 2010; Song et al, 2014). The complex effects of non-floral VOCs or floral/non-floral VOC combinations on bee foraging and other insect behaviors are still not well understood (Junker et al, 2017), and in particular the influence of microorganisms (including viruses) on plant VOC emission is relatively under-investigated (Beck and Vanette, 2017)

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Conclusion