Effects of the cucumber mosaic virus 2a protein on aphid–plant interactions in Arabidopsis thaliana

Abstract

Cucumber mosaic virus (CMV) is an insect-transmitted virus that modifies interactions between its infected host plants and its aphid vectors in ways that increase the probability of transmission over various ranges and timescales (Donnelly et al., 2019; Carr et al., 2020). CMV does not infect its aphid vectors but influences their behaviour by altering the biochemistry of infected host plants. The paradigmatic example of this phenomenon is the interaction of the aphids Aphis gossypii and Myzus persicae with Cucurbita pepo plants infected with the Fny strain of CMV (Fny-CMV) (Mauck et al., 2010). CMV infection causes infected cucurbits to emit a mix of volatile organic compounds that attract aphids, but infection also induces accumulation of antixenotic, that is, feeding-deterrent, compounds in the leaves that ensure that aphids feed for only a brief time before moving to another plant (Mauck et al., 2010; Carmo-Souza et al., 2014). Because CMV is a nonpersistently transmitted virus (virus particles acquired from an infected plant are attached loosely to an aphid's stylet mouthparts), this short feed is sufficient to render the aphids competent to transmit infection to neighbouring hosts (Krenz et al., 2015).

Infection of Arabidopsis by cucumber mosaic virus triggers jasmonate‐dependent resistance to aphids that relies partly on the pattern‐triggered immunity factor BAK1

“…The results are also consistent with previous work showing that CMV and its 2b protein can inhibit induction of JA-mediated gene expression (Lewsey et al, 2010;Westwood et al, 2014;Wu et al, 2017). Sequences within the CMV 2a protein (Rhee et al, 2020) trigger the induction of both the mechanism that inhibits growth of M. persicae (which we have shown here to be BAK1-dependent), as well as the mechanism that inhibits reproduction of M. persicae and B. brassicae (which we have shown here to be BAK1-independent). Taken together, these results suggest that the 2a protein most likely interferes in some manner with JA-mediated signalling, and that this leads to induction of at least two mechanisms that inhibit aphid performance on A. thaliana.…”

“…We recently showed that in A. thaliana the CMV 2a protein induces resistance not only to aphid growth but also to aphid reproduction (Rhee et al, 2020 ). Here, we confirmed that the fecundity of aphids placed on CMV‐infected plants was diminished compared to aphids placed on mock‐inoculated plants (Figure 2 and Spreadsheet S1 ).…”

“…During CMV infection of A. thaliana the CMV 2a protein stimulates at least two forms of resistance to aphids: inhibition of aphid growth and inhibition of aphid reproduction (Rhee et al, 2020 ; Westwood et al, 2013 ). We have shown that the inhibition of growth is dependent on BAK1, consistent with our previously suggested role for PTI, whilst the inhibition of aphid reproduction is BAK1‐independent (Figure 2 ).…”

“…The glucosinolate 4MI3M is a metabolite that aphids find distasteful (Kim et al, 2008 ). The 2a protein, one of five proteins encoded by CMV, is responsible for induction of feeding deterrence and concomitant growth inhibition, and this mechanism predominates during infection over a stronger anti‐aphid resistance mechanism due to direct and indirect interactions between two other viral proteins (the 1a and 2b proteins), and the plant Argonaute 1 protein (Rhee et al, 2020 ; Watt et al, 2020 ; Westwood et al, 2013 ). CMV infection induces expression of several genes known to be responsive to microbe‐associated molecular pattern (MAMP) molecules (Westwood et al, 2013 ).…”

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

“…Some viruses, by altering plant metabolism, particularly by changing emission of VOCs or the accumulation of nutrients or distasteful compounds in plant tissue, can manipulate host-vector interactions in ways that favor their onward transmission ( Casteel et al, 2014 , 2015 ; Mauck et al, 2016 ; Groen et al, 2017 ; Carr et al, 2018 ; Donnelly et al, 2019 ). For example, CMV and potyviral gene products can affect plant VOC emission or accumulation of non-volatile metabolites to stimulate dispersal or settling of aphids on different plant hosts ( Lewsey et al, 2010 ; Ziebell et al, 2011 ; Westwood et al, 2013 ; Casteel et al, 2014 , 2015 ; Rhee et al, 2020 ; Tungadi et al, 2020 ). In squash and cucumber, infection with CMV increases emission of aphid-attracting VOCs while also causing accumulation of distasteful soluble compounds ( Mauck et al, 2010 ; Carmo-Sousa et al, 2014 ).…”