A Trio of Viral Proteins Tunes Aphid-Plant Interactions in Arabidopsis thaliana

Abstract

BackgroundVirus-induced deterrence to aphid feeding is believed to promote plant virus transmission by encouraging migration of virus-bearing insects away from infected plants. We investigated the effects of infection by an aphid-transmitted virus, cucumber mosaic virus (CMV), on the interaction of Arabidopsis thaliana, one of the natural hosts for CMV, with Myzus persicae (common names: ‘peach-potato aphid’, ‘green peach aphid’). Methodology/Principal FindingsInfection of Arabidopsis (ecotype Col-0) with CMV strain Fny (Fny-CMV) induced biosynthesis of the aphid feeding-deterrent 4-methoxy-indol-3-yl-methylglucosinolate (4MI3M). 4MI3M inhibited phloem ingestion by aphids and consequently discouraged aphid settling. The CMV 2b protein is a suppressor of antiviral RNA silencing, which has previously been implicated in altering plant-aphid interactions. Its presence in infected hosts enhances the accumulation of CMV and the other four viral proteins. Another viral gene product, the 2a protein (an RNA-dependent RNA polymerase), triggers defensive signaling, leading to increased 4MI3M accumulation. The 2b protein can inhibit ARGONAUTE1 (AGO1), a host factor that both positively-regulates 4MI3M biosynthesis and negatively-regulates accumulation of substance(s) toxic to aphids. However, the 1a replicase protein moderated 2b-mediated inhibition of AGO1, ensuring that aphids were deterred from feeding but not poisoned. The LS strain of CMV did not induce feeding deterrence in Arabidopsis ecotype Col-0. Conclusions/SignificanceInhibition of AGO1 by the 2b protein could act as a booby trap since this will trigger antibiosis against aphids. However, for Fny-CMV the interplay of three viral proteins (1a, 2a and 2b) appears to balance the need of the virus to inhibit antiviral silencing, while inducing a mild resistance (antixenosis) that is thought to promote transmission. The strain-specific effects of CMV on Arabidopsis-aphid interactions, and differences between the effects of Fny-CMV on this plant and those seen previously in tobacco (inhibition of resistance to aphids) may have important epidemiological consequences.

Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco

“…In Arabidopsis, CMV also induces unpalatability, which encourages aphid dispersion [18]. The effects of CMV on cucurbits and Arabidopsis probably drive spread of this non-persistently transmitted virus, since CMV acquisition and inoculation are favored by brief probe-feeds by aphids, not by prolonged ingestion [42].…”

Inositol hexakisphosphate biosynthesis underpins PAMP‐triggered immunity to Pseudomonas syringae pv. tomato in Arabidopsis thaliana but is dispensable for establishment of systemic acquired resistance

“…The cDNA was diluted 10‐fold and quantitative PCR (qPCR) was performed using SensiMix No ROX (Bioline) in 20 μl reactions, containing 250 nM each of the forward and reverse primers complementary to sequences of interest (Table ). The transcripts for glyceraldehyde‐3‐phosphate dehydrogenase ( GAPDH ) and elongation factor 1A ( EF1α ) were used as internal standards (Westwood et al ., ). PCRs were conducted in triplicate using the CFX96 Touch Real‐Time PCR Detection System (Bio‐Rad).…”

Bean Common Mosaic Virus and Bean Common Mosaic Necrosis Virus

“…This can be due to changes in the emission of volatile compounds to make plants more or less attractive to potential vectors (Mauck et al, 2010), or by modification of soluble plant metabolites to alter "taste," thereby influencing feeding behavior; phenomena which have been observed in the interactions of aphids (including Myzus persicae and Aphis gossypii) with plants infected with CMV (CarmoSousa et al, 2014;Mauck et al, 2010;Westwood et al, 2013;Ziebell et al, 2011). Thus, it has been hypothesized that the virus transmission mode (nonpersistent vs. persistent) may influence the coevolution of plant-virusvector interactions to shape the biochemical reactions of infected plants to indirectly facilitate vectored transmission (Ingwell et al, 2012;Mauck et al, 2012;Westwood et al, 2013). Indeed, virus-induced changes in host biochemistry that influence the onward transmission of the virus might be considered to be "extended" viral phenotypes (discussed in Palukaitis et al, 2013).…”

“…It can be seen that the effects of virus infection on aphid-plant interactions are complex, and it has been proposed that the same virus can have different effects on different hosts in order to promote transmission between some, while enhancing survival and reproduction of vectors on other hosts (Westwood et al, 2013). This complex set of relationships among hosts, vectors, and viruses may offer a new route to control virus infection (reviewed by Bragard et al, 2013) and will be discussed further in Section 8.…”