A viral<scp>RNA</scp>silencing suppressor interferes with abscisic acid‐mediated signalling and induces drought tolerance in<i><scp>A</scp>rabidopsis thaliana</i>

Westwood, Jack H.; Mccann, L. P.; Naish, Matthew; DIXON, H. B. F.; Murphy, Alex M.; Stancombe, Matthew A.; Bennett, Mark H.; Powell, Glen; Webb, Alex A. R.; Carr, John P.

doi:10.1111/j.1364-3703.2012.00840.x

Cited by 98 publications

(108 citation statements)

References 71 publications

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“…However, plants in which viruses inhibit aphid resistance (or at least induce no deleterious effects on the aphids) will foster aphid survival and reproduction (Type 2 hosts: Figure 11). Although onward transmission of the virus from Type 2 hosts will be less frequent, and probably driven by overcrowding of the aphids as their populations grow, these plants may provide a safe haven for aphids during stressful periods of cold or drought [48,49] and allow the vector population to recover after a period of active transmission between Type 1 plants. When conditions improve Type 2 hosts could act as centers from which the aphids and the virus will spread to Type 1 plants and resume a more active phase of transmission.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2013

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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.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2013

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“…; Westwood et al . ) and drastic changes in nutrient levels that both encourage dispersal of viruliferous vectors after probing and deter non‐vector herbivore feeding.…”

Section: Discussionmentioning

confidence: 99%

Virus infection influences host plant interactions with non‐vector herbivores and predators

et al. 2014

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Summary1. Viruses are widespread in both natural and agricultural plant communities and can significantly alter diverse traits of their host plants that mediate key interactions with other organisms. Yet, the impacts of plant viruses on broader community dynamics remain little studied. 2. Here, we explore the effects of Cucumber mosaic virus, a common non-persistently transmitted plant virus, on short-and long-term interactions of herbivorous and predatory insects with squash (Cucurbita pepo) plants in a weedy field setting, as well as virus-induced changes in plant phenotypes that mediate these interactions. Cucumber mosaic virus has previously been shown to have numerous effects on host plants that likely influence interactions with arthropods, including reduced plant size, increased volatile emissions, and diminished plant quality and palatability for aphid vectors. 3. Infection reduced the likelihood of many herbivorous insects arresting and feeding on plants, as well as the apparency of plants to herbivores that base in-flight foraging on visual cues. In particular, infection drastically reduced numbers of a specialist squash herbivore (Anasa tristis) on plants in the field -a pattern likely driven by a reduction of phagostimulatory sugar levels in leaf tissue and concurrent increase in amino acid levels, as nymphal development was not obviously impacted by infection status. Relative to effects on herbivores, virus infection had little impact on the ability of predatory insects to locate aphid prey, although an experiment examining plant visitation in the absence of aphids revealed reduced numbers of foraging Syrphidae (Diptera) and Coccinellidae (Coleoptera) on infected plants but increased visitation and oviposition by Chrysopidae (Neuroptera). 4. CMV infection may reduce overall herbivore pressure on infected plants through effects on palatability and apparency, yet predators appear to locate herbivorous prey that do occur on infected plants as efficiently as those on healthy plants. 5. Virus infection can significantly influence plant interactions with the insect community (including non-vector as well as vector insects) with potential implications both for disease spread and for broader community dynamics.

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“…In one way this was a surprising result because in a number of studies it has been shown that small RNA pathways affect drought responses. For example, where RNA silencing pathways have been compromised through mutation of AGO1 or DCLs 1–4, the mutant plants showed increased resistance to water loss [56], [57], [58]. Hence, although RDR1 is a component of the silencing pathway it does not appear to play a critical role in drought resistance, unlike the DCLs and AGO1.…”

Section: Discussionmentioning

confidence: 99%

“…The plant hormone treatments were SA (1 mM), methyl-JA (250 µM), ABA (50 µM) and ACC (the precursor of ethylene; 1 mM) dissolved in water. Hormone concentrations were selected on the basis of previous optimization for SA and methyl-JA [46], ACC [59], and ABA [58], [60]. Control treatment used water only.…”

Section: Methodsmentioning

confidence: 99%

Regulation of RNA-Dependent RNA Polymerase 1 and Isochorismate Synthase Gene Expression in Arabidopsis

et al. 2013

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BackgroundRNA-dependent RNA polymerases (RDRs) function in anti-viral silencing in Arabidopsis thaliana and other plants. Salicylic acid (SA), an important defensive signal, increases RDR1 gene expression, suggesting that RDR1 contributes to SA-induced virus resistance. In Nicotiana attenuata RDR1 also regulates plant-insect interactions and is induced by another important signal, jasmonic acid (JA). Despite its importance in defense RDR1 regulation has not been investigated in detail.Methodology/Principal FindingsIn Arabidopsis, SA-induced RDR1 expression was dependent on ‘NON-EXPRESSER OF PATHOGENESIS-RELATED GENES 1’, indicating regulation involves the same mechanism controlling many other SA- defense-related genes, including pathogenesis-related 1 (PR1). Isochorismate synthase 1 (ICS1) is required for SA biosynthesis. In defensive signal transduction RDR1 lies downstream of ICS1. However, supplying exogenous SA to ics1-mutant plants did not induce RDR1 or PR1 expression to the same extent as seen in wild type plants. Analysing ICS1 gene expression using transgenic plants expressing ICS1 promoter:reporter gene (β-glucuronidase) constructs and by measuring steady-state ICS1 transcript levels showed that SA positively regulates ICS1. In contrast, ICS2, which is expressed at lower levels than ICS1, is unaffected by SA. The wound-response hormone JA affects expression of Arabidopsis RDR1 but jasmonate-induced expression is independent of CORONATINE-INSENSITIVE 1, which conditions expression of many other JA-responsive genes. Transiently increased RDR1 expression following tobacco mosaic virus inoculation was due to wounding and was not a direct effect of infection. RDR1 gene expression was induced by ethylene and by abscisic acid (an important regulator of drought resistance). However, rdr1-mutant plants showed normal responses to drought.Conclusions/Significance RDR1 is regulated by a much broader range of phytohormones than previously thought, indicating that it plays roles beyond those already suggested in virus resistance and plant-insect interactions. SA positively regulates ICS1.

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A viralRNAsilencing suppressor interferes with abscisic acid‐mediated signalling and induces drought tolerance inArabidopsis thaliana

Cited by 98 publications

References 71 publications

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

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

Virus infection influences host plant interactions with non‐vector herbivores and predators

Regulation of RNA-Dependent RNA Polymerase 1 and Isochorismate Synthase Gene Expression in Arabidopsis

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