Induction of aphid resistance in tobacco by the cucumber mosaic virus CMV∆2b mutant is jasmonate‐dependent

Arinaitwe, Warren; Tungadi, Trisna; Pate, Adrienne E.; Joyce, Joshua; Baek, Eseul; Murphy, Alex M.; Carr, John P.

doi:10.1111/mpp.13305

Cited by 4 publications

(2 citation statements)

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“…The viral protein responsible for inducing this anti-aphid resistance in tobacco is the Fny-CMV 1a protein, but induction of resistance can be prevented by either the Fny-CMV 2b protein or by the LS-CMV 2b protein (Tungadi et al, 2020). Arinaitwe and colleagues (2023) proposed alternative hypotheses to explain how 2b proteins impede induction of resistance to aphids in tobacco: through inhibition of jasmonate-dependent signaling (Lewsey et al, 2010; Westwood et al, 2014), or through formation of 2b-1a protein-protein complexes to prevent the 1a protein interacting with a host factor (based on Watt et al, 2020). Since we show here that the LS-CMV 2b protein does not bind to the Fny-CMV 1a protein, it follows that in tobacco plants the 2b proteins of Fny-CMV and LS-CMV must inhibit 1a protein-induced aphid resistance by inhibition of jasmonate-induced defenses.…”

Section: Discussionmentioning

confidence: 99%

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Strain-specific differences in the interactions of the cucumber mosaic virus 2b protein with the viral 1a and host Argonaute 1 proteins

Crawshaw,

Watt,

Murphy

et al. 2023

Preprint

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The cucumber mosaic virus (CMV) 2b protein is a potent counter-defense protein and symptom determinant that inhibits antiviral silencing by titration of short double-stranded RNAs. Expression of the 2b protein from the CMV Subgroup IA strain Fny-CMV in transgenic Arabidopsis thaliana plants disrupts microRNA-mediated cleavage of host mRNAs by binding ARGONAUTE 1 (AGO1), leading to symptom-like phenotypes. This also triggers AGO2-mediated resistance against CMV and strong resistance to CMVs aphid vectors, which would be deleterious to viral fitness. However, in authentic viral infections the Fny-CMV 1a protein modulates 2b-AGO1 interactions, which inhibits induction of AGO2-mediated virus resistance and resistance to aphid vectors. Contrastingly, the 2b proteins encoded by the Subgroup II LS-CMV strain or the recently discovered Subgroup IA strain Ho-CMV induce no apparent symptoms. Confocal laser scanning microscopy, bimolecular fluorescence complementation and co-immunoprecipitation showed that the Fny-CMV and Ho-CMV 2b proteins interact with the Fny-CMV and LS-CMV 1a proteins whilst the CMV-LS 2b protein does not. However, the Fny-CMV, Ho-CMV and LS-CMV 2b proteins all interacted with AGO1, but while AGO1-Fny2b complexes occurred in the host cell nucleus and cytoplasm, the corresponding AGO1-2b complexes for LS-CMV and Ho-CMV accumulated almost exclusively in nuclei. AGO2 transcript accumulation was used to assess the inhibition of AGO1-mediated miRNA-regulated mRNA cleavage. While Fny-CMV 2b induced a five-fold increase in AGO2 accumulation, the LS-CMV and Ho-CMV 2b proteins induced only two-fold increases. Thus, these 2b proteins bind AGO1 but are less effective at inhibiting AGO1 activity. We conclude that the intracellular localization sites of 2b-AGO1 complexes influences the degree to which a 2b protein can inhibit microRNA-mediated host mRNA degradation and that cytoplasmic AGO1 has the strongest influence on miRNA-mediated cellular mRNA turnover.

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Section: Discussionmentioning

confidence: 99%

“…The copyright holder for this this version posted September 1, 2023. ; https://doi.org/10. 1101/2023 between the sequences of Ho-CMV and Fny-CMV are four differences in the amino acid sequences of their respective 2b proteins.…”

Section: Introductionmentioning

confidence: 99%

Strain-specific differences in the interactions of the cucumber mosaic virus 2b protein with the viral 1a and host Argonaute 1 proteins

Crawshaw,

Watt,

Murphy

et al. 2023

Preprint

Self Cite

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Fortifying crop defenses: unraveling the molecular arsenal against aphids

Yang,

Zhang,

et al. 2024

HORTIC. ADV.

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Aphids cause enormous financial losses to various crop plants on a global scale. Moreover, aphids are vectors for many plant viral diseases that can further hasten crop yield losses. Aphids secrete saliva during feeding that contains effectors that can regulate plants' defense responses and their underlying mechanisms. Although much research has been undertaken to determine the mechanisms contributing to plant-aphid interactions, our understanding of defense mechanisms against aphids is insufficient. The presence of piercing-sucking mouthparts in aphids makes the identification of aphid resistance more challenging, hindering our understanding of the mechanisms of plant resistance to aphids. In this article, we consolidate and assess the evidence that is currently available on plant-aphid interactions, address the gaps in our understanding, and propose new research directions. As an outcome, we present an in-depth review of the molecular mechanisms of aphid resistance in crops from five perspectives: physical protection against aphids using volatile compounds, PAMP-triggered immunity (PTI), effector-triggered immunity (ETI), plant hormone signaling and the inheritance of induced resistance through epigenetics.

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Induction of aphid resistance in tobacco by the cucumber mosaic virus CMV∆2b mutant is jasmonate‐dependent

Arinaitwe

Tungadi

Pate

et al. 2023

Molecular Plant Pathology

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Cucumber mosaic virus (CMV) is vectored by aphids, including Myzus persicae. Tobacco (Nicotiana tabacum ‘Xanthi’) plants infected with a mutant of the Fny strain of CMV (Fny‐CMVΔ2b, which cannot express the CMV 2b protein) exhibit strong resistance against M. persicae, which is manifested by decreased survival and reproduction of aphids confined on the plants. Previously, we found that the Fny‐CMV 1a replication protein elicits aphid resistance in plants infected with Fny‐CMVΔ2b, whereas in plants infected with wild‐type Fny‐CMV this is counteracted by the CMV 2b protein, a counterdefence protein that, among other things, inhibits jasmonic acid (JA)‐dependent immune signalling. We noted that in nontransformed cv. Petit Havana SR1 tobacco plants aphid resistance was not induced by Fny‐CMVΔ2b, suggesting that not all tobacco varieties possess the factor(s) with which the 1a protein interacts. To determine if 1a protein‐induced aphid resistance is JA‐dependent in Xanthi tobacco, transgenic plants were made that expressed an RNA silencing construct to diminish expression of the JA co‐receptor CORONATINE‐INSENSITIVE 1. Fny‐CMVΔ2b did not induce resistance to M. persicae in these transgenic plants. Thus, aphid resistance induction by the 1a protein requires JA‐dependent defensive signalling, which is countered by the CMV 2b protein.

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Induction of aphid resistance in tobacco by the cucumber mosaic virus CMV∆2b mutant is jasmonate‐dependent

Cited by 4 publications

References 25 publications

Strain-specific differences in the interactions of the cucumber mosaic virus 2b protein with the viral 1a and host Argonaute 1 proteins

Strain-specific differences in the interactions of the cucumber mosaic virus 2b protein with the viral 1a and host Argonaute 1 proteins

Fortifying crop defenses: unraveling the molecular arsenal against aphids

Induction of aphid resistance in tobacco by the cucumber mosaic virus CMV∆2b mutant is jasmonate‐dependent

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