Identification of Plant Virus Receptor Candidates in the Stylets of Their Aphid Vectors

Webster, Craig; Pichon, Elodie; Munster, Manuella van; Monsion, Baptiste; Deshoux, Maëlle; Gargani, Daniel; Calevro, Federica; Jiménez, José Luis Ubera; Moreno, Aránzazu; Krenz, Björn; Thompson, Jeremy R.; Perry, Keith L.; Fereres, Alberto; Blanc, Stéphane; Uzest, Marilyne

doi:10.1128/jvi.00432-18

Cited by 61 publications

(106 citation statements)

References 69 publications

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“…Recent fluorescence evidence showed that the binding site of one NPTV Cauliflower mosaic virus is localized in the aphid stylet tip (Uzest et al, 2010). These tips, which are termed "acrostyles," interact with capsid proteins or with virion-encoded accessory proteins (i.e., P2 in Cauliflower mosaic virus) of NPTVs (Uzest et al, 2010;Webster et al, 2018). During a brief period of probing epidermal and mesophyll cells, aphid stylets can access cell contents including virions (Webster et al, 2017).…”

mentioning

confidence: 99%

Aphid-borne Viral Spread Is Enhanced by Virus-induced Accumulation of Plant Reactive Oxygen Species

Guo

Liu

et al. 2018

Plant Physiol.

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Most known plant viruses are spread from plant to plant by insect vectors. There is strong evidence that nonpersistently transmitted viruses manipulate the release of plant volatiles to attract insect vectors, thereby promoting virus spread. The mechanisms whereby aphid settling and feeding is altered on plants infected with these viruses, however, are unclear. Here we employed loss-of-function mutations in cucumber mosaic virus (CMV) and one of its host plants, tobacco (Nicotiana tabacum), to elucidate such mechanisms. We show that, relative to a CMVD2b strain with a deletion of the viral suppressor of RNAi 2b protein in CMV, plants infected with wild-type CMV produce higher concentrations of the reactive oxygen species (ROS) H 2 O 2 in plant tissues. Aphids on wild-type CMV-infected plants engage in shorter probes, less phloem feeding, and exhibit other changes, as detected by electrical penetration graphing technology, relative to CMVD2b-infected plants. Therefore, the frequency of virus acquisition and the virus load per aphid were greater on CMV-infected plants than on CMVD2b-infected plants. Aphids also moved away from initial feeding sites more frequently on wild-type CMV infected versus CMVD2b-infected plants. The role of H 2 O 2 in eliciting these effects on aphids was corroborated using healthy plants infused with H 2 O 2. Finally, H 2 O 2 levels were not elevated, and aphid behavior was unchanged, on CMV-infected RbohD-silenced tobacco plants, which are deficient in the induction of ROS production. These results suggest that CMV uses its viral suppressor of RNAi protein to increase plant ROS levels, thereby enhancing its acquisition and transmission by vector insects.

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confidence: 99%

Aphid-borne Viral Spread Is Enhanced by Virus-induced Accumulation of Plant Reactive Oxygen Species

Guo

Liu

et al. 2018

Plant Physiol.

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“…In aphids, symbiont-mediated RNAi could be used to directly target plant viruses that circulate and/or propagate in aphids (e.g., Luteoviruses such as potato leaf roll virus and Rhabdoviruses such as lettuce necrotic yellows virus) (41,42). It might also be used to reduce the expression of the receptors that noncirculative viruses bind to such as the Stylin-01 receptor bound by cauliflower mosaic virus (43).…”

Section: Discussionmentioning

confidence: 99%

Engineering a culturableSerratia symbioticastrain for aphid paratransgenesis

Elston

Perreau

Maeda

et al. 2020

Preprint

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Aphids are global agricultural pests and important models for bacterial symbiosis. To date, none of the native symbionts of aphids have been genetically manipulated, which limits our understanding of how they interact with their hosts. Serratia symbiotica CWBI-2.3T is a culturable, gut-associated bacterium isolated from the black bean aphid. Closely related Serratia symbiotica strains are facultative aphid endosymbionts that are vertically transmitted from mother to offspring during embryogenesis. We demonstrate that CWBI-2.3T can be genetically engineered using a variety of techniques, plasmids, and gene expression parts. Then, we use fluorescent protein expression to track the dynamics with which CWBI-2.3T colonizes the guts of multiple aphid species, and we measure how this bacterium affects aphid fitness. Finally, we show that we can induce heterologous gene expression from engineered CWBI-2.3T in living aphids. These results inform the development of CWBI-2.3T for aphid paratransgenesis, which could be used to study aphid biology and enable future agricultural technologies.IMPORTANCEInsects have remarkably diverse and integral roles in global ecosystems. Many harbor symbiotic bacteria, but very few of these bacteria have been genetically engineered. Aphids are major agricultural pests and an important model system for the study of symbiosis. This work describes methods for engineering a culturable aphid symbiont, Serratia symbiotica CWBI-2.3T. These approaches and genetic tools could be used in the future to implement new paradigms for the biological study and control of aphids.

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“…viruses transmitted during short punctures without internalization of the viral particles) such as the Cauliflower mosaic virus (CaMV), or the CMV which is transmitted by Ap. glycines (Uzest, 2007;Webster, 2018;Gildow et al, 2008). Indeed Stylin 01, named previously Mpcp4 in M. persicae (Dombrovsky, 2007), was shown to interact in yeast with the coat protein of the CMV.…”

Section: Cuticular Proteinsmentioning

confidence: 99%

“…We present a phylome report, the complete collection of phylogenetic trees of genes encoded in the soybean aphid genome and the currently available aphid genomes to elucidate the evolutionary history of this pest. In addition, because structural cuticular proteins (CPs) are the major constituents of arthropod exoskeleton and also candidates for host receptors of plant viruses we have investigated the full set of structural CPs present in this aphid species (Webster, 2018;Kamanga, 2019). In this study we describe the different CPs subfamilies detected in the Ap.…”

Section: Introductionmentioning

confidence: 99%

Soybean aphid biotype 1 genome: Insights into the invasive biology and adaptive evolution of a major agricultural pest

Giordano

Donthu

Zimin

et al. 2020

Insect Biochemistry and Molecular Biology

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The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) is a serious pest of the soybean plant, Glycine max, a major world-wide agricultural crop. We assembled a de novo genome sequence of Ap. glycines Biotype 1, from a culture established shortly after this species invaded North America. 20.4% of the Ap. glycines proteome is duplicated. These in-paralogs are enriched with Gene Ontology (GO) categories mostly related to apoptosis, a possible adaptation to plant chemistry and other environmental stressors. Approximately one-third of these genes show parallel duplication in other aphids. But Ap. gossypii, its closest related species, has the lowest number of these duplicated genes. An Illumina GoldenGate assay of 2380 SNPs was used to determine the world-wide population structure of Ap. Glycines. China and South Korean aphids are the closest to those in North America. China is the likely origin of other Asian aphid populations. The most distantly related aphids to those in North America are from Australia. The diversity of Ap. glycines in North America has decreased over time since its arrival. The genetic diversity of Ap. glycines North American population sampled shortly after its first detection in 2001 up to 2012 does not appear to correlate with geography. However, aphids collected on soybean Rag experimental varieties in Minnesota (MN), Iowa (IA), and Wisconsin (WI), closer to high density Rhamnus cathartica stands, appear to have higher capacity to colonize resistant soybean plants than aphids sampled in Ohio (OH), North Dakota (ND), and South Dakota (SD). Samples from the former states have SNP alleles with high FST values and frequencies, that overlap with genes involved in iron metabolism, a crucial metabolic pathway that may be affected by the Rag-associated soybean plant response. The Ap. glycines Biotype 1 genome will provide needed information for future analyses of mechanisms of aphid virulence and pesticide resistance as well as facilitate comparative analyses between aphids with differing natural history and host plant range.

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Identification of Plant Virus Receptor Candidates in the Stylets of Their Aphid Vectors

Cited by 61 publications

References 69 publications

Aphid-borne Viral Spread Is Enhanced by Virus-induced Accumulation of Plant Reactive Oxygen Species

Aphid-borne Viral Spread Is Enhanced by Virus-induced Accumulation of Plant Reactive Oxygen Species

Engineering a culturableSerratia symbioticastrain for aphid paratransgenesis

Soybean aphid biotype 1 genome: Insights into the invasive biology and adaptive evolution of a major agricultural pest

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