Ethylene signaling mediates potyvirus spread by aphid vectors

Bak, Aurélie; Patton, MacKenzie F; Perilla‐Henao, Laura M.; Aegerter, B. J.; Casteel, Clare L.

doi:10.1007/s00442-019-04405-0

Cited by 44 publications

(37 citation statements)

References 75 publications

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“…Previous studies have shown the importance of the ethylene pathway for insect vector attraction (Bak et al, 2019;Casteel et al, 2015). Ethylene is involved in plant senescence and development (Koyama, 2014); however, not much is known about how ethylene signalling may mediate plant responses to infection by viruses transmitted in a circulative nonpropagative manner.…”

Section: Discussionmentioning

confidence: 99%

“…1-MCP has previously been shown to block ethylene perception (Huber, 2008;Schaller & Binder, 2017 acid and jasmonic acid, as described above. Ethylene induction and inhibition using these treatments have previously been confirmed (Bak et al, 2019). Insect settling and fecundity bioassays were conducted as described above.…”

Section: Chemical Treatmentsmentioning

confidence: 96%

“…It has been demonstrated that viruses transmitted in a noncirculative manner use specific viral proteins to alter host-vector interactions and promote transmission (Westwood et al, 2014;Wu et al, 2017). For example, potyviruses, such as Turnip mosaic virus, increase plant ethylene production, vector attraction, and vector fecundity using the viral encoded protein NIa-Pro (Bak, Patton, Perilla-Henao, Aegerter, & Casteel, 2019;Casteel et al, 2014). Ethylene is a phytohormone involved in ripening and senescence (Bouchez, Huard, Lorrain, Roby, & Balague, 2007).…”

Section: Introductionmentioning

confidence: 99%

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A polerovirus, Potato leafroll virus, alters plant–vector interactions using three viral proteins

Patton

Bak

Sayre

et al. 2019

Plant Cell & Environment

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Potato leafroll virus (PLRV), genus Polerovirus, family Luteoviridae, is a major pathogen of potato worldwide. PLRV is transmitted among host plants by aphids in a circulative–nonpropagative manner. Previous studies have demonstrated that PLRV infection increases aphid fecundity on, and attraction to, infected plants as compared to controls. However, the molecular mechanisms mediating this relationship are still poorly understood. In this study, we measured the impact of PLRV infection on plant–aphid interactions and plant chemistry in two hosts: Solanum tuberosum and Nicotiana benthamiana. Our study demonstrates that PLRV infection attenuates the induction of aphid‐induced jasmonic acid and ethylene in S. tuberosum and N. benthamiana. Using transient expression experiments, insect bioassays and chemical analysis, we show that expression of three PLRV proteins (P0, P1, and P7) mediate changes in plant–aphid interactions and inhibition of aphid‐induced jasmonic acid and ethylene in N. benthamiana. This study enhances our understanding of the plant‐vector‐pathogen interface by elucidating new mechanisms by which plant viruses transmitted in a circulative manner can manipulate plant hosts.

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Section: Discussionmentioning

confidence: 99%

Section: Chemical Treatmentsmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

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A polerovirus, Potato leafroll virus, alters plant–vector interactions using three viral proteins

Patton

Bak

Sayre

et al. 2019

Plant Cell & Environment

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“…This effect was again attributed to NIa-Pro that alters a specific set of ET-responsive defence transcripts. Bak et al [46] confirmed that ET production promoted aphid attraction to infected plants and virus spread with two potyvirus pathosystems on different host plants (PVY/potato and TuMV/arabidopsis) suggesting that ET signalling may be a general response to potyviruses.…”

Section: Potyviruses: An Intriguing Strategy Of Protein Relocalisatiomentioning

confidence: 99%

Molecular Insights into Host and Vector Manipulation by Plant Viruses

Ziegler-Graff

2020

Viruses

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Plant viruses rely on both host plant and vectors for a successful infection. Essentially to simplify studies, transmission has been considered for decades as an interaction between two partners, virus and vector. This interaction has gained a third partner, the host plant, to establish a tripartite pathosystem in which the players can react with each other directly or indirectly through changes induced in/by the third partner. For instance, viruses can alter the plant metabolism or plant immune defence pathways to modify vector’s attraction, settling or feeding, in a way that can be conducive for virus propagation. Such changes in the plant physiology can also become favourable to the vector, establishing a mutualistic relationship. This review focuses on the recent molecular data on the interplay between viral and plant factors that provide some important clues to understand how viruses manipulate both the host plants and vectors in order to improve transmission conditions and thus ensuring their survival.

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“…For example, it was shown that Cucumber mosaic virus, a non-persistently transmitted virus, drives accumulation of reactive oxygen species through the action of its 2b silencing suppressor, which consequently shortens aphid probes and increases virus acquisition [35]. Another advanced molecular study on viral impacts on aphid performance addresses the role of the nuclear inclusion-a protease (NIa-Pro) from Turnip mosaic virus, which regulates ethylene production and ethylene-related defense mechanisms [36][37][38]. The effect of NIa-Pro on aphid performance correlates with its ability to relocalize to the vacuole after aphid puncture [39].Further functional studies are needed to identify metabolic pathways that are under virus control, influence aphid performance and/or feeding behavior, and ultimately impact virus acquisition and transmission.…”

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confidence: 99%

Impact of Mutations in Arabidopsis thaliana Metabolic Pathways on Polerovirus Accumulation, Aphid Performance, and Feeding Behavior

Bogaert

Marmonier

Pichon

et al. 2020

Viruses

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During the process of virus acquisition by aphids, plants respond to both the virus and the aphids by mobilizing different metabolic pathways. It is conceivable that the plant metabolic responses to both aggressors may be conducive to virus acquisition. To address this question, we analyze the accumulation of the phloem-limited polerovirus Turnip yellows virus (TuYV), which is strictly transmitted by aphids, and aphid's life traits in six Arabidopsis thaliana mutants (xth33, ss3-2, nata1, myc234, quad, atr1D, and pad4-1). We observed that mutations affecting the carbohydrate metabolism, the synthesis of a non-protein amino acid and the glucosinolate pathway had an effect on TuYV accumulation. However, the virus titer did not correlate with the virus transmission efficiency. Some mutations in A. thaliana affect the aphid feeding behavior but often only in infected plants. The duration of the phloem sap ingestion phase, together with the time preceding the first sap ingestion, affect the virus transmission rate more than the virus titer did. Our results also show that the aphids reared on infected mutant plants had a reduced biomass regardless of the mutation and the duration of the sap ingestion phase.Viruses 2020, 12, 146 2 of 16 defenses against M. persicae [10][11][12]. Glucosinolates are herbivores-deterrent secondary metabolites in Brassicaceae that increase upon aphid feeding and reduce A. thaliana susceptibility to aphids [13][14][15]. Finally, callose deposition, modification of starch content, and stimulation of senescence constitute additional modifications that may affect M. persicae [7].Arabidopsis thaliana can, among other plant viruses, be infected by poleroviruses (Polerovirus genus, Luteoviridae family) that are transmitted by aphids in a circulative and non-propagative mode [16]. Polerovirus particles are acquired by aphids during phloem sap ingestion on infected plants. Virions migrate through the gut and internalize into intestinal cells after binding to specific virus receptors [17]. Virus particles are then transported through the intestinal cells and released in the hemolymph. Finally, polerovirus particles cross the salivary gland cells and are released together with saliva into a new plant host during a subsequent feeding event [18].There is growing evidence that aphid-transmitted viruses can affect plant phenotypes and vector behaviors in ways that may ultimately facilitate virus acquisition and inoculation [19,20]. This concept of plant and aphid "manipulation" by the virus also applies to viruses in the Luteoviridae family. Polerovirus infection induces leaf yellowing, which may be visually attractive for aphids [21]. The major viral determinant governing both symptoms expressions, including yellowing, and aphid transmission, is attributed to the minor capsid protein of poleroviruses [22,23]. These viruses also increase volatiles emission from infected plants that attract non-viruliferous aphids [24,25]. In addition, polerovirus infection alters plant palatability and quality that affect...

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Ethylene signaling mediates potyvirus spread by aphid vectors

Cited by 44 publications

References 75 publications

A polerovirus, Potato leafroll virus, alters plant–vector interactions using three viral proteins

A polerovirus, Potato leafroll virus, alters plant–vector interactions using three viral proteins

Molecular Insights into Host and Vector Manipulation by Plant Viruses

Impact of Mutations in Arabidopsis thaliana Metabolic Pathways on Polerovirus Accumulation, Aphid Performance, and Feeding Behavior

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