Exploring how viruses enhance plants' resilience to drought and the limits to this form of viral payback

Carr, John P.

doi:10.1111/pce.13068

Cited by 13 publications

(12 citation statements)

References 19 publications

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“…Several studies have reported increased plant tolerance to abiotic stresses, including water deficit, upon infection by viruses [4,30,32]. Across the quite large number of plant accessions assayed here (n = 44), we did not find any significant positive effect of CaMV infection on plant tolerance to water deficit in terms of vegetative biomass production (see position of accessions relative to line of equal response on S4B Fig).…”

Section: Survival But Not Reproductive Effort Of Infected Plants Iscontrasting

confidence: 43%

“…In contrast with Grime's expectations, the effects of water deficit on plant development and leaf physiology may reduce virus systemic spread, and therefore decrease virulence [13,28,29]. Virus-induced drought tolerance has been demonstrated in several species infected with different viruses [4,[30][31][32][33]. Recent findings in Arabidopsis thaliana demonstrated that spread of Cauliflower mosaic virus (CaMV; Caulimoviridae, a non-circulative virus transmitted by aphids that infects essentially plants of the family Brassicaceae) infection throughout the host plant was slower under water deficit, though the combined effects of CaMV infection and water deficit remained more detrimental to growth compared with either viral infection or water deficit alone [13].…”

Section: Plos Pathogensmentioning

confidence: 89%

“…However, the success of viral infection, and its quantitative variation of pathogenicity depends on the physiological machinery of the host plant, and thus any other environmental change that affects plant physiology may also affect the outcome of viral infection [3]. Conversely, it has been shown that viruses can alter the host plant's response to additional stimuli, and that the outcome of this response can vary from antagonism to mutualism depending on the virus, the host plant and the environment [4][5][6][7]. In particular, limiting soil water availability is an increasingly recurrent condition affecting plant physiology and represents a major constraint to plant growth and productivity [8,9].…”

Section: Introductionmentioning

confidence: 99%

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Natural variation of Arabidopsis thaliana responses to Cauliflower mosaic virus infection upon water deficit

et al. 2020

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Plant virus pathogenicity is expected to vary with changes in the abiotic environment that affect plant physiology. Conversely, viruses can alter the host plant response to additional stimuli from antagonism to mutualism depending on the virus, the host plant and the environment. Ecological theory, specifically the CSR framework of plant strategies developed by Grime and collaborators, states that plants cannot simultaneously optimize resistance to both water deficit and pathogens. Here, we investigated the vegetative and reproductive performance of 44 natural accessions of A. thaliana originating from the Iberian Peninsula upon simultaneous exposure to soil water deficit and viral infection by the Cauliflower mosaic virus (CaMV). Following the predictions of Grime's CSR theory, we tested the hypothesis that the ruderal character of a plant genotype is positively related to its tolerance to virus infection regardless of soil water availability. Our results showed that CaMV infection decreased plant vegetative performance and annihilated reproductive success of all accessions. In general, water deficit decreased plant performance, but, despite differences in behavior, ranking of accessions tolerance to CaMV was conserved under water deficit. Ruderality, quantified from leaf traits following a previously published procedure, varied significantly among accessions, and was positively correlated with tolerance to viral infection under both well-watered and water deficit conditions, although the latter to a lesser extent. Also, in accordance with the ruderal character of the accession and previous findings, our results suggest that accession tolerance to CaMV infection is positively correlated with early flowering. Finally, plant survival to CaMV infection increased under water deficit. The complex interactions between plant, virus and abiotic environment are discussed in terms of the variation in plant ecological strategies at the intraspecific level.

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Section: Survival But Not Reproductive Effort Of Infected Plants Iscontrasting

confidence: 43%

Section: Plos Pathogensmentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

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Natural variation of Arabidopsis thaliana responses to Cauliflower mosaic virus infection upon water deficit

et al. 2020

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“…Perennials can suffer multi-year fitness impacts of viruses, especially viruses whose prevalence in wild communities is driven by amplification in adjacent annual cropping systems (Alexander et al, 2013; Malmstrom and Alexander, 2016; Malmstrom et al, 2017). Alternatively, known and novel viruses may contribute to the drought and heat tolerance characteristics of their hosts (Xu et al, 2008; Davis et al, 2015; Carr, 2017). Both possibilities remain underexplored for wild plants, but manipulative studies with our candidate hosts and their pathogens are now possible with the resources provided by our case study.…”

Section: Resultsmentioning

confidence: 99%

Addressing Research Needs in the Field of Plant Virus Ecology by Defining Knowledge Gaps and Developing Wild Dicot Study Systems

et al. 2019

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Viruses are ubiquitous within all habitats that support cellular life and represent the most important emerging infectious diseases of plants. Despite this, it is only recently that we have begun to describe the ecological roles of plant viruses in unmanaged systems and the influence of ecosystem properties on virus evolution. We now know that wild plants frequently harbor infections by diverse virus species, but much remains to be learned about how viruses influence host traits and how hosts influence virus evolution and vector interactions. To identify knowledge gaps and suggest avenues for alleviating research deficits, we performed a quantitative synthesis of a representative sample of virus ecology literature, developed criteria for expanding the suite of pathosystems serving as models, and applied these criteria through a case study. We found significant gaps in the types of ecological systems studied, which merit more attention. In particular, there is a strong need for a greater diversity of logistically tractable, wild dicot perennial study systems suitable for experimental manipulations of infection status. Based on criteria developed from our quantitative synthesis, we evaluated three California native dicot perennials typically found in Mediterranean-climate plant communities as candidate models: Cucurbita foetidissima (buffalo gourd), Cucurbita palmata (coyote gourd), and Datura wrightii (sacred thorn-apple). We used Illumina sequencing and network analyses to characterize viromes and viral links among species, using samples taken from multiple individuals at two different reserves. We also compared our Illumina workflow with targeted RT-PCR detection assays of varying costs. To make this process accessible to ecologists looking to incorporate virology into existing studies, we describe our approach in detail and discuss advantages and challenges of different protocols. We also provide a bioinformatics workflow based on open-access tools with graphical user interfaces. Our study provides evidence that dicot perennials in xeric habitats support multiple, asymptomatic infections by viruses known to be pathogenic in related crop hosts. Quantifying the impacts of these interactions on plant performance and virus epidemiology in our logistically tractable host systems will provide fundamental information about plant virus ecology outside of crop environments.

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“…To date, environmental conditions and plant physiological mechanisms that can lead to contrasted relationship with viruses, from mutualism to increased pathogenicity, remain poorly studied ( Roossinck, 2015 ). Few recent investigations combining abiotic and biotic stresses clearly demonstrate that in addition to factors related to the virus and plant genotype the fate of plant–virus interactions also depends on the abiotic environment ( Prasch and Sonnewald, 2013 ; Ramegowda and Senthil-Kumar, 2015 ; Fraile and García-Arenal, 2016 ; Aguilar et al, 2017 ; Carr, 2017 ). A growing body of data is uncovering the intimate entanglement of the plant physiological pathways involved in responses to various abiotic stresses and in defense against pathogens and herbivores ( Bostock, 2005 ; Pandey et al, 2015 ; Nejat et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Interactions Between Drought and Plant Genotype Change Epidemiological Traits of Cauliflower mosaic virus

et al. 2018

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Plants suffer from a broad range of abiotic and biotic stresses that do not occur in isolation but often simultaneously. Productivity of natural and agricultural systems is frequently constrained by water limitation, and the frequency and duration of drought periods will likely increase due to global climate change. In addition, phytoviruses represent highly prevalent biotic threat in wild and cultivated plant species. Several hints support a modification of epidemiological parameters of plant viruses in response to environmental changes but a clear quantification of plant–virus interactions under abiotic stresses is still lacking. Here we report the effects of a water deficit on epidemiological parameters of Cauliflower mosaic virus (CaMV), a non-circulative virus transmitted by aphid vectors, in nine natural accessions of Arabidopsis thaliana with known contrasted responses to water deficit. Plant growth-related traits and virus epidemiological parameters were evaluated in PHENOPSIS, an automated high throughput phenotyping platform. Water deficit had contrasted effects on CaMV transmission rate and viral load among A. thaliana accessions. Under well-watered conditions, transmission rate tended to increase with viral load and with CaMV virulence across accessions. Under water deficit, transmission rate and virulence were negatively correlated. Changes in the rate of transmission under water deficit were not related to changes in viral load. Our results support the idea that optimal virulence of a given virus, as hypothesized under the transmission-virulence trade-off, is highly dependent on the environment and growth traits of the host.

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Exploring how viruses enhance plants' resilience to drought and the limits to this form of viral payback

Abstract: This article comments on: Virulence determines beneficial trade-offs in the response of virus-infected plants to drought via induction of salicylic acid.

Cited by 13 publications

References 19 publications

Natural variation of Arabidopsis thaliana responses to Cauliflower mosaic virus infection upon water deficit

Natural variation of Arabidopsis thaliana responses to Cauliflower mosaic virus infection upon water deficit

Addressing Research Needs in the Field of Plant Virus Ecology by Defining Knowledge Gaps and Developing Wild Dicot Study Systems

Interactions Between Drought and Plant Genotype Change Epidemiological Traits of Cauliflower mosaic virus

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