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Plant-mediated interactions between a vector and a non-vector herbivore promote the spread of a plant virus.

ABSTRACT: Herbivores that transmit plant pathogens often share hosts with non-vector herbivores. These co-occurring herbivores can affect vector fitness and behaviour through competition and by altering host plant quality. However, few studies have examined how such interactions may both directly and indirectly influence the spread of a plant pathogen. Here, we conducted field and greenhouse trials to assess whether a defoliating herbivore (Sitona lineatus) mediated the spread of a plant pathogen, Pea enation mosaic virus (PEMV), by affecting the fitness and behaviour of Acrythosiphon pisum, the PEMV vector. We observed higher rates of PEMV spread when infectious A. pisum individuals shared hosts with S. lineatus individuals. Using structural equation models, we showed that herbivory from S. lineatus increased A. pisum fitness, which stimulated vector movement and PEMV spread. Moreover, plant susceptibility to PEMV was indirectly enhanced by S. lineatus, which displaced A. pisum individuals to the most susceptible parts of the plant. Subsequent analyses of plant defence genes revealed considerable differences in plant phytohormones associated with anti-herbivore and anti-pathogen defence when S. lineatus was present. Given that vectors interact with non-vector herbivores in natural and managed ecosystems, characterizing how such interactions affect pathogens would greatly enhance our understanding of disease ecology.

SUBMITTER: Chisholm PJ

PROVIDER: S-EPMC6784723 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Plant-mediated interactions between a vector and a non-vector herbivore promote the spread of a plant virus.

Chisholm Paul J PJ Eigenbrode Sanford D SD Clark Robert E RE Basu Saumik S Crowder David W DW

Proceedings. Biological sciences 20190925 1911

Herbivores that transmit plant pathogens often share hosts with non-vector herbivores. These co-occurring herbivores can affect vector fitness and behaviour through competition and by altering host plant quality. However, few studies have examined how such interactions may both directly and indirectly influence the spread of a plant pathogen. Here, we conducted field and greenhouse trials to assess whether a defoliating herbivore (<i>Sitona lineatus</i>) mediated the spread of a plant pathogen, ...[more]

PMID: 31551062

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Project description:Rice black-streaked dwarf virus (RBSDV) (species Rice black-streaked dwarf virus, genus Fijivirus, family Reoviridae) is the causal agent of rice black-streaked dwarf and maize rough dwarf diseases, which occur in intermittent epidemics in East Asian countries and are responsible for considerable yield losses. Intermittency of epidemics make accurate forecasting and designing of effective management strategies difficult. However, recent insights into host-virus-vector insect interactions are now informing forecasting and disease control measures. Resistance genes are also being identified and mapped.Symptomatology and host rangeRBSDV induces extreme stunting, darkened, and stiff leaves of crops and weeds only in the family Poaceae, including Oryza sativa, Zea mays, and Triticum aestivum. Infected plants produce totally or partially deformed panicles and remain alive through harvest.Genome and gene functionThe nonenveloped virus particles comprise a double-layered capsid, 50-nm core with genomic double-stranded RNA (dsRNA), and six proteins. The genome of RBSDV contains 10 segments of dsRNA, named S1 to S10 in decreasing order of molecular weight. Segments 1, 2, 3, 4, 6, 8, and 10 encode the RNA-dependent RNA polymerase (RdRp), the major core structural protein, a protein with guanylyltransferase activity, an outer-shell B-spike protein, viral RNA-silencing suppressor, the major capsid protein, and the outer capsid protein, respectively. Each of the segments 5, 7, and 9 encodes two proteins: P5-1, a component of viroplasms; P5-2 of unknown function; nonstructural protein P7-1, involved in forming the structural matrix of tubular structures in infected tissues; P7-2 of unknown function; P9-1, the main component of viroplasms in infected cells and involved in viral replication; and P9-2 of unknown function.Transmission and epidemiologyRBSDV is transmitted by Laodelphax striatellus in a persistent propagative manner. The vector insect is the only means of virus spread in nature, so its migration and transmission efficiency are obligatory for disease epidemics to develop. Susceptible varieties are widely planted, but efficient transmission by vectors is the primary reason for the epidemics. Cultivation system, pesticide overuse, and climatic conditions also contribute to epidemics by affecting the development of the vector insects and their population dynamics.Disease managementIn the absence of resistant varieties, integrated disease management aims at disrupting the cycle of virus transmission by the insect vector. Inheritance studies have indicated that resistance is mostly governed by quantitative trait loci or multiple genes. Genetic engineering through RNA-interference and gene-editing strategies are potential approaches for disease control.

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Plant-mediated interactions between a vector and a non-vector herbivore promote the spread of a plant virus.

Publications

Plant-mediated interactions between a vector and a non-vector herbivore promote the spread of a plant virus.

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