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Pathogenic modification of plants enhances long-distance dispersal of nonpersistently transmitted viruses to new hosts.

ABSTRACT: Aphids spread the majority of plant viruses through nonpersistent transmission (NPT), whereby virus particles attach transiently to these insects' probing mouthparts. Virus acquisition from infected plants and inoculation to healthy host plants is favored when aphids briefly probe plant epidermal cells. It is well established that NPT virus infection can alter plant-vector interactions, and, moreover, such pathogen modifications are found in a range of plant and animal systems. In particular, viruses can make plants more attractive to aphids but inhibit aphid settling on infected plants. It is hypothesized that this viral "reprogramming" of plants promotes virus acquisition and encourages dispersal of virus-bearing aphids to fresh hosts. In contrast, it is hypothesized that virus-induced biochemical changes encouraging prolonged feeding on infected hosts inhibit NPT. To understand how these virus-induced modifications affect epidemics, we developed a modeling framework accounting for important but often neglected factors, including feeding behaviors (probing or prolonged feeding) and distinct spatial scales of transmission (as conditioned by wingless or winged aphids). Analysis of our models confirmed that when viruses inhibit aphid settling on infected plants this initially promotes virus transmission. However, initially enhanced transmission is self-limiting because it decreases vector density. Another important finding is that virus-induced changes encouraging settling will stimulate birth of winged aphids, which promotes epidemics of NPT viruses over greater distances. Thus our results illustrate how plant virus modifications influence epidemics by altering vector distribution, density, and even vector form. Our insights are important for understanding how pathogens in general propagate through natural plant communities and crops.

SUBMITTER: Donnelly R

PROVIDER: S-EPMC6619343 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Pathogenic modification of plants enhances long-distance dispersal of nonpersistently transmitted viruses to new hosts.

Donnelly Ruairí R Cunniffe Nik J NJ Carr John P JP Gilligan Christopher A CA

Ecology 20190521 7

Aphids spread the majority of plant viruses through nonpersistent transmission (NPT), whereby virus particles attach transiently to these insects' probing mouthparts. Virus acquisition from infected plants and inoculation to healthy host plants is favored when aphids briefly probe plant epidermal cells. It is well established that NPT virus infection can alter plant-vector interactions, and, moreover, such pathogen modifications are found in a range of plant and animal systems. In particular, vi ...[more]

PMID: 30980528

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Project description:Introduction:Alliaria petiolata, an herbaceous plant, has invaded woodlands in North America. Its ecology has been thoroughly studied, but an overlooked aspect of its biology is seed dispersal distances and mechanisms. We measured seed dispersal distances in the field and tested if epizoochory is a potential mechanism for long-distance seed dispersal. Methods:Dispersal distances were measured by placing seed traps in a sector design around three seed point sources, which consisted of 15 second-year plants transplanted within a 0.25 m radius circle. Traps were placed at intervals ranging from 0.25-3.25 m from the point source. Traps remained in the field until a majority of seeds were dispersed. Eight probability density functions were fitted to seed trap counts via maximum likelihood. Epizoochory was tested as a potential seed dispersal mechanism for A. petiolata through a combination of field and laboratory experiments. To test if small mammals transport A. petiolata seeds in their fur, experimental blocks were placed around dense A. petiolata patches. Each block contained a mammal inclusion treatment (MIT) and control. The MIT consisted of a wood-frame (31 × 61× 31 cm) covered in wire mesh, except for the two 31 × 31 cm ends, placed over a germination tray filled with potting soil. A pan filled with bait was placed in the center of the tray. The control frame (11 × 31 × 61 cm) was placed over a germination tray and completely covered in wire mesh to exclude animal activity. Treatments were in the field for peak seed dispersal. In March, trays were moved to a greenhouse and A. petiolata seedlings were counted and then compared between treatments. To determine if A. petiolata seeds attach to raccoon (Procyon lotor) and white-tailed deer (Odocoileus virginianus) fur, wet and dry seeds were dropped onto wet and dry fur. Furs were rotated 180 degrees and the seeds that remained attached were counted. To measure seed retention, seeds were dropped on furs and rotated as before, then the furs were agitated for one hour. The seeds retained in the fur were counted. Results:For the seed dispersal experiment, the 2Dt function provided the best fit and was the most biologically meaningful. It predicted that seed density rapidly declined with distance from the point source. Mean dispersal distance was 0.52 m and 95% of seeds dispersed within 1.14 m. The epizoochory field experiment showed increased mammal activity and A. petiolata seedlings in germination trays of the MIT compared to control. Laboratory studies showed 3-26% of seeds were attached and retained by raccoon and deer fur. Retention significantly increased if either seed or fur were wet (57-98%). Discussion:Without animal seed vectors, most seeds fall within a short distance of the seed source; however, long distance dispersal may be accomplished by epizoochory. Our data are consistent with A. petiolata's widespread distribution and development of dense clusters of the species in invaded areas.

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Pathogenic modification of plants enhances long-distance dispersal of nonpersistently transmitted viruses to new hosts.

Publications

Pathogenic modification of plants enhances long-distance dispersal of nonpersistently transmitted viruses to new hosts.

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