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.

Different Plant Viruses Induce Changes in Feeding Behavior of Specialist and Generalist Aphids on Common Bean That Are Likely to Enhance Virus Transmission

“…This appears hampered, especially on virus-infected plants, and the resulting reduced phloem feeding is unfavorable to long term colonization. The ensuing dispersal to more favorable hosts would promote local vectoring of non-persistently transmitted viruses (Donnelly et al, 2019). On plants infected with any of the three viruses, A. fabae experienced mechanical stylet difficulties, whereas these difficulties did not occur on mock-inoculated plants.…”

“…For example, in cucurbits and Arabidopsis thaliana, CMV infection causes accumulation of plant metabolites that are distasteful to aphids (Mauck et al, 2010;Westwood et al, 2013). These distasteful compounds deter aphids from settling and encourage their dispersal, which will accelerate virus transmission to plants in the immediate vicinity (Donnelly et al, 2019). EPG measurements showed that aphids on CMV-infected Arabidopsis plants ingested less phloem sap, which would normally be these insects' major nutrition source and aphids confined on these plants grew less well (Westwood et al, 2013).…”

Modelling Vector Transmission and Epidemiology of Co-Infecting Plant Viruses

“…Moreover, it is well known [10,39,40] that vector-implicit models may reasonably approximate vector-explicit models when vector dynamics can be considered to be fast with respect to epidemiological dynamics in the plant host population (such as in non-persistent transmission). Although see [41] for a different model of non-persistent transmission of viruses that goes beyond differential equations to track the epidemiological effects of vector dynamics.…”

Cucumber mosaic virus 2b proteins inhibit virus‐induced aphid resistance in tobacco

“…Viruses alter interactions between plants and insect vectors in ways that may promote virus transmission, or which may foster persistence and spread of vectors in the environment (Casteel et al ., , ; Donnelly et al , ; Groen et al , ; Mauck, ). The effects of CMV on plant–aphid interactions are not the same for all plant hosts.…”