Outcomes of co-infection by two potyviruses: implications for the evolution of manipulative strategies

Abstract

Recent studies have documented effects of plant viruses on host plants that appear to enhance transmission by insect vectors. But, almost no empirical work has explored the implications of such apparent manipulation for interactions among co-infecting pathogens. We examined single and mixed infections of two potyviruses, watermelon mosaic virus (WMV) and zucchini yellow mosaic virus (ZYMV), that frequently co-occur in cucurbitaceae populations and share the same aphid vectors. We found that ZYMV isolates replicated at similar rates in single and mixed infections, whereas WMV strains accumulated to significantly lower levels in the presence of ZYMV. Furthermore, ZYMV induced changes in leaf colour and volatile emissions that enhanced aphid (Aphis gossypii) recruitment to infected plants. By contrast, WMV did not elicit strong effects on plant-aphid interactions. Nevertheless, WMV was still readily transmitted from mixed infections, despite fairing poorly in in-plant competition. These findings suggest that pathogen effects on host-vector interactions may well influence competition among co-infecting pathogens. For example, if non-manipulative pathogens benefit from the increased vector traffic elicited by manipulative competitors, their costs of competition may be mitigated to some extent. Conversely, the benefits of manipulation may be limited by free-rider effects in systems where there is strong competition among pathogens for host resources and/or access to vectors.

Interactions Within Susceptible Hosts Drive Establishment of Genetically Distinct Variants of an Insect-Borne Pathogen

“…Different lowercase letters would indicate differences in overall transmission of GLRaV-3 (I, VI, or both) from source plants infected with different combinations of genetically distinct variants of single source plant with a mixed infection have either concluded that the outcome was due to virus interactions within the vector, or did not discern whether the outcome was determined within vector or susceptible host. Leaf-rub inoculations introduce a much larger quantity of virus than vector-mediated inoculations (Srinivasan et al 2012, Salvaudon et al 2013, Péréfarres et al 2014), and may consequently overpower possible effects of host defenses; therefore, comparing leaf-rub and vector inoculations might lead to erroneous conclusions about the effect of insect vectors on virus establishment in a new host plant (Moury et al 2007, Péréfarres et al 2014). In our study, the signature of superiority of one variant over another was actually stronger when competition within the vector was eliminated, by transferring vectors from each of two singly infected source plants to one uninfected test plant, suggesting that virus-virus interactions during establishment in a new host plant may be more important than interactions within the vector.…”

“…Vectors can affect the differential transmission of plant pathogens and consequent disease spread (Srinivasan et al 2012, Salvaudon et al 2013. In some cases, a pathogen already present at low prevalence can become widespread after a new more effective vector is introduced (Purcell and Feil 2001), or after adaptation by a pathogen to a vector that is already present (Tsetsarkin et al 2011).…”

Incidence of viruses and virus-like diseases of watermelons and pumpkins in Uganda, a hitherto none-investigated pathosystem

“…Dual CMV+WMV and triple CMV+WMV+ZYMV were the most common mixed infections. It is expected that viruses transmitted by a common vector to the same host should depict higher frequencies of mixed infections than those transmitted by different vector agents (Opiyo et al, 2010;Salvaudon et al, 2013;Tugume et al, 2016;Tollenaere et al, 2016). Because all the viruses under this study are known to be aphid-borne (Lecoq and Desbiez, 2012), and their selection for assay was pre-determined, observed differences in single/mixed infections might be a reflection of variable transmission efficiencies, aphid populations, and/or host preferences by the aphid vectors.…”

Biological and molecular events associated with simultaneous transmission of plant viruses by invertebrate and fungal vectors

“…In this respect, this finding is consistent with that reported by Salvaudon et al . (), at the same time giving no support to the common opinion on the positive correlation between virus accumulation in the plant and the rate of its transmission by aphids.…”

“…Interestingly, contrasting results have been obtained recently with another potyvirus, Sweet potato feathery mottle virus (SPFMV), which was transmitted by A. gossypii at a greater rate from plants co‐infected with Sweet potato virus G (SPVG; also potyvirus) than from singly infected plants (Wosula et al ., ). However, the results of the most recent study (Salvaudon et al ., ) show that, even within the same viral genus ( Potyvirus ), diverse outcomes of within‐plant interactions between viruses can be observed, depending on the species of the competing viruses. Isolates of closely related Watermelon mosaic virus (WMV) and ZYMV were transmitted by A. gossypii at generally greater rates from singly infected plants (80% and 40%, respectively) than from co‐infected plants (20%, as a total for co‐infections).…”