Effects of single and mixed infections of Bean pod mottle virus and Soybean mosaic virus on host‐plant chemistry and host–vector interactions

Abstract

Summary Co‐infection by vector‐borne plant viruses is common, yet few studies have explored the effects of mixed infections on host‐plant phenotypes or plant–vector interactions. We documented the effects of single and mixed infection by Bean pod mottle virus (BPMV) and Soybean mosaic virus (SMV) on key biochemical plant traits and the behaviour and performance of virus vectors (BPMV: Epilachna varivestis, SMV: Aphis glycines) in order to understand how virus‐induced changes in plant phenotypes might influence (i) the acquisition and transmission of each virus by its respective vector in single infections, (ii) the likelihood of secondary infection for plants singly infected with either virus and (iii) the implications of co‐infection for virus transmission by vectors. Single infection by either BPMV or SMV increased host‐plant palatability for E. varivestis, potentially enhancing vector acquisition of BPMV from BPMV‐infected plants as well as the risk of secondary BPMV infection in plants infected with SMV. However, co‐infected plants were no more palatable to beetle vectors than mock‐inoculated plants. BPMV infection had minimal impacts on A. glycines. SMV infection reduced A. glycines population growth, but increased aphid feeding preferences for infected plants, a pattern likely not conducive to the (non‐persistent) transmission of SMV. Co‐infection eliminated the negative effects of single SMV infection on aphid population growth, and aphids exhibited a feeding preference for co‐infected (relative to mock‐inoculated) plants. Our results demonstrate that virus effects on host phenotype and vector behaviour can be modified by the presence of a co‐infecting virus, with potentially important implications for disease transmission.

The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores

“…Additional areas of microbe-plant-herbivore interactions that deserve more attention in future work are plant associations with multiple beneficial and/or pathogenic microbes, as well as the influences of insect-associated microbial symbionts. As discussed above, a recent study determined that co-infections or co-associations of multiple microbe species within a host plant are likely to affect the outcomes of herbivore foraging [110]. Additionally, although outside the scope of this review, insect herbivores often rely on microbial symbionts to overcome host-plant defenses [175], obtain nutrients [176], or biosynthesize nutrients the insect needs but the plant does not provide [177].…”

“…The vector of SMV, soybean aphid, was more attracted to SMV-infected, but not BPMV-infected plants, compared to healthy plants. This was correlated with lower levels of defense-related phytohormones (e.g., jasmonic acid) produced by SMV-infected and BPMV+SMV co-infected plants, altering plant attractiveness in a virus and vector-specific manner [110]. Although this is a single example, plant-pathogen co-infection is also likely to modify plant gustatory cues in other pathosystems and influence pathogen transmission dynamics.…”

Soybean mosaic virus: a successful potyvirus with a wide distribution but restricted natural host range

“…Although A. glycines is capable of transmitting SMV experimentally (Clark and Perry, 2002;Hill et al, 2001), it is a poor vector in the field (Wang and Ghabrial, 2002). The growth rates of A. glycines on SMV-infected plants are often significantly lower than on healthy soybean plants (Cassone et al, 2015;Donaldson and Gratton, 2007;Penaflor et al, 2016). SMV isolates can differ significantly in their rates of transmission by a single aphid species Lucas and Hill, 1980;O'Connell Ziegler et al, 1986).…”

Modelling Vector Transmission and Epidemiology of Co-Infecting Plant Viruses

“…There are many examples of two co-infecting virus species with a shared vector species [24][25][26]. Similarly, there are many cases where two co-infecting viruses have quite different vectors taxonomically [27]. Co-infection is manifested in more complex situations with multiple viruses and vectors such as with grapevine leafroll disease [28,29] and sweet potato virus disease (SPVD) [30].…”