Competition within susceptible hosts drives differential transmission of pathogen genotypes

Background/Question/Methods

Co-infections with multiple pathogens are common in many disease systems of humans, other animals, and plants, inevitably leading to interactions between pathogens during transmission. Closely related pathogens will exist in the same niche, competing for the same resources and being similarly affected by a particular host defense, and therefore may not co-occur within a host as readily as more distantly related pathogens. Empirical studies have found both increased and decreased cross immunity with increased pathogen relatedness. We tested interactions between two genetically distinct variants of the viral pathogen Grapevine leafroll-associated virus-3 (GLRaV-3, family Closteroviridae, genus Ampelovirus) during vector transmission to an uninfected host. GLRaV-3 is only known to affect Vitis spp. (grapes), and is the primary virus species that causes grapevine leafroll disease, which affects crop quality worldwide. Co-infections of genetically distinct variants within a single host plant are common. GLRaV-3 is transmitted by several species of mealybugs (Hemiptera, Pseudococcidae) in a semi-persistent manner. Through several linked experiments using varied acquisition and inoculation access periods, we tested each variant’s transmission, the effects of two different vector species, the effects of a co-infected source, and the effects of simultaneous inoculation from multiple hosts to one susceptible host. 

Results/Conclusions

Transmission increased as acquisition access period increased from two to twenty-four hours, but not as inoculation access period increased. The invasive Planococcus ficus (vine mealybug) was a more efficient vector than the longer established Pseudococcus viburni (obscure mealybug). Transmission of the two genetically distinct variants (GLRaV-3-I and GLRaV-3-VI) did not differ from each other in single variant inoculations by either vector species. Overall GLRaV-3 transmission was the same whether from singly infected or co-infected source plants. From co-infected sources, however, GLRaV-3-VI was transmitted more than GLRaV-3-I, indicating competitive superiority. Mixed variant inoculations from singly infected source plants to one uninfected plant also resulted in higher transmission of GLRaV-3-VI than GLRaV-3-I. The stronger effect of acquisition relative to inoculation access period is consistent with previous studies. The current expansion in California of the efficient vector Pl. ficus could lead to increased GLRaV-3 spread. Our results indicate that the outcome of the interaction between the two virus variants was determined subsequent to inoculation of a susceptible plant, rather than within the insect vector. At low pathogen incidence, we expect GLRaV-3-I and GLRaV-3-VI to have similar prevalence, but as pathogen incidence and the opportunity for mixed infections increase, GLRaV-3-VI would become more prevalent.