Endosymbionts affect plant virus transmission by winged and wingless aphids

Vector-borne pathogens frequently modify host-vector interactions, and their influence can be modulated by other microbial symbionts. We recently documented endosymbiont effects on aphid traits involved in plant virus transmission, showing that facultative endobacteria-particularly Hamiltonella defensa-enhanced transmission of pea enation mosaic virus. Here, we examine transmission steps and associated molecular signatures in winged and wingless aphid morphs. Consistent with our previous findings, we observed enhanced pea enation mosaic virus transmission, as well as elevated viral titer in wingless aphids harboring H. defensa. However, winged aphids with this endosymbiont displayed similar effects on virus titer but not transmission. Furthermore, whereas wingless aphids exhibited higher transmission than winged aphids when H. defensa was present, this pattern was reversed for aphids harboring only the obligate endosymbiont Buchnera aphidicola; in parallel, we observed no differences between morphs of lines harboring other facultative endosymbionts. Subsequent experiments comparing lines harboring H. defensa versus the obligate symbiont alone revealed divergent effects on winged and wingless morphs on (i) virus inoculation efficiency (i.e., delivery of acquired virus; H. defensa), (ii) key salivary proteins (carbonic anhydrases, CAs; both lines), and (iii) plant defense-related marker transcripts (PR-1, salicylic acid pathway; LOX, jasmonic acid pathway; both lines). The correspondence of these patterns to the observed transmission effects suggests that endosymbiont-mediated effects on transmission may reflect changes in salivary secretions and related feeding traits. Our findings highlight the role of vector endosymbionts in disease transmission and provide insights into candidate processes by which they may influence virus-vector-host interactions.