Abstract
Asaia is a bacterial symbiont of sugar-feeding insects that has been shown to be vertically transmitted by maternal transmission and paternal transmission mechanism, and to be horizontally transmitted via co-feeding artificial diet and venereal routes. Here, the first case of plant-mediated horizontal transmission of Asaia between white-backed planthoppers (WBPH), Sogatella furcifera, was reported. In Asaia-infected WBPH, Asaia was detected mostly in salivary glands and to a less extent in stylets. The rice leaf sheaths fed by Asaia-infected WBPH for 12 h were all positive with Asaia, where Asaia persisted for at least 30 d but was localized in the feeding sites only. When confined to Asaia-infected leaf sheaths for 7 d at the sites pre-infested by the Asaia-infected WBPH, all Asaia-free WBPH became infected with Asaia and the acquired Asaia could be vertically transmitted to their offspring. Phylogenetic analysis confirmed an identical Asaia strain in the Asaia-infected donor WBPH, the Asaia-infected leaf sheaths, and the newly infected recipient WBPH. Our findings provide direct evidence for the first time that rice plant can mediate horizontal transmission of Asaia between WBPH, which may contribute to the spread of Asaia in the field WBPH populations.
Highlights
With quantitative real-time PCR (qPCR), it is obvious that Asaia density in leaf sheaths increased with the prolonged feeding by the Asaiainfected white-backed planthoppers (WBPH), in a pattern similar to an exponential increase (Figure 2B)
Our fluorescence in situ hybridization (FISH) visualization results showed Asaia in the salivary glands and stylets of the Asaia-infected donor WBPH (Figures 3A,B) and in the guts of the newly infected recipient WBPH (Figure 3C), which is consistent with Asaia localization in mosquitoes and leafhopper (Favia et al, 2007; Crotti et al, 2009; Gonella et al, 2012), and in the leaf sheaths infested by the Asaia-infected donor WBPH (Figures 3D,E)
It is certain that plant-mediated horizontal transmission of Asaia does occur: Asaia harbored in the salivary glands of the Asaia-infected WBPH are injected with saliva via the stylet into the leaf sheaths, producing Asaia-infected rice plants; the Asaia therein are ingested via the stylet into the gut of the recipient WBPH when they feed on the feeding sites of the Asaia-infected WBPH (Figure 1)
Summary
Given the increasing evidence of symbionts’ functions in the interactions among host insects, their host plants and the environment (Oliver et al, 2010), it is crucial to know how the symbionts are transmitted. Symbionts can be transmitted vertically and/or horizontally (Chiel et al, 2009; Chrostek et al, 2017). Vertical transmission occurs in many insect symbionts (Hosokawa et al, 2007), while horizontal transmission exists in some symbionts (Oliver et al, 2010), which can be realized through parasitism, predation, mating, and feeding (Chiel et al, 2009; Gonella et al, 2015). The feeding route occurs in insects co-feeding on host plant, such as the transmission of Hamiltonella defensa in Sitobion miscanthi (Li et al, 2018), Serratia symbiotica in Acyrthosiphon pisum and Aphis
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