Plant-Mediated Horizontal Transmission of Hamiltonella defensa in the Wheat Aphid Sitobion miscanthi

Hamiltonella defensa is mainly vertically transmitted, but evidence suggests that horizontal transmission may occur. Here, the first case of plant-mediated horizontal transmission of H. defensa between wheat aphids, Sitobion miscanthi, was reported. H. defensa was harbored in sheath cells, secondary bacteriocytes, and hemolymph. After Hamiltonella-infected aphids fed on wheat leaves, H. defensa was observed in aphid stylets and plant phloem. H. defensa persisted in wheat leaves for at least 10 days. Most Hamiltonella-uninfected aphids became infected with H. defensa after sustained feeding on infected plant leaves and showed almost 100% stable vertical transmission over the next five generations. These horizontal transmission experiments were replicated using two other plants, rice and corn, and two different wheat aphid species, Rhopalosiphum padi and Schizaphis graminum. Surprisingly, aphid feeding induced plant infection only locally rather than systemically in leaves. Our findings indicate that plants may act as horizontal transmission intermediaries, contributing to the ubiquity of the otherwise maternally inherited H. defensa.