Abstract
Rice gall dwarf virus (RGDV) and its leafhopper vector Recilia dorsalis are plant phloem-inhabiting pests. Currently, how the delivery of plant viruses into plant phloem via piercing-sucking insects modulates callose deposition to promote viral transmission remains poorly understood. Here, we initially demonstrated that nonviruliferous R. dorsalis preferred feeding on RGDV-infected rice plants than viruliferous counterpart. Electrical penetration graph assay showed that viruliferous R. dorsalis encountered stronger physical barriers than nonviruliferous insects during feeding, finally prolonging salivary secretion and ingestion probing. Viruliferous R. dorsalis feeding induced more defense-associated callose deposition on sieve plates of rice phloem. Furthermore, RGDV infection significantly increased the cytosolic Ca2+ level in rice plants, triggering substantial callose deposition. Such a virus-mediated insect feeding behavior change potentially impedes insects from continuously ingesting phloem sap and promotes the secretion of more infectious virions from the salivary glands into rice phloem. This is the first study demonstrating that the delivery of a phloem-limited virus by piercing-sucking insects into the plant phloem activates the defense-associated callose deposition to enhance viral transmission.
Highlights
Numerous devastating insects feeding on the phloem and viral pathogens living in the phloem cause significant economic losses in major crops
Selective preference of viruliferous or nonviruliferous R. dorsalis adults to Rice gall dwarf virus (RGDV) infected or healthy rice plants was recorded for 3 days after insect release
We observed that nonviruliferous R. dorsalis preferred to feed on RGDV-infected plants over RGDV-free rice plants from 12 h (Figure 1A)
Summary
Numerous devastating insects feeding on the phloem and viral pathogens living in the phloem cause significant economic losses in major crops. Piercing-sucking insects, including leafhoppers, planthoppers, aphids, and whiteflies, horizontally transmit viral pathogens via saliva to plant phloem (Jia et al, 2018). Leafhoppers, a large insect family with approximately 22,000 described species, transmit numerous phloem-limited plant viruses (Wang et al, 2017). Several animal-infecting viruses change the ingestion behavior of their insect vectors by increasing their biting rates. There are numerous reports on increased biting rates in mosquitoes infected with La Crosse virus, Semiliki forest virus, Rift Valley fever virus, and Dengue virus (Hurd, 2003)
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