Delivery of Rice Gall Dwarf Virus Into Plant Phloem by Its Leafhopper Vectors Activates Callose Deposition to Enhance Viral Transmission

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.

Plant and insect virus‐like particles: emerging nanoparticles for agricultural pest management

“…137 Rice dwarf virus (RDV) and rice gall dwarf virus (RGDV) belong to the genus of Phytoreovirus, have high similarity in viral structure and components 138,139 and can spread by rice leafhopper vectors after infection in a circulative and propagative manner. 121,140,141 Moreover, to our knowledge, they are the only two plant reoviruses developed for VLP production. The inner core of their capsid is composed of four structural proteins (P1, P3, P5 and P7) and the outer shell of two structural proteins (P2 and P8) that become assembled through electrostatic interactions between charged side chains.…”

Rice Gall Dwarf Virus Promotes the Propagation and Transmission of Rice Stripe Mosaic Virus by Co-infected Insect Vectors

“…We then clarify the effects of rice plants infected with different viruses on R. dorsalis feeding tendency. A glass Y-tube olfactometer was applied to test plant odor selection preference of R. dorsalis following the method described by Signoretti et al (2012) and Yi et al (2021), with minor modifications. Briefly, The Y-shaped tube (4-cm inner diameter) comprised a central tube (10 cm long) and two arms (18 cm long, offset by 75°) connected to bags containing a living plant each.…”

“…We then used EPG analysis to investigate the effects of viral co-infection on insect feeding behavior. The EPG records were obtained using a DC-monitor, GIGA-8 model as described previously (Yi et al, 2021). Briefly, the healthy, RSMV-infected, RGDV-infected, or co-infected rice seedlings were planted into soil-filled plastic pots.…”

Plant Arbovirus Mobilizes a Vector Salivary Protein to Initiate Plant Infection

“…The latter is secreted into the phloem sieve elements to prevent them from plugging up, suppresses plant defense responses, induces pattern-triggered immunity (PTI) through herbivore-associated molecular patterns (HAMPs), and induces effector-triggered immunity (ETI) through avirulent gene, etc. (Huang, Liu, Xu, Bao, & Zhang, 2017;Ji et al, 2017;Yi, Wu, & Wei, 2021).…”