Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem.

Qian Chen,Manni Chen,Dongsheng Jia,Jiping Ren,Panpan Zhong,Yuyan Liu,Taiyun Wei,Hongyan Chen

doi:10.7554/elife.64603

Abstract

Numerous piercing-sucking insects can horizontally transmit viral pathogens together with saliva to plant phloem, but the mechanism remains elusive. Here, we report that an important rice reovirus has hijacked small vesicles, referred to as exosomes, to traverse the apical plasmalemma into saliva-stored cavities in the salivary glands of leafhopper vectors. Thus, virions were horizontally transmitted with exosomes into rice phloem to establish the initial plant infection during vector feeding. The purified exosomes secreted from cultured leafhopper cells were enriched with virions. Silencing the exosomal secretion-related small GTPase Rab27a or treatment with the exosomal biogenesis inhibitor GW4869 strongly prevented viral exosomal release in vivo and in vitro. Furthermore, the specific interaction of the 15-nm-long domain of the viral outer capsid protein with Rab5 induced the packaging of virions in exosomes, ultimately activating the Rab27a-dependent exosomal release pathway. We thus anticipate that exosome-mediated viral horizontal transmission is the conserved strategy hijacked by vector-borne viruses.

Highlights

Many devastating plant, animal, and human viral pathogens are horizontally transmitted by arthropod insects (Eigenbrode et al, 2018; Mayer et al, 2017)
DsRab27a treatment significantly decreased the ability of viruliferous leafhoppers to transmit viruses to rice plants (Figure 3E). These results indicate that the exosomal release of viruses into salivary cavities is greatly impaired by the knockdown of Rab27a expression in leafhoppers, which significantly suppresses the horizontal transmission of Rice dwarf virus (RDV) from insect salivary glands to rice plants
RDV is secreted from cultured insect vector cells via the exosomal release pathway Previously, we demonstrated that multivesicular bodies (MVBs) were involved in the exosomal release of RDV particles from infected cultured leafhopper cells (Wei et al, 2009)

Summary

Introduction

Animal, and human viral pathogens are horizontally transmitted by arthropod insects (Eigenbrode et al, 2018; Mayer et al, 2017). Arthropod-borne viruses (arboviruses) establish their initial infection in the insect midgut, which is disseminated to the hemolymph and spread into the salivary glands, from which virions are introduced into susceptible hosts together with saliva (Hogenhout et al, 2008; Wei and Li, 2016). Insect salivary gland cells are filled with abundant apical plasmalemma-lined cavities, where saliva is stored (Mao et al, 2017; Wei and Li, 2016). Arboviruses have to pass through the apical plasmalemma into insect salivary cavities, thereby moving with salivary flow to establish the initial infection in hosts (Mayer et al, 2017; Wei and Li, 2016). How arboviruses overcome cavity plasmalemma barriers for successful viral transmission is still poorly understood

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