A vector whitefly endocytic receptor facilitates the entry of begomoviruses into its midgut cells via binding to virion capsid proteins.

Jing Zhao,Tian-Yan Yin,Shu-Sheng Liu,Teng Lei,Xin-Jia Zhang,Xiao-Wei Wang,Aiming Wang

doi:10.1371/journal.ppat.1009053

Abstract

Many circulative plant viruses transmitted by insect vectors are devastating to agriculture worldwide. The midgut wall of vector insects represents a major barrier and at the same time the key gate a circulative plant virus must cross for productive transmission. However, how these viruses enter insect midgut cells remains poorly understood. Here, we identified an endocytic receptor complex for begomoviruses in the midgut cells of their whitefly vector. Our results show that two whitefly proteins, BtCUBN and BtAMN, compose a receptor complex BtCubam, for which BtCUBN contributes a viral-binding region and BtAMN contributes to membrane anchorage. Begomoviruses appear to be internalized together with BtCubam via its interaction with the 12–19 CUB domains of BtCUBN via clathrin-dependent endocytosis. Functional analysis indicates that interruption of BtCUBN and BtAMN lead to reduction of virus acquisition and transmission by whitefly. In contrast, CUBN-begomovirus interaction was not observed in two non-competent whitefly-begomovirus combinations. These observations suggest a major role of the specific endocytic receptor in facilitating viral entry into vector midgut cells.

Highlights

Plant viruses make up about half of the agents of emerging infectious plant diseases [1,2,3]
Following ingestion by insect vectors, many viruses need to circulate in the vector via a sequential path of stylet-midgut-haemolymph-salivary glands and are inoculated into plants with saliva secretion
A group of plant viruses of economic significance worldwide, and their insect vectors, the whiteflies of the Bemisia tabaci complex, we found that upon virus infection, two vector proteins, cubilin (CUBN) and amnionless (AMN), form a virus receptor complex to uptake the virions and assist them

Summary

Introduction

Plant viruses make up about half of the agents of emerging infectious plant diseases [1,2,3]. Non-circulative plant viruses are retained in the stylet, food canal or foregut of their insect vectors and transmitted to plant hosts on which the vectors probe/feed [5,6,7]. Circulative plant viruses move through a sequential path of stylet-midgut-haemolymph-salivary glands in their vectors and are inoculated into plants with saliva secretion [8]. Circulative viruses face four major challenges in movement within the vector: midgut invasion, midgut escape, salivary glands invasion and salivary glands escape [8,9]. Midgut cells represent the first cellular barrier to the viruses. Dissection of the cellular components involved in virus translocation from midgut lumen into midgut cells represents a critical step in advancing our understanding of virus-vector interactions

Results

Discussion

Conclusion