title: Specific cells in the primary salivary glands of the whitefly Bemisia tabaci control retention and transmission of begomoviruses.
abstract: The majority of plant viruses are vectored by arthropods via persistent-circulative or noncirculative transmission. Previous studies have shown that specific binding sites for noncirculative viruses reside within the stylet or foregut of insect vectors, whereas the transmission mechanisms of circulative viruses remain ambiguous. Here we report the critical roles of whitefly primary salivary glands (PSGs) in the circulative transmission of two begomoviruses. The Middle East Asia Minor 1 (MEAM1) species of the whitefly Bemisia tabaci complex efficiently transmits both Tomato yellow leaf curl China virus (TYLCCNV) and Tomato yellow leaf curl virus (TYLCV), whereas the Mediterranean (MED) species transmits TYLCV but not TYLCCNV. PCR and fluorescence in situ hybridization experiments showed that TYLCCNV efficiently penetrates the PSGs of MEAM1 but not MED whiteflies. When a fragment of the coat protein of TYLCCNV was exchanged with that of TYLCV, mutated TYLCCNV accumulated in the PSGs of MED whiteflies, while mutant TYLCV was nearly undetectable. Confocal microscopy revealed that virion transport in PSGs follows specific paths to reach secretory cells in the central region, and the accumulation of virions in the secretory region of PSGs was correlated with successful virus transmission. Our findings demonstrate that whitefly PSGs, in particular the cells around the secretory region, control the specificity of begomovirus transmission.
  
  
  OBJECTIVE
  Over 75% of plant viruses are transmitted by insects. However, the mechanisms of virus transmission by insect vectors remain largely unknown. Begomoviruses and whiteflies are a complex of viruses and vectors which threaten many crops worldwide. We investigated the transmission of two begomoviruses by two whitefly species. We show that specific cells of the whitefly primary salivary glands control viral transmission specificity and that virion transport in the glands follows specific paths to reach secretory cells in the central region and then to reach the salivary duct. Our results indicate that the secretory cells in the central region of primary salivary glands determine the recognition and transmission of begomoviruses. These findings set a foundation for future research not only on circulative plant virus transmission but also on other human and animal viruses transmitted by arthropod vectors.
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, China.
authors.forename: Jing
authors.initials: J
authors.lastname: Wei
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, China.
authors.forename: Juan-Juan
authors.initials: JJ
authors.lastname: Zhao
authors.affiliation: Institute of Biotechnology, Zhejiang University, Hangzhou, China.
authors.forename: Tong
authors.initials: T
authors.lastname: Zhang
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, China.
authors.forename: Fang-Fang
authors.initials: FF
authors.lastname: Li
authors.affiliation: Department of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel.
authors.forename: Murad
authors.initials: M
authors.lastname: Ghanim
authors.affiliation: Institute of Biotechnology, Zhejiang University, Hangzhou, China.
authors.forename: Xue-Ping
authors.initials: XP
authors.lastname: Zhou
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, China.
authors.forename: Gong-Yin
authors.initials: GY
authors.lastname: Ye
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, China shshliu@zju.edu.cn xwwang@zju.edu.cn.
authors.forename: Shu-Sheng
authors.initials: SS
authors.lastname: Liu
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, China shshliu@zju.edu.cn xwwang@zju.edu.cn.
authors.forename: Xiao-Wei
authors.initials: XW
authors.lastname: Wang
mesh_terms: D000818:Animals; D053839:Begomovirus / Q000502:physiology*; D005260:Female; D006430:Hemiptera / Q000821:virology*; D017404:In Situ Hybridization, Fluorescence; D018613:Microscopy, Confocal; D010935:Plant Diseases / Q000821:virology*; D010942:Plant Viruses / Q000502:physiology*; D016133:Polymerase Chain Reaction; D012469:Salivary Glands / Q000821:virology*; D014777:Virus Diseases / Q000635:transmission*