Mechanisms of plant virus transmission by the whitefly Bemisia tabaci

The whitefly Bemisia tabaci is a group of small sap-sucking insects, which is now recognized as a cryptic species complex containing at least 35 species. During the last 30 years, the Middle East Asia Minor 1 (MEAM1) and Mediterranean (MED) species of the complex have invaded many countries worldwide with the import and export trade. With the exception of direct feeding, whiteflies harm plants mainly by transmitting plant viruses, causing huge damage to crops, vegetables and ornamental plants worldwide. Tomato yellow leaf curl viruses, cassava mosaic viruses, cotton leaf curl viruses, and tomato chlorosis virus are all transmitted by B. tabaci, and the prevalence of these viral diseases is closely related to the outbreak of these whiteflies. Currently, more than 400 species of plant viruses in five genera, i.e. Begomovirus, Crinivirus, Torradovirus, Ipomovirus and Carlavirus, are transmitted by whiteflies. Among them, begomoviruses are single-stranded DNA viruses and are exclusively transmitted by whiteflies in a persistent-circulative manner. All the others are single-stranded RNA viruses and are transmitted in a semi-persistent or non-persistent manner. Here, we summarize the interactions between B. tabaci and the plant viruses they transmit, particularly recent advances in the understanding of the molecular mechanisms underlying whitefly transmission of plant viruses. There are multiple barriers during the circulative transmission of begomoviruses within the whitefly, including the midgut barrier, hemolymph barrier, salivary gland barrier and transovarial transmission barrier. Passage of viruses through these barriers requires specific interactions between virus and whitefly components. The ability of a virus to cross the barriers within different cryptic species of B. tabaci can lead to differential transmission efficiencies. Moreover, the whitefly immune systems, such as the autophagy pathway and antimicrobial peptides, have been proved to play important roles in suppressing virus infection in B. tabaci. In addition, some whitefly and endosymbiont proteins have been identified that participate in virus circulation within whitefly, which has greatly improved our understanding of this process. However, whether begomoviruses replicate in their whitefly vector is still controversial, and further investigation is urgently needed. We also reviewed the information on the differential transmission efficiency of whitefly-transmitted RNA viruses by different species of whiteflies. However, except the verified critical role of the minor coat protein of criniviruses in virion retention and transmission, the key factors that affect the transmission of these whitefly-transmitted RNA viruses remain largely unknown. A detailed knowledge of the mechanisms underlying plant virus transmission by its whitefly vector can lead to new strategies to combat virus spread in the field. Recent advances in the sequencing of insect genomes, reverse genetic systems and genome editing technologies, such as the CRISPR/Cas9 system, may help us to further reveal the mechanisms of virus transmission and to design novel strategies that interfere with virus transmission.