Vector development and vitellogenin determine the transovarial transmission of begomoviruses

Abstract

The majority of plant viruses are transmitted by insect vectors between hosts, and transovarial transmission of viruses from vector parents to offspring has great significance to their epidemiology. Begomoviruses are transmitted by the whitefly Bemisia tabaci in a circulative manner and are maintained through a plantinsect-plant cycle. Other routes of begomovirus transmission are not clearly known. Here, we report that transovarial transmission from female whiteflies to offspring often happens for one begomovirus, Tomato yellow leaf curl virus (TYLCV), and may have contributed significantly to its global spread. We found that TYLCV entry of the reproductive organ of its vector mainly depended on the developmental stage of the whitefly ovary, and the transovarial transmission of TYLCV to offspring increased with whitefly adult age. The specific interaction between virus coat protein (CP) and whitefly vitellogenin (Vg) was vital for virus entry into whitefly ovary. When knocking down the expression of Vg, the entry of TYLCV into ovary was inhibited and the transovarial transmission efficiency decreased. In contrast, another begomovirus, Papaya leaf curl China virus (PaLCuCNV), CP did not interact with whitefly Vg, and PaLCuCNV could not be transovarially transmitted by whiteflies. We further showed that TYLCV could be maintained for at least two generations in the absence of virusinfected plants, and the adult progenies were able to infect healthy plants in both the laboratory and field. This study reports the transovarial transmission mechanism of begomoviruses, and it may help to explain the evolution and global spread of some begomoviruses.begomovirus | transovarial transmission | vector development | vitellogenin | whitefly

Triazophos‐induced vertical transmission of rice stripe virus is associated with host vitellogenin in the small brown planthopper Laodelphax striatellus

“…Vg is an essential protein for embryo development that is thought to be synthesized in the fat body, then secreted into the hemolymph and eventually taken up into oocytes via VgR‐mediated endocytosis . Insect Vg acts in ovarian infection by viruses or endosymbionts . A previous study showed that LsVg plays a pivotal role in mediating transovarial transmission of RSV .…”

“…11,35,37,38 In addition, Vg or VgR was found to participate in the transmission of other pathogens. [39][40][41] Our previous study first reported that sublethal doses of triazophos increased RSV vertical transmission ability in SBPH. 32 However, the mechanism of triazophos-induced RSV vertical transmission is currently unknown.…”

“…Knockdown of Vg or VgR transcript significantly decreased RSV titers and thus interfered with systemic virus infection . In addition, Vg or VgR was found to participate in the transmission of other pathogens …”

Rice stripe virus hitchhikes the vector insect vitellogenin ligand-receptor pathway for ovary entry

“…Because of the indispensability of insect Vg for embryo development, the Vg-VgR-mediated viral attachment and cell entry might be an evolutionarily conserved mechanism for a virus to overcome the ovarian barrier to achieve vertical transmission. Insect Vg aids in ovarian infection by other viruses or endosymbionts [39,40]. For example, the Spiroplasma endosymbiont can be vertically transmitted by Drosophila.…”

“…Moreover, both L. striatellus and B. tabaci transmit arboviruses that do not invade ovaries, including Rice black-streaked dwarf virus by L. striatellus and Papaya leaf curl China virus by B. tabaci. In each case, the viral coat protein does not bind to the insect Vg, and the virus is unable to invade the insect ovaries [28,39].…”