Insect tissue-specific vitellogenin facilitates transmission of plant virus

PLoS Pathog. 2018 Feb 23;14(2):e1006909. doi: 10.1371/journal.ppat.1006909. eCollection 2018 Feb.

Abstract

Insect vitellogenin (Vg) has been considered to be synthesized in the fat body. Here, we found that abundant Vg protein is synthesized in Laodelphax striatellus hemocytes as well. We also determined that only the hemocyte-produced Vg binds to Rice stripe virus (RSV) in vivo. Examination of the subunit composition of L. striatellus Vg (LsVg) revealed that LsVg was processed differently after its expression in different tissues. The LsVg subunit able to bind to RSV exist stably only in hemocytes, while fat body-produced LsVg lacks the RSV-interacting subunit. Nymph and male L. striatellus individuals also synthesize Vg but only in hemocytes, and the proteins co-localize with RSV. We observed that knockdown of LsVg transcripts by RNA interference decreased the RSV titer in the hemolymph, and thus interfered with systemic virus infection. Our results reveal the sex-independent expression and tissue-specific processing of LsVg and also unprecedentedly connect the function of this protein in mediating virus transmission to its particular molecular forms existing in tissues previously known as non-Vg producing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Hemiptera / virology
  • Insect Proteins / physiology*
  • Insecta / metabolism
  • Insecta / virology*
  • Male
  • Nymph
  • Organ Specificity
  • Oryza / virology
  • Plant Diseases / virology*
  • Plant Viruses / pathogenicity
  • Plant Viruses / physiology*
  • Tenuivirus / physiology
  • Virus Diseases / metabolism
  • Virus Diseases / transmission*
  • Vitellogenins / metabolism
  • Vitellogenins / physiology*

Substances

  • Insect Proteins
  • Vitellogenins

Grants and funding

This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDB11040100) to RF, by the Major State Basic Research Development Program of China (973 Program) (No. 2014CB138401) to XC, and by the National Natural Science Foundation of China (No. 31672000) to LZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.