The bumblebee Bombus terrestris carries a primary inoculum of Tomato brown rugose fruit virus contributing to disease spread in tomatoes

PLoS One. 2019 Jan 17;14(1):e0210871. doi: 10.1371/journal.pone.0210871. eCollection 2019.

Abstract

The bumblebee Bombus terrestris is a beneficial pollinator extensively used in tomato production. Our hypothesis was that bumblebee hives collected from a Tomato brown rugose fruit virus (ToBRFV) infected tomato greenhouse, preserve an infectious primary inoculum. Placing a bumblebee hive collected from a ToBRFV contaminated greenhouse, in a glass-/net-house containing only uninfected healthy tomato plants, spread ToBRFV disease. Control uninfected tomato plants grown in a glass-/net-house devoid of any beehive remained uninfected. ToBRFV-contaminated hives carried infectious viral particles as demonstrated in a biological assay on laboratory test plants of virus extracted from hive components. Viral particles isolated from a contaminated hive had a typical tobamovirus morphology observed in transmission electron microscopy. Assembly of ToBRFV genome was achieved by next generation sequencing analysis of RNA adhering to the bumblebee body. Bumblebee dissection showed that ToBRFV was mostly present in the abdomen suggesting viral disease spread via buzz pollination. These results demonstrate that bumblebee hives collected from ToBRFV-contaminated greenhouses carry a primary inoculum that reflects the status of viruses in the growing area. This new mode of ToBRFV spread by pollinators opens an avenue for detection of viruses in a growing area through analysis of the pollinators, as well as emphasizes the need to reevaluate the appropriate disease management protocols.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bees / physiology
  • Bees / virology*
  • DNA, Viral / genetics
  • Fruit / virology
  • Insect Vectors / physiology
  • Insect Vectors / virology
  • Microscopy, Electron, Transmission
  • Plant Diseases / virology*
  • Pollination
  • Reverse Transcriptase Polymerase Chain Reaction
  • Solanum lycopersicum / virology*
  • Tobamovirus / genetics
  • Tobamovirus / isolation & purification
  • Tobamovirus / pathogenicity*
  • Virion / genetics
  • Virion / ultrastructure

Substances

  • DNA, Viral

Grants and funding

This research was supported by the Israeli Chief Scientist, Ministry of Agriculture on ToBRFV grant number: 20-10-0070 to AD; https://agriscience.co.il/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.