A plant reovirus hijacks endoplasmic reticulum-associated degradation machinery to promote efficient viral transmission by its planthopper vector under high temperature conditions

PLoS Pathog. 2021 Mar 1;17(3):e1009347. doi: 10.1371/journal.ppat.1009347. eCollection 2021 Mar.

Abstract

In the field, many insect-borne crop viral diseases are more suitable for maintenance and spread in hot-temperature areas, but the mechanism remains poorly understood. The epidemic of a planthopper (Sogatella furcifera)-transmitted rice reovirus (southern rice black-streaked dwarf virus, SRBSDV) is geographically restricted to southern China and northern Vietnam with year-round hot temperatures. Here, we reported that two factors of endoplasmic reticulum-associated degradation (ERAD) machinery, the heat shock protein DnaJB11 and ER membrane protein BAP31, were activated by viral infection to mediate the adaptation of S. furcifera to high temperatures. Infection and transmission efficiencies of SRBSDV by S. furcifera increased with the elevated temperatures. We observed that high temperature (35°C) was beneficial for the assembly of virus-containing tubular structures formed by nonstructural protein P7-1 of SRBSDV, which facilitates efficient viral transmission by S. furcifera. Both DnaJB11 and BAP31 competed to directly bind to the tubule protein P7-1 of SRBSDV; however, DnaJB11 promoted whereas BAP31 inhibited P7-1 tubule assembly at the ER membrane. Furthermore, the binding affinity of DnaJB11 with P7-1 was stronger than that of BAP31 with P7-1. We also revealed that BAP31 negatively regulated DnaJB11 expression through their direct interaction. High temperatures could significantly upregulate DnaJB11 expression but inhibit BAP31 expression, thereby strongly facilitating the assembly of abundant P7-1 tubules. Taken together, we showed that a new temperature-dependent protein quality control pathway in the ERAD machinery has evolved for strong activation of DnaJB11 for benefiting P7-1 tubules assembly to support efficient transmission of SRBSDV in high temperatures. We thus deduced that ERAD machinery has been hitchhiked by insect-borne crop viruses to enhance their transmission in tropical climates.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Endoplasmic Reticulum-Associated Degradation / immunology
  • Hot Temperature / adverse effects*
  • Insect Vectors / immunology
  • Insect Vectors / virology*
  • Orthoreovirus / pathogenicity
  • Plant Diseases / virology*
  • Reoviridae / immunology*

Supplementary concepts

  • Southern rice black-streaked dwarf virus

Grants and funding

This project was supported by funds from the National Natural Science Foundation of China to HC under grant number 31772132 (http://www.nsfc.gov.cn/), the National Key R&D Program of China to HC under grant number 2016YFD0300700 (http://service.most.gov.cn/sbksdy/),the National Natural Science Foundation of China to TW under grant number 31730071 (http://www.nsfc.gov.cn/), the Natural Science Foundation of Fujian Province to DJ under grant number 2020J06015 (http://xmgl.kjt.fujian.gov.cn/loginSignout.do), the National Key R&D Program of China to QC under grant number 2017YFD0200900 (http://service.most.gov.cn/sbksdy/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.