A long noncoding RNA acts as a post-transcriptional regulator of heat shock protein (HSP70) synthesis in the cold hardy Diamesa tonsa under heat shock

PLoS One. 2020 Apr 2;15(4):e0227172. doi: 10.1371/journal.pone.0227172. eCollection 2020.

Abstract

Cold stenothermal insects living in glacier-fed streams are stressed by temperature variations resulting from glacial retreat during global warming. The molecular aspects of insect response to environmental stresses remain largely unexplored. The aim of this study was to expand our knowledge of how a cold stenothermal organism controls gene expression at the transcriptional, translational, and protein level under warming conditions. Using the chironomid Diamesa tonsa as target species and a combination of RACE, qPCR, polysomal profiling, western blotting, and bioinformatics techniques, we discovered a new molecular pathway leading to previously overlooked adaptive strategies to stress. We obtained and characterized the complete cDNA sequences of three heat shock inducible 70 (hsp70) and two members of heat-shock cognate 70 (hsc70). Strikingly, we showed that a novel pseudo-hsp70 gene encoding a putative long noncoding RNA (lncRNA) which is transcribed during thermal stress, acting as a ribosome sponge to provide post-transcriptional control of HSP70 protein levels. The expression of the pseudo-hsp70 gene and its function suggest the existence of a new and unexpected mechanism to cope with thermal stress: lowering the pace of protein production to save energy and optimize resources for recovery.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chironomidae / genetics*
  • Gene Expression Profiling
  • Gene Expression Regulation / genetics
  • HSP70 Heat-Shock Proteins / genetics*
  • Heat-Shock Response / genetics
  • Polyribosomes / genetics
  • RNA Processing, Post-Transcriptional / genetics*
  • RNA, Long Noncoding / genetics*
  • Stress, Physiological / genetics

Substances

  • HSP70 Heat-Shock Proteins
  • RNA, Long Noncoding

Grants and funding

This work was partially supported by the Cassa di Risparmio di Trento e Rovereto Foundation within the RACE-TN Project (“Valutazione del rischio ambientale dei contaminanti emergenti nei fiumi trentini: effetti sulla vita selvatica e sull’uomo”/“Environmental Risk assessment of emerging contaminants in Trentino rivers: effects on wildlife and human health”, Grant CARITRO n. 2015.0199; October 2015-January 2018) coordinated by Valeria Lencioni. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The funder supported 1 m/m of the contract of the first author (Paola Bernabò) and the purchase of some consumables. There was no additional external funding received for this study.