Diversified regulation of circadian clock gene expression following whole genome duplication

PLoS Genet. 2020 Oct 8;16(10):e1009097. doi: 10.1371/journal.pgen.1009097. eCollection 2020 Oct.

Abstract

Across taxa, circadian control of physiology and behavior arises from cell-autonomous oscillations in gene expression, governed by a networks of so-called 'clock genes', collectively forming transcription-translation feedback loops. In modern vertebrates, these networks contain multiple copies of clock gene family members, which arose through whole genome duplication (WGD) events during evolutionary history. It remains unclear to what extent multiple copies of clock gene family members are functionally redundant or have allowed for functional diversification. We addressed this problem through an analysis of clock gene expression in the Atlantic salmon, a representative of the salmonids, a group which has undergone at least 4 rounds of WGD since the base of the vertebrate lineage, giving an unusually large complement of clock genes. By comparing expression patterns across multiple tissues, and during development, we present evidence for gene- and tissue-specific divergence in expression patterns, consistent with functional diversification of clock gene duplicates. In contrast to mammals, we found no evidence for coupling between cortisol and circadian gene expression, but cortisol mediated non-circadian regulated expression of a subset of clock genes in the salmon gill was evident. This regulation is linked to changes in gill function necessary for the transition from fresh- to sea-water in anadromous fish. Overall, this analysis emphasises the potential for a richly diversified clock gene network to serve a mixture of circadian and non-circadian functions in vertebrate groups with complex genomes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Circadian Clocks / genetics*
  • Evolution, Molecular*
  • Gene Duplication / genetics*
  • Gene Expression Regulation, Developmental / genetics
  • Gene Regulatory Networks / genetics
  • Genome / genetics
  • Phylogeny
  • Salmo salar / genetics*

Grant support

The work was supported by grants from the Tromsø forskningsstiftelse (TFS) starter grant TFS2016SW and the TFS infrastructure grant (IS3_17_SW) awarded to SHW. ACW is supported by the Tromsø forskningsstiftelse (TFS) grant awarded to DGH (TFS2016DH). Simen Sandve wishes to acknowledge the funding of the Norwegian Research Council project Rewired (NRC project number 274669). The authors also thank Dag Inge Våge and Thu-Hien To at the NMBU Elixir-node for making the orthogroups and gene trees available. Research council of Norway grant number 241016 and Sentinel North Transdisciplinary Research Program Université Laval and UiT awarded to DGH. The publication charges for this article have been part funded by a grant from the publication fund of UiT-The Arctic University of Norway. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.