Abstract

The lamprey Petromyzon marinus belongs to the agnathans, the oldest vertebrate lineage from which jawed vertebrates diverged about 500 million years ago. Therefore, it holds a key phylogenetic position to understand the evolution of vertebrates. As in jawed vertebrates, two thyroid hormone receptors have been described in lamprey. These receptors, referred to as TR1 and TR2, behave as genuine TRs but are considered as an independent duplications when compared to the orthologs characterized in jawed vertebrates, TRα and TRβ. Here, we show that the lamprey genome contains two additional TR sequences. Their assignment to bona fide thyroid hormone receptors is supported by sequence alignments and phylogenetic reconstructions. This led us to revisit the phylogeny of thyroid hormone receptors and to detect an acceleration of their evolutionary rates at the basis of vertebrates. Our analysis therefore suggests that major evolutionary shifts occurred at the receptor level just when the modern synthesis of thyroid hormone was established during early vertebrate evolution.

Highlights

  • Thyroid hormones (THs) are involved in pleiotropic processes in vertebrates [1] such as metabolic control [2], photoperiod signaling [3] or metamorphosis [4]

  • TH signaling is mediated by thyroid hormone receptors (TRs), ligand-dependent transcription factors that belong to the nuclear receptor superfamily

  • The genome of the sea lamprey Petromyzon marinus has been sequenced and assembled, and these data are available in Ensembl [10]

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Summary

Introduction

Thyroid hormones (THs) are involved in pleiotropic processes in vertebrates [1] such as metabolic control [2], photoperiod signaling [3] or metamorphosis [4]. TH signaling is mediated by thyroid hormone receptors (TRs), ligand-dependent transcription factors that belong to the nuclear receptor superfamily. TRs display two major functional domains, the DNA binding domain (DBD) and the ligand binding domain (LBD). TRα and TRβ, which originate from a genome duplication predating the gnathostome radiation, have been characterized in jawed vertebrates. TRα and TRβ display different biological properties such as gene regulation or binding properties [6, 7]. The two sea lamprey TR genes (TR1 and TR2) appear to be the product of an independent duplication [11], but this issue is still debated and complicates our understanding of TR evolution

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