Development Genes and Evolution

, Volume 218, Issue 11, pp 667–680

The amphioxus genome enlightens the evolution of the thyroid hormone signaling pathway

  • Mathilde Paris
  • Frédéric Brunet
  • Gabriel V. Markov
  • Michael Schubert
  • Vincent Laudet
Original Article

DOI: 10.1007/s00427-008-0255-7

Cite this article as:
Paris, M., Brunet, F., Markov, G.V. et al. Dev Genes Evol (2008) 218: 667. doi:10.1007/s00427-008-0255-7

Abstract

Thyroid hormones (THs) have pleiotropic effects on vertebrate development, with amphibian metamorphosis as the most spectacular example. However, developmental functions of THs in non-vertebrate chordates are largely hypothetical and even TH endogenous production has been poorly investigated. In order to get better insight into the evolution of the thyroid hormone signaling pathway in chordates, we have taken advantage of the recent release of the amphioxus genome. We found amphioxus homologous sequences to most of the genes encoding proteins involved in thyroid hormone signaling in vertebrates, except the fast-evolving thyroglobulin: sodium iodide symporter, thyroid peroxidase, deiodinases, thyroid hormone receptor, TBG, and CTHBP. As only some genes encoding proteins involved in TH synthesis regulation were retrieved (TRH, TSH receptor, and CRH receptor but not their corresponding receptors and ligands), there may be another mode of upstream regulation of TH synthesis in amphioxus. In accord with the notion that two whole genome duplications took place at the base of the vertebrate tree, one amphioxus gene often corresponded to several vertebrate homologs. However, some amphioxus specific duplications occurred, suggesting that several steps of the TH pathway were independently elaborated in the cephalochordate and vertebrate lineages. The present results therefore indicate that amphioxus is capable of producing THs. As several genes of the TH signaling pathway were also found in the sea urchin genome, we propose that the thyroid hormone signaling pathway is of ancestral origin in chordates, if not in deuterostomes, with specific elaborations in each lineage, including amphioxus.

Keywords

Branchiostoma floridaeCephalochordateChordateDevelopmentEvolutionThyroid hormoneEndostyle

Supplementary material

427_2008_255_MOESM1_ESM.doc (70 kb)
Table S1Summary of amphioxus genes discussed in this study. (DOC 70.5 KB)
427_2008_255_MOESM2_ESM.doc (394 kb)
Table S2Summary of the other genes used in this study. (DOC 394 KB)
427_2008_255_MOESM3_ESM.doc (36 kb)
Table S3Comparison of evolutionary rates for the vertebrate peroxidases families. (DOC 35.5 KB)
427_2008_255_Fig1_ESM.gif (81 kb)
Fig. S1

Phylogenetic tree of SIS and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of SIS amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences have been boxed in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. A similar tree without sequences from basal vertebrates is shown in Fig. 2. The scale bar indicates the number of changes per site.(GIF 82 KB)

427_2008_255_Fig1_ESM.eps (450 kb)
High resolution image file (EPS 450 KB)
427_2008_255_Fig2_ESM.gif (81 kb)
Fig. S1

Phylogenetic tree of SIS and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of SIS amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences have been boxed in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. A similar tree without sequences from basal vertebrates is shown in Fig. 2. The scale bar indicates the number of changes per site.(GIF 82 KB)

427_2008_255_Fig2_ESM.eps (439 kb)
High resolution image file (EPS 438 KB)
427_2008_255_Fig3_ESM.gif (42 kb)
Fig. S1

Phylogenetic tree of SIS and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of SIS amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences have been boxed in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. A similar tree without sequences from basal vertebrates is shown in Fig. 2. The scale bar indicates the number of changes per site.(GIF 82 KB)

427_2008_255_Fig3_ESM.eps (523 kb)
High resolution image file (EPS 535 KB)
427_2008_255_Fig4_ESM.gif (123 kb)
Fig. S1

Phylogenetic tree of SIS and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of SIS amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences have been boxed in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. A similar tree without sequences from basal vertebrates is shown in Fig. 2. The scale bar indicates the number of changes per site.(GIF 82 KB)

427_2008_255_Fig4_ESM.eps (630 kb)
(EPS 645 KB)
427_2008_255_Fig5_ESM.gif (73 kb)
Fig. S1

Phylogenetic tree of SIS and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of SIS amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences have been boxed in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. A similar tree without sequences from basal vertebrates is shown in Fig. 2. The scale bar indicates the number of changes per site.(GIF 82 KB)

427_2008_255_Fig5_ESM.eps (357 kb)
(EPS 365 KB)
427_2008_255_Fig6_ESM.gif (37 kb)
Fig. S1

Phylogenetic tree of SIS and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of SIS amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences have been boxed in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. A similar tree without sequences from basal vertebrates is shown in Fig. 2. The scale bar indicates the number of changes per site.(GIF 82 KB)

427_2008_255_Fig6_ESM.eps (410 kb)
(EPS 419 KB)
427_2008_255_Fig7_ESM.gif (78 kb)
Fig. S1

Phylogenetic tree of SIS and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of SIS amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences have been boxed in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. A similar tree without sequences from basal vertebrates is shown in Fig. 2. The scale bar indicates the number of changes per site.(GIF 82 KB)

427_2008_255_Fig7_ESM.eps (497 kb)
(EPS 509 KB)
427_2008_255_Fig8_ESM.gif (40 kb)
Fig. S1

Phylogenetic tree of SIS and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of SIS amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences have been boxed in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. A similar tree without sequences from basal vertebrates is shown in Fig. 2. The scale bar indicates the number of changes per site.(GIF 82 KB)

427_2008_255_Fig8_ESM.eps (322 kb)
(EPS 330 KB)
427_2008_255_Fig9_ESM.gif (14 kb)
Fig. S1

Phylogenetic tree of SIS and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of SIS amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences have been boxed in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. A similar tree without sequences from basal vertebrates is shown in Fig. 2. The scale bar indicates the number of changes per site.(GIF 82 KB)

427_2008_255_Fig9_ESM.eps (395 kb)
(EPS 404 KB)

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Mathilde Paris
    • 1
  • Frédéric Brunet
    • 1
  • Gabriel V. Markov
    • 1
  • Michael Schubert
    • 1
  • Vincent Laudet
    • 1
  1. 1.Institut de Génomique Fonctionnelle de Lyon, CNRS UMR5242–INRA 1288–ENS–UCBL, IFR128 BioSciences Lyon-Gerland, Ecole Normale Supérieure de LyonLyon Cedex 07France