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

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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.

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Acknowledgements

We would like to thank Maria Theodosiou for critical reading of the manuscript. This work was supported by funds from the ANR, CNRS, and the MENRT. This study was further supported by CRESCENDO, a European Union Integrated Project of FP6, and by CASCADE, a Network of Excellence of FP6.

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  1. Institut de Génomique Fonctionnelle de Lyon, CNRS UMR5242–INRA 1288–ENS–UCBL, IFR128 BioSciences Lyon-Gerland, Ecole Normale Supérieure de Lyon, 46 allée d’Italie, 69364, Lyon Cedex 07, France

    Mathilde Paris, Frédéric Brunet, Gabriel V. Markov, Michael Schubert & Vincent Laudet

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  1. Mathilde Paris
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  2. Frédéric Brunet
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  3. Gabriel V. Markov
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  4. Michael Schubert
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  5. Vincent Laudet
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Correspondence to Vincent Laudet.

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Communicated by J.J. Gibson-Brown

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Table S1

Summary of amphioxus genes discussed in this study. (DOC 70.5 KB)

Table S2

Summary of the other genes used in this study. (DOC 394 KB)

Table S3

Comparison of evolutionary rates for the vertebrate peroxidases families. (DOC 35.5 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)

High resolution image file (EPS 450 KB)

Fig. S2

Phylogenetic tree of PERT and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of peroxidase amino acid sequences. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequences are 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. 3. PGH: Prostaglandin G/H synthase. The scale bar indicates the number of changes per site (GIF 82 KB)

High resolution image file (EPS 438 KB)

Fig. S3

Phylogenetic and structural analyses of putative deiodinases in amphioxus. a A maximum likelihood (ML) tree was obtained from analysis of deiodinase amino acid sequences. As no outgroup was found for deiodinases, the tree is presented unrooted. Bootstrap percentages obtained after 1000 replicates are shown. The amphioxus sequences have been circled in red. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead. The scale bar indicates the number of changes per site. A similar tree without sequences from basal vertebrates is shown in Fig. 3a. b Amino acid sequence alignment of the active catalytic domain of deiodinases from different animals (human and invertebrates). The site of a selenocysteine is shown in red. In human and H. roretzi, the translation of the TGA codon into a selenocysteine has been experimentally verified and is shown in bold (Berry et al. 1991; Curcio et al. 2001; Baqui et al. 2003). In the C. milii, S. acanthias, and L. erinacea, amphioxus and sea urchin sequences, the homologous TGA is proposed to be translated into a selenocysteine as well (italicized). (GIF 43 KB)

High resolution image file (EPS 535 KB)

Fig. S4

Phylogenetic tree of serpin protein sequences, including TBG. A maximum likelihood (ML) tree was obtained from analysis of serpin amino acid sequences excluding (a) or including (b) basal vertebrates. Bootstrap percentages obtained after 1,000 replicates are shown. Nodes with bootstrap support below 50% were collapsed in a. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead in b. The amphioxus sequences have been boxed in red and the sea urchin-specific duplications are highlighted in green. The scale bar indicates the number of changes per site. (GIF 126 KB)

(EPS 645 KB)

Fig. S5

Phylogenetic tree of CTHBP and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of CTHBP amino acid sequences excluding (a) or including (b) basal vertebrates. Bootstrap percentages obtained after 1,000 replicates are shown. Nodes with bootstrap support below 50% were collapsed in a. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead in b. The amphioxus sequences are boxed in red. The scale bar indicates the number of changes per site. (GIF 74 KB)

(EPS 365 KB)

Fig. S6

Phylogenetic tree of TR protein sequences, from Paris et al. (2008). A maximum likelihood (ML) tree was obtained from analysis of amino acid sequences of TR genes. Bootstrap percentages obtained after 1,000 replicates are shown. Nodes with bootstrap support below 50% were collapsed. Sequences from lamprey are indicated with a large blue arrowhead whereas sequences from the chondrichthyes S. canicula are indicated with a narrow green arrowhead. The amphioxus TR is highlighted in red. The scale bar indicates the number of changes per site. (GIF 74 KB)

(EPS 419 KB)

Fig. S7

Phylogenetic tree of CRHR and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of CFHR amino acid sequences excluding (a) or including (b) basal vertebrates. Bootstrap percentages obtained after 1,000 replicates are shown. Nodes with bootstrap support below 50% were collapsed in a. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead in b. The amphioxus sequences are highlighted in red. The scale bar indicates the number of changes per site. (GIF 79 KB)

(EPS 509 KB)

Fig. S8

Phylogenetic tree of TSHR and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of TSHR amino acid sequences excluding (a) or including (b) basal vertebrates. Nodes with bootstrap support below 50% were collapsed in a. Sequences from lampreys are indicated with a large blue arrowhead and sequences from cartilaginous fishes are indicated with a narrow green arrowhead in b. Bootstrap percentages obtained after 1,000 replicates are shown. The amphioxus sequence is highlighted in red. TSHR: Thyroid stimulating hormone receptor; LSHR: Lutropin-choriogonadotropic hormone receptor; FSHR: follicle stimulating hormone receptor. The scale bar indicates the number of changes per site. (GIF 41 KB)

(EPS 330 KB)

Fig. S9

Phylogenetic tree of TRH and related protein sequences. A maximum likelihood (ML) tree was obtained from analysis of TRH amino acid sequences. As no outgroup was found for TRH, the tree is presented unrooted. Bootstrap percentages obtained after 1,000 replicates are shown. The sequence from the chondrichthyes C. milii is indicated with a narrow green arrowhead. The amphioxus sequence is highlighted in red. TRH: Thyrotropin-releasing hormone. The scale bar indicates the number of changes per site (GIF 14 KB)

(EPS 404 KB)

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Paris, M., Brunet, F., Markov, G.V. et al. The amphioxus genome enlightens the evolution of the thyroid hormone signaling pathway. Dev Genes Evol 218, 667–680 (2008). https://doi.org/10.1007/s00427-008-0255-7

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