Evolutionary diversification of the canonical Wnt signaling effector TCF/LEF in chordates

Nuria P.  Torres-Aguila; Marika Salonna; Stefan Hoppler; David E.K. Ferrier

doi:10.1111/dgd.12771

Evolutionary diversification of the canonical Wnt signaling effector TCF/LEF in chordates

Nuria P. Torres-Aguila, Marika Salonna, Stefan Hoppler, David E.K. Ferrier^* (Corresponding Author)

^*Corresponding author for this work

University of St Andrews

Research output: Contribution to journal › Article › peer-review

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Abstract

Wnt signaling is essential during animal development and regeneration, but also plays an important role in diseases such as cancer and diabetes. The canonical Wnt signaling pathway is one of the most conserved signaling cascades in the animal kingdom, with the T-cell factor/lymphoid enhancer factor (TCF/LEF) proteins the major mediators of Wnt/β-catenin24 regulated gene expression. In comparison to invertebrates, vertebrates possess a high diversity of TCF/LEF family genes, implicating this as a possible key change to Wnt signaling at the evolutionary origin of vertebrates. However, the precise nature of this diversification is only poorly understood. The aim of this study is to clarify orthology, paralogy and isoform relationships within the TCF/LEF gene family within chordates via in silico comparative study of TCF/LEF gene structure, molecular phylogeny and gene synteny. Our results support the notion that the four TCF/LEF paralog subfamilies in jawed vertebrates (gnathostomes) evolved
31 via the two rounds of whole-genome duplication that occurred during early vertebrate evolution. Importantly, gene structure comparisons and synteny analysis of jawless vertebrate (cyclostome) TCFs suggest that a TCF7L2-like form of gene structure is a close proxy for the ancestral vertebrate structure. In conclusion, we propose a detailed evolutionary path based on a new pre-whole-genome duplication vertebrate TCF gene model. This ancestor gene model highlights the chordate and vertebrate innovations of TCF/LEF gene structure,
providing the foundation for understanding the role of Wnt/β-catenin signaling in vertebrate evolution.

Original language	English
Pages (from-to)	120-137
Number of pages	18
Journal	Development, Growth and Differentiation
Volume	64
Issue number	3
Early online date	3 Feb 2022
DOIs	https://doi.org/10.1111/dgd.12771
Publication status	Published - 1 Apr 2022

Bibliographical note

ACKNOWLEDGEMENTS

We thank Madeleine Aase-Remedios for helping with the phylogenetic tree building and for advice on statistical analysis, and Sebastian Shimeld for providing us with lamprey transcriptome data and comments on the manuscript. This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC), linked projects, references BB/S016856/1 and BB/S020640/1.

Keywords

amphioxus
Ciona
cyclostome
lamprey
comparative genomics

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Cite this

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title = "Evolutionary diversification of the canonical Wnt signaling effector TCF/LEF in chordates",

abstract = "Wnt signaling is essential during animal development and regeneration, but also plays an important role in diseases such as cancer and diabetes. The canonical Wnt signaling pathway is one of the most conserved signaling cascades in the animal kingdom, with the T-cell factor/lymphoid enhancer factor (TCF/LEF) proteins the major mediators of Wnt/β-catenin24 regulated gene expression. In comparison to invertebrates, vertebrates possess a high diversity of TCF/LEF family genes, implicating this as a possible key change to Wnt signaling at the evolutionary origin of vertebrates. However, the precise nature of this diversification is only poorly understood. The aim of this study is to clarify orthology, paralogy and isoform relationships within the TCF/LEF gene family within chordates via in silico comparative study of TCF/LEF gene structure, molecular phylogeny and gene synteny. Our results support the notion that the four TCF/LEF paralog subfamilies in jawed vertebrates (gnathostomes) evolved31 via the two rounds of whole-genome duplication that occurred during early vertebrate evolution. Importantly, gene structure comparisons and synteny analysis of jawless vertebrate (cyclostome) TCFs suggest that a TCF7L2-like form of gene structure is a close proxy for the ancestral vertebrate structure. In conclusion, we propose a detailed evolutionary path based on a new pre-whole-genome duplication vertebrate TCF gene model. This ancestor gene model highlights the chordate and vertebrate innovations of TCF/LEF gene structure,providing the foundation for understanding the role of Wnt/β-catenin signaling in vertebrate evolution.",

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N1 - ACKNOWLEDGEMENTS We thank Madeleine Aase-Remedios for helping with the phylogenetic tree building and for advice on statistical analysis, and Sebastian Shimeld for providing us with lamprey transcriptome data and comments on the manuscript. This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC), linked projects, references BB/S016856/1 and BB/S020640/1.

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N2 - Wnt signaling is essential during animal development and regeneration, but also plays an important role in diseases such as cancer and diabetes. The canonical Wnt signaling pathway is one of the most conserved signaling cascades in the animal kingdom, with the T-cell factor/lymphoid enhancer factor (TCF/LEF) proteins the major mediators of Wnt/β-catenin24 regulated gene expression. In comparison to invertebrates, vertebrates possess a high diversity of TCF/LEF family genes, implicating this as a possible key change to Wnt signaling at the evolutionary origin of vertebrates. However, the precise nature of this diversification is only poorly understood. The aim of this study is to clarify orthology, paralogy and isoform relationships within the TCF/LEF gene family within chordates via in silico comparative study of TCF/LEF gene structure, molecular phylogeny and gene synteny. Our results support the notion that the four TCF/LEF paralog subfamilies in jawed vertebrates (gnathostomes) evolved31 via the two rounds of whole-genome duplication that occurred during early vertebrate evolution. Importantly, gene structure comparisons and synteny analysis of jawless vertebrate (cyclostome) TCFs suggest that a TCF7L2-like form of gene structure is a close proxy for the ancestral vertebrate structure. In conclusion, we propose a detailed evolutionary path based on a new pre-whole-genome duplication vertebrate TCF gene model. This ancestor gene model highlights the chordate and vertebrate innovations of TCF/LEF gene structure,providing the foundation for understanding the role of Wnt/β-catenin signaling in vertebrate evolution.

AB - Wnt signaling is essential during animal development and regeneration, but also plays an important role in diseases such as cancer and diabetes. The canonical Wnt signaling pathway is one of the most conserved signaling cascades in the animal kingdom, with the T-cell factor/lymphoid enhancer factor (TCF/LEF) proteins the major mediators of Wnt/β-catenin24 regulated gene expression. In comparison to invertebrates, vertebrates possess a high diversity of TCF/LEF family genes, implicating this as a possible key change to Wnt signaling at the evolutionary origin of vertebrates. However, the precise nature of this diversification is only poorly understood. The aim of this study is to clarify orthology, paralogy and isoform relationships within the TCF/LEF gene family within chordates via in silico comparative study of TCF/LEF gene structure, molecular phylogeny and gene synteny. Our results support the notion that the four TCF/LEF paralog subfamilies in jawed vertebrates (gnathostomes) evolved31 via the two rounds of whole-genome duplication that occurred during early vertebrate evolution. Importantly, gene structure comparisons and synteny analysis of jawless vertebrate (cyclostome) TCFs suggest that a TCF7L2-like form of gene structure is a close proxy for the ancestral vertebrate structure. In conclusion, we propose a detailed evolutionary path based on a new pre-whole-genome duplication vertebrate TCF gene model. This ancestor gene model highlights the chordate and vertebrate innovations of TCF/LEF gene structure,providing the foundation for understanding the role of Wnt/β-catenin signaling in vertebrate evolution.

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KW - Ciona

KW - cyclostome

KW - lamprey

KW - comparative genomics

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DO - 10.1111/dgd.12771

M3 - Article

SN - 0012-1592

VL - 64

SP - 120

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JO - Development, Growth and Differentiation

JF - Development, Growth and Differentiation

IS - 3

ER -

Evolutionary diversification of the canonical Wnt signaling effector TCF/LEF in chordates

Abstract

Bibliographical note

Keywords

UN SDGs

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