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Evolution of a chordate-specific mechanism for myoblast fusion.

ABSTRACT: Vertebrate myoblast fusion allows for multinucleated muscle fibers to compound the size and strength of mononucleated cells, but the evolution of this important process is unknown. We investigated the evolutionary origins and function of membrane-coalescing agents Myomaker and Myomixer in various groups of chordates. Here, we report that Myomaker likely arose through gene duplication in the last common ancestor of tunicates and vertebrates, while Myomixer appears to have evolved de novo in early vertebrates. Functional tests revealed a complex evolutionary history of myoblast fusion. A prevertebrate phase of muscle multinucleation driven by Myomaker was followed by the later emergence of Myomixer that enables the highly efficient fusion system of vertebrates. Evolutionary comparisons between vertebrate and nonvertebrate Myomaker revealed key structural and mechanistic insights into myoblast fusion. Thus, our findings suggest an evolutionary model of chordate fusogens and illustrate how new genes shape the emergence of novel morphogenetic traits and mechanisms.

SUBMITTER: Zhang H

PROVIDER: S-EPMC10848958 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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Evolution of a chordate-specific mechanism for myoblast fusion.

Zhang Haifeng H Shang Renjie R Kim Kwantae K Zheng Wei W Johnson Christopher J CJ Sun Lei L Niu Xiang X Liu Liang L Zhou Jingqi J Liu Lingshu L Zhang Zheng Z Uyeno Theodore A TA Pei Jimin J Fissette Skye D SD Green Stephen A SA Samudra Sukhada P SP Wen Junfei J Zhang Jianli J Eggenschwiler Jonathan T JT Menke Douglas B DB Bronner Marianne E ME Grishin Nick V NV Li Weiming W Ye Kaixiong K Zhang Yang Y Stolfi Alberto A Bi Pengpeng P

Science advances 20220902 35

Vertebrate myoblast fusion allows for multinucleated muscle fibers to compound the size and strength of mononucleated cells, but the evolution of this important process is unknown. We investigated the evolutionary origins and function of membrane-coalescing agents Myomaker and Myomixer in various groups of chordates. Here, we report that <i>Myomaker</i> likely arose through gene duplication in the last common ancestor of tunicates and vertebrates, while <i>Myomixer</i> appears to have evolved de ...[more]

PMID: 36054355

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Project description:BACKGROUND: Chordate evolution is a history of innovations that is marked by physical and behavioral specializations, which led to the development of a variety of forms from a single ancestral group. Among other important characteristics, vertebrates obtained a well developed brain, anterior sensory structures, a closed circulatory system and gills or lungs as blood oxygenation systems. The duplication of pre-existing genes had profound evolutionary implications for the developmental complexity in vertebrates, since mutations modifying the function of a duplicated protein can lead to novel functions, improving the evolutionary success. RESULTS: We analyzed here the evolution of the GPRC5 family of G protein-coupled receptors by comprehensive similarity searches and found that the receptors are only present in chordates and that the size of the receptor family expanded, likely due to genome duplication events in the early history of vertebrate evolution. We propose that a single GPRC5 receptor coding gene originated in a stem chordate ancestor and gave rise by duplication events to a gene family comprising three receptor types (GPRC5A-C) in vertebrates, and a fourth homologue present only in mammals (GPRC5D). Additional duplications of GPRC5B and GPRC5C sequences occurred in teleost fishes. The finding that the expression patterns of the receptors are evolutionarily conserved indicates an important biological function of these receptors. Moreover, we found that expression of GPRC5B is regulated by vitamin A in vivo, confirming previous findings that linked receptor expression to retinoic acid levels in tumor cell lines and strengthening the link between the receptor expression and the development of a complex nervous system in chordates, known to be dependent on retinoic acid signaling. CONCLUSIONS: GPRC5 receptors, a class of G protein-coupled receptors with unique sequence characteristics, may represent a molecular novelty that helped non-chordates to become chordates.

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Evolution of a chordate-specific mechanism for myoblast fusion.

Publications

Evolution of a chordate-specific mechanism for myoblast fusion.

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