Evolution of a chordate-specific mechanism for myoblast fusion

Haifeng Zhang, Renjie Shang, Kwantae Kim, Wei Zheng, Christopher J. Johnson, Lei Sun, Xiang Niu, Liang Liu, Theodore A. Uyeno, Jingqi Zhou, Lingshu Liu, Jimin Pei, Skye D. Fissette, Stephen A. Green, Sukhada P. Samudra, Junfei Wen, Jianli Zhang, Jonathan Eggenschwiler, Doug Menke, Marianne E. Bronner, Nick V. Grishin, Weiming Li, Kaixiong Ye, Yang Zhang, Alberto Stolfi, Pengpeng Bi
2021 · doi:10.1101/2021.07.24.453587
preprint OA: closed CC-BY-NC-ND-4.0
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This study elucidates the evolutionary origins of chordate-specific myoblast fusion genes Myomaker and Myomixer, revealing that Myomaker arose via duplication while Myomixer evolved de novo to enable vertebrate muscle efficiency.

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Abstract

The size of an animal is determined by the size of its musculoskeletal system. Myoblast fusion is an innovative mechanism that allows for multinucleated muscle fibers to compound the size and strength of individual mononucleated cells. However, the evolutionary history of the control mechanism underlying this important process is currently unknown. The phylum Chordata hosts closely related groups that span distinct myoblast fusion states: no fusion in cephalochordates, restricted fusion and multinucleation in tunicates, and extensive, obligatory fusion in vertebrates. To elucidate how these differences may have evolved, we studied 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 an unexpectedly complex evolutionary history of myoblast fusion in chordates. A pre-vertebrate phase of muscle multinucleation driven by Myomaker was followed by the later emergence of Myomixer that enables the highly efficient fusion system of vertebrates. Thus, our findings reveal the evolutionary origins of chordate-specific fusogens and illustrate how new genes can shape the emergence of novel morphogenetic traits and mechanisms.

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License: CC-BY-NC-ND-4.0