Evolution of a chordate-specific mechanism for myoblast fusion

Author:

Zhang Haifeng,Shang Renjie,Kim Kwantae,Zheng Wei,Johnson Christopher J.,Sun Lei,Niu Xiang,Liu Liang,Uyeno Theodore A.,Zhou Jingqi,Liu Lingshu,Pei Jimin,Fissette Skye D.,Green Stephen A.,Samudra Sukhada P.,Wen Junfei,Zhang Jianli,Eggenschwiler Jonathan,Menke Doug,Bronner Marianne E.,Grishin Nick V.,Li Weiming,Ye Kaixiong,Zhang Yang,Stolfi Alberto,Bi PengpengORCID

Abstract

AbstractThe 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.

Publisher

Cold Spring Harbor Laboratory

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