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Evolution of a chordate-specific mechanism for myoblast fusion

Zhang, Haifeng and Shang, Renjie and Kim, Kwantae and Zheng, Wei and Johnson, Christopher J. and Sun, Lei and Niu, Xiang and Liu, Liang and Uyeno, Theodore A. and Zhou, Jingqi and Liu, Lingshu and Pei, Jimin and Fissette, Skye D. and Green, Stephen A. and Samudra, Sukhada P. and Wen, Junfei and Zhang, Jianli and Eggenschwiler, Jonathan and Menke, Doug and Bronner, Marianne E. and Grishin, Nick V. and Li, Weiming and Ye, Kaixiong and Zhang, Yang and Stolfi, Alberto and Bi, Pengpeng (2021) Evolution of a chordate-specific mechanism for myoblast fusion. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20210727-173554020

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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.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.07.24.453587DOIDiscussion Paper
ORCID:
AuthorORCID
Bronner, Marianne E.0000-0003-4274-1862
Bi, Pengpeng0000-0002-9871-6773
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. This version posted July 25, 2021. We thank trainees G. Gopu, A. Baiju, and E. M. Hicks in Bi laboratory and A. L. Womble from Valdosta State University for technical help. We are grateful to E. N. Olson from University of Texas Southwestern Medical Center for critical reading of the manuscript. We thank H. Li from Ocean University of China, C. Cañestro from University of Barcelona, S. Kuraku, R. Kusakabe and S. Kuratani from RIKEN, M. Cui from University of Texas Southwestern Medical Center, S. Du from University of Maryland School of Medicine, J. Ziermann from Howard University, Z. Yang from University of College London, Michael Coates and Tetsuto Miyashita from University of Chicago, and F. Razy-Krajka for advice; A. Bigot and V. Mouly from the Myoline platform of the Myology Institute for myoblast cell lines; X. Li from University of Texas Southwestern Medical Center, N. S. Johnson from United States Geological Survey, M. Brindley from University of Georgia for providing materials and reagents. This work was supported by the starting up fund from the University of Georgia to P.B., NIH R00 award HD084814 and NSF award 1940743 to A.S., an NSF Graduate Research Fellowship to C.J.J., Great Lakes Fishery Commission (540810) to S.D.F. and W.L., and NSF award 1354788 to T.A.U. Author contributions: H.Z., R.S., A.S., P.B. designed research; H.Z., R.S., K.K., W.Z., C.J.J., S.L., X.N., L.L., T.A.U., J.Z., L.L., J.P., S.D.F., S.A.G., S.P.S., J.W., J.Z., J.E., D.M., M.E.B., N.V.G., W.L., K.Y., Z.Y., A.S. and P.B. performed research; H.Z., R.S., K.K., W.Z., C.J.J., L.S., X.N., L.L., J.Z., L.L., J.W., W.L., K.Y., Z.Y., A.S. and P.B. analyzed data; A.S. and P.B. wrote the paper. The authors declare that they have no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Additional data related to this paper may be requested from the authors.
Funders:
Funding AgencyGrant Number
University of GeorgiaUNSPECIFIED
NIHHD084814
NSFIOS-1940743
NSF Graduate Research FellowshipUNSPECIFIED
Great Lakes Fishery Commission540810
NSFIOS-1354788
DOI:10.1101/2021.07.24.453587
Record Number:CaltechAUTHORS:20210727-173554020
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210727-173554020
Official Citation: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. bioRxiv 2021.07.24.453587; doi: https://doi.org/10.1101/2021.07.24.453587
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:110030
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:28 Jul 2021 19:46
Last Modified:16 Nov 2021 19:39

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