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SOXE neofunctionalization and elaboration of the neural crest during chordate evolution

Tai, Andrew and Cheung, Martin and Huang, Yong-Heng and Jauch, Ralf and Bronner, Marianne E. and Cheah, Kathryn S. E. (2016) SOXE neofunctionalization and elaboration of the neural crest during chordate evolution. Scientific Reports, 6 . Art. No. 34964. ISSN 2045-2322. PMCID PMC5062122. https://resolver.caltech.edu/CaltechAUTHORS:20161017-151104599

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Abstract

During chordate evolution, two genome-wide duplications facilitated acquisition of vertebrate traits, including emergence of neural crest cells (NCCs), in which neofunctionalization of the duplicated genes are thought to have facilitated development of craniofacial structures and the peripheral nervous system. How these duplicated genes evolve and acquire the ability to specify NC and their derivatives are largely unknown. Vertebrate SoxE paralogues, most notably Sox9/10, are essential for NC induction, delamination and lineage specification. In contrast, the basal chordate, amphioxus, has a single SoxE gene and lacks NC-like cells. Here, we test the hypothesis that duplication and divergence of an ancestral SoxE gene may have facilitated elaboration of NC lineages. By using an in vivo expression assay to compare effects of AmphiSoxE and vertebrate Sox9 on NC development, we demonstrate that all SOXE proteins possess similar DNA binding and homodimerization properties and can induce NCCs. However, AmphiSOXE is less efficient than SOX9 in transactivation activity and in the ability to preferentially promote glial over neuronal fate, a difference that lies within the combined properties of amino terminal and transactivation domains. We propose that acquisition of AmphiSoxE expression in the neural plate border led to NCC emergence while duplication and divergence produced advantageous mutations in vertebrate homologues, promoting elaboration of NC traits.


Item Type:Article
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URLURL TypeDescription
https://dx.doi.org/10.1038/srep34964DOIArticle
http://www.nature.com/articles/srep34964PublisherArticle
http://www.nature.com/article-assets/npg/srep/2016/161013/srep34964/extref/srep34964-s1.pdfPublisherSupplementary Information
http://readcube.com/view/10.1038/srep34964PublisherFree ReadCube Access
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5062122/PubMed CentralArticle
ORCID:
AuthorORCID
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© The Author(s) 2016. This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ Received: 20 June 2016. Accepted: 15 September 2016. Published online: 13 October 2016. This work was supported by grants from the Research Grants Council and University Grants Council of Hong Kong (7337/01M), (AoE/M-04/04), (T12-708/12-N) and (T12C-714/14-R) to K.S.E.C., GRF_17110715 to M.C and NS086907 to M.E.B. We thank Robin Lovell-Badge and Patrick Tam for helpful discussion, and Hisato Kondoh and Masanori Uchikawa for providing the Sox2-NC1 construct. We thank Yogesh Srivastava (GIBH) for help with structural modeling and May Cheung for technical assistance. R.J. is supported by a 2013 MOST China-EU Science and Technology Cooperation Program (grant number 2013DFE33080), by the National Natural Science Foundation of China (grant number 31471238), a 100 talent award of the Chinese Academy of Sciences and a Science and Technology Planning Project of Guangdong Province, China (2014B030301058). Andrew Tai & Martin Cheung: These authors contributed equally to this work. Author Contributions: A.T. and M.C. designed and performed experiments, analyzed data, and wrote the manuscript. Y.-H.H. designed and performed experiments. R.J. designed experiments, analyzed data and wrote the manuscript. M.E.B. and K.S.E.C. designed experiments, analyzed data and wrote the manuscript. The authors declare no competing financial interests. Accession codes: Accession numbers for the sequences used in this study are as follows: Rattus norvegicus (Sox8: NP_001100458; Sox10: NP_); Mus musculus (Sox8: NP_035577; Sox9: NM_035578; Sox10: NP_035567); Gallus gallus (Sox8: NP_990062; Sox9: NP_989612; Sox10: NP_990123); Homo sapiens (Sox8: NM_055402; Sox9: NP_000337; Sox10: NP_990123); Xenopus laevis (Sox8: NP_001083964; Sox9: NP_001084276; Sox10: NP_001082358); Danio rerio (Sox8: NP_001020636; Sox9a: NP_571718; Sox9b: AAH67133; Sox10: NP_571950); Petromyzon marinus (SoxE1: AAW34332; SoxE2: ABC58684; SoxE3: ABC58685); Eptatretus burgeri (Sox9: BAG11536); Ciona intestinalis (SoxE: CAD58841); Lytechinus variegatus (SoxE: ABY40629); Drosophila melanogaster (Sox100B: NP_651839); Apis mellifera (SoxE1: XP_001122993; SoxE2: XP_001122996) and Nasonia vitripennis (SoxE1: XP_001604913; SoxE2: XP_008213434).
Funders:
Funding AgencyGrant Number
Research Grants Council of Hong Kong7337/01M
Research Grants Council of Hong KongAoE/M-04/04
Research Grants Council of Hong KongT12-708/12-N
Research Grants Council of Hong KongT12C-714/14-R
NIH Graduate FellowshipGRF_17110715
NIHNS086907
Ministry of Science and Technology (China)2013DFE33080
National Natural Science Foundation of China31471238
100-Talent Project of Chinese Academy of SciencesUNSPECIFIED
Guangdong Province2014B030301058
PubMed Central ID:PMC5062122
Record Number:CaltechAUTHORS:20161017-151104599
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20161017-151104599
Official Citation:Tai, A. et al. SOXE neofunctionalization and elaboration of the neural crest during chordate evolution. Sci. Rep. 6, 34964; doi: 10.1038/srep34964 (2016).
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:71191
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:17 Oct 2016 22:21
Last Modified:03 Oct 2019 16:04

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