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Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis

Major evolutionary transitions are enigmas, and the most notable enigma is between invertebrates and vertebrates, with numerous spectacular innovations. To search for the molecular connections involved, we asked whether global epigenetic changes may offer a clue by surveying the inheritance and repr...

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Autores principales: Xu, Xiaocui, Li, Guoqiang, Li, Congru, Zhang, Jing, Wang, Qiang, Simmons, David K, Chen, Xuepeng, Wijesena, Naveen, Zhu, Wei, Wang, Zhanyang, Wang, Zhenhua, Ju, Bao, Ci, Weimin, Lu, Xuemei, Yu, Daqi, Wang, Qian-fei, Aluru, Neelakanteswar, Oliveri, Paola, Zhang, Yong E, Martindale, Mark Q, Liu, Jiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8291442/
https://www.ncbi.nlm.nih.gov/pubmed/34691960
http://dx.doi.org/10.1093/nsr/nwz064
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author Xu, Xiaocui
Li, Guoqiang
Li, Congru
Zhang, Jing
Wang, Qiang
Simmons, David K
Chen, Xuepeng
Wijesena, Naveen
Zhu, Wei
Wang, Zhanyang
Wang, Zhenhua
Ju, Bao
Ci, Weimin
Lu, Xuemei
Yu, Daqi
Wang, Qian-fei
Aluru, Neelakanteswar
Oliveri, Paola
Zhang, Yong E
Martindale, Mark Q
Liu, Jiang
author_facet Xu, Xiaocui
Li, Guoqiang
Li, Congru
Zhang, Jing
Wang, Qiang
Simmons, David K
Chen, Xuepeng
Wijesena, Naveen
Zhu, Wei
Wang, Zhanyang
Wang, Zhenhua
Ju, Bao
Ci, Weimin
Lu, Xuemei
Yu, Daqi
Wang, Qian-fei
Aluru, Neelakanteswar
Oliveri, Paola
Zhang, Yong E
Martindale, Mark Q
Liu, Jiang
author_sort Xu, Xiaocui
collection PubMed
description Major evolutionary transitions are enigmas, and the most notable enigma is between invertebrates and vertebrates, with numerous spectacular innovations. To search for the molecular connections involved, we asked whether global epigenetic changes may offer a clue by surveying the inheritance and reprogramming of parental DNA methylation across metazoans. We focused on gametes and early embryos, where the methylomes are known to evolve divergently between fish and mammals. Here, we find that methylome reprogramming during embryogenesis occurs neither in pre-bilaterians such as cnidarians nor in protostomes such as insects, but clearly presents in deuterostomes such as echinoderms and invertebrate chordates, and then becomes more evident in vertebrates. Functional association analysis suggests that DNA methylation reprogramming is associated with development, reproduction and adaptive immunity for vertebrates, but not for invertebrates. Interestingly, the single HOX cluster of invertebrates maintains unmethylated status in all stages examined. In contrast, the multiple HOX clusters show dramatic dynamics of DNA methylation during vertebrate embryogenesis. Notably, the methylation dynamics of HOX clusters are associated with their spatiotemporal expression in mammals. Our study reveals that DNA methylation reprogramming has evolved dramatically during animal evolution, especially after the evolutionary transitions from invertebrates to vertebrates, and then to mammals.
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spelling pubmed-82914422021-10-21 Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis Xu, Xiaocui Li, Guoqiang Li, Congru Zhang, Jing Wang, Qiang Simmons, David K Chen, Xuepeng Wijesena, Naveen Zhu, Wei Wang, Zhanyang Wang, Zhenhua Ju, Bao Ci, Weimin Lu, Xuemei Yu, Daqi Wang, Qian-fei Aluru, Neelakanteswar Oliveri, Paola Zhang, Yong E Martindale, Mark Q Liu, Jiang Natl Sci Rev Research Article Major evolutionary transitions are enigmas, and the most notable enigma is between invertebrates and vertebrates, with numerous spectacular innovations. To search for the molecular connections involved, we asked whether global epigenetic changes may offer a clue by surveying the inheritance and reprogramming of parental DNA methylation across metazoans. We focused on gametes and early embryos, where the methylomes are known to evolve divergently between fish and mammals. Here, we find that methylome reprogramming during embryogenesis occurs neither in pre-bilaterians such as cnidarians nor in protostomes such as insects, but clearly presents in deuterostomes such as echinoderms and invertebrate chordates, and then becomes more evident in vertebrates. Functional association analysis suggests that DNA methylation reprogramming is associated with development, reproduction and adaptive immunity for vertebrates, but not for invertebrates. Interestingly, the single HOX cluster of invertebrates maintains unmethylated status in all stages examined. In contrast, the multiple HOX clusters show dramatic dynamics of DNA methylation during vertebrate embryogenesis. Notably, the methylation dynamics of HOX clusters are associated with their spatiotemporal expression in mammals. Our study reveals that DNA methylation reprogramming has evolved dramatically during animal evolution, especially after the evolutionary transitions from invertebrates to vertebrates, and then to mammals. Oxford University Press 2019-10 2019-05-24 /pmc/articles/PMC8291442/ /pubmed/34691960 http://dx.doi.org/10.1093/nsr/nwz064 Text en © The Author(s) 2019. Published by Oxford University Press on behalf of China Science Publishing & Media Ltd. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Xu, Xiaocui
Li, Guoqiang
Li, Congru
Zhang, Jing
Wang, Qiang
Simmons, David K
Chen, Xuepeng
Wijesena, Naveen
Zhu, Wei
Wang, Zhanyang
Wang, Zhenhua
Ju, Bao
Ci, Weimin
Lu, Xuemei
Yu, Daqi
Wang, Qian-fei
Aluru, Neelakanteswar
Oliveri, Paola
Zhang, Yong E
Martindale, Mark Q
Liu, Jiang
Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis
title Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis
title_full Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis
title_fullStr Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis
title_full_unstemmed Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis
title_short Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis
title_sort evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8291442/
https://www.ncbi.nlm.nih.gov/pubmed/34691960
http://dx.doi.org/10.1093/nsr/nwz064
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