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Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis

Authors :
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
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
Publication Year :
2020

Abstract

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Xu, X., Li, G., Li, C., Zhang, J., Wang, Q., Simmons, D. K., Chen, X., Wijesena, N., Zhu, W., Wang, Z., Wang, Z., Ju, B., Ci, W., Lu, X., Yu, D., Wang, Q., Aluru, N., Oliveri, P., Zhang, Y. E., Martindale, M. Q., & Liu, J. Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis. National Science Review, 6(5), (2019):993-1003, doi:10.1093/nsr/nwz064.<br />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.<br />This work was supported by the National Key Research and Development Program of China (2018YFC1003303), the Strategic Priority Research Program of the CAS (XDB13040200), the National Natural Science Foundation of China (91519306, 31425015), the Youth Innovation Promotion Association of the CAS and the Key Research Program of Frontier Sciences, CAS (QYZDY-SSW-SMC016).

Details

Database :
OAIster
Publication Type :
Electronic Resource
Accession number :
edsoai.on1195523620
Document Type :
Electronic Resource