Emergence, Retention and Selection: A Trilogy of Origination for Functional De Novo Proteins from Ancestral LncRNAs in Primates

While some human-specific protein-coding genes have been proposed to originate from ancestral lncRNAs, the transition process remains poorly understood. Here we identified 64 hominoid-specific de novo genes and report a mechanism for the origination of functional de novo proteins from ancestral lncR...

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Main Authors:	Chen, Jia-Yu, Shen, Qing Sunny, Zhou, Wei-Zhen, Peng, Jiguang, He, Bin Z., Li, Yumei, Liu, Chu-Jun, Luan, Xuke, Ding, Wanqiu, Li, Shuxian, Chen, Chunyan, Tan, Bertrand Chin-Ming, Zhang, Yong E., He, Aibin, Li, Chuan-Yun
Format:	Online
Language:	English
Published:	Public Library of Science 2015
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4503675/

id	pubmed-4503675
recordtype	oai_dc
spelling	pubmed-45036752015-07-17 Emergence, Retention and Selection: A Trilogy of Origination for Functional De Novo Proteins from Ancestral LncRNAs in Primates Chen, Jia-Yu Shen, Qing Sunny Zhou, Wei-Zhen Peng, Jiguang He, Bin Z. Li, Yumei Liu, Chu-Jun Luan, Xuke Ding, Wanqiu Li, Shuxian Chen, Chunyan Tan, Bertrand Chin-Ming Zhang, Yong E. He, Aibin Li, Chuan-Yun Research Article While some human-specific protein-coding genes have been proposed to originate from ancestral lncRNAs, the transition process remains poorly understood. Here we identified 64 hominoid-specific de novo genes and report a mechanism for the origination of functional de novo proteins from ancestral lncRNAs with precise splicing structures and specific tissue expression profiles. Whole-genome sequencing of dozens of rhesus macaque animals revealed that these lncRNAs are generally not more selectively constrained than other lncRNA loci. The existence of these newly-originated de novo proteins is also not beyond anticipation under neutral expectation, as they generally have longer theoretical lifespan than their current age, due to their GC-rich sequence property enabling stable ORFs with lower chance of non-sense mutations. Interestingly, although the emergence and retention of these de novo genes are likely driven by neutral forces, population genetics study in 67 human individuals and 82 macaque animals revealed signatures of purifying selection on these genes specifically in human population, indicating a proportion of these newly-originated proteins are already functional in human. We thus propose a mechanism for creation of functional de novo proteins from ancestral lncRNAs during the primate evolution, which may contribute to human-specific genetic novelties by taking advantage of existed genomic contexts. Public Library of Science 2015-07-15 /pmc/articles/PMC4503675/ /pubmed/26177073 http://dx.doi.org/10.1371/journal.pgen.1005391 Text en © 2015 Chen et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Chen, Jia-Yu Shen, Qing Sunny Zhou, Wei-Zhen Peng, Jiguang He, Bin Z. Li, Yumei Liu, Chu-Jun Luan, Xuke Ding, Wanqiu Li, Shuxian Chen, Chunyan Tan, Bertrand Chin-Ming Zhang, Yong E. He, Aibin Li, Chuan-Yun
spellingShingle	Chen, Jia-Yu Shen, Qing Sunny Zhou, Wei-Zhen Peng, Jiguang He, Bin Z. Li, Yumei Liu, Chu-Jun Luan, Xuke Ding, Wanqiu Li, Shuxian Chen, Chunyan Tan, Bertrand Chin-Ming Zhang, Yong E. He, Aibin Li, Chuan-Yun Emergence, Retention and Selection: A Trilogy of Origination for Functional De Novo Proteins from Ancestral LncRNAs in Primates
author_facet	Chen, Jia-Yu Shen, Qing Sunny Zhou, Wei-Zhen Peng, Jiguang He, Bin Z. Li, Yumei Liu, Chu-Jun Luan, Xuke Ding, Wanqiu Li, Shuxian Chen, Chunyan Tan, Bertrand Chin-Ming Zhang, Yong E. He, Aibin Li, Chuan-Yun
author_sort	Chen, Jia-Yu
title	Emergence, Retention and Selection: A Trilogy of Origination for Functional De Novo Proteins from Ancestral LncRNAs in Primates
title_short	Emergence, Retention and Selection: A Trilogy of Origination for Functional De Novo Proteins from Ancestral LncRNAs in Primates
title_full	Emergence, Retention and Selection: A Trilogy of Origination for Functional De Novo Proteins from Ancestral LncRNAs in Primates
title_fullStr	Emergence, Retention and Selection: A Trilogy of Origination for Functional De Novo Proteins from Ancestral LncRNAs in Primates
title_full_unstemmed	Emergence, Retention and Selection: A Trilogy of Origination for Functional De Novo Proteins from Ancestral LncRNAs in Primates
title_sort	emergence, retention and selection: a trilogy of origination for functional de novo proteins from ancestral lncrnas in primates
description	While some human-specific protein-coding genes have been proposed to originate from ancestral lncRNAs, the transition process remains poorly understood. Here we identified 64 hominoid-specific de novo genes and report a mechanism for the origination of functional de novo proteins from ancestral lncRNAs with precise splicing structures and specific tissue expression profiles. Whole-genome sequencing of dozens of rhesus macaque animals revealed that these lncRNAs are generally not more selectively constrained than other lncRNA loci. The existence of these newly-originated de novo proteins is also not beyond anticipation under neutral expectation, as they generally have longer theoretical lifespan than their current age, due to their GC-rich sequence property enabling stable ORFs with lower chance of non-sense mutations. Interestingly, although the emergence and retention of these de novo genes are likely driven by neutral forces, population genetics study in 67 human individuals and 82 macaque animals revealed signatures of purifying selection on these genes specifically in human population, indicating a proportion of these newly-originated proteins are already functional in human. We thus propose a mechanism for creation of functional de novo proteins from ancestral lncRNAs during the primate evolution, which may contribute to human-specific genetic novelties by taking advantage of existed genomic contexts.
publisher	Public Library of Science
publishDate	2015
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4503675/
_version_	1613248293221957632

Emergence, Retention and Selection: A Trilogy of Origination for Functional De Novo Proteins from Ancestral LncRNAs in Primates

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