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

被引:47
作者
Chen, Jia-Yu [1 ]
Shen, Qing Sunny [1 ]
Zhou, Wei-Zhen [2 ]
Peng, Jiguang [1 ]
He, Bin Z. [3 ,4 ]
Li, Yumei [1 ]
Liu, Chu-Jun [1 ]
Luan, Xuke [1 ,5 ]
Ding, Wanqiu [1 ]
Li, Shuxian [1 ]
Chen, Chunyan [6 ]
Tan, Bertrand Chin-Ming [7 ]
Zhang, Yong E. [6 ]
He, Aibin [1 ,5 ]
Li, Chuan-Yun [1 ]
机构
[1] Peking Univ, Inst Mol Med, Beijing Key Lab Cardiometab Mol Med, Beijing 100871, Peoples R China
[2] Peking Univ, Coll Life Sci, Natl Lab Prot Engn & Plant Genet Engn, Ctr Bioinformat, Beijing 100871, Peoples R China
[3] Harvard Univ, FAS Ctr Syst Biol, Cambridge, MA 02138 USA
[4] Harvard Univ, Howard Hughes Med Inst, Cambridge, MA 02138 USA
[5] Peking Tsinghua Ctr Life Sci, Beijing, Peoples R China
[6] Chinese Acad Sci, Inst Zool, Key Lab Zool Systemat & Evolut, Beijing, Peoples R China
[7] Chang Gung Univ, Mol Med Res Ctr, Taoyuan, Taiwan
来源
PLOS GENETICS | 2015年 / 11卷 / 07期
基金
中国国家自然科学基金;
关键词
RHESUS MACAQUE; GC-CONTENT; DROSOPHILA-MELANOGASTER; PEPTIDEATLAS PROJECT; NONCODING RNAS; HUMAN PROTEOME; ORPHAN GENES; EVOLUTION; GENOME; EXPRESSION;
D O I
10.1371/journal.pgen.1005391
中图分类号
Q3 [遗传学];
学科分类号
071007 ; 090102 ;
摘要
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.
引用
收藏
页数:24
相关论文
共 69 条
[1]   Characterization of the human ESC transcriptome by hybrid sequencing [J].
Au, Kin Fai ;
Sebastiano, Vittorio ;
Afshar, Pegah Tootoonchi ;
Durruthy, Jens Durruthy ;
Lee, Lawrence ;
Williams, Brian A. ;
van Bakel, Harm ;
Schadt, Eric E. ;
Reijo-Pera, Renee A. ;
Underwood, Jason G. ;
Wong, Wing Hung .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2013, 110 (50) :E4821-E4830
[2]   Evidence for de novo evolution of testis-expressed genes in the Drosophila yakuba Drosophila erecta clade [J].
Begun, David J. ;
Lindfors, Heather A. ;
Kern, Andrew D. ;
Jones, Corbin D. .
GENETICS, 2007, 176 (02) :1131-1137
[3]   Recently evolved genes identified from Drosophila yakuba and Drosophila erecta accessory gland expressed sequence tags [J].
Begun, DJ ;
Lindfors, HA ;
Thompson, ME ;
Holloway, AK .
GENETICS, 2006, 172 (03) :1675-1681
[4]   The evolution of gene expression levels in mammalian organs [J].
Brawand, David ;
Soumillon, Magali ;
Necsulea, Anamaria ;
Julien, Philippe ;
Csardi, Gabor ;
Harrigan, Patrick ;
Weier, Manuela ;
Liechti, Angelica ;
Aximu-Petri, Ayinuer ;
Kircher, Martin ;
Albert, Frank W. ;
Zeller, Ulrich ;
Khaitovich, Philipp ;
Gruetzner, Frank ;
Bergmann, Sven ;
Nielsen, Rasmus ;
Paeaebo, Svante ;
Kaessmann, Henrik .
NATURE, 2011, 478 (7369) :343-+
[5]   Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses [J].
Cabili, Moran N. ;
Trapnell, Cole ;
Goff, Loyal ;
Koziol, Magdalena ;
Tazon-Vega, Barbara ;
Regev, Aviv ;
Rinn, John L. .
GENES & DEVELOPMENT, 2011, 25 (18) :1915-1927
[6]   De novo origination of a new protein-coding gene in Saccharomyces cerevisiae [J].
Cai, Jing ;
Zhao, Ruoping ;
Jiang, Huifeng ;
Wang, Wen .
GENETICS, 2008, 179 (01) :487-496
[7]   Proto-genes and de novo gene birth [J].
Carvunis, Anne-Ruxandra ;
Rolland, Thomas ;
Wapinski, Ilan ;
Calderwood, Michael A. ;
Yildirim, Muhammed A. ;
Simonis, Nicolas ;
Charloteaux, Benoit ;
Hidalgo, Cesar A. ;
Barbette, Justin ;
Santhanam, Balaji ;
Brar, Gloria A. ;
Weissman, Jonathan S. ;
Regev, Aviv ;
Thierry-Mieg, Nicolas ;
Cusick, Michael E. ;
Vidal, Marc .
NATURE, 2012, 487 (7407) :370-374
[8]   Hearing silence: non-neutral evolution at synonymous sites in mammals [J].
Chamary, JV ;
Parmley, JL ;
Hurst, LD .
NATURE REVIEWS GENETICS, 2006, 7 (02) :98-108
[9]   Effective population size and patterns of molecular evolution and variation [J].
Charlesworth, Brian .
NATURE REVIEWS GENETICS, 2009, 10 (03) :195-205
[10]  
Chen Hou-Yang, 2010, Zhonghua Nan Ke Xue, V16, P883