Centromere Remodeling in Hoolock leuconedys (Hylobatidae) by a New Transposable Element Unique to the Gibbons

被引:51
作者
Carbone, Lucia [1 ,2 ]
Harris, R. Alan [3 ]
Mootnick, Alan R. [4 ]
Milosavljevic, Aleksandar [3 ]
Martin, David I. K. [1 ]
Rocchi, Mariano [5 ]
Capozzi, Oronzo [5 ]
Archidiacono, Nicoletta [5 ]
Konkel, Miriam K. [6 ]
Walker, Jerilyn A. [6 ]
Batzer, Mark A. [6 ]
de Jong, Pieter J. [1 ]
机构
[1] Childrens Hosp Oakland Res Inst, Oakland, CA USA
[2] Oregon Hlth & Sci Univ, Oregon Natl Primate Res Ctr, Portland, OR 97201 USA
[3] Baylor Coll Med, Houston, TX 77030 USA
[4] Gibbon Conservat Ctr, Santa Clarita, CA USA
[5] Univ Bari, Bari, Italy
[6] Louisiana State Univ, Baton Rouge, LA 70803 USA
基金
美国国家卫生研究院;
关键词
gibbon; centromere; transposable element; SVA; hybrid; WHITE-CHEEKED GIBBON; HUMAN GENOME; EVOLUTION; METHYLATION; HYBRIDIZATION; CONSTRUCTION; ORGANIZATION; INHERITANCE; PHYLOGENY; DYNAMICS;
D O I
10.1093/gbe/evs048
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Gibbons (Hylobatidae) shared a common ancestor with the other hominoids only 15-18 million years ago. Nevertheless, gibbons show very distinctive features that include heavily rearranged chromosomes. Previous observations indicate that this phenomenon may be linked to the attenuated epigenetic repression of transposable elements (TEs) in gibbon species. Here we describe the massive expansion of a repeat in almost all the centromeres of the eastern hoolock gibbon (Hoolock leuconedys). We discovered that this repeat is a new composite TE originating from the combination of portions of three other elements (L1ME5, AluSz6, and SVA_A) and thus named it LAVA. We determined that this repeat is found in all the gibbons but does not occur in other hominoids. Detailed investigation of 46 different LAVA elements revealed that the majority of them have target site duplications (TSDs) and a poly-A tail, suggesting that they have been retrotransposing in the gibbon genome. Although we did not find a direct correlation between the emergence of LAVA elements and human-gibbon synteny breakpoints, this new composite transposable element is another mark of the great plasticity of the gibbon genome. Moreover, the centromeric expansion of LAVA insertions in the hoolock closely resembles the massive centromeric expansion of the KERV-1 retroelement reported for wallaby (marsupial) interspecific hybrids. The similarity between the two phenomena is consistent with the hypothesis that evolution of the gibbons is characterized by defects in epigenetic repression of TEs, perhaps triggered by interspecific hybridization.
引用
收藏
页码:760 / 770
页数:11
相关论文
共 47 条
[1]   Genome-wide characterization of centromeric satellites from multiple mammalian genomes [J].
Alkan, Can ;
Cardone, Maria Francesca ;
Catacchio, Claudia Rita ;
Antonacci, Francesca ;
O'Brien, Stephen J. ;
Ryder, Oliver A. ;
Purgato, Stefania ;
Zoli, Monica ;
Della Valle, Giuliano ;
Eichler, Evan E. ;
Ventura, Mario .
GENOME RESEARCH, 2011, 21 (01) :137-145
[2]   A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice [J].
Aravin, Alexei A. ;
Sachidanandam, Ravi ;
Bourc'his, Deborah ;
Schaefer, Christopher ;
Pezic, Dubravka ;
Toth, Katalin Fejes ;
Bestor, Timothy ;
Hannon, Gregory J. .
MOLECULAR CELL, 2008, 31 (06) :785-799
[3]   Natural hybridization in primates: One evolutionary mechanism [J].
Arnold, Michael L. ;
Meyer, Axel .
ZOOLOGY, 2006, 109 (04) :261-276
[4]   Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project [J].
Birney, Ewan ;
Stamatoyannopoulos, John A. ;
Dutta, Anindya ;
Guigo, Roderic ;
Gingeras, Thomas R. ;
Margulies, Elliott H. ;
Weng, Zhiping ;
Snyder, Michael ;
Dermitzakis, Emmanouil T. ;
Stamatoyannopoulos, John A. ;
Thurman, Robert E. ;
Kuehn, Michael S. ;
Taylor, Christopher M. ;
Neph, Shane ;
Koch, Christoph M. ;
Asthana, Saurabh ;
Malhotra, Ankit ;
Adzhubei, Ivan ;
Greenbaum, Jason A. ;
Andrews, Robert M. ;
Flicek, Paul ;
Boyle, Patrick J. ;
Cao, Hua ;
Carter, Nigel P. ;
Clelland, Gayle K. ;
Davis, Sean ;
Day, Nathan ;
Dhami, Pawandeep ;
Dillon, Shane C. ;
Dorschner, Michael O. ;
Fiegler, Heike ;
Giresi, Paul G. ;
Goldy, Jeff ;
Hawrylycz, Michael ;
Haydock, Andrew ;
Humbert, Richard ;
James, Keith D. ;
Johnson, Brett E. ;
Johnson, Ericka M. ;
Frum, Tristan T. ;
Rosenzweig, Elizabeth R. ;
Karnani, Neerja ;
Lee, Kirsten ;
Lefebvre, Gregory C. ;
Navas, Patrick A. ;
Neri, Fidencio ;
Parker, Stephen C. J. ;
Sabo, Peter J. ;
Sandstrom, Richard ;
Shafer, Anthony .
NATURE, 2007, 447 (7146) :799-816
[5]   Evolutionary Breakpoints in the Gibbon Suggest Association between Cytosine Methylation and Karyotype Evolution [J].
Carbone, Lucia ;
Harris, R. Alan ;
Vessere, Gery M. ;
Mootnick, Alan R. ;
Humphray, Sean ;
Rogers, Jane ;
Kim, Sung K. ;
Wall, Jeffrey D. ;
Martin, David ;
Jurka, Jerzy ;
Milosavljevic, Aleksandar ;
de Jong, Pieter J. .
PLOS GENETICS, 2009, 5 (06)
[6]   A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres [J].
Carone, Dawn M. ;
Longo, Mark S. ;
Ferreri, Gianni C. ;
Hall, Laura ;
Harris, Melissa ;
Shook, Nicole ;
Bulazel, Kira V. ;
Carone, Benjamin R. ;
Obergfell, Craig ;
O'Neill, Michael J. ;
O'Neill, Rachel J. .
CHROMOSOMA, 2009, 118 (01) :113-125
[7]   New Insights into Centromere Organization and Evolution from the White-Cheeked Gibbon and Marmoset [J].
Cellamare, A. ;
Catacchio, C. R. ;
Alkan, C. ;
Giannuzzi, G. ;
Antonacci, F. ;
Cardone, M. F. ;
Della Valle, G. ;
Malig, M. ;
Rocchi, M. ;
Eichler, E. E. ;
Ventura, M. .
MOLECULAR BIOLOGY AND EVOLUTION, 2009, 26 (08) :1889-1900
[8]  
Chen Liping, 2007, Genomics Proteomics & Bioinformatics, V5, P207, DOI 10.1016/S1672-0229(08)60008-X
[9]   Centromere DNA dynamics: Latent centromeres and neocentromere formation [J].
Choo, KHA .
AMERICAN JOURNAL OF HUMAN GENETICS, 1997, 61 (06) :1225-1233
[10]   The impact of retrotransposons on human genome evolution [J].
Cordaux, Richard ;
Batzer, Mark A. .
NATURE REVIEWS GENETICS, 2009, 10 (10) :691-703