LINEs and SINEs of primate evolution

The primate order is a monophyletic group thought to have diverged from the Euarchonta more than 65 mya. 1 Recent paleontological and molecular evolution studies place the last common ancestor of primates even earlier (≥ 85 mya). 2 More than 300 extant primate species are recognized today, 3 , 4 clearly emphasizing their diversity and success. Our understanding of the evolution of primates and the composition of their genomes has been revolutionized within the last decade through the increasing availability and analyses of sequenced genomes. However, several aspects of primate evolution have yet to be resolved. DNA sequencing of a wider array of primate species now underway will provide an opportunity to investigate and expand on these questions in great detail. One of the most surprising findings of the human (Homo sapiens) genome project was the high content of repetitive sequences, in particular of mobile DNA. 5 This finding has been replicated in all available and analyzed primate draft genome sequences analyzed to date. 5–7 In fact, transposable elements (TEs) contribute about 50% of the genome size of humans, 5 chimpanzees (Pan troglodytes), 6 and rhesus macaques (Macacca mulatta). 7 The proportion of TEs among the overall genome content is likely even higher due to the decay of older mobile elements beyond recognition, rearrangements of genomes over the course of evolution, and the challenge of sequencing and assembling repeat‐rich regions of the genome. 8 , 9 Retrotransposons, in particular L1, long interspersed element 1 (LINE1), and Alu, a short interspersed element (SINE), are prominent in primate genomes, and have played a major role in genome evolution and architecture. The evolution and success of the primate‐specific LINE and SINE subfamilies (L1 and Alu in particular), their application in phylogenetic studies, and their impact on the architecture of primate genomes will be the focus of this review. In addition, we will briefly cover the emergence and impact of SVA (SINE‐R/VNTR/Alu), a composite retrotransposon of relatively recent origin, and of other SINEs that are not common to all primates.

[1]  A. Korol,et al.  Non-alignment comparison of human and high primate genomes , 2011, 1111.6172.

[2]  M. Batzer,et al.  Phylogeny of the macaques (Cercopithecidae: Macaca) based on Alu elements. , 2009, Gene.

[3]  C. Groves,et al.  Estimating the phylogeny and divergence times of primates using a supermatrix approach , 2009, BMC Evolutionary Biology.

[4]  M. Batzer,et al.  The impact of retrotransposons on human genome evolution , 2009, Nature Reviews Genetics.

[5]  E. Kirkness,et al.  Mobile elements create structural variation: analysis of a complete human genome. , 2009, Genome research.

[6]  E. Eichler,et al.  Comparative analysis of Alu repeats in primate genomes. , 2009, Genome research.

[7]  P. Deininger,et al.  Diverse cis factors controlling Alu retrotransposition: what causes Alu elements to die? , 2009, Genome research.

[8]  M. Batzer,et al.  An alternative pathway for Alu retrotransposition suggests a role in DNA double-strand break repair. , 2009, Genomics.

[9]  L. Walter,et al.  Retropositional events consolidate the branching order among New World monkey genera. , 2009, Molecular phylogenetics and evolution.

[10]  M. Batzer,et al.  L1 recombination-associated deletions generate human genomic variation , 2008, Proceedings of the National Academy of Sciences.

[11]  Ryan E. Mills,et al.  Active Alu retrotransposons in the human genome. , 2008, Genome research.

[12]  H. Kazazian,et al.  Retrotransposons Revisited: The Restraint and Rehabilitation of Parasites , 2008, Cell.

[13]  P. Deininger,et al.  LINE-1 ORF1 protein enhances Alu SINE retrotransposition. , 2008, Gene.

[14]  M. Batzer,et al.  Evolution of Human Retrosequences: Alu , 2008 .

[15]  P. Deininger,et al.  Mammalian non-LTR retrotransposons: for better or worse, in sickness and in health. , 2008, Genome research.

[16]  H. Kazazian,et al.  Progress in understanding the biology of the human mutagen LINE‐1 , 2007, Human mutation.

[17]  G. Schumann.  APOBEC3 proteins: major players in intracellular defence against LINE-1-mediated retrotransposition. , 2007, Biochemical Society transactions.

[18]  M. Batzer,et al.  Endonuclease-independent insertion provides an alternative pathway for L1 retrotransposition in the human genome , 2007, Nucleic acids research.

[19]  Bronwen L. Aken,et al.  Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences , 2007, Nature.

[20]  Webb Miller,et al.  Mobile DNA in Old World Monkeys: A Glimpse Through the Rhesus Macaque Genome , 2007, Science.

[21]  M. Batzer,et al.  A SINE-based dichotomous key for primate identification. , 2007, Gene.

[22]  M. Batzer,et al.  Different evolutionary fates of recently integrated human and chimpanzee LINE-1 retrotransposons. , 2007, Gene.

[23]  Miriam K. Konkel,et al.  Identification and characterization of novel polymorphic LINE-1 insertions through comparison of two human genome sequence assemblies. , 2007, Gene.

[24]  Jinchuan Xing,et al.  A mobile element-based evolutionary history of guenons (tribe Cercopithecini) , 2007, BMC Biology.

[25]  M. Batzer,et al.  SINEs of a nearly perfect character. , 2006, Systematic biology.

[26]  J. V. Moran,et al.  The Impact of LINE-1 Retro transposition on the Human Genome , 2006 .

[27]  M. Batzer,et al.  Emergence of primate genes by retrotransposon-mediated sequence transduction , 2006, Proceedings of the National Academy of Sciences.

[28]  S. Boissinot,et al.  Human Population Genetic Structure and Diversity Inferred from Polymorphic L1(LINE-1) and Alu Insertions , 2006, Human Heredity.

[29]  Matthew D. Dyer,et al.  Human genomic deletions mediated by recombination between Alu elements. , 2006, American journal of human genetics.

[30]  J. V. Moran,et al.  Cis-preferential LINE-1 reverse transcriptase activity in ribonucleoprotein particles , 2006, Nature Structural &Molecular Biology.

[31]  J. V. Moran,et al.  Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Batzer,et al.  Recently integrated Alu retrotransposons are essentially neutral residents of the human genome. , 2006, Gene.

[33]  M. Batzer,et al.  Birth of a chimeric primate gene by capture of the transposase gene from a mobile element. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[34]  T. Ishida,et al.  Alu-mediated 100-kb deletion in the primate genome: the loss of the agouti signaling protein gene in the lesser apes. , 2006, Genome research.

[35]  E. L. Prak,et al.  DNA Damage and L1 Retrotransposition , 2006, Journal of biomedicine & biotechnology.

[36]  S. Tishkoff,et al.  Whole genome computational comparative genomics: A fruitful approach for ascertaining Alu insertion polymorphisms. , 2006, Gene.

[37]  Stéphane Boissinot,et al.  Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. , 2005, Genome research.

[38]  Jerilyn A. Walker,et al.  SVA elements: a hominid-specific retroposon family. , 2005, Journal of molecular biology.

[39]  Jinchuan Xing,et al.  A mobile element based phylogeny of Old World monkeys. , 2005, Molecular phylogenetics and evolution.

[40]  Jerilyn A. Walker,et al.  Inference of human geographic origins using Alu insertion polymorphisms. , 2005, Forensic science international.

[41]  M. Batzer,et al.  Tracking Alu evolution in New World primates , 2005, BMC Evolutionary Biology.

[42]  Liane Gagnier,et al.  Genomic deletions and precise removal of transposable elements mediated by short identical DNA segments in primates. , 2005, Genome research.

[43]  Derek E Wildman,et al.  Moving primate genomics beyond the chimpanzee genome. , 2005, Trends in genetics : TIG.

[44]  Jean L. Chang,et al.  Initial sequence of the chimpanzee genome and comparison with the human genome , 2005, Nature.

[45]  M. Batzer,et al.  From the margins of the genome: mobile elements shape primate evolution , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[46]  J. Brosius,et al.  Alu-SINE exonization: en route to protein-coding function. , 2005, Molecular biology and evolution.

[47]  Jeffrey S. Han,et al.  LINE‐1 retrotransposons: Modulators of quantity and quality of mammalian gene expression? , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[48]  M. Batzer,et al.  Genomic rearrangements by LINE-1 insertion-mediated deletion in the human and chimpanzee lineages , 2005, Nucleic acids research.

[49]  S. Boissinot,et al.  The recent evolution of human L1 retrotransposons , 2005, Cytogenetic and Genome Research.

[50]  T. Heidmann,et al.  LINEs, SINEs and processed pseudogenes: parasitic strategies for genome modeling , 2005, Cytogenetic and Genome Research.

[51]  P. Stenson,et al.  A systematic analysis of LINE-1 endonuclease-dependent retrotranspositional events causing human genetic disease , 2005, Human Genetics.

[52]  M. Batzer,et al.  Alu retrotransposition-mediated deletion. , 2005, Journal of molecular biology.

[53]  M. Batzer,et al.  Under the genomic radar: the stealth model of Alu amplification. , 2005, Genome research.

[54]  Jinchuan Xing,et al.  Alu insertion loci and platyrrhine primate phylogeny. , 2005, Molecular phylogenetics and evolution.

[55]  M. Batzer,et al.  Straightening out the LINEs: LINE-1 orthologous loci. , 2005, Genomics.

[56]  Jinchuan Xing,et al.  Alu element mutation spectra: molecular clocks and the effect of DNA methylation. , 2004, Journal of molecular biology.

[57]  P. Pevzner,et al.  Whole-genome analysis of Alu repeat elements reveals complex evolutionary history. , 2004, Genome research.

[58]  J. Schmitz,et al.  Primate phylogeny: molecular evidence from retroposons , 2004, Cytogenetic and Genome Research.

[59]  M. Batzer,et al.  Identity by descent and DNA sequence variation of human SINE and LINE elements , 2004, Cytogenetic and Genome Research.

[60]  M. Batzer,et al.  Retrotransposition of Alu elements: how many sources? , 2004, Trends in genetics : TIG.

[61]  J. Schmitz,et al.  Primate jumping genes elucidate strepsirrhine phylogeny. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[62]  S. Boissinot,et al.  The insertional history of an active family of L1 retrotransposons in humans. , 2004, Genome research.

[63]  Jinchuan Xing,et al.  Differential alu mobilization and polymorphism among the human and chimpanzee lineages. , 2004, Genome research.

[64]  M. Hattori,et al.  DNA sequence and comparative analysis of chimpanzee chromosome 22 , 2004, Nature.

[65]  H. Kazazian.  Mobile Elements: Drivers of Genome Evolution , 2004, Science.

[66]  E. Ostertag,et al.  SVA elements are nonautonomous retrotransposons that cause disease in humans. , 2003, American journal of human genetics.

[67]  M. Batzer,et al.  Alu elements and hominid phylogenetics , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[68]  E. Eichler,et al.  An Alu transposition model for the origin and expansion of human segmental duplications. , 2003, American journal of human genetics.

[69]  Thierry Heidmann,et al.  LINE-mediated retrotransposition of marked Alu sequences , 2003, Nature Genetics.

[70]  J. Schmitz,et al.  A novel family of tRNA-derived SINEs in the colugo and two new retrotransposable markers separating dermopterans from primates. , 2003, Molecular phylogenetics and evolution.

[71]  Jerilyn A. Walker,et al.  Following the LINEs: an analysis of primate genomic variation at human-specific LINE-1 insertion sites. , 2003, Molecular biology and evolution.

[72]  Jerilyn A. Walker,et al.  Genetic variation among world populations: inferences from 100 Alu insertion polymorphisms. , 2003, Genome research.

[73]  Noam Shomron,et al.  The Birth of an Alternatively Spliced Exon: 3' Splice-Site Selection in Alu Exons , 2003, Science.

[74]  J. V. Moran,et al.  Hot L1s account for the bulk of retrotransposition in the human population , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Hans Zischler,et al.  Molecular cladistic markers in New World monkey phylogeny (Platyrrhini, Primates). , 2003, Molecular phylogenetics and evolution.

[76]  E. Eichler,et al.  Analysis of primate genomic variation reveals a repeat-driven expansion of the human genome. , 2003, Genome research.

[77]  Michael J Bamshad,et al.  Human population genetic structure and inference of group membership. , 2003, American journal of human genetics.

[78]  R. Deberardinis,et al.  A mouse model of human L1 retrotransposition , 2002, Nature Genetics.

[79]  J. Schmitz,et al.  The colugo (Cynocephalus variegatus, Dermoptera): the primates' gliding sister? , 2002, Molecular biology and evolution.

[80]  Jef D Boeke,et al.  Human L1 element target‐primed reverse transcription in vitro , 2002, The EMBO journal.

[81]  N. Okada,et al.  Characterization of novel Alu- and tRNA-related SINEs from the tree shrew and evolutionary implications of their origins. , 2002, Molecular biology and evolution.

[82]  Jef D Boeke,et al.  Molecular archeology of L1 insertions in the human genome , 2002, Genome Biology.

[83]  Lisa Deininger,et al.  Active Alu element "A-tails": size does matter. , 2002, Genome research.

[84]  J. V. Moran,et al.  A comprehensive analysis of recently integrated human Ta L1 elements. , 2002, American journal of human genetics.

[85]  Dan Graur,et al.  Alu-containing exons are alternatively spliced. , 2002, Genome research.

[86]  J. V. Moran,et al.  DNA repair mediated by endonuclease-independent LINE-1 retrotransposition , 2002, Nature Genetics.

[87]  M. Batzer,et al.  Alu repeats and human genomic diversity , 2002, Nature Reviews Genetics.

[88]  S. Tavaré,et al.  Using the fossil record to estimate the age of the last common ancestor of extant primates , 2002, Nature.

[89]  S. Boissinot,et al.  Adaptive evolution in LINE-1 retrotransposons. , 2001, Molecular biology and evolution.

[90]  E. Ostertag,et al.  Biology of mammalian L1 retrotransposons. , 2001, Annual review of genetics.

[91]  M. Hammer,et al.  Genetic Evidence on the Origins of Indian Caste Populations Material Supplemental , 2022 .

[92]  Jef D. Boeke,et al.  Human L1 Retrotransposition: cisPreference versus trans Complementation , 2001, Molecular and Cellular Biology.

[93]  J. Schmitz,et al.  SINE insertions in cladistic analyses and the phylogenetic affiliations of Tarsius bancanus to other primates. , 2001, Genetics.

[94]  P. Deininger,et al.  Upstream flanking sequences and transcription of SINEs. , 2000, Journal of molecular biology.

[95]  M. Nachman,et al.  Estimate of the mutation rate per nucleotide in humans. , 2000, Genetics.

[96]  S. Boissinot,et al.  L1 (LINE-1) retrotransposon evolution and amplification in recent human history. , 2000, Molecular biology and evolution.

[97]  Thierry Heidmann,et al.  Human LINE retrotransposons generate processed pseudogenes , 2000, Nature Genetics.

[98]  N Okada,et al.  SINE insertions: powerful tools for molecular systematics. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[99]  A. Smit.  Interspersed repeats and other mementos of transposable elements in mammalian genomes. , 1999, Current opinion in genetics & development.

[100]  D. Labuda,et al.  Monophyletic Origin of Alu Elements in Primates , 1998, Journal of Molecular Evolution.

[101]  M. Stoneking,et al.  Alu insertion polymorphisms and human evolution: evidence for a larger population size in Africa. , 1997, Genome research.

[102]  J. Jurka,et al.  Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[103]  A. Smit,et al.  The origin of interspersed repeats in the human genome. , 1996, Current opinion in genetics & development.

[104]  Jef D Boeke,et al.  Human L1 Retrotransposon Encodes a Conserved Endonuclease Required for Retrotransposition , 1996, Cell.

[105]  T. Shaikh,et al.  Dispersion and insertion polymorphism in two small subfamilies of recently amplified human Alu repeats. , 1995, Journal of molecular biology.

[106]  A. Smit,et al.  Ancestral, mammalian-wide subfamilies of LINE-1 repetitive sequences. , 1995, Journal of molecular biology.

[107]  M. Batzer,et al.  Gene conversion as a secondary mechanism of short interspersed element (SINE) evolution , 1995, Molecular and cellular biology.

[108]  R. J. Herrera,et al.  African origin of human-specific polymorphic Alu insertions. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[109]  R. Britten,et al.  Evidence that most human Alu sequences were inserted in a process that ceased about 30 million years ago. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[110]  C. Y. Yu,et al.  Structure and genetics of the partially duplicated gene RP located immediately upstream of the complement C4A and the C4B genes in the HLA class III region. Molecular cloning, exon-intron structure, composite retroposon, and breakpoint of gene duplication. , 1994, The Journal of biological chemistry.

[111]  C. Schmid,et al.  Phylogenetic isolation of a human alu flounder gene: Drift to new subfamily identity , 1993, Journal of Molecular Evolution.

[112]  N. Okada,et al.  Determination of the phylogenetic relationships among Pacific salmonids by using short interspersed elements (SINEs) as temporal landmarks of evolution. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[113]  A. Dugaiczyk,et al.  The emergence of new DNA repeats and the divergence of primates. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[114]  T. Eickbush,et al.  Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: A mechanism for non-LTR retrotransposition , 1993, Cell.

[115]  C. Hutchison,et al.  Master genes in mammalian repetitive DNA amplification. , 1992, Trends in genetics : TIG.

[116]  J. Boeke,et al.  Reverse transcriptase encoded by a human transposable element. , 1991, Science.

[117]  A. F. Scott,et al.  Isolation of an active human transposable element. , 1991, Science.

[118]  C. Schmid.  Human Alu subfamilies and their methylation revealed by blot hybridization. , 1991, Nucleic acids research.

[119]  M. Batzer,et al.  Evolution of the master Alu gene(s) , 1991, Journal of Molecular Evolution.

[120]  David W. Foltz,et al.  Amplification dynamics of human-specific (HS) Alu family members , 1991, Nucleic Acids Res..

[121]  P. Deininger,et al.  Characterization of a third major SINE family of repetitive sequences in the galago genome. , 1991, Nucleic acids research.

[122]  M. Batzer,et al.  A human-specific subfamily of Alu sequences. , 1991, Genomics.

[123]  A. Furano,et al.  Amplification of an ancestral mammalian L1 family of long interspersed repeated DNA occurred just before the murine radiation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[124]  A. Dugaiczyk,et al.  Newly arisen DNA repeats in primate phylogeny. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[125]  D. Labuda,et al.  Sequence conservation in Alu evolution. , 1989, Nucleic acids research.

[126]  T. Smith,et al.  A fundamental division in the Alu family of repeated sequences. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[127]  M. Miyamoto,et al.  Phylogenetic relations of humans and African apes from DNA sequences in the psi eta-globin region. , 1987, Science.

[128]  C. Schmid,et al.  Species-specific homogeneity of the primate Alu family of repeated DNA sequences. , 1983, Nucleic acids research.

[129]  B. Mcclintock.  The origin and behavior of mutable loci in maize , 1950, Proceedings of the National Academy of Sciences.

[130]  Miriam K. Konkel,et al.  Tumour invasion and metastasis initiated by microRNA-10b in breast cancer , 2008, Nature.

[131]  M. Batzer,et al.  Mobile DNA elements in primate and human evolution. , 2007, American journal of physical anthropology.

[132]  M. Batzer,et al.  Retrotransposable elements and human disease. , 2006, Genome dynamics.

[133]  A. Furano,et al.  The evolution of long interspersed repeated DNA (L1, LINE 1) as revealed by the analysis of an ancient rodent L1 DNA family , 2006, Journal of Molecular Evolution.

[134]  C. Schmid,et al.  Flanking sequences of an Alu source stimulate transcription in vitro by interacting with sequence-specific transcription factors , 2004, Journal of Molecular Evolution.

[135]  Carl W. Schmid,et al.  Standardized nomenclature for Alu repeats , 2004, Journal of Molecular Evolution.

[136]  S. Boissinot,et al.  L1 (LINE-1) retrotransposon diversity differs dramatically between mammals and fish. , 2004, Trends in genetics : TIG.

[137]  P. Chevret,et al.  Amplification of the ancient murine Lx family of long interspersed repeated DNA occurred during the murine radiation , 2004, Journal of Molecular Evolution.

[138]  N. Okada,et al.  Retroposon mapping in molecular systematics. , 2004, Methods in molecular biology.

[139]  V. Kapitonov,et al.  The age of Alu subfamilies , 2004, Journal of Molecular Evolution.

[140]  S. Boissinot,et al.  Different Rates of LINE-1 (L1) Retrotransposon Amplification and Evolution in New World Monkeys , 2003, Journal of Molecular Evolution.

[141]  International Human Genome Sequencing Consortium.  Initial sequencing and analysis of the human genome , 2001, Nature.

[142]  A. Furano,et al.  The biological properties and evolutionary dynamics of mammalian LINE-1 retrotransposons. , 2000, Progress in nucleic acid research and molecular biology.

[143]  C. Schmid,et al.  Phylogenetic isolation of a human Alu founder gene: drift to new subfamily identity [corrected]. , 1993, Journal of molecular evolution.

[144]  T. Shaikh,et al.  Structure and variability of recently inserted Alu family members. , 1990, Nucleic acids research.

[145]  P. Deininger,et al.  Repeat sequence families derived from mammalian tRNA genes , 1985, Nature.

[146]  J. Rogers,et al.  The origin and evolution of retroposons. , 1985, International review of cytology.