Primate and Rodent Specific Intron Gains and the Origin of Retrogenes with Splice Variants

Retroposition, a leading mechanism for gene duplication, is an important process shaping the evolution of genomes. Retrogenes are also involved in the gene structure evolution as a major player in the process of intron deletion. Here, we demonstrate the role of retrogenes in intron gain in mammals. We identified one case of “intronization,” the transformation of exonic sequences into an intron, in the primate specific retrogene RNF113B and two independent “intronization” events in the retrogene DCAF12L2, one in the common ancestor of primates and rodents and another one in the rodent lineage. Intron gain resulted from the origin of new splice variants, and both genes have two transcript forms, one with retained intron and one with the intron spliced out. Evolution of these genes, especially RNF113B, has been very dynamic and has been accompanied by several additional events including parental gene loss, secondary retroposition, and exaptation of transposable elements.

[1]  Abraham E. Tucker,et al.  Extensive, Recent Intron Gains in Daphnia Populations , 2009, Science.

[2]  H. Kaessmann,et al.  Evolutionary origin and functions of retrogene introns. , 2009, Molecular biology and evolution.

[3]  D. Haussler,et al.  Retrocopy contributions to the evolution of the human genome , 2008, BMC Genomics.

[4]  J. Garcia-Fernández,et al.  Origin of introns by 'intronization' of exonic sequences. , 2008, Trends in genetics : TIG.

[5]  N. Vinckenbosch,et al.  Chromosomal Gene Movements Reflect the Recent Origin and Biology of Therian Sex Chromosomes , 2008, PLoS biology.

[6]  S. Brenner,et al.  Investigation of loss and gain of introns in the compact genomes of pufferfishes (Fugu and Tetraodon). , 2008, Molecular biology and evolution.

[7]  J. Coulombe-Huntington,et al.  Intron loss and gain in Drosophila. , 2007, Molecular biology and evolution.

[8]  E. Koonin,et al.  Three distinct modes of intron dynamics in the evolution of eukaryotes. , 2007, Genome research.

[9]  Agnes Hotz-Wagenblatt,et al.  Comparative analysis of transposed element insertion within human and mouse genomes reveals Alu's unique role in shaping the human transcriptome , 2007, Genome Biology.

[10]  J. Turner,et al.  Meiotic sex chromosome inactivation , 2007, Current Biology.

[11]  J. Coulombe-Huntington,et al.  Characterization of intron loss events in mammals. , 2006, Genome research.

[12]  J. Chen,et al.  A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. , 2006, Molecular cell.

[13]  Walter Gilbert,et al.  The evolution of spliceosomal introns: patterns, puzzles and progress , 2006, Nature Reviews Genetics.

[14]  N. Vinckenbosch,et al.  Evolutionary fate of retroposed gene copies in the human genome. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Reymond,et al.  Emergence of Young Human Genes after a Burst of Retroposition in Primates , 2005, PLoS biology.

[16]  Arlin Stoltzfus,et al.  The evolutionary gain of spliceosomal introns: sequence and phase preferences. , 2004, Molecular biology and evolution.

[17]  R. Ellis,et al.  A phylogeny of caenorhabditis reveals frequent loss of introns during nematode evolution. , 2004, Genome research.

[18]  E. Koonin,et al.  Remarkable Interkingdom Conservation of Intron Positions and Massive, Lineage-Specific Intron Loss and Gain in Eukaryotic Evolution , 2003, Current Biology.

[19]  W. Gilbert,et al.  Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Alexei Fedorov,et al.  Large-scale comparison of intron positions among animal, plant, and fungal genes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Page,et al.  Retroposition of autosomal mRNA yielded testis-specific gene family on human Y chromosome , 1999, Nature Genetics.

[22]  Evan L. Mulligan,et al.  The Mouse Gene Encoding the Testis-Specific Isoform of Poly(A) Binding Protein (Pabp2) Is an Expressed Retroposon: Intimations That Gene Expression in Spermatogenic Cells Facilitates the Creation of New Genes , 1998, Journal of Molecular Evolution.

[23]  R. O’Neill,et al.  De novo insertion of an intron into the mammalian sex determining gene, SRY. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Phillip A. Sharp,et al.  Split genes and RNA splicing , 1994, Cell.

[25]  J. Brosius,et al.  Retroposons--seeds of evolution. , 1991, Science.

[26]  T. Cavalier-smith,et al.  Selfish DNA and the origin of introns , 1985, Nature.

[27]  R. Roberts,et al.  An amazing sequence arrangement at the 5′ ends of adenovirus 2 messenger RNA , 1977, Cell.

[28]  N. Vinckenbosch,et al.  RNA-based gene duplication: mechanistic and evolutionary insights , 2009, Nature Reviews Genetics.