21 - Retrotransposition and Its Regulation Cytogenet Genome...

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Retrotransposition and Its Regulation Cytogenet Genome Res 110:242–249 (2005) DOI: 10.1159/000084958 Host defenses to transposable elements and the evolution of genomic imprinting J.F. McDonald, a M.A. Matzke, b A.J. Matzke b a Department of Biology, Georgia Institute of Technology, Atlanta, GA (USA); b Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences UZAII, Vienna (Austria) Manuscript received 27 December 2003; accepted in revised form for publication by J.-N- Volff 14 April 2004. Request reprints from: Dr. John F. McDonald, Department of Biology Georgia Institute of Technology, Atlanta, GA 30332 (USA) telephone: +1-404-894-3700; fax: +1-404-894-0519 e-mail: [email protected] ABC Fax + 41 61 306 12 34 E-mail [email protected] www.karger.com © 2005 S. Karger AG, Basel 1424–8581/05/1104–0242$22.00/0 Accessible online at: www.karger.com/cgr Abstract. Genomic imprinting is the differential expression of maternally and paternally inherited alleles of specific genes. Several organismic level hypotheses have been offered to explain the evolution of genomic imprinting. We argue that evolutionary explanations of the origin of imprinting that focus exclusively on the organismic level are incomplete. We propose that the complex molecular mechanisms that underlie genomic imprinting originally evolved as an adaptive response to the mutagenic potential of transposable elements (TEs). We also present a model of how these mechanisms may have been co- opted by natural selection to evolve molecular features charac- teristic of genomic imprinting. Copyright © 2005 S. Karger AG, Basel Traditional explanations of the evolution of adaptive traits postulate that natural selection operates on the organismic level consequences of random mutational events. While the general validity of this explanatory paradigm is well established, recent evidence indicates that it may not be complete (e.g. McDonald, 1999; Dover, 2002; Kazazian, 2004). The fact that genomes consist of selfish DNA, in addition to DNA encoding an organ- ism’s structure and function, raises the possibility of intra- genomic conflicts and consequent genomic level selection. For example, the inherent tendency of transposable elements (TEs) to replicate and expand in copy number may be mutagenic to an organism’s genes and thus selectively favor the evolution of mechanisms to reduce TE activity. The evolution of such repression systems by the host genome might, in turn, be expected to place selective pressure on TEs to escape repres- sion. This ongoing host genome-TE conflict can be equated to an arms race resulting in the evolution of ever more complex regulatory systems over time (McDonald, 1999). At least some of these regulatory systems may subsequently become co-opted for unrelated host functions and thereby accelerate evolution at the organismic level as well. According to this view, evolutiona- ry explanations of adaptive traits that focus exclusively on organismic level selection may be incomplete. One possible
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21 - Retrotransposition and Its Regulation Cytogenet Genome...

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