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The following HTML text is provided to enhance online readability. Many aspects of typography translate only awkwardly to HTML. Please use the page image as the authoritative form to ensure accuracy. couple of essays written two decades ago, one by Doolittle and Sapienza (109) and one by Orgel and Crick (110). These essays sought rightly to free us from the then prevalent notion that genome structure is optimized by phenotypic selection. But the persistence of the moniker “selfish DNA” has become an impediment to further understanding of the origin, historical contribution, and contemporary role of transposons in chromosome structure. Transposons may be an inevitable by-product of the evolution of sequence-specific endonucleases. Complete transposons have been shown to arise from a single cleavage site and an endonuclease gene (111). Although the successful constitution of a transposon from the recognition sequences used in Ig gene rearrangement and the RAG1 and RAG2 proteins was interpreted as evidence that the V(D)J recombination system evolved from an ancient mobile DNA element, the fact is that the critical components of a transposon and a site-specific rearrangement system are the same (112). Thus questions about the origin of certain kinds of transposons may devolve to questions about the association of sequence-specific DNA binding domains with endonuclease domains. Although the majority of methylated sequences in a genome can be transposable elements, the view that DNA methylation evolved to control transposons seems implausible in the light of evidence that duplications of any kind trigger methylation in organisms that methylate DNA ( 108,113,114). And organisms that do not methylate DNA also have mechanisms for detecting duplications and sequestering repeats (115 –117). Genome expansion by duplication is predicated on preventing illegitimate recombination between duplicated sequences. Although different eukaryotic lineages appear to have invented different mechanisms, what is common to repeat-induced silencing in all eukaryotes is the stable packaging of DNA into “repressive” chromatin. It may be that the evolution of mechanisms that recognize, mark, and sequester duplications into repressive chromatin structures, among which some involve DNA methylation, were the prerequisites for expansion of genomes by endoreduplication at all scales. The additional benefit of such “repressive” mechanisms in minimizing spurious transcription could be secondary sequelae. Because sequence duplication is inherent in transposition, the ability to recognize and repress duplications would serve to minimize both the activity and the adverse impacts of transposons, rendering them genetically invisible and favoring their gradual accumulation. An important and as yet underappreciated property of compacted, inactive genomic regions is their ability to impose their organization on adjacent, as well as nonadjacent, active regions, often in a homology-dependent manner. This is evidenced in position effect variegation in Drosophila, an organism that does not methylate its DNA, as well as in plant paramutation, which involves DNA methylation (98,117). What has been learned recently from analyzing gene silencing and paramutation suggests that it does not take many tandem duplications to trigger the formation of a compacted, silenced region. A silenced region then may become a “sink” for insertions within it, as well as a silencer for homologous sequences located adjacent to it or elsewhere in the genome (117,118). ConclusionsThe key to understanding the prevalence of transposons in contemporary genomes, as well as their genetic invisibility, therefore may lie not in transposons themselves, but in the much more fundamental capacity of eukaryotic organisms to recognize and sequester duplications. Whether transposons, retrotransposons, and other repetitive elements accumulate extensively in a given evolutionary lineage may depend on several factors, among them the efficiency of repressive mechanisms and the rate at which the sequences undergo mutational and deletional decay. For example, methylation of C residues enhances the mutability of CG base pairs, hence methylation accelerates the divergence rate of newly arising duplications. This happens in an extreme form in Neurospora, in which many methylated CGs are mutated in the span of a single generation, and at more measured rates in plants and mammals, in which the mutability can be detected by virtue of a marked deficiency of the base pairs and triplets that are normally methylated (62,119,120). The burgeoning analyses of genomes also makes it evident that repressive mechanisms are imperfect. However slowly, genomes are inexorably restructured by transposition and rearrangements arising from ectopic interactions between dispersed transposons. Thus there is little remaining doubt that transposons are central to genome evolution. What is less clear is the relationship between genome restructuring and morphological change. We know that the magnitude of the morphological differences between species does not necessarily reflect the magnitude of the genetic or chromosomal differences between them. It recently has become evident, for example, that the marked morphological and developmental differences between teosinte and maize are attributable to a very small number of genes and that for some genes, the differences are regulatory, rather than structural (58,121). It is also well known that genes are expressed differently depending on their chromosomal position. But what remains to be discovered is the extent to which chromosomal restructuring contributes to organismal evolution. 1. McClintock, B. ( 1945) Am. J. Bot. 32, 671–678. 2. Stebbins, L. G., Jr. ( 1950) Variation and Evolution in Plants (Columbia Univ. Press, New Tirj). 3. McClintock, B. ( 1987) The Discovery and Characterization of Transposable Elements (Garland, New York). 4. Watson, J. D. & Crick, F. H. C. ( 1953) Nature (London) 171, 737–738. 5. Carlson, E. A. ( 1966) The Gene: A Critical History (Saunders, Philadelphia). 6. de Vries, H. ( 1905) Species and Varieties: Their Origin by Mutation (Open Court, Chicago), 2nd Ed. 7. Emerson, R. A. ( 1914) Am. Nat. 48, 87–115. 8. Emerson, R. A. ( 1917) Genetics 2, 1–35. 9. Emerson, R. A. ( 1929) Genetics 14, 488–511. 10. Goldschmidt, R. ( 1938) Physiological Genetics (McGraw–Hill, New York). 11. Fedoroff, N. V. ( 1998) in Discoveries in Plant Biology, eds. Kung, S.-D. & Yang, S.-F. (World Scientific, Singapore), pp. 89–104. 12. Rhoades, M. M. ( 1936) J. Genet. 33, 347–354. 13. Rhoades, M. M. ( 1938) Genetics 23, 377–397. 14. McClintock, B. ( 1946) Year Book Carnegie Inst. Washington 45, 176–186. 15. McClintock, B. ( 1947) Year Book Carnegie Inst. Washington 46, 146–152. 16. McClintock, B. ( 1948) Year Book Carnegie Inst. Washington 47, 155–169. 17. McClintock, B. ( 1949) Year Book Carnegie Inst. Washington 48, 142–154. 18. McClintock, B. ( 1951) Year Book Carnegie Inst. Washington 50, 174–181. 19. McClintock, B. ( 1954) Year Book Carnegie Inst. Washington 53, 254–260. 20. Fedoroff, N. ( 1989) in Mobile DNA, eds. Howe, M. & Berg, D. (Am. Soc. Microbiol., Washington, DC), pp. 375–411. 21. McClintock, B. ( 1978) Stadler Genet. Symp. 10, 25–48. 22. Fedoroff, N., Wessler, S. & Shure, M. ( 1983) Cell 35, 243–251. 23. Pereira, A., Schwarz-Sommer, Z., Gierl, A., Bertram, I., Peterson, P. A. & Saedler, H. ( 1985) EMBO J. 4, 17–23. 24. Masson, P., Surosky, R., Kingsbury, J. A. & Fedoroff, N. V. ( 1987) Genetics 117, 117–137. 25. Fedoroff, N., Furtek, D. & Nelson, O. ( 1984) Proc. Natl. Acad. Sci. USA 81, 3825–3829. 26. Banks, J. A. & Fedoroff, N. ( 1989) Dev. Genet. 10, 425–437. 27. Shepherd, N. S., Schwarz-Sommer, Z., Blumberg vel Spalve, J., Gupta, M., Wienand, U. & Saedler, H. ( 1984) Nature (London) 307, 185–187. 28. Flavell, A. J. ( 1992) Genetica 86, 203–214. 29. Purugganan, M. D. & Wessler, S. R. ( 1994) Proc. Natl. Acad. Sci. USA 91, 11674–11678. 30. White, S. E., Habera, L. F. & Wessler, S. R. ( 1994) Proc. Natl. Acad. Sci. USA 91, 11792–11796. 31. Suoniemi, A., Schmidt, D. & Schulman, A. H. ( 1997) Genetica 100, 219–230.
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