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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. Colloquium Transposons and genome evolution in plantsNina Fedoroff* The Pennsylvania State University, University Park, PA 16803 Although it is known today that transposons comprise a significant fraction of the genomes of many organisms, they eluded discovery through the first half century of genetic analysis and even once discovered, their ubiquity and abundance were not recognized for some time. This genetic invisibility of transposons focuses attention on the mechanisms that control not only transposition, but illegitimate recombination. The thesis is developed that the mechanisms that control transposition are a reflection of the more general capacity of eukaryotic organisms to detect, mark, and retain duplicated DNA through repressive chromatin structures. The 50 years that have elapsed since the publication of Stebbins' “Variation and Evolution in Plants” have seen extraordinary changes in our understanding of how genomes are structured and how they change in evolution. The book's publication date roughly coincides with the first reports by Barbara McClintock that there are genetic elements capable of transposing to different chromosomal locations in maize plants (1). The book contains a brief mention of Marcus Rhoades' observation that a standard recessive a1 allele of a gene in the anthocyanin biosynthetic pathway can become unstable and revert at a high frequency to the dominant A1 allele in a background containing a dominant Dt (“dotted”) allele (2). But transposable elements were not yet common fare, nor was it known that Dt is a transposon. Today we know that transposons constitute a large fraction—even a majority—of the DNA in some species of plants and animals, among them mice, humans, and such agriculturally important plants as corn and wheat. Given what we now know about genome organization, it is paradoxical that the discovery of transposable elements lagged so far behind the discovery of the basic laws of genetic transmission. And it is equally curious that even when they were discovered, acceptance of their generality and recognition of their ubiquity came so slowly. It is perhaps an understatement to say that McClintock's early communications describing transposition were not widely hailed for their explanatory power. Indeed, McClintock commented in the introduction to her collected papers that the response to her first effort in 1950 to communicate her discovery of transposition in “. . . a journal with wide readership . . . ,” specifically the Proceedings of the National Academy of Sciences, convinced her that “. . . the presented thesis, and evidence for it, could not be accepted by the majority of geneticists or by other biologists” (3). By contrast, the explanatory power of Watson and Crick's 1953 Nature paper on the structure and mode of replication of nucleic acids was recognized immediately (4). An informative parallel is provided by the contrast between the immediate recognition of the importance of Darwin's theory of evolution and the long delay between Mendel's articulation of the laws of heredity and their wide acceptance in evolutionary thinking (5). It can be speculated that this was because Darwin's theory provided immediate explanations in the realm of the perceptible, whereas the hereditary mechanisms underlying variation were obscure. Variation, in Darwin's view, was continuous. Geneticists sharing his view formed the “biometrical school,” devoted to the statistical analysis of inheritance. It was not at all clear how the simple rules derived by Mendel for the hereditary behavior of “differentiating characters” bore on the problem of evolution (5). The relevance of discontinuous variation or the production of “sports,” as morphological mutations were called, was even less obvious, because the biometric approach treated offspring as statistical combinations of parental traits. Thus the idea that the study of mutations was central to understanding evolution was close to unimaginable a century ago. Equally unimaginable at mid-20th century was the idea that transposable elements are essential to understanding chromosome structure and evolution, much less organismal evolution. The efforts of Bateson and other geneticists had firmly established Mendelian “laws” as the central paradigm of genetics and the identification and mapping of genetic “loci” through the study of mutant alleles was proceeding apace. Because genetic mapping is predicated on the invariance of recombination frequencies, there was plentiful evidence that genes have fixed chromosomal locations. Written at this time, Stebbins' book in general and in particular his third chapter, titled “The Basis of Individual Variation, ” clearly acknowledges the existence of many chromosomal differences among organisms in a population, including duplications, inversions, translocations, and deletions. At the same time, the book reflects the prevailing view that these “. . . are not the materials that selection uses to fashion the diverse kinds of organisms which are the products of evolution” (2). Instead, Stebbins concludes that the majority of evolutionarily important changes in physiology and morphology are attributable to classical genetic “point” mutations. Another half century has elapsed and the geneticist's “black box,” sprung open, spills nucleotide sequences at an ever accelerating pace. Our computers sift through genomes in search of genes, knee-deep in transposons. How could we not have seen them before? The answer is as straightforward as it is mysterious and worthy of consideration: they are invisible to the geneticist. Well, almost invisible. And of course it depends on the geneticist. The Discovery of TranspositionThe study of unstable mutations that cause variegation dates back to De Vries, who formulated the concept of “ever-sporting varieties ” and eventually came to the conclusion that these types of mutations do not obey Mendel's rules (6). The first person to make substantial sense of their inheritance was the maize geneticist Emerson, who analyzed a variegating allele of the maize P locus during the first decades of this century (7 –9). His first paper on the subject opens with the statement that variegation “. . . is distinguished from other color patterns by its
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