Transposable elements as sources of variation in animals and plants

Abstract

A tremendous wealth of data is accumulating on the variety and distribution of transposable elements (TEs) in natural populations. There is little doubt that TEs provide new genetic variation on a scale, and with a degree of sophistication, previously unimagined. There are many examples of mutations and other types of genetic variation associated with the activity of mobile elements. Mutant phenotypes range from subtle changes in tissue specificity to dramatic alterations in the development and organization of tissues and organs. Such changes can occur because of insertions in coding regions, but the more sophisticated TE-mediated changes are more often the result of insertions into 5 flanking regions and introns. Here, TE-induced variation is viewed from three evolutionary perspectives that are not mutually exclusive. First, variation resulting from the intrinsic parasitic nature of TE activity is examined. Second, we describe possible coadaptations between elements and their hosts that appear to have evolved because of selection to reduce the deleterious effects of new insertions on host fitness. Finally, some possible cases are explored in which the capacity of TEs to generate variation has been exploited by their hosts. The number of well documented cases in which element sequences appear to confer useful traits on the host, although small, is growing rapidly.The book whose publication we are celebrating in this colloquium indicates that Theodosius Dobzhansky had a very special interest in gene mutation and its causes. Dobzhansky recognized mutation as the ''raw material'' on which natural selection acts and as the first of three steps necessary for evolution to take place. However, the discovery of transposable elements (TEs) in the 1940s by Barbara McClintock occurred a decade later, and it was a further 30 years before the significance of her findings started to be fully appreciated. Sixty years ago, Dobzhansky was well aware of the mutagenic properties of ionizing radiation discovered in 1927 by H. J. Muller but acknowledged that much less than 1% of spontaneous mutations were attributable to this cause. He distinguished between spontaneous and induced mutations: ''The former are those which arise in strains not consciously exposed to known or suspected mutation-producing agents.'' He also pointed out that ''since the name spontaneous constitutes only a thinlyveiled [sic] admission of the ignorance of the phenomenon to which it is applied, the quest for the causes of mutation has always occupied the attention of geneticists.'' Although at that time no clues to its nature were yet available, Dobzhansky realized that a major piece of the mutation puzzle was still missing. We believe he would have been intrigued with the discoveries of TEs in natural populations that have taken place during the last 20 years and that he would have been an active participant in the continuing debate about their role in evolution.

Distributions of epistasis in microbes fit predictions from a fitness landscape model

“…Different methods were used in each species to produce mutations (transposons for E. coli versus point mutations for VSV), but reviews of the empirical literature suggest that this should not result in strong differences for mutation effects on phenotype 30 or fitness traits 6 . The model we have presented here depends directly on phenotypic effects of mutations, not on their genetic nature, which may explain why it seems to accurately account for both the VSV and E. coli data sets.…”

Transgenerational Epigenetic Inheritance: Prevalence, Mechanisms, and Implications for the Study of Heredity and Evolution

“…It has been known for some time that the rates of mutation, transposition, and recombination are lower in condensed than in open chromatin (Belyaev and Borodin 1982;Jablonka and Lamb 1995), and that the movement of transposable elements, which is recognized as a major cause of genomic change (Kidwell and Lisch 1997), is markedly influenced by various types of internal (genetic) and external (environmental) stresses. It is therefore clear that epigenetic variations bias genetic changes.…”

“…It is involved in many important functions (for general reviews see Casadesú s and Low 2006;Vanyushin 2006a,b), including defence against genomic parasites (Kidwell and Lisch 1997), regulation and maintenance of gene activity patterns (Barlow and Bartolomei 2007;Li and Bird 2007), stabilization of chromosomal structure (Karpen and Hawley 2007), and DNA replication and repair (Mortusewicz et al 2005;Schermelleh et al 2007). In eukaryotes, methylation usually occurs on the cytosines in CpG doublets and also in CpNpG triplets in plants.…”

Different scales of Ty1/copia-like retrotransposon proliferation in the genomes of three diploid hybrid sunflower species

“…These mechanisms represent fundamentally different modes of mobilization, use different molecular processes, and have different implications from the perspective of evolutionary changes in genome size. Recent years have witnessed renewed interest in the potential ability of transposable elements to impact the evolution of genes and genomes in plant and animal systems (McDonald, 1995;SanMiguel et al, 1996;Kidwell and Lisch, 1997;Miller et al, 1999;Bennetzen, 2000;van de Lagemaat et al, 2003;DeBarry et al, 2006;Hawkins et al, 2006;Ungerer et al, 2006;Feschotte, 2008).…”