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Transposable Elements and Host Genome Evolution

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Transposable Elements and Host Genome Evolution TRANSPOSABLE ELEMENTS AND HOST GENOME EVOLUTION Margaret G. Kidwell and Damon R. Lisch Margaret Kidwell is at the Dept of Ecology and Evolutionary Biology, The University of Arizona, 116 BSW Building, Tucson, AZ 85721, USA (email: [email protected]). Damon Lisch is at the Dept of Plant and Microbial Biology, 111 Koshland Hall, U.C Berkeley, Berkeley, CA 94720, USA (email: [email protected]) Corresponding author: Dr. Margaret G. Kidwell, Department of Ecology and Evolutionary Biology, The University of Arizona, 116 BSW Building, Tucson, AZ 85721, USA. Phone:(520) 621-1784. Fax: (520) 621- 9190. Email: [email protected] Keywords: Animal, Plant, Transposable Elements, Enhancer Elements, Evolution, Gene Expression, Gene Regulation, Molecular Sequence Data, Repetitive Sequences, DNA Methylation 1 A number of recent reports have challenged the idea that TEs are mainly "selfish" or "junk" DNA with little importance for host evolution. It has been proposed that TEs have the potential to provide host genomes with the ability to enhance their own evolution. They might also be a major source of genetic diversity that allows response to environmental changes. Because the relationships between TEs and host genomes are highly variable and the selfish, junk and beneficial DNA hypotheses are by no means mutually exclusive, a single label for these relationships appears to be inappropriate and potentially misleading. Transposable elements (TEs) are mobile DNA sequences that are widely distributed in bacteria, plants and animals. At least two levels of selection can apply to TEs: selection at the DNA level and selection at the level of the host organism. Positive selection at the DNA level results from the ability of TE sequences to replicate faster than those of the host genome. This aspect of selection is the basis of "the selfish DNA hypothesis", or, more accurately, "the parasitic DNA hypothesis". Negative selection at the host organismal level commonly results from either TE- induced insertional mutations that are deleterious to hosts or ectopic recombination between homologous TE sequences located in nonhomologous regions of the genome. Neutrality of TEs at the organismal level is also common, especially for inactive TEs that make up the vast majority of the TE complement of many eukaryotic genomes. This neutrality is the basis of "the junk DNA hypothesis". Although it is generally accepted that positive selection of TEs is possible at the organismal level, expert opinion is currently sharply divided about the frequency of the beneficial effects of TEs on host genomes. One school of thought claims that positive selection is so rare that it has virtually no impact on host evolution. A second perspective, increasingly expressed in recent months, is that TEs might provide beneficial effects to their hosts more frequently than previously acknowledged, and sometimes in unexpected ways. This review summarizes some recent ideas concerning actual and potential beneficial effects of TEs on host evolution and focuses on evidence that TEs have the capacity to restructure genomes in particularly interesting ways. This capacity might not have been exploited very often, nor has it necessarily been subject to positive selection. However, given the opportunistic nature of evolution, the presence of such a potent agent for change at the molecular level is at least potentially important for host evolution at the phenotypic level. Eukaryotic TEs are divided into two main classes according to their structural organization and mechanism of transposition. Class I elements use an RNA-mediated mode of transposition and encode a reverse transcriptase (RT). There are three distinct subclasses of RT-encoding TEs found throughout eukaryotes, the retrotransposons, the retroposons and the retrointrons (McClure, 1999). The retroposons include the short interspersed nuclear elements (SINES) and the long interspersed nuclear elements (LINES). Class II elements, the transposons (sensu strictu), use a DNA based mode of transposition. Although wide variation exists from one species to another in copy number, distribution and type, TEs comprise a huge fraction of the genomes of many animals and plants. For example, the human genome consists of at least 35% TEs(Smit & Riggs, 1996). Also, retrotransposons constitute more than 50% of the maize genome (Fig. 1). TE insertions have resulted in a doubling of the size of this genome within the last few million years(SanMiguel et al., 1998). More compact plant genomes, such as that of Arabidopsis thaliana, carry a smaller fraction of TEs and might have mechanisms to prevent amplification of extant element families(Wright et al., 1996) (Table 1). 2 Opie-3 Ji-5 solo Opie-2 Huck-2 Grande-zm1 Opie-1 Ji-2 solo Ji-3 Ji-5 Milt Fourf Huck-1 Ji-1 Ji-6 Victim Adh1-F u22 Fig. 1. Arrangement of retrotransposons Opie, Ji, Huck, Grande, Milt, Fourf and Victim identified within a 280 Kb fragment of the maize genome containing the Adh1-F and u22 genes. Note the insertion patterns of the elements nested within one another and within intergenic regions. Modified from(SanMiguel et al., 1996). In contrast to earlier interpretations that large genomic TE fractions provide evidence for the absence of any important role in organismal evolution, Henikoff et al.(Henikoff et al., 1997) conclude that they "may be a manifestation of the evolutionary benefits of genomic flexibility". However, given the huge variation in TE copy number among a wide variety of successful eukaryotic lineages, it is unclear whether or not increased TE copy number is itself subject to positive selection by virtue of its potential to increase genome flexibility. Charlesworth et al.(Charlesworth et al., 1994) have documented the low frequency of fixed TE sites in Drosophila melanogaster. They concluded that apart from the deleterious consequences of induced mutation and recombination, these elements are of little or no importance to the evolution of their hosts. However, it has not been demonstrated that these results are generally applicable to a wide range of species. Indeed, a large number of TE insertions are fixed within mammalian species, leaving open the possibility that a subset of insertions has been subject to positive selection(Deininger, 1989). In contrast to Drosophila melanogaster, in which TEs are distributed randomly along the distal sections of the chromosome arms(Charlesworth et al., 1992), TEs are distributed nonrandomly in the genomes of many other species. Clustering of TEs appears to be facilitated by specific characteristics of particular regions of host genomes. For instance, the TE complement of the compact genome of Saccharomyces cerevisiae is restricted to five families of retroelements(Kim et al., 1998). In this yeast, target site preference can be altered by mutations in genes encoding proteins involved in chromatin assembly and chromatin-mediated gene silencing(Huang et al., 1999; Zou & Voytas, 1997) and TEs are clearly targeted to specific regions of the genome. Further, even in D. melanogaster, TEs are non-randomly distributed within heterochromatin, with each class of TE occupying a distinct region(Pimpinelli et al., 1995). It is possible that TEs might play an especially useful role as mutators in evolution because of the broad spectrum of mutations produced by their activity(Kidwell & Lisch, 1997). It has been claimed that "although simple DNA base substitutions are well suited for the generation, diversification and optimization of local protein space, a hierarchy of mutational events is required for the rapid generation of protein diversity in evolution"(Bogarad & Deem, 1999). If this turns out to be true, then it should be noted that TEs and viruses are important generators of the more complex types of mutations in the mutational hierarchy. Table 1. Comparative genomic proportions occupied by transposable elements in a variety of model organisms 3 Species Haploid genome TEs as % of TE types References size in Mbp genome Homo sapiens 3300 35 LINES, Alu (10%) (Kazazian & Moran, 1998) HERVs (1.3%) DNA TEs (1.6%) Zea mays 2400 >50 Retrotransposons (SanMiguel et al., 1996) DNA elements Drosophila 140 10-18 >40 families of Class I (Biemont & and II elements Cizeron, 1999) melanogaster Arabidopsis thaliana 97 5 AthE1 Stephen Wright, pers. comm., Retroposons (Wright et al., 1996),(Waterston MITEs & Sulston, 1995) Caenorhabditis 100 10 DNA elements (Waterston & elegans Sulston, 1995), LTR retrotranposons Nathan Bowen, pers. comm. Saccharomyces 20 3.1 Ty-1, Ty-2, (Kim et al., cerevisiae 1998) Ty-3, Ty-4, and Ty-5 retrotransposons only The role of TEs as potent genomic reorganizers continues to be documented. In contrast to the high stability of the yeast genome during mitosis, chromosomal reorganization occurs with very high frequency in meiosis(Codon et al., 1997). A major factor in this instability is interchromosomal translocation between multiple copies of the Ty1 and Ty2 TE families. The direct implication of TEs in inversion break formation in natural populations of many species has long been hypothesized. Now the presence of a TE at the junction of the naturally occurring inversion 2Rd' in the malaria mosquito, Anopheles arabiensis, has been documented(Mathiopoulos et al., 1998). This species is rich in paracentric inversions, perhaps due to TE activity. The massive amplification of retroelements in a single generation in wallaby species hybrids(O'Neill et al., 1998) provides an impressive example of the capacity of TEs to
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