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Horizontal Gene Transfer a. Genet., Vol. 75, Number 2, August 1996, pp. 219-232, (O~ Indian Academyof Sciences REVIEW ARTICLE Horizontal gene transfer VIJI KRISHNAPILLAI Department of Genetics and Developmental Biology, Monash University, Clayton 3168, Victoria, Australia MS received22 August 1996 Abstract. This review explores examples of horizontal genetic transfer in eukaryotes and prokaryotes. The best understood of these involvesvarious conserved familiesof transposable elements, but examples of non-transposable-element-based movement of genes or gene clusters have also been identifiedin prokaryotic gcnomes. A unifying theme is the structural and DNA-sequence homology of transposable elements from widely unrelated genomes, suggesting evolutionarilyconserved mechanisms for horizontal transfer. This is reinforced by the fundamental similarity in the enzymaticmechanisms of retroviral integration (by integ- rases) and of transposition (by transposases). The reviewdeals with various types of horizontal transfer, the mechanismsavailable for such transfer, potential barriers, and the evolutionary significanceof horizontal genetictransfer. Keywords. Horizontal transfer; eukaryotes;prokaryotes; transposable dements. 1. Introduction The biological world is composed of a vast array of simple and complex organisms, and current evolutionary ideas place all of them within two major biological classifications, namely the Prokarya (Bacteria and Archaea) and the Eukarya (protists, fungi, plants and animals). Considerable evidence has been accumulated on the biological relation- ships between these two major groupings (Margulis 1996). However, revealed behind this panoramic view of the biological universe is the considerable complexity of individual genomes. 2. Genome complexity At one level of complexity are the huge size differences between the genomes of organisms. Starting with bacteria, but excluding the even smaller genomes of viruses, genome sizes vary from 580 kb for Mycoplasma to 9500 kb for Myxococcus (Krawiec and Riley 1990). This range of about 15-fold is to be contrasted with the large genome-size differences observed in the eukaryotes. For example, in plants of the family Graminae (which includes the cereal crops) genome size varies from the rice genome of 430Mb to that of the hexaploid wheat of 16,000Mb, a range of about 37-fold (Moore et al. 1993). Other estimates show that among flowering plants the range is between 50,000 and 80,000 Mb (Bennett and Smith 1976). The largest genome known (102,000 Mb) is that of the primitive South American lungfish (Kornberg and Baker 1992). For comparison, the human genome is only 3000 Mb. One immediately striking and distinctive difference in the structure of prokaryotic and eukaryotic genomes is the incredible excess of noncoding over coding DNA in the 219 220 Viji Krishnapillai latter. For example, 97% of the human genome is noncoding DNA and only 3% has coding functions, e.g. for synthesis and regulation of proteins and structural compo- nents of the cell (Bernardi t995). Among the genomes of barley (Hordeum vulgare), wheat (Triticum aestivum) and rice (Oryza sativa) 50-80% is noncoding and comprised of different types of repetitive DNA (Moore et al. 1993). There are a range of different types of repetitive DNA in eukaryotic genomes, including minisatellite (15-bp repeats) and microsatellite (2-5 bp) DNA and transposable elements. The former two types are composed of moderately and tandemly repeated DNAs, while the latter represent dispersed and mobile sequences (Charlesworth et al. 1994). Well-characterized repeats in the mammalian genome include the LINES (tong interspersed repeat sequences) and SINES (short interspersed repeat sequences), which are present in 20,000-60,000 and 500,000 copies respectively (Passarge 1995). In comparison, less than about 2% of prokaryotic genomes is comprised of different types of repetitive DNA, either ribosomal RNA operons, transfer RNA genes, or insertion sequences and other transposable elements (transposons); the bulk of the genome (98 %), however, is coding DNA (Lupski and Weinstock 1992). A further distinctive feature of eukaryotic genomes is its compositional compartmen- talization into distinct isochores or 'islands' of varying GC content (Bernardi 1995). For example, in the human genome this can be identified physically by ultracentrifugation into three major fractions: GC-poor (<40%), GC-rich (40-50%) and GC-very-rich (> 55%) DNA. This last category makes up 3-4% of the genome, and contains all the coding sequences (Bernardi 1995). Within related genomes, such as those of the verte- brates, the GC compositional distribution is highly conserved but different fi'om that of the avians. Such compositional differences are also evident in plants. For example, 10-20% of the maize genome contains all the coding genes; the GC range is restricted to 1-2% and this isochore is called the 'gene space' (Bernardi 1995). Current major thrusts in genome research are identification and characterization of genes of medical, veterinary and agricultural interest (in human, animal and plant genome research respectively) and also identification and functional elucidation of the vast array of tandem and dispersed repetitive DNAs in genomes, These are being investigated in the large number of genome sequencing projects for various organisms, of which the Human Genome Sequence Project is paramount. The rapid pace of these sequencing projects is attested to by the achievement of high-density physical/genetic maps of the human and mouse genomes on the basis of use of microsatellite-DNA markers and their mapping correlation with genetic markers. The human genome is now delineated by markers about 700,000 bp apart and the mouse genome by markers 400,000 bp apart (Dib et al. 1996; Dietrich et al. 1996). Shnilar sequencing projects are also under way for a range of other organisms, including the plant Arabidopsis, the nematode Caenorhabditis eIegans and the yeast Saccharomyces cerevisiae, and, increasingly, also for other plants and animals of agronomic, agricultural and veterinary importance. With the completion of sequencing of the genomes of the prokaryotes HaemophiIus influenzae (1,830,137 bp; Fleischmann et al. 1995), Myeoplasma genitalium (580,070 bp; Fraser et aI. 1995), Methanococcus jannaschii (Bult et al. 1996), Synechocystis (Holden 1996), and of the lower eukaryote Saccharomyces cerevisiae (Dujon 1996), a suite of others are being considered for sequencing on the basis of medical, industrial and scientific interest. Among those favoured are two extremophiles, Archaeoglobus fuIgidus (an archaebacterium) and Thermatoga maririma (a eubacterium), and either a Synechococcus sp. (a cyanobacterium) or Clostridium acetobutylicum (a eubactefium) (Holm,nan 1996). Horizontal gene transfer 221 3. Horizontal gene transfer It is in the context of organizational features of genomes that the issue of horizontal genetic transmission has to be considered, as much of this, but not all, pertains to the repetitive DNA in genomes. This review will be restricted to natural examples of horizontal transfer and will not include those achieved in the laboratory by gene manipulation techniques. An example of the dramatic and frightening consequences of horizontal genetic transfer are the dreaded human immunodeficiency viruses (HIV), which, it is speculated, have been transferred from wild primates (chimpanzees and sooty mangabeys) to humans (Reines 1996). We have been aware traditionally that much of the genetic variability within species is generated by homologous recombina- tion during meiosis, and the enzymology of this process is now welI understood (Leach 1996). This is what we understand by Mendelian inheritance as it simply involves the reassortment of alleles of genes from generation to generation, i.e. by germinal vertical transmission. However, it has become increasingly clear that an alternative mechanism of inheritance is at work in prokaryotes and eukaryotes, namely horizontal (or lateral) genetic transmission, and this is based not on homologous recombination (requiring extensive sequence homology) but on site-specific, transpositional or illegitimate recombination (not requiring sequence homology) (Leach 1996). It is such a mechanism that accounts for the movement of transposable elements fi'om genome to genome, between both related and unrelated genomes. There are three main types of transposable elements in eukaryotes, distinguished on the basis of their genetic and DNA/protein sequence organization (Leach 1996). These are: (i) Transposons, which have perfect or imperfect terminal repeats, which transpose using a DNA intermediate and produce target-site duplications of 8 bp. Examples include the Ac element of maize (4565 bp) (Kunze 1996) and the P element of Drosophila (2907bp) (Engels 1996); these resemble prokaryotic transposons (see below). Very promiscuous elements, found in organisms ranging from fungi to vertebrates, include TcI from C. elegans and mariner from Drosophila. (ii) Retrotransposons, which are similar to retroviruses in their genome organization, e.g. by having long terminal repeats (LTR) and a mode of transposition via an RNA intermediate, generation of 5-bp duplications at the target site, and in their gene products. Examples include the mating-type element Tyl of yeast (6000 bp) and copia of Drosophila. (iii) Retroposons, which are chiefly distinguished by the absence of LTR and the generation of target-site duplications of 12 bp. The enzymatic process of transposition
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