Genome Evolution: Gene and Genome Duplications and the Origin of Novel Gene Functions

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These comparisons typically reveal dramatic expansions and contractions of gene families that can be related to underlying biological differences.

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For example, humans and mice differ in their sensory reliance on sight and smell respectively; colour vision in humans has been significantly enhanced by the duplication of an Opsin gene that allows us to distinguish light at three different wavelengths, while mice can distinguish only two. By contrast, a much higher proportion of the large gene family of olfactory receptors have retained their functionality in mice, as compared to humans.

Given the apparent importance of gene duplication for the evolution of new biological functions over all evolutionary timescales, it is of great interest to be able to comprehensively document the duplicative differences that exist between our own species and our closest relatives, the great apes. The study by Fortna et al. This is the first time that copy number changes among apes have been assayed for the vast majority of human genes, and we can expect that the biological consequences of the human-specific copy number changes identified in this study will be heavily investigated over the coming years.

The various mechanisms by which genes become duplicated are often classified on the basis of the size of duplication generated, and whether they involve an RNA intermediate Figure 1. A two-exon gene is flanked by two Alu elements and a neighbouring replication termination site.

Recombination between the two Alu elements leads to a tandem duplication event, as does a replication error instigated by the replication termination site. Retrotransposition of the mRNA of the gene leads to the random integration of an intron-less paralogue at a distinct genomic location. The resultant duplicated genes retrogenes lack introns and have poly-A tails. Separated from their regulatory elements, these integrated sequences rarely give rise to expressed full-length coding sequences, although functional retrogenes have been identified in most genomes.

These recombination events can also give rise to the deletion or inversion of intervening sequences. Recent evidence suggests that the explosion of segmental duplications in recent primate evolution has been caused in part by the rapid proliferation of Alu elements about 40 MYA. The striking enrichment of Alu elements at the junctions between duplicated and single copy sequences implicates unequal crossing over between these repeats in the generation of segmental duplications Bailey et al.

The observation of segmental duplication events with no evidence for homology-driven unequal crossing over suggests that segmental duplications can also arise through non-homologous mechanisms. A recent screen for spontaneous duplications in yeast suggests that replication-dependent chromosome breakages also play a significant role in generating tandem duplications, because duplication breakpoints are enriched at replication termination sites Koszul et al.

Genome duplication events generate a duplicate for every gene in the genome, representing a huge opportunity for a step-change in organismal complexity. However, genome duplication presents significant problems for the faithful transmission of a genome from one generation to the next, and is consequently a rare event, at least in Metazoa. In principle, genome duplications should be easily identified through the coincident emergence within a phylogeny of many gene families.

Unfortunately, this signal is complicated by subsequent piecemeal loss and gain of gene family members. Consequently, there is heated debate over possible ancient genome duplication events in early vertebrate evolution and more recently in teleost fish, both of which must have occurred hundreds of millions of years ago McLysaght et al.

References and Recommended Reading

So what are the relative contributions of these different mechanisms? Not all interspersed duplicate genes are generated by retrotransposition. The initially tandem arrangement of segmental duplications can be broken up by subsequent rearrangements. In keeping with this hypothesis, duplicated genes in a tandem arrangement typically represent more recent duplication events Friedman and Hughes A duplicated gene newly arisen in a single genome must overcome substantial hurdles before it can be observed in evolutionary comparisons. First, it must become fixed in the population, and second, it must be preserved over time.

Population genetics tells us that for new alleles, fixation is a rare event, even for new mutations that confer an immediate selective advantage. Nevertheless, it has been estimated that one in a hundred genes is duplicated and fixed every million years Lynch and Conery , although it should be clear from the duplication mechanisms described above that it is highly unlikely that duplication rates are constant over time.

However, once fixed, three possible fates are typically envisaged for our gene duplication. Despite the slackened selective constraints, mutations can still destroy the incipient functionality of a duplicated gene: for example, by introducing a premature stop codon or a mutation that destroys the structure of a major protein domain. These degenerative mutations result in the creation of a pseudogene nonfunctionalization.

Over time, the likelihood of such a mutation being introduced increases. Recent studies suggest that there is a relatively narrow time window for evolutionary exploration before degradation becomes the most likely outcome, typically of the order of 4 million years Lynch and Conery During the relatively brief period of relaxed selection following gene duplication, a new, advantageous allele may arise as a result of one of the gene copies gaining a new function neofunctionalization. This can be revealed by an accelerated rate of amino-acid change after duplication in one of the gene copies.

This burst of selection is necessarily episodic—once a new function is attained by one of the duplicates, selective constraints on this gene are reasserted. These patterns of selection can be observed in real data: most recently duplicated gene pairs in the human genome have diverged at different rates from their ancestral amino-acid sequence Zhang et al.

A convincing instance of neofunctionalization is the evolution of antibacterial activity in the ECP gene in Old World Monkeys and hominoids after a burst of amino-acid changes following the tandem duplication of the progenitor gene EDN a ribonuclease some 30 MYA Zhang et al.

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  • The divergence of duplicated genes over time can be also monitored in genome-wide functional studies. In both yeast and nematodes, the ability of a gene to buffer the loss of its duplicate declines over time as their functional overlap decreases. Rather than one gene duplicate retaining the original function, while the other either degrades or evolves a new function, the original functions of the single-copy gene may be partitioned between the duplicates subfunctionalization. Many genes perform a multiplicity of subtly distinct functions, and selective pressures have resulted in a compromise between optimal sequences for each role.

    Partitioning these functions between the duplicates may increase the fitness of the organism by removing the conflict between two or more functions. This outcome has become associated with a population genetic model known as the Duplication—Degeneration—Complementation DDC model, which focuses attention on the regulatory changes after duplication Force et al.

    In this model, degenerative changes occur in regulatory sequences of both duplicates, such that these changes complement each other, and the union of the expression patterns of the two duplicates reconstitutes the expression pattern of the original Figure 2. A new duplication in a gene blue with two tissue-specific promoters arrows arises in a population of single copy genes. Fixation within the population results in a minority of cases.

    After fixation, one gene is inactivated degradation or assumes a new function neofunctionalization , or the expression pattern of the original gene is partitioned between the two duplicates as one promoter is silenced in each duplicate in a complementary manner subfunctionalization. A recent study by Dorus and colleagues Dorus et al. In the mouse, both Cdyl genes produce two distinct transcripts, one of which is expressed ubiquitously while the other is testis-specific.

    By contrast, in humans both CDYL genes produce a single ubiquitously expressed transcript, and CDY exhibits testis-specific expression. As CDY is a retrogene see above that has not been duplicated together with its ancestral regulatory sequences, it is clear that the DDC model is not the only route by which to achieve spatial partitioning of ancestral expression patterns. Subfunctionalization can also lead to the partitioning of temporal as well as spatial expression patterns. One gene is expressed in embryos, another in foetuses, and the third from neonates onwards.

    In addition, coding sequence changes have co-evolved with the regulatory changes so that the O 2 binding affinity of haemoglobin is optimised for each developmental stage. This coupling between coding and regulatory change is similarly noted at a genomic level when expression differences between many duplicated genes pairs are correlated with their coding sequence divergence Makova and Li If duplication results in the formation of a novel function as a result of interaction between the two diverged duplicates, which of the above categories of evolutionary outcome does this innovation fall into?

    Not all new biological functions resulting from gene duplications can be ascribed to individual genes. Protein—protein interactions often occur between diverged gene duplicates. This is especially true for ligand—receptor pairs, which are often supposed to coevolve after a gene duplication event, and thus progress from homophilic to heterophilic interactions.

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    This emergent function of the new gene pair does not fit comfortably into any of the scenarios outlined above: both genes are functional yet neither retains the original function, nor has the original function been partitioned. Volff, J. Genome evolution and biodiversity in teleost fish. Heredity 94 , — De Bodt, S. Genome duplication and the origin of angiosperms. Bowers, J. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events.

    Genome Evolution

    Angiosperm diversification through time. Vandepoele, K. Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Christoffels, A. Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Hoegg, S. Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish.

    [PDF] Gene and genome duplication and the evolution of novel gene functions | Semantic Scholar

    Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis. Chain, F. Multiple mechanisms promote the retained expression of gene duplicates in the tetraploid frog Xenopus laevis. PLoS Genet. Duplicate gene evolution and expression in the wake of vertebrate allopolyploidization. BMC Evol. McPeek, M. Clade age and not diversification rate explains species richness among animal taxa.

    Sole, R. Adaptive walks in a gene network model of morphogenesis: insights into the Cambrian explosion.

    Academic Bibliography

    Maere, S. Modeling gene and genome duplications in eukaryotes. Seoighe, C.

    Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Blomme, T. The gain and loss of genes during million years of vertebrate evolution. Genome Biol. Brunet, F. Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Yeast genome evolution in the post-genome era.

    Genome Evolution: Gene and Genome Duplications and the Origin of Novel Gene Functions
    Genome Evolution: Gene and Genome Duplications and the Origin of Novel Gene Functions
    Genome Evolution: Gene and Genome Duplications and the Origin of Novel Gene Functions
    Genome Evolution: Gene and Genome Duplications and the Origin of Novel Gene Functions
    Genome Evolution: Gene and Genome Duplications and the Origin of Novel Gene Functions

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