Consequences of genome duplication

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Polyploidy has been widely appreciated as an important force in the evolution of plant genomes, but now it is recognized as a common phenomenon throughout eukaryotic evolution. Insight into this process has been gained by analyzing the plant, animal, fungal, and recently protozoan genomes that show evidence of whole genome duplication (a transient doubling of the entire gene repertoire of an organism). Moreover, comparative analyses are revealing the evolutionary processes that occur as multiple related genomes diverge from a shared polyploid ancestor, and in individual genomes that underwent several successive rounds of duplication. Recent research including laboratory studies on synthetic polyploids indicates that genome content and gene expression can change quickly after whole genome duplication and that cross-genome regulatory interactions are important. We have a growing understanding of the relationship between whole genome duplication and speciation. Further, recent studies are providing insights into why some gene pairs survive in duplicate, whereas others do not.

Introduction

A change in ploidy is typically expected to be deleterious and an evolutionary dead-end [1]. Despite the problems that might arise in early polyploid generations, the hallmarks of whole genome duplication (WGD) are evident in many sequenced genomes. The prevalence of polyploidy varies across eukaryotic lineages, but evidence of WGD is particularly rampant in plants. It has been demonstrated recently that most eudicot plants descended from an ancient hexaploid ancestor [2••], followed by lineage-specific tetraploidizations in some taxa: one in Populus [3], two in Arabidopsis [4, 5, 6], one in legumes [7], but none in Vitis [2••]. Consequently, a gene that was single-copy in an ancestral angiosperm about 200 million years (Myr) ago could, in principle, have turned into a 12-member family in Arabidopsis by means of polyploidizations alone. In practice, of course, each round of polyploidization was followed by many gene deletions, and gene duplications have also happened by mechanisms other than polyploidization.

Detecting natural polyploidization events can be challenging, especially if the events are ancient. Recent duplications can be detected by the identification of species whose karyotypes contain twice as many chromosomes as those of closely related species. Time erases this signal, however: WGD is typically followed by a period of diploidization, at the end of which the genome looks like a diploid. This period involves extensive gene loss, genomic rearrangements, and distinctive modes of evolution of the genes retained in duplicate. The diploidization process has been extensively studied using whole genome data in different paleopolyploid plants [2••, 3•, 8•, 9, 10, 11], teleost fishes [13•, 14], yeasts [15••], Paramecium [12••], and basal vertebrates [16]. Here we review some of these studies, from a wide range of eukaryotic taxa, with emphasis on the consequences of WGD for speciation and the diversification of gene families.

Section snippets

Genomic changes after WGD

Genomic modifications that occur in the first few generations after WGD can be monitored in synthetic polyploid plants (reviewed in reference [17]). For example, Brassica napus genomes in the first polyploid generation [18] display few rearrangements but numerous and recurrent CpG methylation changes. To study the longer term evolutionary effects of WGD, however, comparative genomic analyses are required.

Interchromosomal rearrangements are a frequent feature of post-WGD evolution. In a recent

Rapid functional divergence as an explanation for duplicate gene retention

After duplication, one of the two redundant copies of a gene should theoretically be free to degenerate and become lost from the genome without consequence. As we have seen, contrary to this prediction some genes survive in duplicate long after WGD. Several models, some implying a functional divergence between the two copies, have been proposed to account for these observations. We summarize these models in Figure 2 and discuss them briefly below.

In plants, it is possible to quantify the

Conclusion

The plant kingdom is the uncontested big kahuna of polyploidization, but simpler non-plant systems still offer many lessons that can help us understand the waves of successive WGDs that have washed over angiosperm evolution. Recurrent trends can be observed in very different taxa, such as the tendency to retain regulatory genes in duplicate in many paleopolyploid genomes. It would be a mistake, however, to think that the outcomes of all WGDs are the same. (i) Different models of duplicate gene

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This work was supported by Irish Research Council for Science, Engineering and Technology, and Science Foundation Ireland. We apologize to authors whose work we could not discuss because of space limits. We thank Kevin Byrne, Gavin Conant, Brian Cusack, Carolin Frank, Jonathan Gordon, Nora Khaldi, Jeffrey Mower, Devin Scannell, Matthew Webster, and Meg Woolfit for helpful discussions.

References (53)

  • G. Blanc et al.

    A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome

    Genome Res

    (2003)
  • C. Simillion et al.

    The hidden duplication past of Arabidopsis thaliana

    Proc Natl Acad Sci USA

    (2002)
  • S.B. Cannon et al.

    Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes

    Proc Natl Acad Sci USA

    (2006)
  • B.A. Chapman et al.

    Buffering of crucial functions by paleologous duplicated genes may contribute cyclicality to angiosperm genome duplication

    Proc Natl Acad Sci USA

    (2006)
  • T. Casneuf et al.

    Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana

    Genome Biol

    (2006)
  • G. Blanc et al.

    Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution

    Plant Cell

    (2004)
  • S. Maere et al.

    Modeling gene and genome duplications in eukaryotes

    Proc Natl Acad Sci USA

    (2005)
  • J.M. Aury et al.

    Global trends of whole-genome duplications revealed by the ciliate Parameciumtetraurelia

    Nature

    (2006)
  • F.G. Brunet et al.

    Gene loss and evolutionary rates following whole-genome duplication in teleost fishes

    Mol Biol Evol

    (2006)
  • D. Steinke et al.

    Many genes in fish have species-specific asymmetric rates of molecular evolution

    BMC Genomics

    (2006)
  • D.R. Scannell et al.

    Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication

    Proc Natl Acad Sci USA

    (2007)
  • T. Blomme et al.

    The gain and loss of genes during 600 million years of vertebrate evolution

    Genome Biol

    (2006)
  • T.C. Osborn et al.

    Understanding mechanisms of novel gene expression in polyploids

    Trends Genet

    (2003)
  • L.N. Lukens et al.

    Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids

    Plant Physiol

    (2006)
  • M. Kasahara et al.

    The medaka draft genome and insights into vertebrate genome evolution

    Nature

    (2007)
  • M. Semon et al.

    Rearrangement rate following the whole-genome duplication in teleosts

    Mol Biol Evol

    (2007)
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