Consequences of genome duplication
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)
- et al.
Genome duplication, divergent resolution and speciation
Trends Genet
(2001) - et al.
Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid
Genetics
(2004) - et al.
Preservation of duplicate genes by complementary, degenerative mutations
Genetics
(1999) - et al.
The probability of duplicate gene preservation by subfunctionalization
Genetics
(2000) - et al.
Preferential duplication of conserved proteins in eukaryotic genomes
PLoS Biol
(2004) - et al.
The regulatory utilization of genetic redundancy through responsive backup circuits
Proc Natl Acad Sci USA
(2006) - et al.
Polyploid incidence and evolution
Annu Rev Genet
(2000) - et al.
The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla
Nature
(2007) - et al.
The genome of black cottonwood, Populus trichocarpa (Torr. & Gray)
Science
(2006) - et al.
Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events
Nature
(2003)
A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome
Genome Res
The hidden duplication past of Arabidopsis thaliana
Proc Natl Acad Sci USA
Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes
Proc Natl Acad Sci USA
Buffering of crucial functions by paleologous duplicated genes may contribute cyclicality to angiosperm genome duplication
Proc Natl Acad Sci USA
Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana
Genome Biol
Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution
Plant Cell
Modeling gene and genome duplications in eukaryotes
Proc Natl Acad Sci USA
Global trends of whole-genome duplications revealed by the ciliate Parameciumtetraurelia
Nature
Gene loss and evolutionary rates following whole-genome duplication in teleost fishes
Mol Biol Evol
Many genes in fish have species-specific asymmetric rates of molecular evolution
BMC Genomics
Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication
Proc Natl Acad Sci USA
The gain and loss of genes during 600 million years of vertebrate evolution
Genome Biol
Understanding mechanisms of novel gene expression in polyploids
Trends Genet
Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids
Plant Physiol
The medaka draft genome and insights into vertebrate genome evolution
Nature
Rearrangement rate following the whole-genome duplication in teleosts
Mol Biol Evol
Cited by (335)
Membrane fusion and fission during eukaryogenesis
2024, Current Opinion in Cell BiologyHow to utilize comparative transcriptomics to dissect morphological diversity in plants
2023, Current Opinion in Plant BiologyAn ancient whole-genome duplication in barnacles contributes to their diversification and intertidal sessile life adaptation
2023, Journal of Advanced ResearchDifferential expression of aquaporin genes and the influence of environmental hypertonicity on their expression in juveniles of air-breathing stinging catfish (Heteropneustes fossilis)
2022, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative Physiology