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Yesterday's polyploids and the mystery of diploidization

Key Points

  • The 2R hypothesis, which states that two rounds of genome duplication occurred during the early evolution of vertebrates, is difficult to test because its predictions are not clear.

  • Map-based studies have tended to support the 2R hypothesis, whereas tree-based (phylogenetic) studies have not.

  • Inaccurate phylogenetic trees, gene conversion and ancient tandem duplications can all interfere with tree-based approaches to testing the 2R hypothesis.

  • We know little about the molecular basis of diploidization, the evolutionary process by which a tetraploid species 'decays' to become a diploid.

  • Different loci can appear to have different duplication dates due to either segmental allotetraploidy or independent diploidization of each locus.

  • The draft sequence of the human genome does not provide strong support for the 2R hypothesis.

  • Extensive gene deletion and genomic rearrangement could potentially obliterate any evidence of paleopolyploidy, even if it had occurred.

Abstract

Thirty years after Susumu Ohno proposed that vertebrate genomes are degenerate polyploids, the extent to which genome duplication contributed to the evolution of the vertebrate genome, if at all, is still uncertain. Sequence-level studies on model organisms whose genomes show clearer evidence of ancient polyploidy are invaluable because they indicate what the evolutionary products of genome duplication can look like. The greatest mystery is the molecular basis of diploidization, the evolutionary process by which a polyploid genome turns into a diploid one.

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Figure 1: Phylogenetic positions of some likely polyploidy events during eukaryote evolution.
Figure 2: Model of the 2R hypothesis and its phylogenetic implications.
Figure 3: Dot-matrix plots of yeast and Arabidopsis.
Figure 4: Computer simulations of the dot-matrix patterns expected from one or two rounds of genome duplication.
Figure 5: Effect of genetic drift and diploidization on inter-locus age estimates in an allotetraploid.

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Acknowledgements

I am grateful to K. Hokamp, A. McLysaght and L. Skrabanek for discussion.

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DATABASE LINKS

CDK7

CDK3

Pip2

Oaf1

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FURTHER INFORMATION

Saccharomyces Genome Database

The Arabidopsis Information Resource

Maize Database

The Zebrafish Information Network

Arabidopsis Genome Initiative

Génolevures project

UCSC Draft Human Genome Browser

Ken Wolfe's lab

Yeast gene duplications

Glossary

SYNTENY

The property of being located on the same chromosome.

ANEUPLOIDY

Presence of extra copies, or no copies, of some chromosomes.

HOX GENE CLUSTERS

Tandem arrays of homeobox genes that have crucial roles in development. There are four Hox clusters in humans but only one in invertebrates.

AUTOPOLYPLOIDY

Doubling the copy number of each chromosome in a species.

ALLOPOLYPLOIDY

The fusion of two distinct parental species to form a hybrid, the genome of which is the sum of the two parental genomes.

ORTHOLOGUES

Homologous genes that originated through speciation (for example, human α-globin and mouse α-globin).

DICOT

The larger subclass of angiosperms that has two seed leaves (cotyledons) in the embryo.

MOLECULAR CLOCK

The principle that any gene or protein has a near-constant rate of evolution in all organisms, which means that the amount of sequence divergence between two sequences will be proportional to the amount of time elapsed since their shared ancestor existed.

OUTGROUP

A species or sequence that is known to diverge earlier than the other species or sequences being analysed.

OHNOLOGUE

A pair of duplicate genes (paralogues) produced by the process of genome duplication.

PARALOGUES

Homologous genes that originated by gene duplication (for example, human α-globin and human β-globin).

HOMOLOGUES

Genes that share a common ancestor and are usually similar in sequence.

TOPOLOGY

The branching arrangement of a phylogenetic tree.

TELEOST

Bony fish.

TETRAPOD

Four-limbed animal.

GENE CONVERSION

Non-reciprocal allelic exchange.

BOOTSTRAP ANALYSIS

Type of statistical analysis to test the reliability of certain branches in the evolutionary tree. The bootstrap proceeds by re-sampling the original data, with replacement, to create a series of bootstrap samples of the same size as the original data. The bootstrap value of a node is the percentage of times that node is present in the set of trees constructed from the new data sets.

QUADRIVALENT

A cytological structure in which four copies of a chromosome are aligned on the meiotic spindle.

BIVALENT

A cytological structure in which two copies of a chromosome are aligned on the meiotic spindle.

HOMEOLOGUES

Sister chromosomes (or sister loci) resulting from polyploidy in plants.

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Wolfe, K. Yesterday's polyploids and the mystery of diploidization. Nat Rev Genet 2, 333–341 (2001). https://doi.org/10.1038/35072009

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