Polyploidy and genome evolution in plants

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Genome doubling (polyploidy) has been and continues to be a pervasive force in plant evolution. Modern plant genomes harbor evidence of multiple rounds of past polyploidization events, often followed by massive silencing and elimination of duplicated genes. Recent studies have refined our inferences of the number and timing of polyploidy events and the impact of these events on genome structure. Many polyploids experience extensive and rapid genomic alterations, some arising with the onset of polyploidy. Survivorship of duplicated genes are differential across gene classes, with some duplicate genes more prone to retention than others. Recent theory is now supported by evidence showing that genes that are retained in duplicate typically diversify in function or undergo subfunctionalization. Polyploidy has extensive effects on gene expression, with gene silencing accompanying polyploid formation and continuing over evolutionary time.

Introduction

Among the more illuminating realizations to emerge from the genomics era has been the extent to which genome doubling (polyploidy) has been a pervasive force in plant evolution. Analyses of whole-genome sequences, extensive expressed sequence tag (EST) sets, and duplicated genomic regions have led to the realization that genome doubling has occurred repeatedly during plant evolution and that even plants with relatively small genomes, such as Arabidopsis thaliana, have been impacted by polyploidy [1, 2]. Recent studies convincingly demonstrate that polyploidy entails far more than the mere merger of two genomes who passively acquiesce to their sudden collaboration, but instead involves a whole spectrum of molecular and physiological adjustments. Extensive genomic rearrangements, including exchanges between genomes and gene loss, often arise with the onset of polyploidization [3]. Genome doubling also significantly effects gene expression, resulting in epigenetically induced gene silencing [4, 5]. Novel phenotypes are known to emerge from this genomic amalgam, including some with high visibility to natural selection, such as organ size and flowering time. Thus, polyploidy is a prominent and significant force in plant evolution, at temporal scales ranging from ancient to contemporary, and with profound effects at scales ranging from molecular to ecological.

In this review, we draw attention to some of the more surprising and important recent advances in our understanding of polyploidy that have arisen from numerous studies, providing a gateway to the recent literature in the process.

Section snippets

Polyploidy is an ancient and recurrent process leading to differential gene loss

Several studies have revealed that multiple rounds of polyploidy have occurred during angiosperm evolution. Empirical observations come from diverse sources, including analysis of complete genomes, comparative genome mapping, micro-colinearity studies, and analyses of EST collections. Illustrative of these approaches are the many studies that have inferred polyploidy events at different times in the evolutionary history of Arabidopsis [6, 7, 8, 9•, 10•, 11, 12, 13]. Inferences of the number and

Divergence and functional diversification following genome duplication

The foregoing discussion encapsulates the important observations that although much of the genetic redundancy created by ancient polyploidy vanishes through gene loss, some duplicated gene pairs are retained over millions of years. This observation constitutes prima facie evidence for a functional role of duplicated genes, and suggests that polyploidy provides fodder for evolutionary adaptation via divergence following duplication [25]. Additional support for this notion stems from the fact

Genome evolution in recently formed polyploids

The foregoing discussion has centered on paleopolyploid events (i.e. polyploid events that occurred many millions of years ago) and their consequences, but polyploidy is an active and ongoing process in many plant genera. Several allopolyploids that formed within the past five million years or so, including wheat, cotton, Brassica napus, Arabidopsis suecica, soybean, and tobacco, have become experimental systems for addressing questions in younger allopolyploids. Even more recent are

Polyploidy can lead to immediate and extensive changes in gene expression

Genes that are duplicated by polyploidy could be expressed at equal levels, or there could be unequal expression or silencing of one copy. An interesting recent revelation is that the silencing of some duplicated genes often accompanies the onset of allopolyploidy, as shown by studies of newly created synthetic polyploids [43•, 44, 45, 46••, 47•], indicating that gene silencing is a common response to polyploidy. Silencing can occur as early as the first generation following polyploidy,

Conclusions and perspectives

Insights into polyploidy at the molecular level have experienced a quantum leap forward during the past few years, concomitant with the exponential increase in sequence information, the availability of bioinformatic tools, and new approaches to study gene expression. These advances have increased our awareness of the frequency and timing of polyploidy, as well as of phenomena such as duplicate gene retention and loss, gene silencing, functional diversification, and subfunctionalization. In

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

We thank Doug Soltis, Chris Pires, Ken Wolfe, and Jen Tate for comments on the manuscript. We gratefully acknowledge the support of the US National Science Foundation, the US Department of Agriculture, and the National Science and Engineering Research Council of Canada.

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