Novel patterns of gene expression in polyploid plants

Genome doubling, or polyploidy, is a major factor accounting for duplicate genes found in most eukaryotic genomes. Polyploidy has considerable effects on duplicate gene expression, including silencing and up- or downregulation of one of the duplicated genes. These changes can arise with the onset of polyploidization or within several generations after polyploid formation and they can have epigenetic causal factors. Many expression alterations are organ-specific. Specific genes can be independently and repeatedly silenced during polyploidization, whereas patterns for other genes appear to be more stochastic. Three recent reports have provided intriguing new insights into the patterns, timing and mechanisms of gene expression changes that accompany polyploidy in plants.

Introduction

Most eukaryotic genomes have numerous duplicated genes, many of which appear to have arisen from one or more cycles of polyploidy (genome doubling), either by allopolyploidy or autopolyploidy (see Glossary). Well-documented examples of polyploidy exist in various groups of vertebrates, insects, yeasts and plants 1, 2. Ancient polyploidy events (paleopolyploidy) have been inferred to have occurred during the evolutionary history of vertebrates, yeast and flowering plants [3]. Following paleopolyploidy there has been extensive loss of duplicated genes. Polyploidy has been especially common in flowering plants, where most species are inferred to have experienced at least one polyploidy event in their evolutionary history [4]. For example, at least two and probably three paleopolyploidy events are thought to have occurred during the evolutionary history of Arabidopsis thaliana [5]. Approximately 27% of the gene pairs that were formed by polyploidy have been retained in A. thaliana [6] and more than half of these gene pairs show evidence of functional divergence [7].

The merging and doubling of two genomes sets in motion extensive modifications of the genome and/or transcriptome, creating cascades of novel expression patterns, regulatory interactions and new phenotypic variation for evaluation by natural selection 5, 8, 9. Recent studies have demonstrated that many of these effects arise following the onset of polyploid formation, whereas others play out over a longer evolutionary timescale. Key to these recent insights is the use of newly created, synthetic plant polyploids that mimic natural systems. These have proven to be excellent systems for studying the immediate consequences of polyploidy and they provide insights into processes that occur following polyploidy in many eukaryotes. Extensive genomic rearrangements, including exchanges between genomes and gene loss, have been documented in certain systems 10, 11, 12 but not others [13]. Studies of synthetic polyploids have shown that genes duplicated by polyploidy, termed ‘homoeologs’, can become silenced immediately or soon after polyploidy 14, 15, 16, 17, 18, similar to tandemly repeated rRNA genes 19, 20. Here we highlight recent studies of synthetic plant polyploids that have provided intriguing new insights into the patterns, timing and mechanisms of gene expression changes in plant polyploids 21, 22, 23.