Polyploidy and genome evolution in plants

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.     

Gene duplication as a major force in evolution

Gene duplication is an important mechanism for acquiring new genes and creating genetic novelty in organisms. Many new gene functions have evolved through gene duplication and it has contributed tremendously to the evolution of developmental programmes in various organisms. Gene duplication can result from unequal crossing over, retroposition or chromosomal (or genome) duplication. Understanding the mechanisms that generate duplicate gene copies and the subsequent dynamics among gene duplicates is vital because these investigations shed light on localized and genomewide aspects of evolutionary forces shaping intra-specific and inter-specific genome contents, evolutionary relationships, and interactions. Based on whole-genome analysis of Arabidopsis thaliana, there is compelling evidence that angiosperms underwent two whole-genome duplication events early during their evolutionary history. Recent studies have shown that these events were crucial for creation of many important developmental and regulatory genes found in extant angiosperm genomes. Recent studies also provide strong indications that even yeast (Saccharomyces cerevisiae), with its compact genome, is in fact an ancient tetraploid. Gene duplication can provide new genetic material for mutation, drift and selection to act upon, the result of which is specialized or new gene functions. Without gene duplication the plasticity of a genome or species in adapting to changing environments would be severely limited. Whether a duplicate is retained depends upon its function, its mode of duplication, (i.e. whether it was duplicated during a whole-genome duplication event), the species in which it occurs, and its expression rate. The exaptation of preexisting secondary functions is an important feature in gene evolution, just as it is in morphological evolution.     

Differential accumulation of retroelements and diversification of NB-LRR disease resistance genes in duplicated regions following polyploidy in the ancestor of soybean

The genomes of most, if not all, flowering plants have undergone whole genome duplication events during their evolution. The impact of such polyploidy events is poorly understood, as is the fate of most duplicated genes. We sequenced an approximately 1 million-bp region in soybean (Glycine max) centered on the Rpg1-b disease resistance gene and compared this region with a region duplicated 10 to 14 million years ago. These two regions were also compared with homologous regions in several related legume species (a second soybean genotype, Glycine tomentella, Phaseolus vulgaris, and Medicago truncatula), which enabled us to determine how each of the duplicated regions (homoeologues) in soybean has changed following polyploidy. The biggest change was in retroelement content, with homoeologue 2 having expanded to 3-fold the size of homoeologue 1. Despite this accumulation of retroelements, over 77% of the duplicated low-copy genes have been retained in the same order and appear to be functional. This finding contrasts with recent analyses of the maize (Zea mays) genome, in which only about one-third of duplicated genes appear to have been retained over a similar time period. Fluorescent in situ hybridization revealed that the homoeologue 2 region is located very near a centromere. Thus, pericentromeric localization, per se, does not result in a high rate of gene inactivation, despite greatly accelerated retrotransposon accumulation. In contrast to low-copy genes, nucleotide-binding-leucine-rich repeat disease resistance gene clusters have undergone dramatic species/homoeologue-specific duplications and losses, with some evidence for partitioning of subfamilies between homoeologues.     

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.     

Molecular Evidence for Asymmetric Evolution of Sister Duplicated Blocks after Cereal Polyploidy

Polyploidy (genome duplication) is thought to have contributed to the evolution of the eukaryotic genome, but complex genome structures and massive gene loss during evolution has complicated detection of these ancestral duplication events. The major factors determining the fate of duplicated genes are currently unclear, as are the processes by which duplicated genes evolve after polyploidy. Fine-scale analysis between homologous regions may allow us to better understand post-polyploidy evolution. Here, using gene-by-gene and gene-by-genome strategies, we identified the S5 region and four homologous regions within the japonica genome. Additional phylogenomic analyses of the comparable duplicated blocks indicate that four successive duplication events gave rise to these five regions, allowing us to propose a model for this local chromosomal evolution. According to this model, gene loss may play a major role in post-duplication genetic evolution at the segmental level. Moreover, we found molecular evidence that one of the sister duplicated blocks experienced more gene loss and a more rapid evolution subsequent to two recent duplication events. Given that these two recent duplication events were likely involved in polyploidy, this asymmetric evolution (gene loss and gene divergence) may be one possible mechanism accounting for the diploidization at the segmental level. Supplementary material to this paper is available in electronic form at http://dx.doi.org/10.1007/s11103-005-4414-1     

Birth and death of duplicated genes in completely sequenced eukaryotes

Gene and genome duplications are commonly regarded as being of major evolutionary significance. But how often does gene duplication occur? And, once duplicated, what are the fates of duplicated genes? How do they contribute to evolution? In a recent article, Lynch and Conery analyze divergence between duplicate genes from six eukaryotic genomes. They estimate the rate of gene duplication, the rate of gene loss after duplication and the strength of selection experienced by duplicate genes. They conclude that although the rate of gene duplications is high, so is the rate of gene loss, and they argue that gene duplications could be a major factor in speciation.     

Gene duplication,transfer, and evolution in the chloroplast genome

In addition to the nuclear genome, organisms have organelle genomes. Most of the DNA present in eukaryotic organisms is located in the cell nucleus. Chloroplasts have independent genomes which are inherited from the mother. Duplicated genes are common in the genomes of all organisms. It is believed that gene duplication is the most important step for the origin of genetic variation, leading to the creation of new genes and new gene functions. Despite the fact that extensive gene duplications are rare among the chloroplast genome, gene duplication in the chloroplast genome is an essential source of new genetic functions and a mechanism of neo-evolution. The events of gene transfer between the chloroplast genome and nuclear genome via duplication and subsequent recombination are important processes in evolution. The duplicated gene or genome in the nucleus has been the subject of several recent reviews. In this review, we will briefly summarize gene duplication and evolution in the chloroplast genome. Also, we will provide an overview of gene transfer events between chloroplast and nuclear genomes.     

Characterising protein/detergent complexes by triple-detection size-exclusion chromatography

Background

The number of species with completed genomes, including those with evidence for recent whole genome duplication events has exploded. The recently sequenced Atlantic salmon genome has been through two rounds of whole genome duplication since the divergence of teleost fish from the lineage that led to amniotes. This quadrupoling of the number of potential genes has led to complex patterns of retention and loss among gene families.

Results

Methods have been developed to characterize the interplay of duplicate gene retention processes across both whole genome duplication events and additional smaller scale duplication events. Further, gene expression divergence data has become available as well for Atlantic salmon and the closely related, pre-whole genome duplication pike and methods to describe expression divergence are also presented. These methods for the characterization of duplicate gene retention and gene expression divergence that have been applied to salmon are described.

Conclusions

With the growth in available genomic and functional data, the opportunities to extract functional inference from large scale duplicates using comparative methods have expanded dramatically. Recently developed methods that further this inference for duplicated genes have been described.

     

Gene complexity and gene duplicability

Eukaryotic genes are on average more complex than prokaryotic genes in terms of expression regulation, protein length, and protein-domain structure [1-5]. Eukaryotes are also known to have a higher rate of gene duplication than prokaryotes do [6, 7]. Because gene duplication is the primary source of new genes [], the average gene complexity in a genome may have been increased by gene duplication if complex genes are preferentially duplicated. Here, we test this "gene complexity and gene duplicability" hypothesis with yeast genomic data. We show that, on average, duplicate genes from either whole-genome or individual-gene duplication have longer protein sequences, more functional domains, and more cis-regulatory motifs than singleton genes. This phenomenon is not a by-product of previously known mechanisms, such as protein function [10-13], evolutionary rate [14, 15], dosage [11], and dosage balance [16], that influence gene duplicability. Rather, it appears to have resulted from the sub-neo-functionalization process in duplicate-gene evolution [11]. Under this process, complex genes are more likely to be retained after duplication because they are prone to subfunctionalization, and gene complexity is regained via subsequent neofunctionalization. Thus, gene duplication increases both gene number and gene complexity, two important factors in the origin of genomic and organismal complexity.     

Consequences of genome duplication

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.     

Divergence in expression between duplicated genes in Arabidopsis

New genes may arise through tandem duplication, dispersed small-scale duplication, and polyploidy, and patterns of divergence between duplicated genes may vary among these classes. We have examined patterns of gene expression and coding sequence divergence between duplicated genes in Arabidopsis thaliana. Due to the simultaneous origin of polyploidy-derived gene pairs, we can compare covariation in the rates of expression divergence and sequence divergence within this group. Among tandem and dispersed duplicates, much of the divergence in expression profile appears to occur at or shortly after duplication. Contrary to findings from other eukaryotic systems, there is little relationship between expression divergence and synonymous substitutions, whereas there is a strong positive relationship between expression divergence and nonsynonymous substitutions. Because this pattern is pronounced among the polyploidy-derived pairs, we infer that the strength of purifying selection acting on protein sequence and expression pattern is correlated. The polyploidy-derived pairs are somewhat atypical in that they have broader expression patterns and are expressed at higher levels, suggesting differences among polyploidy- and nonpolyploidy-derived duplicates in the types of genes that revert to single copy. Finally, within many of the duplicated pairs, 1 gene is expressed at a higher level across all assayed conditions, which suggests that the subfunctionalization model for duplicate gene preservation provides, at best, only a partial explanation for the patterns of expression divergence between duplicated genes.     

Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae

Recent studies have elucidated the ancient polyploid history of the Arabidopsis thaliana (Brassicaceae) genome. The studies concur that there was at least one polyploidy event occurring some 14.5 to 86 million years ago (Mya), possibly near the divergence of the Brassicaceae from its sister family, Cleomaceae. Using a comparative genomics approach, we asked whether this polyploidy event was unique to members of the Brassicaceae, shared with the Cleomaceae, or an independent polyploidy event in each lineage. We isolated and sequenced three genomic regions from diploid Cleome spinosa (Cleomaceae) that are each homoeologous to a duplicated region shared between At3 and At5, centered on the paralogs of SEPALLATA (SEP) and CONSTANS (CO). Phylogenetic reconstructions and analysis of synonymous substitution rates support the hypothesis that a genomic triplication in Cleome occurred independently of and more recently than the duplication event in the Brassicaceae. There is a strong correlation in the copy number (single versus duplicate) of individual genes, suggesting functionally consistent influences operating on gene copy number in these two independently evolving lineages. However, the amount of gene loss in Cleome is greater than in Arabidopsis. The genome of C. spinosa is only 1.9 times the size of A. thaliana, enabling comparative genome analysis of separate but related polyploidy events.     

How many genes are there in plants (… and why are they there)?

Annotation of the first few complete plant genomes has revealed that plants have many genes. For Arabidopsis, over 26,500 gene loci have been predicted, whereas for rice, the number adds up to 41,000. Recent analysis of the poplar genome suggests more than 45,000 genes, and partial sequence data from Medicago and Lotus also suggest that these plants contain more than 40,000 genes. Nevertheless, estimations suggest that ancestral angiosperms had no more than 12,000-14,000 genes. One explanation for the large increase in gene number during angiosperm evolution is gene duplication. It has been shown previously that the retention of duplicates following small- and large-scale duplication events in plants is substantial. Taking into account the function of genes that have been duplicated, we are now beginning to understand why many plant genes might have been retained, and how their retention might be linked to the typical lifestyle of plants.