Evolutionary Dynamics and Functional Specialization of Plant Paralogs Formed by Whole and Small-Scale Genome Duplications (original) (raw)

Evolutionary dynamics of duplicated genes in plants

Molecular Phylogenetics and Evolution, 2003

Gene duplication, arising from region-specific duplication or genome-wide polyploidization, is a prominent feature in plant genome evolution. Understanding the mechanisms generating duplicate gene copies and the subsequent dynamics among gene duplicates is vital because these investigations shed light on regional and genome-wide aspects of evolutionary forces shaping intraand interspecific genome contents, evolutionary relationships, and interactions. This review discusses recent gene duplication analyses in plants, focusing on the molecular and evolutionary dynamics occurring at three different timescales following duplication: (1) initial establishment and persistence of cytotypes, (2) interactions among duplicate gene copies, and (3) longer term differentiation between duplicated genes. These relative time points are presented in terms of their potential adaptive significance and impact on plant evolutionary genomics research.

Impact of recurrent gene duplication on adaptation of plant genomes

BMC Plant Biology, 2014

Background: Recurrent gene duplication and retention played an important role in angiosperm genome evolution. It has been hypothesized that these processes contribute significantly to plant adaptation but so far this hypothesis has not been tested at the genome scale. Results: We studied available sequenced angiosperm genomes to assess the frequency of positive selection footprints in lineage specific expanded (LSE) gene families compared to single-copy genes using a d N /d S -based test in a phylogenetic framework. We found 5.38% of alignments in LSE genes with codons under positive selection. In contrast, we found no evidence for codons under positive selection in the single-copy reference set. An analysis at the branch level shows that purifying selection acted more strongly on single-copy genes than on LSE gene clusters. Moreover we detect significantly more branches indicating evolution under positive selection and/or relaxed constraint in LSE genes than in single-copy genes.

Duplications and Turnover in Plant Genomes

Plant Genome Diversity Volume 1, 2012

Plant and other eukaryotic genomes contain an abundance of duplications with a variety of origins. The power of these duplications to influence evolution is attenuated by the rate and nature of gene birth and death. In most eukaryotes, including plants, plots of the age of all gene duplications in

Selection for Higher Gene Copy Number after Different Types of Plant Gene Duplications

Genome Biology and Evolution, 2011

The evolutionary origins of the multitude of duplicate genes in the plant genomes are still incompletely understood. To gain an appreciation of the potential selective forces acting on these duplicates, we phylogenetically inferred the set of metabolic gene families from 10 flowering plant (angiosperm) genomes. We then compared the metabolic fluxes for these families, predicted using the Arabidopsis thaliana and Sorghum bicolor metabolic networks, with the families' duplication propensities. For duplications produced by both small scale (small-scale duplications) and genome duplication (wholegenome duplications), there is a significant association between the flux and the tendency to duplicate. Following this global analysis, we made a more fine-scale study of the selective constraints observed on plant sodium and phosphate transporters. We find that the different duplication mechanisms give rise to differing selective constraints. However, the exact nature of this pattern varies between the gene families, and we argue that the duplication mechanism alone does not define a duplicated gene's subsequent evolutionary trajectory. Collectively, our results argue for the interplay of history, function, and selection in shaping the duplicate gene evolution in plants.

Prevalent Role of Gene Features in Determining Evolutionary Fates of Whole-Genome Duplication Duplicated Genes in Flowering Plants

PLANT PHYSIOLOGY, 2013

The evolution of genes and genomes after polyploidization has been the subject of extensive studies in evolutionary biology and plant sciences. While a significant number of duplicated genes are rapidly removed during a process called fractionation, which operates after the whole-genome duplication (WGD), another considerable number of genes are retained preferentially, leading to the phenomenon of biased gene retention. However, the evolutionary mechanisms underlying gene retention after WGD remain largely unknown. Through genome-wide analyses of sequence and functional data, we comprehensively investigated the relationships between gene features and the retention probability of duplicated genes after WGDs in six plant genomes, Arabidopsis (Arabidopsis thaliana), poplar (Populus trichocarpa), soybean (Glycine max), rice (Oryza sativa), sorghum (Sorghum bicolor), and maize (Zea mays). The results showed that multiple gene features were correlated with the probability of gene retenti...

Gene duplication as a major force in evolution

Journal of Genetics, 2013

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 wholegenome 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.

Escape from Preferential Retention Following Repeated Whole Genome Duplications in Plants

2012

The well supported gene dosage hypothesis predicts that genes encoding proteins engaged in dose-sensitive interactions cannot be reduced back to single copies once all interacting partners are simultaneously duplicated in a whole genome duplication. The genomes of extant flowering plants are the result of many sequential rounds of whole genome duplication, yet the fraction of genomes devoted to encoding complex molecular machines does not increase as fast as expected through multiple rounds of whole genome duplications. Using parallel interspecies genomic comparisons in the grasses and crucifers, we demonstrate that genes retained as duplicates following a whole genome duplication have only a 50% chance of being retained as duplicates in a second whole genome duplication. Genes which fractionated to a single copy following a second whole genome duplication tend to be the member of a gene pair with less complex promoters, lower levels of expression, and to be under lower levels of purifying selection. We suggest the copy with lower levels of expression and less purifying selection contributes less to effective gene-product dosage and therefore is under less dosage constraint in future whole genome duplications, providing an explanation for why flowering plant genomes are not overrun with subunits of large dose-sensitive protein complexes.

Widespread genome duplications throughout the history of flowering plants

Genome Research, 2006

Genomic comparisons provide evidence for ancient genome-wide duplications in a diverse array of animals and plants. We developed a birth–death model to identify evidence for genome duplication in EST data, and applied a mixture model to estimate the age distribution of paralogous pairs identified in EST sets for species representing the basal-most extant flowering plant lineages. We found evidence for episodes of ancient genome-wide duplications in the basal angiosperm lineages including Nuphar advena (yellow water lily: Nymphaeaceae) and the magnoliids Persea americana (avocado: Lauraceae), Liriodendron tulipifera (tulip poplar: Magnoliaceae), and Saruma henryi (Aristolochiaceae). In addition, we detected independent genome duplications in the basal eudicot Eschscholzia californica (California poppy: Papaveraceae) and the basal monocot Acorus americanus (Acoraceae), both of which were distinct from duplications documented for ancestral grass (Poaceae) and core eudicot lineages. Amo...

Multiple Paleopolyploidizations during the Evolution of the Compositae Reveal Parallel Patterns of Duplicate Gene Retention after Millions of Years

Molecular Biology and Evolution, 2008

Of the approximately 250,000 species of flowering plants, nearly one in ten are members of the Compositae (Asteraceae), a diverse family found in almost every habitat on all continents except Antarctica. With an origin in the mid Eocene, the Compositae is also a relatively young family with remarkable diversifications during the last 40 My. Previous cytologic and systematic investigations suggested that paleopolyploidy may have occurred in at least one Compositae lineage, but a recent analysis of genomic data was equivocal. We tested for evidence of paleopolyploidy in the evolutionary history of the family using recently available expressed sequence tag (EST) data from the Compositae Genome Project. Combined with data available on GenBank, we analyzed nearly 1 million ESTs from 18 species representing seven genera and four tribes. Our analyses revealed at least three ancient whole-genome duplications in the Compositae-a paleopolyploidization shared by all analyzed taxa and placed near the origin of the family just prior to the rapid radiation of its tribes and independent genome duplications near the base of the tribes Mutisieae and Heliantheae. These results are consistent with previous research implicating paleopolyploidy in the evolution and diversification of the Heliantheae. Further, we observed parallel retention of duplicate genes from the basal Compositae genome duplication across all tribes, despite divergence times of 33-38 My among these lineages. This pattern of retention was also repeated for the paleologs from the Heliantheae duplication. Intriguingly, the categories of genes retained in duplicate were substantially different from those in Arabidopsis. In particular, we found that genes annotated to structural components or cellular organization Gene Ontology categories were significantly enriched among paleologs, whereas genes associated with transcription and other regulatory functions were significantly underrepresented. Our results suggest that paleopolyploidy can yield strikingly consistent signatures of gene retention in plant genomes despite extensive lineage radiations and recurrent genome duplications but that these patterns vary substantially among higher taxonomic categories.

Locating Large-Scale Gene Duplication Events through Reconciled Trees: Implications for Identifying Ancient Polyploidy Events in Plants

Journal of Computational Biology, 2009

Recent analyses of plant genomic data have found extensive evidence of ancient whole genome duplication (or polyploidy) events, but there are many unresolved questions regarding the number and timing of such events in plant evolutionary history. We describe the first exact and efficient algorithm for the Episode Clustering problem, which, given a collection of rooted gene trees and a rooted species tree, seeks the minimum number of locations on the species tree of gene duplication events. Solving this problem allows one to place gene duplication events onto nodes of a given species tree and potentially detect large-scale gene duplication events. We examined the performance of an implementation of our algorithm using 85 plant gene trees that contain genes from a total of 136 plant taxa. We found evidence of large-scale gene duplication events in Populus, Gossypium, Poaceae, Asteraceae, Brassicaceae, Solanaceae, Fabaceae, and near the root of the eudicot clade that are consistent with previous genomic evidence. However, a lack of phylogenetic signal within the gene trees can produce erroneous evidence of large-scale duplication events, especially near the root of the species tree. Although the results of our algorithm should be interpreted cautiously, they provide hypotheses for precise locations of large-scale gene duplication events with data from relatively few gene trees and can complement other genomic approaches to provide a more comprehensive view of ancient large-scale gene duplication events.