Evolutionary dynamics of duplicated genes in plants

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 intra- and 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.     

Evolutionary change of the numbers of homeobox genes in bilateral animals

It has been known that the conservation or diversity of homeobox genes is responsible for the similarity and variability of some of the morphological or physiological characters among different organisms. To gain some insights into the evolutionary pattern of homeobox genes in bilateral animals, we studied the change of the numbers of these genes during the evolution of bilateral animals. We analyzed 2,031 homeodomain sequences compiled from 11 species of bilateral animals ranging from Caenorhabditis elegans to humans. Our phylogenetic analysis using a modified reconciled-tree method suggested that there were at least about 88 homeobox genes in the common ancestor of bilateral animals. About 50-60 genes of them have left at least one descendant gene in each of the 11 species studied, suggesting that about 30-40 genes were lost in a lineage-specific manner. Although similar numbers of ancestral genes have survived in each species, vertebrate lineages gained many more genes by duplication than invertebrate lineages, resulting in more than 200 homeobox genes in vertebrates and about 100 in invertebrates. After these gene duplications, a substantial number of old duplicate genes have also been lost in each lineage. Because many old duplicate genes were lost, it is likely that lost genes had already been differentiated from other groups of genes at the time of gene loss. We conclude that both gain and loss of homeobox genes were important for the evolutionary change of phenotypic characters in bilateral animals.     

Tomato and barley contain duplicated copies of cryptochrome 1

The cryptochrome family of blue‐light photoreceptors is involved in the control of plant photomorphogenesis and photoperiodic responses. Two cryptochromes have been described in Arabidopsis and tomato. To investigate the composition of the cryptochrome gene family in angiosperms, we used a ‘garden PCR’ approach, amplifying DNA from different plant species with the same pair of degenerated oligonucleotides representing conserved sequences from the flavin‐binding domain. Different numbers of Cry‐homologous sequences were found in different species: two each in Arabidopsis (Dicots, Brassicaceae), melon (Dicots, Cucurbitaceae) and banana tree (Monocots, Musaceae); three each in tomato (Dicots, Solanaceae) and barley (Monocots, Graminaceae). These sequences contain open reading frames (OFRs) with high homology to cryptochromes, but not photolyases, and are transcribed into RNA. In each case, a Cry1‐ and a Cry2‐like sequence was recognizable. The third gene of tomato and barley seems to have arisen from recent, independent duplications of Cry1, and was thus named Cry1b. The tomato Cry1b gene encodes a protein of 583 amino acids (the shortest of the three tomato cryptochromes), with a high similarity to Cry1. The C‐terminus of Cry1b is truncated before the conserved Ser‐Thr‐Ala‐Glu‐Ser‐Ser‐Ser (STAESSS) motif found in both Cry1a and Cry2. The Cry1b mRNA is expressed throughout the tomato plant, reaching maximal levels of expression in the flower (like Cry1a and Cry2). We conclude that tomato and barley contain at least one additional expressed member of the Cry1 gene family.     

Population genetic models of duplicated genes

Various population genetic models of duplicated genes are introduced. The problems covered in this review include the fixation process of a duplicated copy, copy number polymorphism, the fates of duplicated genes and single nucleotide polymorphism in duplicated genes. Because of increasing evidence for concerted evolution by gene conversion, this review introduces recently developed gene conversion models. In the first half, models assuming independent evolution of duplicated genes are introduced, and then the effect of gene conversion is considered in the second half.     

Recent gene conversions between duplicated glutamate decarboxylase genes (gadA and gadB) in pathogenic Escherichia coli

Escherichia coli have evolved adaptive systems to resist strongly acidic habitats in part through the production of 2 biochemically identical isoforms of glutamate decarboxylase (GAD), encoded by the gadA and gadB genes. These genes occur in E. coli and other members of the genospecies (e.g., Shigella spp.) and originated as part of a genomic fitness island acquired early in Escherichia evolution. The present duplicated gad loci are widely spaced on the E. coli chromosome, and the 2 genes are 97% similar in sequence. Comparison of the nucleotide sequences of the gadA and gadB in 16 strains of pathogenic E. coli revealed 3.8% and 5.0% polymorphism in the 2 genes, respectively. Alignment of the homologous genes identified a total of 120 variable sites, including 21 fixed nucleotide differences between the loci within the first 82 codons of the genes. Twenty-three phylogenetically informative sites were polymorphic for the same nucleotides in both genes suggesting recent gene conversions or intergenic recombination. Phylogenetic analysis based on the synonymous substitutions per synonymous site indicated 2 cases in which specific gadA and gadB alleles were more closely related to one another than to other alleles at the corresponding locus. The results indicate that at least 3 gene conversion events have occurred after the gad gene duplication in the evolution of E. coli. Despite multiple gene conversion events, the upstream regulatory regions and the 5' end of each gene remains distinct, suggesting that maintaining functionally different gad genes is important in this acid-resistance mechanism in pathogenic E. coli.     

Molecular evolution and population genetics of duplicated accessory gland protein genes in Drosophila

To investigate the potential importance of gene duplication in D. melanogaster accessory gland protein (Acp) gene evolution we carried out a computational analysis comparing annotated D. melanogaster Acp genes to the entire D. melanogaster genome. We found that two known Acp genes are actually members of small multigene families. Polymorphism and divergence data from these duplicated genes suggest that in at least four cases, protein divergence between D. melanogaster and D. simulans is a result of directional selection. One putative Acp revealed by our computational analysis shows evidence of a recent selective sweep in a non-African population (but not in an African population). These data support the idea that selection on reproduction-related genes may drive divergence of populations within species, and strengthen the conclusion that Acps may often be under directional selection in Drosophila.     

水稻抗逆相关基因的分子进化分析

植物在进化过程中为了适应外界环境,已经具有一套完整的抵抗外界特殊环境的调控系统。但是,关于水稻抗逆相关基因的分子进化方面的研究还未见报道。文章通过Plant Tolerance Gene Database数据库,获得22个水稻抗逆相关基因。利用比较基因组学和生物信息学方法对水稻抗逆相关基因的进化动态进行研究,结果表明水稻抗逆相关基因在低等植物中比较保守;随着植物的不断进化和生存环境的改变,其基因数量也随之增加。具有相似抗性功能的基因往往具有相似的基因结构和基序(motif)结构。文章还发现4个保守motif 的存在：HRDXK、DXXSXG、LLPR和GXGXXG(X代表任意氨基酸)。在GSK1、RAN2抗逆基因中发现了3个特有的motif结构：GSK1特有的P-rich motif,RAN2特有的G-rich motif和E-rich motif。推测这些保守的motif结构与基因的抗逆功能密切相关。进化速率分析结果表明,尽管植物抗逆性相关基因在进化过程中受到较强的纯化选择作用,但是仍然有50%的抗逆性相关基因存在正选择位点。这些正选择位点的存在有可能为基因适应外界环境变化提供了重要的物质基础。     

Evolutionary history of the somatostatin and somatostatin receptors

Somatostatin and its receptors have a critical role in mammalian growth through their control pattern of secretion of growth hormone, but the evolutionary history of somatostatin and somatostatin receptors are ill defined. We used comparative whole genome analysis of Danio rerio, Carassius auratus, Xenopus tropicalis, Gallus gallus, Monodelphis domestica, Homo sapiens, Sus scrofa, Bos taurus, Mus musculus, Rattus norvegicus, Canis lupus familiaris, Ovis aries, Equus caballus, Pan troglodytes and Macaca mulatto to identify somatostatin and somatostatin receptors in each species. To date, we have identified a minimum of two genes of somatostatin and five somatostatin receptor genes in mammalian species with variable forms. We established a clear evolutionary history of the somatostatin system and traced the origin of the somatostatin system to 395 million years ago (MYA), identifying critical steps in their evolution.     

Deciphering the evolutionary interplay between subgenomes following polyploidy: A paleogenomics approach in grasses

How did plant species emerge from their most recent common ancestors (MRCAs) 250 million years ago? Modern plant genomes help to address such key questions in unveiling precise species genealogies. The field of paleogenomics is undergoing a paradigm shift for investigating species evolution from the study of ancestral genomes from extinct species to deciphering the evolutionary forces (in terms of duplication, fusion, fission, deletion, and translocation) that drove present‐day plant diversity (in terms of chromosome/gene number and genome size). In this review, inferred ancestral karyotype genomes are shown to be powerful tools to (1) unravel the past history of extant species by recovering the variations of ancestral genomic compartments and (2) accelerate translational research by facilitating the transfer of genomic information from model systems to species of agronomic interest.     

Conservation and divergence of APETALA1/FRUITFULL-like gene function in grasses: evidence from gene expression analyses

Duplicated APETALA1/FRUITFULL (AP1/FUL) genes show distinct but overlapping patterns of expression within rice (Oryza sativa) and within ryegrass (Lolium temulentum), suggesting discrete functional roles in the transition to flowering, specification of spikelet meristem identity, and specification of floral organ identity. In this study, we analyzed the expression of the AP1/FUL paralogues FUL1 and FUL2 across phylogenetically disparate grasses to test hypotheses of gene function. In combination with other studies, our data support similar roles for both genes in spikelet meristem identity, a general role for FUL1 in floral organ identity, and a more specific role for FUL2 in outer floral whorl identity. In contrast to Arabidopsis AP1/FUL genes, expression of FUL1 and FUL2 is consistent with an early role in the transition to flowering. In general, FUL1 has a wider expression pattern in all spikelet organs than FUL2, but both genes are expressed in all spikelet organs in some cereals. FUL1 and FUL2 appear to have multiple redundant functions in early inflorescence development. We hypothesize that sub-functionalization of FUL2 and interaction of FUL2 with LHS1 could specify lemma and palea identity in the grass floret.     

Reproductive effort and phenology of seed production of savanna grasses with different growth form and life history

The phenology of seed production in natural savanna grasslands was studied in the grass speciesAristida congesta, Cymbopogon plurinodis, Cynodon dactylon, Digitaria eriantha ssp.pentzii, Eragrostis rigidior, Eragrostis superba, Panicum coloratum, Schmidtia pappophoroides, Tragus berteronianus andUrochloa panicoides. Maximum seed production varied according to life history strategy and growth form from 0.03 mg seed g^-1 shoot dry weight in the perennialD. eriantha ssp.pentzii which produces long stolons and 14.8 mg seed g^-1 shoot inE rigidior, which produces short geniculate stolons, to 169.1 mg g^-1 in the annualT. berteronianus. Seed production was in most species divided over several peaks during the season. Peaks of seed production were observed 3 to 7 months after the onset of the growth season depending on the start of the rains and the life history strategy and growth form of the species. Seed production varied from maxima of 180 seeds m^-2 inD. eriantha ssp.pentzii to 47000 seeds m^-2 in annual stands ofT. berteronianus. Except for annual grasslands withU. panicoides, seedling emergence data reported are smaller by at least a factor of 10 than the observed seed production. Among other factors, a low quality of produced seeds, predation by birds and insects and previous grazing by livestock may have contributed to this difference.     

Multiple origins and rapid evolution of duplicated mitochondrial genes in parthenogenetic geckos (Heteronotia binoei; Squamata, Gekkonidae)

Accumulating evidence for alternative gene orders demonstrates that vertebrate mitochondrial genomes are more evolutionarily dynamic than previously thought. Several lineages of parthenogenetic lizards contain large, tandem duplications that include rRNA, tRNA, and protein-coding genes, as well as the control region. Such duplications are hypothesized as intermediate stages in gene rearrangement, but the early stages of their evolution have not been previously studied. To better understand the evolutionary dynamics of duplicated segments of mitochondrial DNA, we sequenced 10 mitochondrial genomes from recently formed ( approximately 300,000 years ago) hybrid parthenogenetic geckos of the Heteronotia binoei complex and 1 from a sexual form. These genomes included some with an arrangement typical of vertebrates and others with tandem duplications varying in size from 5.7 to 9.4 kb, each with different gene contents and duplication endpoints. These results, together with phylogenetic analyses, indicate independent and frequent origins of the duplications. Small, direct repeats at the duplication endpoints imply slipped-strand error as a mechanism generating the duplications as opposed to a false initiation/termination of DNA replication mechanism that has been invoked to explain duplications in other lizard mitochondrial systems. Despite their recent origin, there is evidence for nonfunctionalization of genes due primarily to deletions, and the observed pattern of gene disruption supports the duplication-deletion model for rearrangement of mtDNA gene order. Conversely, the accumulation of mutations between these recent duplicates provides no evidence for gene conversion, as has been reported in some other systems. These results demonstrate that, despite their long-term stasis in gene content and arrangement in some lineages, vertebrate mitochondrial genomes can be evolutionary dynamic even at short timescales.     

Molecular and functional evolution of human DHRS2 and DHRS4 duplicated genes

Human DHRS2 and DHRS4 genes code for similar NADP-dependent short-chain carbonyl-reductase enzymes having different substrate specificity. Human DHRS2 and DHRS4 enzymes share several common sequence motives including residues responsible for coenzyme binding as well as for the intimate catalytic oxido-reductase mechanism, while their substrate-binding sequences have very low similarity. We found that DHRS2 and DHRS4 genes are syntenic outparalogues originated from a duplication of the DHRS4 gene that took place before the formation of the mammalian clade. DHRS2 gene evolved more rapidly and underwent positive selection on more sites than the DHRS4 gene. DHRS2 sites under positive selection were mainly located on the enzyme active site thus showing that substrate specificity drove the divergence from the DHRS4 enzyme. Rapid divergent evolution brought the human DHRS2 enzyme to have subcellular localization, synthesis regulation and specialized cellular functions very different from those of the human DHRS4 enzyme.     

Long-term conservation of six duplicated structural genes in cephalopod mitochondrial genomes

The complete nucleotide sequences of the mitochondrial (mt) genomes of three cephalopods, Octopus vulgaris (Octopodiformes, Octopoda, Incirrata), Todarodes pacificus (Decapodiformes, Oegopsida, Ommastrephidae), and Watasenia scintillans (Decapodiformes, Oegopsida, Enoploteuthidae), were determined. These three mt genomes encode the standard set of metazoan mt genes. However, W. scintillans and T. pacificus mt genomes share duplications of the longest noncoding region, three cytochrome oxidase subunit genes and two ATP synthase subunit genes, and the tRNA(Asp) gene. Southern hybridization analysis of the W. scintillans mt genome shows that this single genome carries both duplicated regions. The near-identical sequence of the duplicates suggests that there are certain concerted evolutionary mechanisms, at least in cephalopod mitochondria. Molecular phylogenetic analyses of mt protein genes are suggestive, although not statistically significantly so, of a monophyletic relationship between W. scintillans and T. pacificus.     

Evolutionary analyses of non‐family genes in plants

There are a large number of ‘non‐family’ (NF) genes that do not cluster into families with three or more members per genome. While gene families have been extensively studied, a systematic analysis of NF genes has not been reported. We performed comparative studies on NF genes in 14 plant species. Based on the clustering of protein sequences, we identified ~94 000 NF genes across these species that were divided into five evolutionary groups: Viridiplantae wide, angiosperm specific, monocot specific, dicot specific, and those that were species specific. Our analysis revealed that the NF genes resulted largely from less frequent gene duplications and/or a higher rate of gene loss after segmental duplication relative to genes in both low‐copy‐number families (LF; 3–10 copies per genome) and high‐copy‐number families (HF; >10 copies). Furthermore, we identified functions enriched in the NF gene set as compared with the HF genes. We found that NF genes were involved in essential biological processes shared by all plant lineages (e.g. photosynthesis and translation), as well as gene regulation and stress responses associated with phylogenetic diversification. In particular, our analysis of an Arabidopsis protein–protein interaction network revealed that hub proteins with the top 10% most connections were over‐represented in the NF set relative to the HF set. This research highlights the roles that NF genes may play in evolutionary and functional genomics research.     

Functional specialization of duplicated AP3‐like genes in Medicago truncatula

The B–class of MADS box genes has been studied in a wide range of plant species, but has remained largely uncharacterized in legumes. Here we investigate the evolutionary fate of the duplicated AP3‐like genes of a legume species. To obtain insight into the extent to which B‐class MADS box gene functions are conserved or have diversified in legumes, we isolated and characterized the two members of the AP3 lineage in Medicago truncatula: MtNMH7 and MtTM6 (euAP3 and paleoAP3 genes, respectively). A non‐overlapping and complementary expression pattern of both genes was observed in petals and stamens. MtTM6 was expressed predominantly in the outer cell layers of both floral organs, and MtNMH7 in the inner cell layers of petals and stamens. Functional analyses by reverse genetics approaches (RNAi and Tnt1 mutagenesis) showed that the contribution of MtNMH7 to petal identity is more important than that of MtTM6, whereas MtTM6 plays a more important role in stamen identity than its paralog MtNMH7. Our results suggest that the M. truncatula AP3‐like genes have undergone a functional specialization process associated with complete partitioning of gene expression patterns of the ancestral gene lineage. We provide information regarding the similarities and differences in petal and stamen development among core eudicots.     

Transcriptional divergence of the duplicated oxidative stress-responsive genes in the Arabidopsis genome

Previous studies have indicated that Arabidopsis thaliana experienced a genome-wide duplication event shortly before its divergence from Brassica followed by extensive chromosomal rearrangements and deletions. While a large number of the duplicated genes have significantly diverged or lost their sister genes, we found 4222 pairs that are still highly conserved, and as a result had similar functional assignments during the annotation of the genome sequence. Using whole-genome DNA microarrays, we identified 906 duplicated gene pairs in which at least one member exhibited a significant response to oxidative stress. Among these, only 117 pairs were up- or down-regulated in both pairs and many of these exhibited dissimilar patterns of expression. Examination of the expression patterns of PAL1 and PAL2, ACD1 and ACD2, genes coding for two Hsp20s, various P450s, and electron transfer flavoproteins suggests Arabidopsis evolved a number of distinct oxidative stress response mechanisms using similar gene sets following the duplication of its genome.