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Evolution of parallel spindles like genes in plants and highlight of unique domain architecture#.

ABSTRACT: BACKGROUND:Polyploidy has long been recognized as playing an important role in plant evolution. In flowering plants, the major route of polyploidization is suggested to be sexual through gametes with somatic chromosome number (2n). Parallel Spindle1 gene in Arabidopsis thaliana (AtPS1) was recently demonstrated to control spindle orientation in the 2nd division of meiosis and, when mutated, to induce 2n pollen. Interestingly, AtPS1 encodes a protein with a FHA domain and PINc domain putatively involved in RNA decay (i.e. Nonsense Mediated mRNA Decay). In potato, 2n pollen depending on parallel spindles was described long time ago but the responsible gene has never been isolated. The knowledge derived from AtPS1 as well as the availability of genome sequences makes it possible to isolate potato PSLike (PSL) and to highlight the evolution of PSL family in plants. RESULTS:Our work leading to the first characterization of PSLs in potato showed a greater PSL complexity in this species respect to Arabidopsis thaliana. Indeed, a genomic PSL locus and seven cDNAs affected by alternative splicing have been cloned. In addition, the occurrence of at least two other PSL loci in potato was suggested by the sequence comparison of alternatively spliced transcripts.Phylogenetic analysis on 20 Viridaeplantae showed the wide distribution of PSLs throughout the species and the occurrence of multiple copies only in potato and soybean.The analysis of PSLFHA and PSLPINc domains evidenced that, in terms of secondary structure, a major degree of variability occurred in PINc domain respect to FHA. In terms of specific active sites, both domains showed diversification among plant species that could be related to a functional diversification among PSL genes. In addition, some specific active sites were strongly conserved among plants as supported by sequence alignment and by evidence of negative selection evaluated as difference between non-synonymous and synonymous mutations. CONCLUSIONS:In this study, we highlight the existence of PSLs throughout Viridaeplantae, from mosses to higher plants. We provide evidence that PSLs occur mostly as singleton in the analyzed genomes except in soybean and potato both characterized by a recent whole genome duplication event. In potato, we suggest the candidate PSL gene having a role in 2n pollen that should be deeply investigated.We provide useful insight into evolutionary conservation of FHA and PINc domains throughout plant PSLs which suggest a fundamental role of these domains for PSL function.

SUBMITTER: Cigliano RA

PROVIDER: S-EPMC3071787 | biostudies-literature | 2011 Mar

REPOSITORIES: biostudies-literature

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Evolution of parallel spindles like genes in plants and highlight of unique domain architecture#.

Cigliano Riccardo Aiese RA Sanseverino Walter W Cremona Gaetana G Consiglio Federica M FM Conicella Clara C

BMC evolutionary biology 20110324

<h4>Background</h4>Polyploidy has long been recognized as playing an important role in plant evolution. In flowering plants, the major route of polyploidization is suggested to be sexual through gametes with somatic chromosome number (2n). Parallel Spindle1 gene in Arabidopsis thaliana (AtPS1) was recently demonstrated to control spindle orientation in the 2nd division of meiosis and, when mutated, to induce 2n pollen. Interestingly, AtPS1 encodes a protein with a FHA domain and PINc domain puta ...[more]

PMID: 21435253

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Project description:BACKGROUND: Plant genomes contain a high proportion of duplicated genes as a result of numerous whole, segmental and local duplications. These duplications lead up to the formation of gene families, which are the usual material for many evolutionary studies. However, all characterized genomes include single-copy (unique) genes that have not received much attention. Unlike gene duplication, gene loss is not an unspecific mechanism but is rather influenced by a functional selection. In this context, we have established and used stringent criteria in order to identify suitable sets of unique genes present in plant proteomes. Comparisons of unique genes in the green phylum were used to characterize the gene and protein features exhibited by both conserved and species-specific unique genes. RESULTS: We identified the unique genes within both A. thaliana and O. sativa genomes and classified them according to the number of homologs in the alternative species: none (U{1:0}), one (U{1:1}) or several (U{1:m}). Regardless of the species, all the genes in these groups present some conserved characteristics, such as small average protein size and abnormal intron number. In order to understand the origin and function of unique genes, we further characterized the U{1:1} gene pairs. The possible involvement of sequence convergence in the creation of U{1:1} pairs was discarded due to the frequent conservation of intron positions. Furthermore, an orthology relationship between the two members of each U{1:1} pair was strongly supported by a high conservation in the protein sizes and transcription levels. Within the promoter of the unique conserved genes, we found a number of TATA and TELO boxes that specifically differed from their mean number in the whole genome. Many unique genes have been conserved as unique through evolution from the green alga Ostreococcus lucimarinus to higher plants. Plant unique genes may also have homologs in bacteria and we showed a link between the targeting towards plastids of proteins encoded by plant nuclear unique genes and their homology with a bacterial protein. CONCLUSION: Many of the A. thaliana and O. sativa unique genes are conserved in plants for which the ancestor diverged at least 725 million years ago (MYA). Half of these genes are also present in other eukaryotic and/or prokaryotic species. Thus, our results indicate that (i) a strong negative selection pressure has conserved a number of genes as unique in genomes throughout evolution, (ii) most unique genes are subjected to a low divergence rate, (iii) they have some features observed in housekeeping genes but for most of them there is no functional annotation and (iv) they may have an ancient origin involving a possible gene transfer from ancestral chloroplasts or bacteria to the plant nucleus.

Project description:MotivationSimulation is an essential technique for generating biomolecular data with a 'known' history for use in validating phylogenetic inference and other evolutionary methods. On longer time scales, simulation supports investigations of equilibrium behavior and provides a formal framework for testing competing evolutionary hypotheses. Twenty years of molecular evolution research have produced a rich repertoire of simulation methods. However, current models do not capture the stringent constraints acting on the domain insertions, duplications, and deletions by which multidomain architectures evolve. Although these processes have the potential to generate any combination of domains, only a tiny fraction of possible domain combinations are observed in nature. Modeling these stringent constraints on domain order and co-occurrence is a fundamental challenge in domain architecture simulation that does not arise with sequence and gene family simulation.ResultsHere, we introduce a stochastic model of domain architecture evolution to simulate evolutionary trajectories that reflect the constraints on domain order and co-occurrence observed in nature. This framework is implemented in a novel domain architecture simulator, DomArchov, using the Metropolis-Hastings algorithm with data-driven transition probabilities. The use of a data-driven event module enables quick and easy redeployment of the simulator for use in different taxonomic and protein function contexts. Using empirical evaluation with metazoan datasets, we demonstrate that domain architectures simulated by DomArchov recapitulate properties of genuine domain architectures that reflect the constraints on domain order and adjacency seen in nature. This work expands the realm of evolutionary processes that are amenable to simulation.Availability and implementationDomArchov is written in Python 3 and is available at http://www.cs.cmu.edu/~durand/DomArchov. The data underlying this article are available via the same link.Supplementary informationSupplementary data are available at Bioinformatics online.

Project description:Protein domains are the structural, functional and evolutionary units of the protein. Protein domain architectures are the linear arrangements of domain(s) in individual proteins. Although the evolutionary history of protein domain architecture has been extensively studied in microorganisms, the evolutionary dynamics of domain architecture in the plant kingdom remains largely undefined. To address this question, we analyzed the lineage-based protein domain architecture content in 14 completed green plant genomes.Our analyses show that all 14 plant genomes maintain similar distributions of species-specific, single-domain, and multi-domain architectures. Approximately 65% of plant domain architectures are universally present in all plant lineages, while the remaining architectures are lineage-specific. Clear examples are seen of both the loss and gain of specific protein architectures in higher plants. There has been a dynamic, lineage-wise expansion of domain architectures during plant evolution. The data suggest that this expansion can be largely explained by changes in nuclear ploidy resulting from rounds of whole genome duplications. Indeed, there has been a decrease in the number of unique domain architectures when the genomes were normalized into a presumed ancestral genome that has not undergone whole genome duplications.Our data show the conservation of universal domain architectures in all available plant genomes, indicating the presence of an evolutionarily conserved, core set of protein components. However, the occurrence of lineage-specific domain architectures indicates that domain architecture diversity has been maintained beyond these core components in plant genomes. Although several features of genome-wide domain architecture content are conserved in plants, the data clearly demonstrate lineage-wise, progressive changes and expansions of individual protein domain architectures, reinforcing the notion that plant genomes have undergone dynamic evolution.

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Evolution of parallel spindles like genes in plants and highlight of unique domain architecture#.

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Evolution of parallel spindles like genes in plants and highlight of unique domain architecture#.

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