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      The Arabidopsis Kinome: phylogeny and evolutionary insights into functional diversification

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          Abstract

          Background

          Protein kinases constitute a particularly large protein family in Arabidopsis with important functions in cellular signal transduction networks. At the same time Arabidopsis is a model plant with high frequencies of gene duplications. Here, we have conducted a systematic analysis of the Arabidopsis kinase complement, the kinome, with particular focus on gene duplication events. We matched Arabidopsis proteins to a Hidden-Markov Model of eukaryotic kinases and computed a phylogeny of 942 Arabidopsis protein kinase domains and mapped their origin by gene duplication.

          Results

          The phylogeny showed two major clades of receptor kinases and soluble kinases, each of which was divided into functional subclades. Based on this phylogeny, association of yet uncharacterized kinases to families was possible which extended functional annotation of unknowns. Classification of gene duplications within these protein kinases revealed that representatives of cytosolic subfamilies showed a tendency to maintain segmentally duplicated genes, while some subfamilies of the receptor kinases were enriched for tandem duplicates. Although functional diversification is observed throughout most subfamilies, some instances of functional conservation among genes transposed from the same ancestor were observed. In general, a significant enrichment of essential genes was found among genes encoding for protein kinases.

          Conclusions

          The inferred phylogeny allowed classification and annotation of yet uncharacterized kinases. The prediction and analysis of syntenic blocks and duplication events within gene families of interest can be used to link functional biology to insights from an evolutionary viewpoint. The approach undertaken here can be applied to any gene family in any organism with an annotated genome.

          Electronic supplementary material

          The online version of this article (doi:10.1186/1471-2164-15-548) contains supplementary material, which is available to authorized users.

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          Most cited references41

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          Lethality and centrality in protein networks

          In this paper we present the first mathematical analysis of the protein interaction network found in the yeast, S. cerevisiae. We show that, (a) the identified protein network display a characteristic scale-free topology that demonstrate striking similarity to the inherent organization of metabolic networks in particular, and to that of robust and error-tolerant networks in general. (b) the likelihood that deletion of an individual gene product will prove lethal for the yeast cell clearly correlates with the number of interactions the protein has, meaning that highly-connected proteins are more likely to prove essential than proteins with low number of links to other proteins. These results suggest that a scale-free architecture is a generic property of cellular networks attributable to universal self-organizing principles of robust and error-tolerant networks and that will likely to represent a generic topology for protein-protein interactions.
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            The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana

            Background Most genes in Arabidopsis thaliana are members of gene families. How do the members of gene families arise, and how are gene family copy numbers maintained? Some gene families may evolve primarily through tandem duplication and high rates of birth and death in clusters, and others through infrequent polyploidy or large-scale segmental duplications and subsequent losses. Results Our approach to understanding the mechanisms of gene family evolution was to construct phylogenies for 50 large gene families in Arabidopsis thaliana, identify large internal segmental duplications in Arabidopsis, map gene duplications onto the segmental duplications, and use this information to identify which nodes in each phylogeny arose due to segmental or tandem duplication. Examples of six gene families exemplifying characteristic modes are described. Distributions of gene family sizes and patterns of duplication by genomic distance are also described in order to characterize patterns of local duplication and copy number for large gene families. Both gene family size and duplication by distance closely follow power-law distributions. Conclusions Combining information about genomic segmental duplications, gene family phylogenies, and gene positions provides a method to evaluate contributions of tandem duplication and segmental genome duplication in the generation and maintenance of gene families. These differences appear to correspond meaningfully to differences in functional roles of the members of the gene families.
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              Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition.

              Each mode of gene duplication (tandem, tetraploid, segmental, transpositional) retains genes in a biased manner. A reciprocal relationship exists between plant genes retained postpaleotetraploidy versus genes retained after an ancient tandem duplication. Among the models (C, neofunctionalization, balanced gene drive) and ideas that might explain this relationship, only balanced gene drive predicts reciprocity. The gene balance hypothesis explains that more "connected" genes--by protein-protein interactions in a heteromer, for example--are less likely to be retained as a tandem or transposed duplicate and are more likely to be retained postpaleotetraploidy; otherwise, selectively negative dosage effects are created. Biased duplicate retention is an instant and neutral by-product, a spandrel, of purifying selection. Balanced gene drive expanded plant gene families, including those encoding proteasomal proteins, protein kinases, motors, and transcription factors, with each paleotetraploidy, which could explain trends involving complexity. Balanced gene drive is a saltation mechanism in the mutationist tradition.
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                Author and article information

                Contributors
                zulawski@mpimp-golm.mpg.de
                Gunnar.Schulze@gmx.de
                braginets@mpimp-golm.mpg.de
                stefanie.hartmann@uni-potsdam.de
                wschulze@uni-hohenheim.de
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                1 July 2014
                1 July 2014
                2014
                : 15
                : 1
                : 548
                Affiliations
                [ ]Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1, Golm, 14476 Germany
                [ ]Bioinformatics, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, Golm, 14476 Germany
                [ ]Department of Plant Systems Biology, University of Hohenheim, Garbenstraße 30, Stuttgart, 70599 Germany
                Article
                6281
                10.1186/1471-2164-15-548
                4112214
                24984858
                90c3293b-cb90-471f-9f92-c74059ff2933
                © Zulawski et al.; licensee BioMed Central Ltd. 2014

                This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 23 March 2014
                : 25 June 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Genetics
                Genetics

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