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      Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach

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          Abstract

          A method for a high-throughput genome screening for horizontally acquired genes is presented, and is illustrated using EST data from three species of root-knot nematode, Meloidogyne species.

          Abstract

          Background

          Published accounts of horizontally acquired genes in plant-parasitic nematodes have not been the result of a specific search for gene transfer per se, but rather have emerged from characterization of individual genes. We present a method for a high-throughput genome screen for horizontally acquired genes, illustrated using expressed sequence tag (EST) data from three species of root-knot nematode, Meloidogyne species.

          Results

          Our approach identified the previously postulated horizontally transferred genes and revealed six new candidates. Screening was partially dependent on sequence quality, with more candidates identified from clustered sequences than from raw EST data. Computational and experimental methods verified the horizontal gene transfer candidates as bona fide nematode genes. Phylogenetic analysis implicated rhizobial ancestors as donors of horizontally acquired genes in Meloidogyne.

          Conclusions

          High-throughput genomic screening is an effective way to identify horizontal gene transfer candidates. Transferred genes that have undergone amelioration of nucleotide composition and codon bias have been identified using this approach. Analysis of these horizontally transferred gene candidates suggests a link between horizontally transferred genes in Meloidogyne and parasitism.

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          Most cited references47

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications.

            P. Sharp, W Li (1987)
            A simple, effective measure of synonymous codon usage bias, the Codon Adaptation Index, is detailed. The index uses a reference set of highly expressed genes from a species to assess the relative merits of each codon, and a score for a gene is calculated from the frequency of use of all codons in that gene. The index assesses the extent to which selection has been effective in moulding the pattern of codon usage. In that respect it is useful for predicting the level of expression of a gene, for assessing the adaptation of viral genes to their hosts, and for making comparisons of codon usage in different organisms. The index may also give an approximate indication of the likely success of heterologous gene expression.
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              Amelioration of bacterial genomes: rates of change and exchange.

              Although bacterial species display wide variation in their overall GC contents, the genes within a particular species' genome are relatively similar in base composition. As a result, sequences that are novel to a bacterial genome-i.e., DNA introduced through recent horizontal transfer-often bear unusual sequence characteristics and can be distinguished from ancestral DNA. At the time of introgression, horizontally transferred genes reflect the base composition of the donor genome; but, over time, these sequences will ameliorate to reflect the DNA composition of the new genome because the introgressed genes are subject to the same mutational processes affecting all genes in the recipient genome. This process of amelioration is evident in a large group of genes involved in host-cell invasion by enteric bacteria and can be modeled to predict the amount of time required after transfer for foreign DNA to resemble native DNA. Furthermore, models of amelioration can be used to estimate the time of introgression of foreign genes in a chromosome. Applying this approach to a 1.43-megabase continuous sequence, we have calculated that the entire Escherichia coli chromosome contains more than 600 kb of horizontally transferred, protein-coding DNA. Estimates of amelioration times indicate that this DNA has accumulated at a rate of 31 kb per million years, which is on the order of the amount of variant DNA introduced by point mutations. This rate predicts that the E. coli and Salmonella enterica lineages have each gained and lost more than 3 megabases of novel DNA since their divergence.
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                Author and article information

                Journal
                Genome Biol
                Genome Biology
                BioMed Central (London )
                1465-6906
                1465-6914
                2003
                19 May 2003
                : 4
                : 6
                : R39
                Affiliations
                [1 ]Center for the Biology of Nematode Parasitism, Box 7253, North Carolina State University, Raleigh, NC 27695, USA
                [2 ]Bioinformatics Research Center, Box 7566, North Carolina State University, Raleigh, NC 27695, USA
                [3 ]Genome Sequencing Center, Department of Genetics, Box 8501, Washington University School of Medicine, St. Louis, MO 63108, USA
                [4 ]Divergence Inc., 893 North Warson Road, St. Louis, MO 63141, USA
                Article
                gb-2003-4-6-r39
                10.1186/gb-2003-4-6-r39
                193618
                12801413
                7ccce4c1-f819-4c23-854b-98bd12a55c85
                Copyright © 2003 Scholl et al.; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.
                History
                : 31 January 2003
                : 27 March 2003
                : 22 April 2003
                Categories
                Research

                Genetics
                Genetics

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