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      The Natural History of Class I Primate Alcohol Dehydrogenases Includes Gene Duplication, Gene Loss, and Gene Conversion

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          Abstract

          Background

          Gene duplication is a source of molecular innovation throughout evolution. However, even with massive amounts of genome sequence data, correlating gene duplication with speciation and other events in natural history can be difficult. This is especially true in its most interesting cases, where rapid and multiple duplications are likely to reflect adaptation to rapidly changing environments and life styles. This may be so for Class I of alcohol dehydrogenases ( ADH1s), where multiple duplications occurred in primate lineages in Old and New World monkeys (OWMs and NWMs) and hominoids.

          Methodology/Principal Findings

          To build a preferred model for the natural history of ADH1s, we determined the sequences of nine new ADH1 genes, finding for the first time multiple paralogs in various prosimians (lemurs, strepsirhines). Database mining then identified novel ADH1 paralogs in both macaque (an OWM) and marmoset (a NWM). These were used with the previously identified human paralogs to resolve controversies relating to dates of duplication and gene conversion in the ADH1 family. Central to these controversies are differences in the topologies of trees generated from exonic (coding) sequences and intronic sequences.

          Conclusions/Significance

          We provide evidence that gene conversions are the primary source of difference, using molecular clock dating of duplications and analyses of microinsertions and deletions (micro-indels). The tree topology inferred from intron sequences appear to more correctly represent the natural history of ADH1s, with the ADH1 paralogs in platyrrhines (NWMs) and catarrhines (OWMs and hominoids) having arisen by duplications shortly predating the divergence of OWMs and NWMs. We also conclude that paralogs in lemurs arose independently. Finally, we identify errors in database interpretation as the source of controversies concerning gene conversion. These analyses provide a model for the natural history of ADH1s that posits four ADH1 paralogs in the ancestor of Catarrhine and Platyrrhine primates, followed by the loss of an ADH1 paralog in the human lineage.

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          Most cited references 51

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          The neighbor-joining method: a new method for reconstructing phylogenetic trees.

          A new method called the neighbor-joining method is proposed for reconstructing phylogenetic trees from evolutionary distance data. The principle of this method is to find pairs of operational taxonomic units (OTUs [= neighbors]) that minimize the total branch length at each stage of clustering of OTUs starting with a starlike tree. The branch lengths as well as the topology of a parsimonious tree can quickly be obtained by using this method. Using computer simulation, we studied the efficiency of this method in obtaining the correct unrooted tree in comparison with that of five other tree-making methods: the unweighted pair group method of analysis, Farris's method, Sattath and Tversky's method, Li's method, and Tateno et al.'s modified Farris method. The new, neighbor-joining method and Sattath and Tversky's method are shown to be generally better than the other methods.
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            MrBayes 3: Bayesian phylogenetic inference under mixed models.

            MrBayes 3 performs Bayesian phylogenetic analysis combining information from different data partitions or subsets evolving under different stochastic evolutionary models. This allows the user to analyze heterogeneous data sets consisting of different data types-e.g. morphological, nucleotide, and protein-and to explore a wide variety of structured models mixing partition-unique and shared parameters. The program employs MPI to parallelize Metropolis coupling on Macintosh or UNIX clusters.
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              BLAT--the BLAST-like alignment tool.

               W. Kent (2002)
              Analyzing vertebrate genomes requires rapid mRNA/DNA and cross-species protein alignments. A new tool, BLAT, is more accurate and 500 times faster than popular existing tools for mRNA/DNA alignments and 50 times faster for protein alignments at sensitivity settings typically used when comparing vertebrate sequences. BLAT's speed stems from an index of all nonoverlapping K-mers in the genome. This index fits inside the RAM of inexpensive computers, and need only be computed once for each genome assembly. BLAT has several major stages. It uses the index to find regions in the genome likely to be homologous to the query sequence. It performs an alignment between homologous regions. It stitches together these aligned regions (often exons) into larger alignments (typically genes). Finally, BLAT revisits small internal exons possibly missed at the first stage and adjusts large gap boundaries that have canonical splice sites where feasible. This paper describes how BLAT was optimized. Effects on speed and sensitivity are explored for various K-mer sizes, mismatch schemes, and number of required index matches. BLAT is compared with other alignment programs on various test sets and then used in several genome-wide applications. http://genome.ucsc.edu hosts a web-based BLAT server for the human genome.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                31 July 2012
                : 7
                : 7
                Affiliations
                [1 ]Foundation for Applied Molecular Evolution, Gainesville, Florida, United States of America
                [2 ]Department of Biochemistry and Molecular Biology, Indiana University School of Medicine, Indianapolis, Indiana, United States of America
                University of Lausanne, Switzerland
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MAC SAB. Performed the experiments: MAC OU LMZ. Analyzed the data: MAC SAB. Contributed reagents/materials/analysis tools: TDH RPD LMZ. Wrote the paper: MAC SAB.

                PONE-D-11-08927
                10.1371/journal.pone.0041175
                3409193
                22859968

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Counts
                Pages: 24
                Funding
                This grant was funded by the National Institute of Alcohol Abuse and Alcoholism (niaaa.nih.gov, RO1AA017723), and the National Aeronautics and Space Administration (nasa.gov, NNX08A023G). The Wisconsin National Primate Research Center provided samples used in this research, and was supported by grant number RR000167. The Southwest National Primate Research Center also provided samples used in this research, and was supported by the National Center for Research Resources (grant number p51RR013986) and the Office of Research Infrastructure Programs/OD (grant number P51OD011107). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Evolutionary Biology
                Forms of Evolution
                Concerted Evolution
                Convergent Evolution
                Organismal Evolution
                Human Evolution
                Evolutionary Processes
                Genetics
                Molecular Genetics
                Gene Duplication
                Medicine
                Gastroenterology and Hepatology
                Liver Diseases
                Alcoholic Liver Disease
                Public Health
                Alcohol

                Uncategorized

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