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      Identification and assessment of variable single-copy orthologous (SCO) nuclear loci for low-level phylogenomics: a case study in the genus Rosa (Rosaceae)

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          Abstract

          Background

          With an ever-growing number of published genomes, many low levels of the Tree of Life now contain several species with enough molecular data to perform shallow-scale phylogenomic studies. Moving away from using just a few universal phylogenetic markers, we can now target thousands of other loci to decipher taxa relationships. Making the best possible selection of informative sequences regarding the taxa studied has emerged as a new issue. Here, we developed a general procedure to mine genomic data, looking for orthologous single-copy loci capable of deciphering phylogenetic relationships below the generic rank. To develop our strategy, we chose the genus Rosa, a rapid-evolving lineage of the Rosaceae family in which several species genomes have recently been sequenced. We also compared our loci to conventional plastid markers, commonly used for phylogenetic inference in this genus.

          Results

          We generated 1856 sequence tags in putative single-copy orthologous nuclear loci. Associated in silico primer pairs can potentially amplify fragments able to resolve a wide range of speciation events within the genus Rosa. Analysis of parsimony-informative site content showed the value of non-coding genomic regions to obtain variable sequences despite the fact that they may be more difficult to target in less related species. Dozens of nuclear loci outperform the conventional plastid phylogenetic markers in terms of phylogenetic informativeness, for both recent and ancient evolutionary divergences. However, conflicting phylogenetic signals were found between nuclear gene tree topologies and the species-tree topology, shedding light on the many patterns of hybridization and/or incomplete lineage sorting that occur in the genus Rosa.

          Conclusions

          With recently published genome sequence data, we developed a set of single-copy orthologous nuclear loci to resolve species-level phylogenomics in the genus Rosa. This genome-wide scale dataset contains hundreds of highly variable loci which phylogenetic interest was assessed in terms of phylogenetic informativeness and topological conflict. Our target identification procedure can easily be reproduced to identify new highly informative loci for other taxonomic groups and ranks.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-019-1479-z) contains supplementary material, which is available to authorized users.

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          Most cited references73

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          Comparison of phylogenetic trees

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            TESTING SIGNIFICANCE OF INCONGRUENCE

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              Gene Trees in Species Trees

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                Author and article information

                Contributors
                kevin.debray@univ-angers.fr
                jordan.marie-magdelaine@inra.fr
                tom.ruttink@ilvo.vlaanderen.be
                jeremy.clotault@univ-angers.fr
                fabrice.foucher@inra.fr
                valery.malecot@agrocampus-ouest.fr
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                24 July 2019
                24 July 2019
                2019
                : 19
                : 152
                Affiliations
                [1 ]ISNI 0000 0004 0613 5301, GRID grid.452456.4, IRHS, Agrocampus-Ouest, INRA, UNIV Angers, SFR 4207 QuaSaV, ; Beaucouzé, France
                [2 ]ISNI 0000 0001 2203 8438, GRID grid.418605.e, ILVO, Flanders Research Institute for Agriculture, Fisheries and Food, Plant Sciences Unit, ; Melle, Belgium
                Author information
                http://orcid.org/0000-0003-2898-9415
                Article
                1479
                10.1186/s12862-019-1479-z
                6657147
                31340752
                7eef363c-ba94-4689-af19-9db90df0e483
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
                : 16 April 2019
                : 16 July 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100012948, Ministère de l'Enseignement supérieur, de la Recherche et de l'Innovation;
                Award ID: NA
                Award Recipient :
                Funded by: Région Pays de la Loire
                Award ID: NA
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100007745, Angers Loire Métropole;
                Award ID: NA
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100008530, European Regional Development Fund;
                Award ID: NA
                Award Recipient :
                Categories
                Methodology Article
                Custom metadata
                © The Author(s) 2019

                Evolutionary Biology
                species-level phylogenomics,nuclear single-copy orthologs,phylogenetic informativeness,conflicting topologies

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