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      Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts

      research-article
      1 , 2 , , 3 , 4 , 5 , 6 , 7 , 8 , 7 , 9 , 10 , 11 , 9 , 12 , 13 , 6 , 4 , 14 , 1 , 10 , 4 , 15 , 16 , 17 , 4 , 18 , 1 , 2 , 19 , 8 , 20 , 21 , 22 , 23 , 17 , 24 , 25 , 26 , 27 , 4 , 28 ,
      Nature Plants
      Nature Publishing Group UK
      Genetics, Plant sciences, Genomics, Evolution

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          Abstract

          Hornworts comprise a bryophyte lineage that diverged from other extant land plants >400 million years ago and bears unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis and a pyrenoid-based carbon-concentrating mechanism (CCM). Here, we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses place hornworts as a sister clade to liverworts plus mosses with high support. The Anthoceros genomes lack repeat-dense centromeres as well as whole-genome duplication, and contain a limited transcription factor repertoire. Several genes involved in angiosperm meristem and stomatal function are conserved in Anthoceros and upregulated during sporophyte development, suggesting possible homologies at the genetic level. We identified candidate genes involved in cyanobacterial symbiosis and found that LCIB, a Chlamydomonas CCM gene, is present in hornworts but absent in other plant lineages, implying a possible conserved role in CCM function. We anticipate that these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.

          Abstract

          Analyses of three high-quality genomes of Anthoceros hornworts place hornworts as a sister clade to the lineage including liverworts and mosses, and provide insights into the unique biological features of hornworts.

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          Most cited references135

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          Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

          In comparative high-throughput sequencing assays, a fundamental task is the analysis of count data, such as read counts per gene in RNA-seq, for evidence of systematic changes across experimental conditions. Small replicate numbers, discreteness, large dynamic range and the presence of outliers require a suitable statistical approach. We present DESeq2, a method for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates. This enables a more quantitative analysis focused on the strength rather than the mere presence of differential expression. The DESeq2 package is available at http://www.bioconductor.org/packages/release/bioc/html/DESeq2.html. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0550-8) contains supplementary material, which is available to authorized users.
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            Trimmomatic: a flexible trimmer for Illumina sequence data

            Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.
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              The Sequence Alignment/Map format and SAMtools

              Summary: The Sequence Alignment/Map (SAM) format is a generic alignment format for storing read alignments against reference sequences, supporting short and long reads (up to 128 Mbp) produced by different sequencing platforms. It is flexible in style, compact in size, efficient in random access and is the format in which alignments from the 1000 Genomes Project are released. SAMtools implements various utilities for post-processing alignments in the SAM format, such as indexing, variant caller and alignment viewer, and thus provides universal tools for processing read alignments. Availability: http://samtools.sourceforge.net Contact: rd@sanger.ac.uk
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                Author and article information

                Contributors
                fl329@cornell.edu
                peter.szoevenyi@systbot.uzh.ch
                Journal
                Nat Plants
                Nat Plants
                Nature Plants
                Nature Publishing Group UK (London )
                2055-0278
                13 March 2020
                13 March 2020
                2020
                : 6
                : 3
                : 259-272
                Affiliations
                [1 ]ISNI 000000041936877X, GRID grid.5386.8, Boyce Thompson Institute, ; Ithaca, NY USA
                [2 ]ISNI 000000041936877X, GRID grid.5386.8, Plant Biology Section, , Cornell University, ; Ithaca, NY USA
                [3 ]ISNI 0000 0001 2308 3329, GRID grid.9707.9, Advanced Science Research Center, , Kanazawa University, ; Ishikawa, Japan
                [4 ]ISNI 0000 0004 1937 0650, GRID grid.7400.3, Department of Systematic and Evolutionary Botany, , University of Zurich, ; Zurich, Switzerland
                [5 ]ISNI 0000000121885934, GRID grid.5335.0, Department of Plant Sciences, , University of Cambridge, ; Cambridge, UK
                [6 ]ISNI 0000 0001 2353 1689, GRID grid.11417.32, LRSV, , Université de Toulouse, CNRS, UPS Castanet-Tolosan, ; Toulouse, France
                [7 ]ISNI 0000 0001 2168 186X, GRID grid.134563.6, Department of Ecology and Evolutionary Biology, , University of Arizona, ; Tucson, AZ USA
                [8 ]ISNI 0000 0004 1936 9756, GRID grid.10253.35, Faculty of Biology, , Philipps University of Marburg, ; Marburg, Germany
                [9 ]ISNI 0000 0004 1936 8403, GRID grid.9909.9, Centre for Plant Sciences, Faculty of Biological Sciences, , University of Leeds, ; Leeds, UK
                [10 ]ISNI 0000 0004 1770 5832, GRID grid.157927.f, Instituto de Biología Molecular y Celular de Plantas, , CSIC-Universidad Politécnica de Valencia, ; Valencia, Spain
                [11 ]GRID grid.488316.0, Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, , Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, ; Shenzhen, China
                [12 ]ISNI 0000 0001 2364 4210, GRID grid.7450.6, Institute for Microbiology and Genetics, Department of Applied Bioinformatics, , Georg-August University Göttingen, ; Göttingen, Germany
                [13 ]ISNI 0000 0001 2176 9917, GRID grid.411327.2, Institute of Population Genetics, , Heinrich Heine University Düsseldorf, ; Düsseldorf, Germany
                [14 ]ISNI 0000 0004 1936 7603, GRID grid.5337.2, School of Biological Sciences, , University of Bristol, ; Bristol, UK
                [15 ]ISNI 0000 0004 1936 9684, GRID grid.27860.3b, Department of Microbiology and Molecular Genetics, , University of California, ; Davis, CA USA
                [16 ]ISNI 0000 0004 1937 0650, GRID grid.7400.3, Department of Plant and Microbial Biology, , University of Zurich, ; Zurich, Switzerland
                [17 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, Laboratory of Biochemistry, , Wageningen University & Research, ; Wageningen, the Netherlands
                [18 ]ISNI 0000 0001 2240 3300, GRID grid.10388.32, Nees Institute for Biodiversity of Plants, , University of Bonn, ; Bonn, Germany
                [19 ]ISNI 0000 0000 8711 3200, GRID grid.257022.0, Graduate School of Integrated Sciences for Life, , Hiroshima University, ; Hiroshima, Japan
                [20 ]GRID grid.5963.9, BIOSS Centre for Biological Signalling Studies, , University of Freiburg, ; Freiburg, Germany
                [21 ]ISNI 0000 0004 1936 9756, GRID grid.10253.35, LOEWE Center for Synthetic Microbiology (SYNMIKRO), , University of Marburg, ; Marburg, Germany
                [22 ]ISNI 0000 0004 1936 8390, GRID grid.23856.3a, Department of Biology, , Laval University, ; Quebec City, Quebec Canada
                [23 ]ISNI 0000 0001 2296 9689, GRID grid.438006.9, Smithsonian Tropical Research Institute, ; Balboa, Panamá
                [24 ]ISNI 0000 0001 2172 9288, GRID grid.5949.1, Institute for Evolution and Biodiversity, , University of Muenster, ; Münster, Germany
                [25 ]GRID grid.17089.37, Department of Biological Sciences, Department of Medicine, , University of Alberta, ; Edmonton, Alberta Canada
                [26 ]ISNI 0000 0001 2034 1839, GRID grid.21155.32, BGI-Shenzhen, ; Shenzhen, China
                [27 ]ISNI 0000 0001 1092 0677, GRID grid.262564.1, Department of Life Science, , Rikkyo University, ; Tokyo, Japan
                [28 ]Zurich-Basel Plant Science Center, Zurich, Switzerland
                Author information
                http://orcid.org/0000-0002-0076-0152
                http://orcid.org/0000-0003-1279-7806
                http://orcid.org/0000-0002-5198-0331
                http://orcid.org/0000-0002-6489-5566
                http://orcid.org/0000-0001-7173-1319
                http://orcid.org/0000-0003-1612-4019
                http://orcid.org/0000-0001-5743-0448
                http://orcid.org/0000-0003-2562-2052
                http://orcid.org/0000-0003-3507-5195
                http://orcid.org/0000-0002-5267-8935
                http://orcid.org/0000-0002-6211-157X
                http://orcid.org/0000-0003-2526-8639
                http://orcid.org/0000-0002-7058-8343
                http://orcid.org/0000-0003-3376-2354
                http://orcid.org/0000-0002-0225-873X
                http://orcid.org/0000-0002-0770-1446
                http://orcid.org/0000-0003-4378-141X
                http://orcid.org/0000-0001-5785-9500
                http://orcid.org/0000-0001-6108-5560
                http://orcid.org/0000-0003-4420-9351
                http://orcid.org/0000-0002-0324-4639
                Article
                618
                10.1038/s41477-020-0618-2
                8075897
                32170292
                5d12ee8c-82b7-40bb-a1c4-c4f67405b5db
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 14 October 2019
                : 11 February 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000155, NSF | BIO | Division of Environmental Biology (DEB);
                Award ID: DEB1831428
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100000646, Japan Society for the Promotion of Science London (JSPS London);
                Award ID: KAKENHI 15H04413
                Award ID: PE14780
                Award Recipient :
                Funded by: National Institute for Basic Biology (NIBB) Collaborative Research Program (13-710)
                Funded by: FundRef https://doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation);
                Award ID: 160004
                Award ID: 131726
                Award ID: 160004
                Award ID: 131726
                Award ID: 160004
                Award ID: 131726
                Award Recipient :
                Funded by: The Forschungskredit of the University of Zurich The University Research Priority Program “Evolution in Action” of the University of Zurich The Georges and Antoine Claraz Foundation (Switzerland)
                Funded by: FundRef https://doi.org/10.13039/100000154, NSF | BIO | Division of Integrative Organismal Systems (IOS);
                Award ID: IOS-1339156
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000156, NSF | BIO | Division of Emerging Frontiers (EF);
                Award ID: EF-1550838
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100010663, EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council);
                Award ID: TerreStriAL
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000865, Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation);
                Award ID: OPP11772165
                Award Recipient :
                Funded by: Spanish Ministry of Science, Innovation and Universities (BFU2016-80621-P)
                Funded by: FundRef https://doi.org/10.13039/100010665, EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 Marie Skłodowska-Curie Actions (H2020 Excellent Science - Marie Skłodowska-Curie Actions);
                Award ID: PlantHUB
                Award Recipient :
                Funded by: The Georges and Antoine Claraz Foundation (Switzerland) The Research Priority Program “Evolution in Action” of the University of Zurich
                Funded by: Foundation of German Business (sdw), Georges and Antoine Claraz Foundation, URPP Evolution in Action of the University of Zurich
                Funded by: Special Grant for Innovation in Research Program of the Technical University of Dresden (Germany).
                Funded by: FundRef https://doi.org/10.13039/501100003246, Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Netherlands Organisation for Scientific Research);
                Award ID: 865.14.001
                Award ID: 865.14.001
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (German Research Foundation);
                Award ID: WI4507/3-1
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100004050, Kato Foundation for Promotion of Science;
                Award ID: 25113001
                Award ID: 26650143
                Award ID: 18K06367
                Award Recipient :
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                © The Author(s), under exclusive licence to Springer Nature Limited 2020

                genetics,plant sciences,genomics,evolution
                genetics, plant sciences, genomics, evolution

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