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      Fern genomes elucidate land plant evolution and cyanobacterial symbioses

      , 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 1 , 11 , 12 , 13 , 14 , 12 , 11 , 15 , 14 , 16 , 1 , 17 , 18 , 19 , 6 , 4 , 5 , 13 , 1 , 20 , 21 , 22 , 23 , 24 , 6 , 14 , 4 , 5 , 25 , 6 , 21 , 22 , 6 , 12 , 3 , 6 , 26 , 9

      Nature Plants

      Nature Publishing Group UK

      Plant symbiosis, Natural variation in plants, Phylogenetics, Comparative genomics, Genome evolution

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.


          Ferns are the closest sister group to all seed plants, yet little is known about their genomes other than that they are generally colossal. Here, we report on the genomes of Azolla filiculoides and Salvinia cucullata (Salviniales) and present evidence for episodic whole-genome duplication in ferns—one at the base of ‘core leptosporangiates’ and one specific to Azolla. One fern-specific gene that we identified, recently shown to confer high insect resistance, seems to have been derived from bacteria through horizontal gene transfer. Azolla coexists in a unique symbiosis with N 2-fixing cyanobacteria, and we demonstrate a clear pattern of cospeciation between the two partners. Furthermore, the Azolla genome lacks genes that are common to arbuscular mycorrhizal and root nodule symbioses, and we identify several putative transporter genes specific to Azolla–cyanobacterial symbiosis. These genomic resources will help in exploring the biotechnological potential of Azolla and address fundamental questions in the evolution of plant life.


          The genomes of two fern species, Azolla filiculoides and Salvinia cucullata, are reported and provide insights into fern-specific whole-genome duplications, fern-specific insect-resistant gene evolution and fern–cyanobacterial symbiosis.

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          Most cited references 130

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          Is Open Access

          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: Contact:
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            MUSCLE: multiple sequence alignment with high accuracy and high throughput.

             Robert Edgar (2004)
            We describe MUSCLE, a new computer program for creating multiple alignments of protein sequences. Elements of the algorithm include fast distance estimation using kmer counting, progressive alignment using a new profile function we call the log-expectation score, and refinement using tree-dependent restricted partitioning. The speed and accuracy of MUSCLE are compared with T-Coffee, MAFFT and CLUSTALW on four test sets of reference alignments: BAliBASE, SABmark, SMART and a new benchmark, PREFAB. MUSCLE achieves the highest, or joint highest, rank in accuracy on each of these sets. Without refinement, MUSCLE achieves average accuracy statistically indistinguishable from T-Coffee and MAFFT, and is the fastest of the tested methods for large numbers of sequences, aligning 5000 sequences of average length 350 in 7 min on a current desktop computer. The MUSCLE program, source code and PREFAB test data are freely available at http://www.drive5. com/muscle.
              • Record: found
              • Abstract: found
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              Is Open Access

              Fast and accurate short read alignment with Burrows–Wheeler transform

              Motivation: The enormous amount of short reads generated by the new DNA sequencing technologies call for the development of fast and accurate read alignment programs. A first generation of hash table-based methods has been developed, including MAQ, which is accurate, feature rich and fast enough to align short reads from a single individual. However, MAQ does not support gapped alignment for single-end reads, which makes it unsuitable for alignment of longer reads where indels may occur frequently. The speed of MAQ is also a concern when the alignment is scaled up to the resequencing of hundreds of individuals. Results: We implemented Burrows-Wheeler Alignment tool (BWA), a new read alignment package that is based on backward search with Burrows–Wheeler Transform (BWT), to efficiently align short sequencing reads against a large reference sequence such as the human genome, allowing mismatches and gaps. BWA supports both base space reads, e.g. from Illumina sequencing machines, and color space reads from AB SOLiD machines. Evaluations on both simulated and real data suggest that BWA is ∼10–20× faster than MAQ, while achieving similar accuracy. In addition, BWA outputs alignment in the new standard SAM (Sequence Alignment/Map) format. Variant calling and other downstream analyses after the alignment can be achieved with the open source SAMtools software package. Availability: Contact:

                Author and article information

                [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 0000000120346234, GRID grid.5477.1, Molecular Plant Physiology Department, , Utrecht University, ; Utrecht, the Netherlands
                [4 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Bioinformatics Institute Ghent and Department of Plant Biotechnology and Bioinformatics, , Ghent University, ; Ghent, Belgium
                [5 ]ISNI 0000000104788040, GRID grid.11486.3a, VIB Center for Plant Systems Biology, ; Ghent, Belgium
                [6 ]ISNI 0000 0001 2034 1839, GRID grid.21155.32, BGI-Shenzhen, Beishan Industrial Zone, ; Shenzhen, China
                [7 ]ISNI 0000 0004 1936 8200, GRID grid.55602.34, Department of Biochemistry and Molecular Biology, , Dalhousie University, ; Halifax, Nova Scotia Canada
                [8 ]Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, Castanet Tolosan, France
                [9 ]ISNI 0000 0004 1936 7961, GRID grid.26009.3d, Department of Biology, , Duke University, ; Durham, NC USA
                [10 ]ISNI 0000 0001 2176 9917, GRID grid.411327.2, Department of Plant Biochemistry, Cluster of Excellence on Plant Sciences, , Heinrich Heine University Düsseldorf, ; Dusseldorf, Germany
                [11 ]ISNI 0000 0001 2168 186X, GRID grid.134563.6, Department of Ecology and Evolutionary Biology, , University of Arizona, ; Tucson, AZ USA
                [12 ]ISNI 0000 0001 2292 8158, GRID grid.253559.d, Department of Biological Science, , California State University, ; Fullerton, CA USA
                [13 ]ISNI 0000 0004 1936 7910, GRID grid.1012.2, ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, , The University of Western Australia, ; Crawley, Western Australia Australia
                [14 ]ISNI 0000 0001 2097 4281, GRID grid.29857.31, Department of Biology, Huck Institutes of the Life Sciences, , Pennsylvania State University, ; University Park, PA USA
                [15 ]ISNI 0000 0001 0944 9128, GRID grid.7491.b, Faculty of Biology, , Bielefeld University, ; Bielefeld, Germany
                [16 ]ISNI 0000 0001 2176 9917, GRID grid.411327.2, Institute for Molecular Evolution, , Heinrich Heine University Düsseldorf, ; Dusseldorf, Germany
                [17 ]GRID grid.410768.c, Taiwan Forestry Research Institute, ; Taipei, Taiwan
                [18 ]ISNI 0000 0001 0660 6765, GRID grid.419498.9, Max Planck Genome Centre Cologne, , Max Planck Institute for Plant Breeding, ; Cologne, Germany
                [19 ]ISNI 0000 0001 2151 536X, GRID grid.26999.3d, Institute for Sustainable Agro-ecosystem Services, , University of Tokyo, ; Tokyo, Japan
                [20 ]ISNI 0000000120346234, GRID grid.5477.1, Geolab, Faculty of Geosciences, , Utrecht University, ; Utrecht, the Netherlands
                [21 ]ISNI 0000 0004 1936 9756, GRID grid.10253.35, Faculty of Biology, , University of Marburg, ; Marburg, Germany
                [22 ]ISNI 0000 0001 2185 8768, GRID grid.53857.3c, Department of Biology, , Utah State University, ; Logan, UT USA
                [23 ]ISNI 0000 0001 2181 7878, GRID grid.47840.3f, University Herbarium and Department of Integrative Biology, , University of California, ; Berkeley, CA USA
                [24 ]ISNI 0000 0000 9831 5270, GRID grid.266621.7, Department of Biology, , University of Louisiana, ; Lafayette, LA USA
                [25 ]ISNI 0000 0001 2107 2298, GRID grid.49697.35, Department of Biochemistry, Genetics and Microbiology, , University of Pretoria, ; Pretoria, South Africa
                [26 ]GRID grid.17089.37, Department of Biological Sciences, Department of Medicine, , University of Alberta, ; Edmonton, Alberta Canada
                Nat Plants
                Nat Plants
                Nature Plants
                Nature Publishing Group UK (London )
                2 July 2018
                2 July 2018
                : 4
                : 7
                : 460-472
                29967517 6786969 188 10.1038/s41477-018-0188-8
                © The Author(s) 2018

                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

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