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      The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp

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          Abstract

          Background

          The protist Plasmodiophora brassicae is a soil-borne pathogen of cruciferous species and the causal agent of clubroot disease of Brassicas including agriculturally important crops such as canola/rapeseed ( Brassica napus). P. brassicae has remained an enigmatic plant pathogen and is a rare example of an obligate biotroph that resides entirely inside the host plant cell. The pathogen is the cause of severe yield losses and can render infested fields unsuitable for Brassica crop growth due to the persistence of resting spores in the soil for up to 20 years.

          Results

          To provide insight into the biology of the pathogen and its interaction with its primary host B. napus, we produced a draft genome of P. brassicae pathotypes 3 and 6 (Pb3 and Pb6) that differ in their host range. Pb3 is highly virulent on B. napus (but also infects other Brassica species) while Pb6 infects only vegetable Brassica crops. Both the Pb3 and Pb6 genomes are highly compact, each with a total size of 24.2 Mb, and contain less than 2 % repetitive DNA. Clustering of genome-wide single nucleotide polymorphisms (SNP) of Pb3, Pb6 and three additional re-sequenced pathotypes (Pb2, Pb5 and Pb8) shows a high degree of correlation of cluster grouping with host range. The Pb3 genome features significant reduction of intergenic space with multiple examples of overlapping untranslated regions (UTRs). Dependency on the host for essential nutrients is evident from the loss of genes for the biosynthesis of thiamine and some amino acids and the presence of a wide range of transport proteins, including some unique to P. brassicae. The annotated genes of Pb3 include those with a potential role in the regulation of the plant growth hormones cytokinin and auxin. The expression profile of Pb3 genes, including putative effectors, during infection and their potential role in manipulation of host defence is discussed.

          Conclusion

          The P. brassicae genome sequence reveals a compact genome, a dependency of the pathogen on its host for some essential nutrients and a potential role in the regulation of host plant cytokinin and auxin. Genome annotation supported by RNA sequencing reveals significant reduction in intergenic space which, in addition to low repeat content, has likely contributed to the P. brassicae compact genome.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12864-016-2597-2) contains supplementary material, which is available to authorized users.

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          Most cited references49

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          Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences

          Increased reliance on computational approaches in the life sciences has revealed grave concerns about how accessible and reproducible computation-reliant results truly are. Galaxy http://usegalaxy.org, an open web-based platform for genomic research, addresses these problems. Galaxy automatically tracks and manages data provenance and provides support for capturing the context and intent of computational methods. Galaxy Pages are interactive, web-based documents that provide users with a medium to communicate a complete computational analysis.
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            Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads.

            High-volume sequencing of DNA and RNA is now within reach of any research laboratory and is quickly becoming established as a key research tool. In many workflows, each of the short sequences ("reads") resulting from a sequencing run are first "mapped" (aligned) to a reference sequence to infer the read from which the genomic location derived, a challenging task because of the high data volumes and often large genomes. Existing read mapping software excel in either speed (e.g., BWA, Bowtie, ELAND) or sensitivity (e.g., Novoalign), but not in both. In addition, performance often deteriorates in the presence of sequence variation, particularly so for short insertions and deletions (indels). Here, we present a read mapper, Stampy, which uses a hybrid mapping algorithm and a detailed statistical model to achieve both speed and sensitivity, particularly when reads include sequence variation. This results in a higher useable sequence yield and improved accuracy compared to that of existing software.
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              Horizontal gene transfer in eukaryotic evolution.

              Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.
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                Author and article information

                Contributors
                s.rolfe@sheffield.ac.uk
                strelkov@ualberta.ca
                matthew.links@agr.gc.ca
                wclarke@nygenome.org
                steve.robinson@agr.gc.ca
                mohammad.djavaheri@agr.gc.ca
                rmal@igr.poznan.pl
                Parham.haddadi@agr.gc.ca
                Sateesh.Kagale@nrc-cnrc.gc.ca
                isobel.parkin@agr.gc.ca
                ataheri1@tnstate.edu
                hossein.borhan@agr.gc.ca
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                31 March 2016
                31 March 2016
                2016
                : 17
                : 272
                Affiliations
                [ ]Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN UK
                [ ]Department of Agricultural, Food and Nutritional Science, University of Alberta, 410 Agriculture/Forestry Centre, Edmonton, AB T6G 2P5 Canada
                [ ]Agriculture and Agri-Food Canada, 107 Science Place, Saskatoon, SK S7N 0X2 Canada
                [ ]Department of Integrative Plant Biology, Institute of Plant Genetics of the Polish Academy of Sciences, ul. Strzeszynska 34, 60-479 Poznan, Poland
                [ ]National Research Council Canada, 110 Gymnasium Place, Saskatoon, SK, S7N 0W9 Canada
                [ ]Present address: New York Genome Center, 101 6th Ave, New York, NY 10013 USA
                [ ]Present address: Department of Agricultural and Environmental Sciences, College of Agriculture, Human and Natural Sciences, Tennessee State University, 3500 John A Merritt Blvd, Nashville, TN 37209 USA
                Article
                2597
                10.1186/s12864-016-2597-2
                4815078
                27036196
                b43e119d-207f-4dc6-b8fe-2a297c9982fb
                © Rolfe et al. 2016

                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
                : 20 November 2015
                : 16 March 2016
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                Genetics
                plasmodiophora brassicae,clubroot,brassica napus,effectors,biotroph
                Genetics
                plasmodiophora brassicae, clubroot, brassica napus, effectors, biotroph

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