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      Genome sequencing of the staple food crop white Guinea yam enables the development of a molecular marker for sex determination

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      1 , 1 , 1 , 2 , 1 , 1 , 3 , 1 , 1 , 1 , 4 , 5 , 6 , 7 , 7 , 7 , 8 , 8 , 8 , 8 , 8 , 8 , 8 , 9 , 9 , 2 , 2 , 10 , 11 , 7 , , 8 , , 1 , 12 ,
      BMC Biology
      BioMed Central
      Yam, Dioscorea, Whole-genome sequence, Dioecy, Sex determination

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          Abstract

          Background

          Root and tuber crops are a major food source in tropical Africa. Among these crops are several species in the monocotyledonous genus Dioscorea collectively known as yam, a staple tuber crop that contributes enormously to the subsistence and socio-cultural lives of millions of people, principally in West and Central Africa. Yam cultivation is constrained by several factors, and yam can be considered a neglected “orphan” crop that would benefit from crop improvement efforts. However, the lack of genetic and genomic tools has impeded the improvement of this staple crop.

          Results

          To accelerate marker-assisted breeding of yam, we performed genome analysis of white Guinea yam ( Dioscorea rotundata) and assembled a 594-Mb genome, 76.4% of which was distributed among 21 linkage groups. In total, we predicted 26,198 genes. Phylogenetic analyses with 2381 conserved genes revealed that Dioscorea is a unique lineage of monocotyledons distinct from the Poales (rice), Arecales (palm), and Zingiberales (banana). The entire Dioscorea genus is characterized by the occurrence of separate male and female plants (dioecy), a feature that has limited efficient yam breeding. To infer the genetics of sex determination, we performed whole-genome resequencing of bulked segregants (quantitative trait locus sequencing [QTL-seq]) in F1 progeny segregating for male and female plants and identified a genomic region associated with female heterogametic (male = ZZ, female = ZW) sex determination. We further delineated the W locus and used it to develop a molecular marker for sex identification of Guinea yam plants at the seedling stage.

          Conclusions

          Guinea yam belongs to a unique and highly differentiated clade of monocotyledons. The genome analyses and sex-linked marker development performed in this study should greatly accelerate marker-assisted breeding of Guinea yam. In addition, our QTL-seq approach can be utilized in genetic studies of other outcrossing crops and organisms with highly heterozygous genomes. Genomic analysis of orphan crops such as yam promotes efforts to improve food security and the sustainability of tropical agriculture.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12915-017-0419-x) contains supplementary material, which is available to authorized users.

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          Most cited references45

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            R/qtl: QTL mapping in experimental crosses

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              Automatic clustering of orthologs and in-paralogs from pairwise species comparisons.

              Orthologs are genes in different species that originate from a single gene in the last common ancestor of these species. Such genes have often retained identical biological roles in the present-day organisms. It is hence important to identify orthologs for transferring functional information between genes in different organisms with a high degree of reliability. For example, orthologs of human proteins are often functionally characterized in model organisms. Unfortunately, orthology analysis between human and e.g. invertebrates is often complex because of large numbers of paralogs within protein families. Paralogs that predate the species split, which we call out-paralogs, can easily be confused with true orthologs. Paralogs that arose after the species split, which we call in-paralogs, however, are bona fide orthologs by definition. Orthologs and in-paralogs are typically detected with phylogenetic methods, but these are slow and difficult to automate. Automatic clustering methods based on two-way best genome-wide matches on the other hand, have so far not separated in-paralogs from out-paralogs effectively. We present a fully automatic method for finding orthologs and in-paralogs from two species. Ortholog clusters are seeded with a two-way best pairwise match, after which an algorithm for adding in-paralogs is applied. The method bypasses multiple alignments and phylogenetic trees, which can be slow and error-prone steps in classical ortholog detection. Still, it robustly detects complex orthologous relationships and assigns confidence values for both orthologs and in-paralogs. The program, called INPARANOID, was tested on all completely sequenced eukaryotic genomes. To assess the quality of INPARANOID results, ortholog clusters were generated from a dataset of worm and mammalian transmembrane proteins, and were compared to clusters derived by manual tree-based ortholog detection methods. This study led to the identification with a high degree of confidence of over a dozen novel worm-mammalian ortholog assignments that were previously undetected because of shortcomings of phylogenetic methods.A WWW server that allows searching for orthologs between human and several fully sequenced genomes is installed at http://www.cgb.ki.se/inparanoid/. This is the first comprehensive resource with orthologs of all fully sequenced eukaryotic genomes. Programs and tables of orthology assignments are available from the same location. Copyright 2001 Academic Press.
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                Author and article information

                Contributors
                olimt@ibrc.or.jp
                s-natsume@ibrc.or.jp
                h-takagi@ibrc.or.jp
                Ben.White@earlham.ac.uk
                h-yaegashi@ibrc.or.jp
                m-shimizu@ibrc.or.jp
                kentaro.yoshida@port.kobe-u.ac.jp
                a-uemura@ibrc.or.jp
                kaori-o@ibrc.or.jp
                a-abe@ibrc.or.jp
                uraskiny@pref.okinawa.lg.jp
                hideoma@shinshu-u.ac.jp
                tp201893@nodai.ac.jp
                syamanak@affrc.go.jp
                r.matsumoto@cgiar.org
                smuranaka@affrc.go.jp
                gezgrm@yahoo.com
                mijuamarel@gmail.com
                m.gedil@cgiar.org
                r.bhattacharjee@cgiar.org
                m.abberton@cgiar.org
                L.Kumar@cgiar.org
                i.rabbi@cgiar.org
                mai_tsujimura@cc.kyoto-su.ac.jp
                terachi@cc.kyoto-su.ac.jp
                wilfried.haerty@earlham.ac.uk
                manuel.corpas@earlham.ac.uk
                sophien.kamoun@tsl.ac.uk
                hiroko55105@gmail.com
                r.asiedu@cgiar.org
                terauchi@ibrc.or.jp
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                19 September 2017
                19 September 2017
                2017
                : 15
                : 86
                Affiliations
                [1 ]ISNI 0000 0004 0376 441X, GRID grid.277489.7, Iwate Biotechnology Research Center, ; Kitakami, Japan
                [2 ]The Earlham Institute, Norwich, UK
                [3 ]ISNI 0000 0001 1092 3077, GRID grid.31432.37, Kobe University, ; Kobe, Japan
                [4 ]Okinawa Agricultural Research Center, Naha, Japan
                [5 ]ISNI 0000 0001 1507 4692, GRID grid.263518.b, Shinshu University, ; Nagano, Japan
                [6 ]GRID grid.410772.7, Tokyo University of Agriculture, ; Tokyo, Japan
                [7 ]ISNI 0000 0001 2107 8171, GRID grid.452611.5, Japan International Research Center for Agricultural Sciences, ; Tsukuba, Japan
                [8 ]ISNI 0000 0001 0943 0718, GRID grid.425210.0, International Institute of Tropical Agriculture, ; Ibadan, Nigeria
                [9 ]ISNI 0000 0001 0674 6688, GRID grid.258798.9, Kyoto Sangyo University, ; Kyoto, Japan
                [10 ]ISNI 0000 0001 0036 6123, GRID grid.18888.31, The Sainsbury Laboratory, ; Norwich, UK
                [11 ]ISNI 0000 0004 1936 9721, GRID grid.7839.5, University of Frankfurt, ; Frankfurt, Germany
                [12 ]ISNI 0000 0004 0372 2033, GRID grid.258799.8, Kyoto University, ; Kyoto, Japan
                Article
                419
                10.1186/s12915-017-0419-x
                5604175
                28927400
                38e5bdbb-1b19-4798-81a9-49d9c4a0ed33
                © The Author(s). 2017

                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
                : 3 May 2017
                : 10 August 2017
                Categories
                Research
                Custom metadata
                © The Author(s) 2017

                Life sciences
                yam,dioscorea,whole-genome sequence,dioecy,sex determination
                Life sciences
                yam, dioscorea, whole-genome sequence, dioecy, sex determination

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