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      The Medicago Genome Provides Insight into the Evolution of Rhizobial Symbioses

      research-article
      1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 2 , 3 , 11 , 12 , 12 , 13 , 14 , 10 , 15 , 5 , 15 , 10 , 16 , 17 , 17 , 4 , 8 , 8 , 13 , 18 , 15 , 12 , 8 , 1 , 19 , 2 , 3 , 16 , 20 , 19 , 20 , 15 , 5 , 21 , 19 , 19 , 1 , 22 , 8 , 23 , 2 , 3 , 17 , 19 , 5 , 2 , 3 , 13 , 16 , 24 , 14 , 25 , 5 , 22 , 26 , 14 , 22 , 25 , 22 , 13 , 27 , 25 , 22 , 5 , 22 , 22 , 19 , 26 , 15 , 15 , 13 , 28 , 22 , 26 , 29 , 22 , 1 , 19 , 2 , 3 , 22 , 22 , 17 , 26 , 2 , 3 , 19 , 2 , 3 , 22 , 2 , 3 , 19 , 29 , 19 , 7 , 14 , 22 , 26 , 30 , 8 , 12 , 19 , 1 , 22 , 8 , 1 , 25 , 19 , 22 , 22 , 22 , 19 , 22 , 22 , 22 , 22 , 14 , 22 , 2 , 3 , 2 , 3 , 8 , 17 , 16 , 31 , 19 , 15 , 22
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          Abstract

          Legumes ( Fabaceae or Leguminosae) are unique among cultivated plants for their ability to carry out endosymbiotic nitrogen fixation with rhizobial bacteria, a process that takes place in a specialized structure known as the nodule. Legumes belong to one of the two main groups of eurosids, the Fabidae, which includes most species capable of endosymbiotic nitrogen fixation 1 . Legumes comprise several evolutionary lineages derived from a common ancestor 60 million years ago (Mya). Papilionoids are the largest clade, dating nearly to the origin of legumes and containing most cultivated species 2 . Medicago truncatula ( Mt) is a long-established model for the study of legume biology. Here we describe the draft sequence of the Mt euchromatin based on a recently completed BAC-assembly supplemented with Illumina-shotgun sequence, together capturing ~94% of all Mt genes. A whole-genome duplication (WGD) approximately 58 Mya played a major role in shaping the Mt genome and thereby contributed to the evolution of endosymbiotic nitrogen fixation. Subsequent to the WGD, the Mt genome experienced higher levels of rearrangement than two other sequenced legumes, Glycine max ( Gm) and Lotus japonicus ( Lj). Mt is a close relative of alfalfa ( M. sativa), a widely cultivated crop with limited genomics tools and complex autotetraploid genetics. As such, the Mt genome sequence provides significant opportunities to expand alfalfa’s genomic toolbox.

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          Most cited references24

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          Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps.

          Large-scale (segmental or whole) genome duplication has been recurring in angiosperm evolution. Subsequent gene loss and rearrangements further affect gene copy numbers and fractionate ancestral gene linkages across multiple chromosomes. The fragmented "multiple-to-multiple" correspondences resulting from this distinguishing feature of angiosperm evolution complicates comparative genomic studies. Using a robust computational framework that combines information from multiple orthologous and duplicated regions to construct local syntenic networks, we show that a shared ancient hexaploidy event (or perhaps two roughly concurrent genome fusions) can be inferred based on the sequences from several divergent plant genomes. This "paleo-hexaploidy" clearly preceded the rosid-asterid split, but it remains equivocal whether it also affected monocots. The model resulting from our multi-alignments lays the foundation for approximating the number and arrangement of genes in the last universal common ancestor of angiosperms. Comparative analysis of inferred homologous genes derived from this model shows patterns of preferential gene retention or loss after polyploidy and reveals large variability of nucleotide substitution rates among plant nuclear genomes.
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            Coordinating nodule morphogenesis with rhizobial infection in legumes.

            The formation of nitrogen-fixing nodules on legumes requires an integration of infection by rhizobia at the root epidermis and the initiation of cell division in the cortex, several cell layers away from the sites of infection. Several recent developments have added to our understanding of the signaling events in the epidermis associated with the perception of rhizobial nodulation factors and the role of plant hormones in the activation of cell division leading to nodule morphogenesis. This review focuses on the tissue-specific nature of the developmental processes associated with nodulation and the mechanisms by which these processes are coordinated during the formation of a nodule.
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              Recent duplications dominate NBS-encoding gene expansion in two woody species.

              Most disease resistance genes in plants encode NBS-LRR proteins. However, in woody species, little is known about the evolutionary history of these genes. Here, we identified 459 and 330 respective NBS-LRRs in grapevine and poplar genomes. We subsequently investigated protein motif composition, phylogenetic relationships and physical locations. We found significant excesses of recent duplications in perennial species, compared with those of annuals, represented by rice and Arabidopsis. Consequently, we observed higher nucleotide identity among paralogs and a higher percentage of NBS-encoding genes positioned in numerous clusters in the grapevine and poplar. These results suggested that recent tandem duplication played a major role in NBS-encoding gene expansion in perennial species. These duplication events, together with a higher probability of recombination revealed in this study, could compensate for the longer generation time in woody perennial species e.g. duplication and recombination could serve to generate novel resistance specificities. In addition, we observed extensive species-specific expansion in TIR-NBS-encoding genes. Non-TIR-NBS-encoding genes were poly- or paraphyletic, i.e. genes from three or more plant species were nested in different clades, suggesting different evolutionary patterns between these two gene types.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                18 October 2011
                16 November 2011
                22 June 2012
                : 480
                : 7378
                : 520-524
                Affiliations
                [1 ]Departments of Plant Pathology and Plant Biology, University of Minnesota, St. Paul, MN 55108, USA
                [2 ]INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, BP 52627, F-31326 Castanet-Tolosan CEDEX, France
                [3 ]CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, BP 52627, F-31326 Castanet-Tolosan CEDEX, France
                [4 ]Department of Disease and Stress Biology, John Innes Centre, Norwich NR4 7UH, UK
                [5 ]Laboratory of Molecular Biology, Department of Plant Science, Wageningen University, Droevendaalsesteeg 1, 6708PB Wageningen, Netherlands
                [6 ]USDA-ARS Corn Insects and Crop Genetics Research Unit, Ames, IA, 50011, USA
                [7 ]Department of Agronomy, Iowa State University, Ames, IA 50011, USA
                [8 ]Plant Biology Division, Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, OK 73401, USA
                [9 ]Department of Genetics and Developmental Biology, Plant and Soil Science Division, West Virginia University, Morgantown, WV 26506, USA
                [10 ]MIPS/Institute for Bioinformatics and Systems Biology, Helmholtz Center Munich, Ingolstädter Landstr.1, Neuherberg, Germany
                [11 ]University of Bonn, INRES Crop Bioinformatics, Katzenburgweg 2, 53115 Bonn, Germany
                [12 ]Department of Plant Systems Biology, VIB, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium
                [13 ]Department of Plant Pathology, University of California, Davis, Davis, CA 95616, USA
                [14 ]Department of Plant & Soil Sciences and Delaware Biotechnology Institute, University of Delaware, Newark, DE 19711, USA
                [15 ]J. Craig Venter Institute, 9712 Medical Center Drive, Rockville, Maryland 20850, USA
                [16 ]Laboratory for Molecular and Computational Genomics, University of Wisconsin-Madison, Wisconsin 53706 USA
                [17 ]National Center for Genome Resources, 2935 Rodeo Park Drive East, Santa Fe, NM 87505 USA
                [18 ]Masonic Cancer Center, Biostatistics and Bioinformatics Group, University of Minnesota, Minneapolis, MN 55455 USA
                [19 ]Genoscope/Centre National de Séquençage, 2, rue Gaston Crémieux, CP 5706, 91057 Evry Cedex, France
                [20 ]INRA, Centre National de Ressources Génomiques Végétales (CNRGV), BP 52627, F-31326 Castanet-Tolosan CEDEX, France
                [21 ]College of Science, King Saud University, Post Office Box 2455, Riyadh 11451, Saudi Arabia
                [22 ]Advanced Center for Genome Technology, Department of Chemistry and Biochemistry, Stephenson Research and Technology Center, University of Oklahoma, Norman, OK 73019, USA
                [23 ]Department of Plant Biology, Cornell University, Ithaca, NY, 14853 USA
                [24 ]Department of Computer & Information Sciences, and Delaware Biotechnology Institute, University of Delaware, Newark, DE, 19711, USA
                [25 ]Max Planck Institute for Plant Breeding Research, Plant Computational Biology, Carl von Linné Weg 10, 50829 Köln, Germany
                [26 ]Illumina, Chesterford Research Park,, Saffron Walden, Essex CB10 1XJ, UK
                [27 ]International Institute for Tropical Agriculture, (c/o P.O. Box 30709 Nairobi, Kenya 00100), Ibadan, Nigeria
                [28 ]National Institute of Agricultural Biotechnology, Rural Development Administration, 225 Seodun-dong, Gwonseon-gu, Suwon 441-707, South Korea
                [29 ]INRA, Unité de Biométrie et d’Intelligence Artificielle (UBIA), UR875, BP 52627, F-31326 Castanet-Tolosan CEDEX, France
                [30 ]Department of Biology, Carleton College, Northfield, MN, 55057 USA
                [31 ]The Genome Analysis Centre, Norwich Research Park, Norwich, Norfolk NR4 7UH, UK
                Author notes
                Correspondence and requests for materials should be addressed to N.D.Y. ( neviny@ 123456umn.edu ).
                [*]

                These authors contributed equally to this work.

                Author Contributions: Planning, Coordination and Writing: N.D.Y., J.J.D., F.Q., J. Weissenbach, P.W., K.F.X.M., C.D.T., G.O., G.D.M., J. Mudge, E.F.R., R.A.D., M.K.U., F.D., J.D., D.R.C., P.J.G., B.C.M., J.D.S., C.R.P., B.A.R., D.C.S., S.B.C., Y.V.P., R.G., T.B., J.R.; BAC Libraries: B.S., A. Bellec, H.B., J. Gish, D.K.; Mapping and Assembly: V.B., N.C., S.F., G.M., S. Samain, E.M., F.P., N.S., O.S., A.Z., G.C., J.-H. Mun, R.D., M.B., S.Z., C.L., M.H., C.F., C. Nicholson, C.R.; Sequencing: A. Berger, J.P., A.V., D.J., S.D., Y.J., H.L., S.L.M., F.Z.N., B.Q., C.Q., M. Seigfried, I.S., R.S., K.W., D.D.W., G.B.W., Y.X., L.Y., Z.Y., F.Y., L.Z., S.J.H., L.M., S. Sims; Annotation and Bioinformatics: A.C., C.S., H.G., M. Spannagl, C. Noirot, T.S., A.J.S., S.B., F.C., V.K., J. McCorrison, H.T., A. Hallab, A.J., K.K., J. Warfsmann, A.K.B., A.D.F., V.A.B., J.D.M., M.A.N., S. Sinharoy, P.X.Z., P.B., A.D., J. Gouzy, E.S., H.S., B.R., A.J.G., J.Z., B.W., X.W., P.Z., K.A.T.S., A. Hua, S.M.K., S.L., J.D.W., S.G., S.P., S.R., L.S., S.D.M.

                Article
                UKMS36923
                10.1038/nature10625
                3272368
                22089132
                d927a524-19f1-414c-aaae-d1410ab034c7

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                Funding
                Funded by: Biotechnology and Biological Sciences Research Council :
                Award ID: BBS/B/11524 || BB_
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