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      The genome of broomcorn millet

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          Abstract

          Broomcorn millet ( Panicum miliaceum L.) is the most water-efficient cereal and one of the earliest domesticated plants. Here we report its high-quality, chromosome-scale genome assembly using a combination of short-read sequencing, single-molecule real-time sequencing, Hi-C, and a high-density genetic map. Phylogenetic analyses reveal two sets of homologous chromosomes that may have merged ~5.6 million years ago, both of which exhibit strong synteny with other grass species. Broomcorn millet contains 55,930 protein-coding genes and 339 microRNA genes. We find Paniceae-specific expansion in several subfamilies of the BTB (broad complex/tramtrack/bric-a-brac) subunit of ubiquitin E3 ligases, suggesting enhanced regulation of protein dynamics may have contributed to the evolution of broomcorn millet. In addition, we identify the coexistence of all three C 4 subtypes of carbon fixation candidate genes. The genome sequence is a valuable resource for breeders and will provide the foundation for studying the exceptional stress tolerance as well as C 4 biology.

          Abstract

          Broomcorn millet is one of the earliest domesticated plants and has the highest water use efficiency among cereals. Here, the authors report its genome assembly and annotation, which provides a valuable resource for breeders and paves the way for studying plant drought tolerance and C 4 photosynthesis.

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          Most cited references41

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          A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data

          (2013)
          Motivation: Most existing methods for DNA sequence analysis rely on accurate sequences or genotypes. However, in applications of the next-generation sequencing (NGS), accurate genotypes may not be easily obtained (e.g. multi-sample low-coverage sequencing or somatic mutation discovery). These applications press for the development of new methods for analyzing sequence data with uncertainty. Results: We present a statistical framework for calling SNPs, discovering somatic mutations, inferring population genetical parameters and performing association tests directly based on sequencing data without explicit genotyping or linkage-based imputation. On real data, we demonstrate that our method achieves comparable accuracy to alternative methods for estimating site allele count, for inferring allele frequency spectrum and for association mapping. We also highlight the necessity of using symmetric datasets for finding somatic mutations and confirm that for discovering rare events, mismapping is frequently the leading source of errors. Availability: http://samtools.sourceforge.net. Contact: hengli@broadinstitute.org.
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            Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition.

            Each mode of gene duplication (tandem, tetraploid, segmental, transpositional) retains genes in a biased manner. A reciprocal relationship exists between plant genes retained postpaleotetraploidy versus genes retained after an ancient tandem duplication. Among the models (C, neofunctionalization, balanced gene drive) and ideas that might explain this relationship, only balanced gene drive predicts reciprocity. The gene balance hypothesis explains that more "connected" genes--by protein-protein interactions in a heteromer, for example--are less likely to be retained as a tandem or transposed duplicate and are more likely to be retained postpaleotetraploidy; otherwise, selectively negative dosage effects are created. Biased duplicate retention is an instant and neutral by-product, a spandrel, of purifying selection. Balanced gene drive expanded plant gene families, including those encoding proteasomal proteins, protein kinases, motors, and transcription factors, with each paleotetraploidy, which could explain trends involving complexity. Balanced gene drive is a saltation mechanism in the mutationist tradition.
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              Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics.

              Integration of structural genomic data from a largely assembled rice genome sequence, with phylogenetic analysis of sequence samples for many other taxa, suggests that a polyploidization event occurred approximately 70 million years ago, before the divergence of the major cereals from one another but after the divergence of the Poales from the Liliales and Zingiberales. Ancient polyploidization and subsequent "diploidization" (loss) of many duplicated gene copies has thus shaped the genomes of all Poaceae cereal, forage, and biomass crops. The Poaceae appear to have evolved as separate lineages for approximately 50 million years, or two-thirds of the time since the duplication event. Chromosomes that are predicted to be homoeologs resulting from this ancient duplication event account for a disproportionate share of incongruent loci found by comparison of the rice sequence to a detailed sorghum sequence-tagged site-based genetic map. Differential gene loss during diploidization may have contributed many of these incongruities. Such predicted homoeologs also account for a disproportionate share of duplicated sorghum loci, further supporting the hypothesis that the polyploidization event was common to sorghum and rice. Comparative gene orders along paleo-homoeologous chromosomal segments provide a means to make phylogenetic inferences about chromosome structural rearrangements that differentiate among the grasses. Superimposition of the timing of major duplication events on taxonomic relationships leads to improved understanding of comparative gene orders, enhancing the value of data from botanical models for crop improvement and for further exploration of genomic biodiversity. Additional ancient duplication events probably remain to be discovered in other angiosperm lineages.
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                Author and article information

                Contributors
                jkzhu@sibs.ac.cn
                zhangheng@sibs.ac.cn
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                25 January 2019
                25 January 2019
                2019
                : 10
                : 436
                Affiliations
                [1 ]ISNI 0000000119573309, GRID grid.9227.e, Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, , Chinese Academy of Sciences, ; 3888 Chenhua Rd, 201602 Shanghai, China
                [2 ]ISNI 0000 0000 9139 560X, GRID grid.256922.8, Key Laboratory of Plant Stress Biology, State Key Laboratory of Cotton Biology, School of Life Sciences, , Henan University, ; 85 Minglun Street, 475001 Kaifeng, Henan China
                [3 ]Data2Bio LLC, Ames, IA 50011-3650 USA
                [4 ]Dryland Genetics LLC, Ames, IA 50010 USA
                [5 ]ISNI 0000 0004 0530 8290, GRID grid.22935.3f, China Agricultural University, ; 100193 Beijing, China
                [6 ]ISNI 0000 0004 1936 7312, GRID grid.34421.30, Department of Agronomy, , Iowa State University, ; Ames, IA 50011-3650 USA
                [7 ]ISNI 0000 0001 0526 1937, GRID grid.410727.7, Agricultural Genomes Institute at Shenzhen, , Chinese Academy of Agricultural Sciences, ; 518120 Shenzhen, China
                [8 ]GRID grid.410585.d, Key Laboratory of Plant Stress Research, , Shandong Normal University, ; No. 88 Wenhua East Rd, Jinan, 250014 Shandong China
                [9 ]ISNI 0000 0004 1760 4150, GRID grid.144022.1, School of Agronomy, , Northwest Agriculture & Forestry University, ; 3 Weihui Rd, 712100 Yangling, China
                [10 ]ISNI 0000000119573309, GRID grid.9227.e, National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, , Chinese Academy of Sciences, ; 300 Fenglin Rd, 200032 Shanghai, China
                [11 ]ISNI 0000 0004 1937 0060, GRID grid.24434.35, Department of Agriculture and Horticulture, , University of Nebraska-Lincoln, ; Lincoln, NE 68588 USA
                [12 ]ISNI 0000 0004 1937 2197, GRID grid.169077.e, Department of Horticulture and Landscape Architecture, , Purdue University, ; West Lafayette, IN 47907 USA
                [13 ]ISNI 0000000119573309, GRID grid.9227.e, National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, , Chinese Academy of Sciences, ; 3888 Chenhua Rd, 201602 Shanghai, China
                Author information
                http://orcid.org/0000-0001-6805-3545
                http://orcid.org/0000-0002-9606-2497
                http://orcid.org/0000-0001-9169-5204
                http://orcid.org/0000-0002-0703-3732
                http://orcid.org/0000-0001-6739-5527
                http://orcid.org/0000-0002-1541-3890
                Article
                8409
                10.1038/s41467-019-08409-5
                6347628
                30683860
                58f84ae5-ae09-4746-93d0-71aafde7b1ad
                © The Author(s) 2019

                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/.

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                : 19 June 2018
                : 4 December 2018
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