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      Hardwood Tree Genomics: Unlocking Woody Plant Biology

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          Abstract

          Woody perennial angiosperms (i.e., hardwood trees) are polyphyletic in origin and occur in most angiosperm orders. Despite their independent origins, hardwoods have shared physiological, anatomical, and life history traits distinct from their herbaceous relatives. New high-throughput DNA sequencing platforms have provided access to numerous woody plant genomes beyond the early reference genomes of Populus and Eucalyptus, references that now include willow and oak, with pecan and chestnut soon to follow. Genomic studies within these diverse and undomesticated species have successfully linked genes to ecological, physiological, and developmental traits directly. Moreover, comparative genomic approaches are providing insights into speciation events while large-scale DNA resequencing of native collections is identifying population-level genetic diversity responsible for variation in key woody plant biology across and within species. Current research is focused on developing genomic prediction models for breeding, defining speciation and local adaptation, detecting and characterizing somatic mutations, revealing the mechanisms of gender determination and flowering, and application of systems biology approaches to model complex regulatory networks underlying quantitative traits. Emerging technologies such as single-molecule, long-read sequencing is being employed as additional woody plant species, and genotypes within species, are sequenced, thus enabling a comparative (“evo-devo”) approach to understanding the unique biology of large woody plants. Resource availability, current genomic and genetic applications, new discoveries and predicted future developments are illustrated and discussed for poplar, eucalyptus, willow, oak, chestnut, and pecan.

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          Most cited references 103

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          A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping.

          We use in situ Hi-C to probe the 3D architecture of genomes, constructing haploid and diploid maps of nine cell types. The densest, in human lymphoblastoid cells, contains 4.9 billion contacts, achieving 1 kb resolution. We find that genomes are partitioned into contact domains (median length, 185 kb), which are associated with distinct patterns of histone marks and segregate into six subcompartments. We identify ∼10,000 loops. These loops frequently link promoters and enhancers, correlate with gene activation, and show conservation across cell types and species. Loop anchors typically occur at domain boundaries and bind CTCF. CTCF sites at loop anchors occur predominantly (>90%) in a convergent orientation, with the asymmetric motifs "facing" one another. The inactive X chromosome splits into two massive domains and contains large loops anchored at CTCF-binding repeats. Copyright © 2014 Elsevier Inc. All rights reserved.
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            The genome of black cottonwood, Populus trichocarpa (Torr. & Gray).

            We report the draft genome of the black cottonwood tree, Populus trichocarpa. Integration of shotgun sequence assembly with genetic mapping enabled chromosome-scale reconstruction of the genome. More than 45,000 putative protein-coding genes were identified. Analysis of the assembled genome revealed a whole-genome duplication event; about 8000 pairs of duplicated genes from that event survived in the Populus genome. A second, older duplication event is indistinguishably coincident with the divergence of the Populus and Arabidopsis lineages. Nucleotide substitution, tandem gene duplication, and gross chromosomal rearrangement appear to proceed substantially more slowly in Populus than in Arabidopsis. Populus has more protein-coding genes than Arabidopsis, ranging on average from 1.4 to 1.6 putative Populus homologs for each Arabidopsis gene. However, the relative frequency of protein domains in the two genomes is similar. Overrepresented exceptions in Populus include genes associated with lignocellulosic wall biosynthesis, meristem development, disease resistance, and metabolite transport.
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              Real-time DNA sequencing from single polymerase molecules.

              We present single-molecule, real-time sequencing data obtained from a DNA polymerase performing uninterrupted template-directed synthesis using four distinguishable fluorescently labeled deoxyribonucleoside triphosphates (dNTPs). We detected the temporal order of their enzymatic incorporation into a growing DNA strand with zero-mode waveguide nanostructure arrays, which provide optical observation volume confinement and enable parallel, simultaneous detection of thousands of single-molecule sequencing reactions. Conjugation of fluorophores to the terminal phosphate moiety of the dNTPs allows continuous observation of DNA synthesis over thousands of bases without steric hindrance. The data report directly on polymerase dynamics, revealing distinct polymerization states and pause sites corresponding to DNA secondary structure. Sequence data were aligned with the known reference sequence to assay biophysical parameters of polymerization for each template position. Consensus sequences were generated from the single-molecule reads at 15-fold coverage, showing a median accuracy of 99.3%, with no systematic error beyond fluorophore-dependent error rates.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                17 December 2018
                2018
                : 9
                Affiliations
                1Center for Bioenergy Innovation, Biosciences Division, Oak Ridge National Laboratory (DOE) , Oak Ridge, TN, United States
                2Pacific Southwest Research Station, USDA Forest Service , Davis, CA, United States
                3HudsonAlpha Institute for Biotechnology , Huntsville, AL, United States
                4Joint Genome Institute , Walnut Creek, CA, United States
                5Department of Biology, West Virginia University , Morgantown, WV, United States
                6Department of Biochemistry, Genetics and Microbiology, Forestry and Agricultural Biotechnology Institute, University of Pretoria , Pretoria, South Africa
                7Embrapa Recursos Genéticos e Biotecnologia , Brasília, Brazil
                8Universidade Católica de Brasília , Brasília, Brazil
                9Horticulture Section, School of Integrative Plant Science, Cornell University , Geneva, NY, United States
                10The Key Laboratory for Poplar Improvement of Jiangsu Province, Nanjing Forestry University , Nanjing, China
                11Commissariat à l’Energie Atomique, Genoscope, Institut de Biologie François-Jacob , Evry, France
                12BIOGECO, INRA, Université de Bordeaux , Cestas, France
                13ISEM, CNRS, IRD, EPHE, Université de Montpellier , Montpellier, France
                14Schatz Center for Tree Molecular Genetics, Department of Ecosystem Science and Management, Pennsylvania State University , University Park, PA, United States
                15Department of Entomology, Plant Pathology and Weed Science, New Mexico State University , Las Cruces, NM, United States
                16The American Chestnut Foundation , Asheville, NC, United States
                Author notes

                Edited by: Ronald Ross Sederoff, North Carolina State University, United States

                Reviewed by: Hua Cassan Wang, Université de Toulouse, France; Deqiang Zhang, Beijing Forestry University, China

                *Correspondence: Gerald A. Tuskan, gtk@ 123456ornl.gov

                This article was submitted to Plant Biotechnology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.01799
                6304363
                30619389
                Copyright © 2018 Tuskan, Groover, Schmutz, DiFazio, Myburg, Grattapaglia, Smart, Yin, Aury, Kremer, Leroy, Le Provost, Plomion, Carlson, Randall, Westbrook, Grimwood, Muchero, Jacobson and Michener.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 111, Pages: 9, Words: 0
                Funding
                Funded by: U.S. Department of Energy 10.13039/100000015
                Award ID: DE-AC05-00OR22725
                Categories
                Plant Science
                Mini Review

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