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      Insights into the Evolution of Longevity from the Bowhead Whale Genome

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          Summary

          The bowhead whale ( Balaena mysticetus) is estimated to live over 200 years and is possibly the longest-living mammal. These animals should possess protective molecular adaptations relevant to age-related diseases, particularly cancer. Here, we report the sequencing and comparative analysis of the bowhead whale genome and two transcriptomes from different populations. Our analysis identifies genes under positive selection and bowhead-specific mutations in genes linked to cancer and aging. In addition, we identify gene gain and loss involving genes associated with DNA repair, cell-cycle regulation, cancer, and aging. Our results expand our understanding of the evolution of mammalian longevity and suggest possible players involved in adaptive genetic changes conferring cancer resistance. We also found potentially relevant changes in genes related to additional processes, including thermoregulation, sensory perception, dietary adaptations, and immune response. Our data are made available online ( http://www.bowhead-whale.org) to facilitate research in this long-lived species.

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          Highlights

          • •

            Genome and two transcriptomes of the bowhead whale, the longest-lived mammal

          • •

            Bowhead-specific mutations in genes associated with cancer and aging (e.g., ERCC1)

          • •

            Duplications in genes associated with DNA repair, cell cycle, and aging (e.g., PCNA)

          • •

            Changes in genes related to thermoregulation (UCP1) and other bowhead traits

          Abstract

          The bowhead whale is the longest-lived mammal, possibly living over 200 years. Keane et al. sequence the bowhead genome and transcriptome and perform a comparative analysis with other cetaceans and mammals. Changes in bowhead genes related to cell cycle, DNA repair, cancer, and aging suggest alterations that may be biologically relevant.

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          Most cited references44

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          TimeTree: a public knowledge-base of divergence times among organisms.

          S Blair Hedges, Joel T Dudley, Sudhir Kumar (2006)
          Biologists and other scientists routinely need to know times of divergence between species and to construct phylogenies calibrated to time (timetrees). Published studies reporting time estimates from molecular data have been increasing rapidly, but the data have been largely inaccessible to the greater community of scientists because of their complexity. TimeTree brings these data together in a consistent format and uses a hierarchical structure, corresponding to the tree of life, to maximize their utility. Results are presented and summarized, allowing users to quickly determine the range and robustness of time estimates and the degree of consensus from the published literature. TimeTree is available at http://www.timetree.net
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            RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO.

            Carsten Hoege, Boris Pfander, George-Lucian Moldovan … (2002)
            The RAD6 pathway is central to post-replicative DNA repair in eukaryotic cells; however, the machinery and its regulation remain poorly understood. Two principal elements of this pathway are the ubiquitin-conjugating enzymes RAD6 and the MMS2-UBC13 heterodimer, which are recruited to chromatin by the RING-finger proteins RAD18 and RAD5, respectively. Here we show that UBC9, a small ubiquitin-related modifier (SUMO)-conjugating enzyme, is also affiliated with this pathway and that proliferating cell nuclear antigen (PCNA) -- a DNA-polymerase sliding clamp involved in DNA synthesis and repair -- is a substrate. PCNA is mono-ubiquitinated through RAD6 and RAD18, modified by lysine-63-linked multi-ubiquitination--which additionally requires MMS2, UBC13 and RAD5--and is conjugated to SUMO by UBC9. All three modifications affect the same lysine residue of PCNA, suggesting that they label PCNA for alternative functions. We demonstrate that these modifications differentially affect resistance to DNA damage, and that damage-induced PCNA ubiquitination is elementary for DNA repair and occurs at the same conserved residue in yeast and humans.
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              The genome sequence of taurine cattle: a window to ruminant biology and evolution.

              Christine G Elsik, Ross L Tellam, Kim C. Worley … (2009)
              To understand the biology and evolution of ruminants, the cattle genome was sequenced to about sevenfold coverage. The cattle genome contains a minimum of 22,000 genes, with a core set of 14,345 orthologs shared among seven mammalian species of which 1217 are absent or undetected in noneutherian (marsupial or monotreme) genomes. Cattle-specific evolutionary breakpoint regions in chromosomes have a higher density of segmental duplications, enrichment of repetitive elements, and species-specific variations in genes associated with lactation and immune responsiveness. Genes involved in metabolism are generally highly conserved, although five metabolic genes are deleted or extensively diverged from their human orthologs. The cattle genome sequence thus provides a resource for understanding mammalian evolution and accelerating livestock genetic improvement for milk and meat production.
              Article 0 comments Cited 467 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                João Pedro de Magalhães
                Journal
                Journal ID (nlm-ta): Cell Rep
                Journal ID (iso-abbrev): Cell Rep
                Title: Cell Reports
                Publisher: Cell Press
                ISSN (Electronic): 2211-1247
                Publication date PMC-release: 06 January 2015
                Publication date Collection: 06 January 2015
                Publication date (Electronic): 06 January 2015
                Volume: 10
                Issue: 1
                Pages: 112-122
                Affiliations
                [1 ]Integrative Genomics of Ageing Group, Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK
                [2 ]Howard Hughes Medical Institute and Departments of Biophysics and Biochemistry, University of Texas Southwestern Medical Center, Dallas, TX 75390-9050, USA
                [3 ]Bioinformatics and Molecular Evolution Group, School of Biotechnology, Dublin City University, Glasnevin, Dublin 9, Ireland
                [4 ]MRC Functional Genomics Unit, University of Oxford, Oxford OX1 3QX, UK
                [5 ]Departamento de Bioquímica y Biología Molecular, Instituto Universitario de Oncología (IUOPA), Universidad de Oviedo, 33006 Oviedo, Spain
                [6 ]Department of Molecular Biology and Genetics, Aarhus University, 8830 Tjele, Denmark
                [7 ]Virginia Bioinformatics Institute, Virginia Tech, Blacksburg, VA 24061, USA
                [8 ]Personal Genomics Institute, Genome Research Foundation, Suwon 443-270, Republic of Korea
                [9 ]KIOST, Korea Institute of Ocean Science and Technology, Ansan 426–744, Republic of Korea
                [10 ]Greenland Institute of Natural Resources, 3900 Nuuk, Greenland
                [11 ]Department of Environmental Science, Center for Reservoir and Aquatic Systems Research (CRASR) and Institute for Biomedical Studies, Baylor University, Waco, TX 76798, USA
                [12 ]Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
                [13 ]The Center for Genomic Advocacy (TCGA) and Department of Biology, Indiana State University, Terre Haute, IN 47809, USA
                [14 ]Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907, USA
                [15 ]North Slope Borough, Department of Wildlife Management, Barrow, AK 99723, USA
                [16 ]Battelle Memorial Institute, Houston, TX 77079, USA
                [17 ]Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843, USA
                Author notes
                [∗ ]Corresponding author jp@ 123456senescence.info
                [18]

                Co-first author

                [19]

                Present address: Department of Genetics, Stanford University, Stanford, CA 94305, USA

                Article
                Publisher ID: S2211-1247(14)01019-5
                DOI: 10.1016/j.celrep.2014.12.008
                PMC ID: 4536333
                PubMed ID: 25565328
                SO-VID: 63682e4e-3b43-4552-b364-227ab16045a4
                Copyright © © 2015 The Authors
                License:

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).

                History
                Date received : 7 September 2014
                Date revision received : 21 November 2014
                Date accepted : 3 December 2014
                Categories
                Subject: Resource

                ScienceOpen disciplines: Cell biology
                Data availability:
                ScienceOpen disciplines: Cell biology

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