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http://dx.doi.org/10.14348/molcells.2019.0190

Whole Genome Analysis of the Red-Crowned Crane Provides Insight into Avian Longevity  

Lee, HyeJin (Personal Genomics Institute, Genome Research Foundation)
Kim, Jungeun (Personal Genomics Institute, Genome Research Foundation)
Weber, Jessica A. (Department of Genetics, Harvard Medical School)
Chung, Oksung (Clinomics)
Cho, Yun Sung (Clinomics)
Jho, Sungwoong (Personal Genomics Institute, Genome Research Foundation)
Jun, JeHoon (Clinomics)
Kim, Hak-Min (KOGIC, Ulsan National Institute of Science and Technology)
Lim, Jeongheui (National Science Museum, Ministry of Science and ICT)
Choi, Jae-Pil (Personal Genomics Institute, Genome Research Foundation)
Jeon, Sungwon (KOGIC, Ulsan National Institute of Science and Technology)
Blazyte, Asta (KOGIC, Ulsan National Institute of Science and Technology)
Edwards, Jeremy S. (Chemistry and Chemical Biology, UNM Comprehensive Cancer Center, University of New Mexico)
Paek, Woon Kee (National Science Museum, Ministry of Science and ICT)
Bhak, Jong (Personal Genomics Institute, Genome Research Foundation)
Publication Information
Molecules and Cells / v.43, no.1, 2020 , pp. 86-95 More about this Journal
Abstract
The red-crowned crane (Grus japonensis) is an endangered, large-bodied crane native to East Asia. It is a traditional symbol of longevity and its long lifespan has been confirmed both in captivity and in the wild. Lifespan in birds is known to be positively correlated with body size and negatively correlated with metabolic rate, though the genetic mechanisms for the red-crowned crane's long lifespan have not previously been investigated. Using whole genome sequencing and comparative evolutionary analyses against the grey-crowned crane and other avian genomes, including the long-lived common ostrich, we identified redcrowned crane candidate genes with known associations with longevity. Among these are positively selected genes in metabolism and immunity pathways (NDUFA5, NDUFA8, NUDT12, SOD3, CTH, RPA1, PHAX, HNMT, HS2ST1, PPCDC, PSTK CD8B, GP9, IL-9R, and PTPRC). Our analyses provide genetic evidence for low metabolic rate and longevity, accompanied by possible convergent adaptation signatures among distantly related large and long-lived birds. Finally, we identified low genetic diversity in the red-crowned crane, consistent with its listing as an endangered species, and this genome should provide a useful genetic resource for future conservation studies of this rare and iconic species.
Keywords
genome; longevity; red-crowned crane;
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1 Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504.   DOI
2 Speakman, J.R. (2005). Body size, energy metabolism and lifespan. J. Exp. Biol. 208, 1717-1730.   DOI
3 Stroud, D.A., Surgenor, E.E., Formosa, L.E., Reljic, B., Frazier, A.E., Dibley, M.G., Osellame, L.D., Stait, T., Beilharz, T.H., Thorburn, D.R., et al. (2016). Accessory subunits are integral for assembly and function of human mitochondrial complex I. Nature 538, 123.   DOI
4 Tacutu, R., Craig, T., Budovsky, A., Wuttke, D., Lehmann, G., Taranukha, D., Costa, J., Fraifeld, V.E., and de Magalhaes, J.P. (2013). Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res. 41, D1027-D1033.   DOI
5 Tkemaladze, J.V. and Chichinadze, K.N. (2005). Centriolar mechanisms of differentiation and replicative aging of higher animal cells. Biochemistry (Mosc) 70, 1288-1303.   DOI
6 Valentine, R.C. and Valentine, D.L. (2014). Human Longevity: Omega-3 Fatty Acids, Bioenergetics, Molecular Biology, and Evolution (Florida: CRC Press).
7 Van der Auwera, G.A., Carneiro, M.O., Hartl, C., Poplin, R., del Angel, G., Levy-Moonshine, A., Jordan, T., Shakir, K., Roazen, D., Thibault, J., et al. (2013). From FastQ data to high confidence variant calls: the genome analysis toolkit best practices pipeline. Curr. Protoc. Bioinformatics 43, 11.10.1-11.10.33.
8 Walkinshaw, L. (1973). Cranes of the World (New York: Winchester Press).
9 Yang, Z. (1997). PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555-556.
10 Wasser, D.E. and Sherman, P.W. (2010). Avian longevities and their interpretation under evolutionary theories of senescence. J. Zool. 280, 103-155.   DOI
11 Yu, J., Liu, J., and Jin, W. (2001). Analysis of the environment feature of breeding area and endangered factors of red-crowned crane in China. Chin. Geogr. Sci. 11, 186-191.   DOI
12 Zhang, G., Li, C., Li, Q., Li, B., Larkin, D.M., Lee, C., Storz, J.F., Antunes, A., Greenwold, M.J., Meredith, R.W., et al. (2014). Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346, 1311-1320.   DOI
13 Collins, K. (2008). Physiological assembly and activity of human telomerase complexes. Mech. Ageing Dev. 129, 91-98.   DOI
14 Wang, Z., Li, Z., Beauchamp, G., and Jiang, Z. (2011). Flock size and human disturbance affect vigilance of endangered red-crowned cranes (Grus japonensis). Biol. Conserv. 144, 101-105.   DOI
15 Accardi, G. and Caruso, C. (2018). Immune-inflammatory responses in the elderly: an update. Immun. Ageing 15, 11.   DOI
16 Adzhubei, I.A., Schmidt, S., Peshkin, L., Ramensky, V.E., Gerasimova, A., Bork, P., Kondrashov, A.S., and Sunyaev, S.R. (2010). A method and server for predicting damaging missense mutations. Nat. Methods 7, 248-249.   DOI
17 Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T., et al. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29.   DOI
18 Boulon, S., Verheggen, C., Jady, B.E., Girard, C., Pescia, C., Paul, C., Ospina, J.K., Kiss, T., Matera, A.G., Bordonne, R., et al. (2004). PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol. Cell 16, 777-787.   DOI
19 Chen, W., Ma, J., Zhang, H., Li, D., and Zhang, X. (2012). Behavioural alterations in domestication process: comparative studies between wild, captive and inbred red-crowned cranes (Grus japonensis). J. Anim. Vet. Adv. 11, 2711-2715.   DOI
20 Choi, Y., Sims, G.E., Murphy, S., Miller, J.R., and Chan, A.P. (2012). Predicting the functional effect of amino acid substitutions and indels. PLoS One 7, e46688.   DOI
21 Collins, K. and Mitchell, J.R. (2002). Telomerase in the human organism. Oncogene 21, 564-579.   DOI
22 del Hoyo, J., Elliott, A., and Sargatal, J. (1996). Handbook of the Birds of the World (Barcelona: Lynx Edicions).
23 Egan, E.D. and Collins, K. (2012). Biogenesis of telomerase ribonucleoproteins. RNA 18, 1747-1759.   DOI
24 Hernanz, A., Fernandez-Vivancos, E., Montiel, C., Vazquez, J.J., and Arnalich, F. (2000). Changes in the intracellular homocysteine and glutathione content associated with aging. Life Sci. 67, 1317-1324.   DOI
25 Eggenschwiler, J.T. and Anderson, K.V. (2007). Cilia and developmental signaling. Annu. Rev. Cell Dev. Biol. 23, 345-373.   DOI
26 Gentschew, L., Flachsbart, F., Kleindorp, R., Badarinarayan, N., Schreiber, S., and Nebel, A. (2013). Polymorphisms in the superoxidase dismutase genes reveal no association with human longevity in Germans: a case-control association study. Biogerontology 14, 719-727.   DOI
27 Ghosh, S., Lertwattanarak, R., Lefort, N., Molina-Carrion, M., Joya-Galeana, J., Bowen, B.P., Garduno-Garcia Jde, J., Abdul-Ghani, M., Richardson, A., DeFronzo, R.A., et al. (2011). Reduction in reactive oxygen species production by mitochondria from elderly subjects with normal and impaired glucose tolerance. Diabetes 60, 2051-2060.   DOI
28 Hedges, S.B., Marin, J., Suleski, M., Paymer, M., and Kumar, S. (2015). Tree of life reveals clock-like speciation and diversification. Mol. Biol. Evol. 32, 835-845.   DOI
29 Held, P. (2012). An Introduction to Reactive Oxygen Species: Measurement of ROS in Cells. Application Guide (Winooski: BioTek Instruments).
30 Hine, C., Harputlugil, E., Zhang, Y., Ruckenstuhl, C., Lee, B.C., Brace, L., Longchamp, A., Trevino-Villarreal, J.H., Mejia, P., Ozaki, C.K., et al. (2015). Endogenous hydrogen sulfide production is essential for dietary restriction benefits. Cell 160, 132-144.   DOI
31 Huang, D.W., Sherman, B.T., and Lempicki, R.A. (2008). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.   DOI
32 Krajewski, C., Sipiorski, J.T., and Anderson, F.E. (2010). Complete mitochondrial genome sequences and the phylogeny of cranes (gruiformes: gruidae). Auk 127, 440-452.   DOI
33 IUCN (International Union for Conservation of Nature) (2017). The IUCN Red List of Threatened Species. IUCN Data, https://www.iucnredlist.org/species/22692167/93339099.
34 Jarvis, E.D., Mirarab, S., Aberer, A.J., Li, B., Houde, P., Li, C., Ho, S.Y.W., Faircloth, B.C., Nabholz, B., Howard, J.T., et al. (2015). Phylogenomic analyses data of the avian phylogenomics project. GigaScience 4, 4.   DOI
35 Ji, Y. and DeWoody, J.A. (2017). Relationships among powered flight, metabolic rate, body mass, genome size, and the retrotransposon complement of volant birds. Evol. Biol. 44, 261-272.   DOI
36 John, B. and Dunning, J. (2008). CRC Handbook of Avian Body Masses (Florida: CRC Press).
37 Kanehisa, M. and Goto, S. (2000). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30.   DOI
38 Li, H. and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760.   DOI
39 Li, H. and Durbin, R. (2011). Inference of human population history from individual whole-genome sequences. Nature 475, 493-496.   DOI
40 Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., and Genome Project Data Processing, S. (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079.   DOI
41 Li, L., Stoeckert, C.J., Jr., and Roos, D.S. (2003). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189.   DOI
42 Loncarek, J. and Bettencourt-Dias, M. (2017). Building the right centriole for each cell type. J. Cell Biol. 217, 823-835.   DOI
43 Osada, N. (2014). Extracting population genetics information from a diploid genome sequence. Front. Ecol. Evol. 2, 7.   DOI
44 Loytynoja, A. and Goldman, N. (2010). webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics 11, 579.   DOI
45 Marcais, G. and Kingsford, C. (2011). A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764-770.   DOI
46 McKechnie, A.E. and Wolf, B.O. (2004). The allometry of avian basal metabolic rate: good predictions need good data. Physiol. Biochem. Zool. 77, 502-521.   DOI
47 McKenna, A.H., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al. (2010). The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303.   DOI
48 Mendez, J.I., Nicholson, W.J., and Taylor, W.R. (2005). SOD isoforms and signaling in blood vessels: evidence for the importance of ROS compartmentalization. Arterioscler. Thromb. Vasc. Biol. 25, 887-888.   DOI
49 Rasmussen, P.C. and Engstrom, R.T. (2004). Threatened birds of Asia: the Birdlife international red data book. Auk 121, 619-622.   DOI
50 Schmidt, J.C. and Cech, T.R. (2015). Human telomerase: biogenesis, trafficking, recruitment, and activation. Genes Dev. 29, 1095-1105.   DOI
51 Scholander, P.F., Hock, R., Walters, V., and Irving, L. (1950). Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biol. Bull 99, 259-271.   DOI