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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)
  • 투고 : 2019.08.26
  • 심사 : 2019.12.18
  • 발행 : 2020.01.31

초록

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.

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참고문헌

  1. Accardi, G. and Caruso, C. (2018). Immune-inflammatory responses in the elderly: an update. Immun. Ageing 15, 11. https://doi.org/10.1186/s12979-018-0117-8
  2. 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. https://doi.org/10.1038/nmeth0410-248
  3. 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. https://doi.org/10.1038/75556
  4. 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. https://doi.org/10.1016/j.molcel.2004.11.013
  5. 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. https://doi.org/10.3923/javaa.2012.2711.2715
  6. 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. https://doi.org/10.1371/journal.pone.0046688
  7. Collins, K. (2008). Physiological assembly and activity of human telomerase complexes. Mech. Ageing Dev. 129, 91-98. https://doi.org/10.1016/j.mad.2007.10.008
  8. Collins, K. and Mitchell, J.R. (2002). Telomerase in the human organism. Oncogene 21, 564-579. https://doi.org/10.1038/sj.onc.1205083
  9. del Hoyo, J., Elliott, A., and Sargatal, J. (1996). Handbook of the Birds of the World (Barcelona: Lynx Edicions).
  10. Egan, E.D. and Collins, K. (2012). Biogenesis of telomerase ribonucleoproteins. RNA 18, 1747-1759. https://doi.org/10.1261/rna.034629.112
  11. Eggenschwiler, J.T. and Anderson, K.V. (2007). Cilia and developmental signaling. Annu. Rev. Cell Dev. Biol. 23, 345-373. https://doi.org/10.1146/annurev.cellbio.23.090506.123249
  12. 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. https://doi.org/10.1007/s10522-013-9470-3
  13. 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. https://doi.org/10.2337/db11-0121
  14. 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. https://doi.org/10.1093/molbev/msv037
  15. Held, P. (2012). An Introduction to Reactive Oxygen Species: Measurement of ROS in Cells. Application Guide (Winooski: BioTek Instruments).
  16. 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. https://doi.org/10.1016/S0024-3205(00)00722-0
  17. 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. https://doi.org/10.1016/j.cell.2014.11.048
  18. 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. https://doi.org/10.1038/nprot.2008.211
  19. IUCN (International Union for Conservation of Nature) (2017). The IUCN Red List of Threatened Species. IUCN Data, https://www.iucnredlist.org/species/22692167/93339099.
  20. 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. https://doi.org/10.1186/s13742-014-0038-1
  21. 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. https://doi.org/10.1007/s11692-016-9405-4
  22. John, B. and Dunning, J. (2008). CRC Handbook of Avian Body Masses (Florida: CRC Press).
  23. Kanehisa, M. and Goto, S. (2000). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30. https://doi.org/10.1093/nar/28.1.27
  24. 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. https://doi.org/10.1525/auk.2009.09045
  25. Li, H. and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760. https://doi.org/10.1093/bioinformatics/btp324
  26. Li, H. and Durbin, R. (2011). Inference of human population history from individual whole-genome sequences. Nature 475, 493-496. https://doi.org/10.1038/nature10231
  27. 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. https://doi.org/10.1093/bioinformatics/btp352
  28. Li, L., Stoeckert, C.J., Jr., and Roos, D.S. (2003). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189. https://doi.org/10.1101/gr.1224503
  29. Loncarek, J. and Bettencourt-Dias, M. (2017). Building the right centriole for each cell type. J. Cell Biol. 217, 823-835. https://doi.org/10.1083/jcb.201704093
  30. Loytynoja, A. and Goldman, N. (2010). webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics 11, 579. https://doi.org/10.1186/1471-2105-11-579
  31. Marcais, G. and Kingsford, C. (2011). A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764-770. https://doi.org/10.1093/bioinformatics/btr011
  32. 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. https://doi.org/10.1086/383511
  33. 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. https://doi.org/10.1101/gr.107524.110
  34. 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. https://doi.org/10.1161/01.ATV.0000164043.24549.50
  35. Osada, N. (2014). Extracting population genetics information from a diploid genome sequence. Front. Ecol. Evol. 2, 7. https://doi.org/10.3389/fevo.2014.00007
  36. Rasmussen, P.C. and Engstrom, R.T. (2004). Threatened birds of Asia: the Birdlife international red data book. Auk 121, 619-622. https://doi.org/10.1642/0004-8038(2004)121[0619:TBOATB]2.0.CO;2
  37. Schmidt, J.C. and Cech, T.R. (2015). Human telomerase: biogenesis, trafficking, recruitment, and activation. Genes Dev. 29, 1095-1105. https://doi.org/10.1101/gad.263863.115
  38. 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. https://doi.org/10.2307/1538742
  39. 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. https://doi.org/10.1101/gr.1239303
  40. Speakman, J.R. (2005). Body size, energy metabolism and lifespan. J. Exp. Biol. 208, 1717-1730. https://doi.org/10.1242/jeb.01556
  41. 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. https://doi.org/10.1038/nature19754
  42. 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. https://doi.org/10.1093/nar/gks1155
  43. Tkemaladze, J.V. and Chichinadze, K.N. (2005). Centriolar mechanisms of differentiation and replicative aging of higher animal cells. Biochemistry (Mosc) 70, 1288-1303. https://doi.org/10.1007/s10541-005-0261-6
  44. Valentine, R.C. and Valentine, D.L. (2014). Human Longevity: Omega-3 Fatty Acids, Bioenergetics, Molecular Biology, and Evolution (Florida: CRC Press).
  45. 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.
  46. Walkinshaw, L. (1973). Cranes of the World (New York: Winchester Press).
  47. 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. https://doi.org/10.1016/j.biocon.2010.06.025
  48. Wasser, D.E. and Sherman, P.W. (2010). Avian longevities and their interpretation under evolutionary theories of senescence. J. Zool. 280, 103-155. https://doi.org/10.1111/j.1469-7998.2009.00671.x
  49. Yang, Z. (1997). PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555-556.
  50. 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. https://doi.org/10.1007/s11769-001-0041-1
  51. 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. https://doi.org/10.1126/science.1251385

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  1. Lifespan Extension in Long-Lived Vertebrates Rooted in Ecological Adaptation vol.9, 2020, https://doi.org/10.3389/fcell.2021.704966
  2. Comprehensive transcriptome characterization of Grus japonensis using PacBio SMRT and Illumina sequencing vol.11, pp.1, 2020, https://doi.org/10.1038/s41598-021-03474-7