Reconstruction of the ancestral marsupial karyotype from comparative gene maps

BMC Evolutionary Biology

Jennifer A Marshall Graves¹  Vidushi S Patel⁶  Chenwei Wang³  Amber E Alsop⁷  Nerida Harley²  Edda Koina⁴  Margaret L Delbridge⁶  Janine E Deakin⁵ 

[1] La Trobe Institute of Molecular Sciences, La Trobe University, Melbourne, Victoria 3086, Australia;Current Address: Surgery, The University of Western Australia, 35 Stirling Highway, Crawley WA 6009, Australia;Australian Prostate Cancer Research Centre-Queensland, Queensland University of Technology, 199 Ipswich Rd, Brisbane, QLD 4102, Australia;Current Address: Cytogenetics Department, ACT Pathology, The Canberra Hospital, Yamba Drive, Canberra 2605, Australia;Institute of Applied Ecology, University of Canberra, Canberra ACT 2601, Australia;Evolution, Ecology and Genetics; Research School of Biology, The Australian National University, Canberra ACT 0200, Australia;Current Address: Walter & Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Victoria 3052, Australia

关键词: Ancestral karyotype;    Marsupial;    Physical map;    Comparative mapping;    Comparative genomics;   

Others  :  1084701
DOI  :  10.1186/1471-2148-13-258

 received in 2013-09-26, accepted in 2013-11-19,  发布年份 2013

【 摘 要 】

Background

The increasing number of assembled mammalian genomes makes it possible to compare genome organisation across mammalian lineages and reconstruct chromosomes of the ancestral marsupial and therian (marsupial and eutherian) mammals. However, the reconstruction of ancestral genomes requires genome assemblies to be anchored to chromosomes. The recently sequenced tammar wallaby (Macropus eugenii) genome was assembled into over 300,000 contigs. We previously devised an efficient strategy for mapping large evolutionarily conserved blocks in non-model mammals, and applied this to determine the arrangement of conserved blocks on all wallaby chromosomes, thereby permitting comparative maps to be constructed and resolve the long debated issue between a 2n = 14 and 2n = 22 ancestral marsupial karyotype.

Results

We identified large blocks of genes conserved between human and opossum, and mapped genes corresponding to the ends of these blocks by fluorescence in situ hybridization (FISH). A total of 242 genes was assigned to wallaby chromosomes in the present study, bringing the total number of genes mapped to 554 and making it the most densely cytogenetically mapped marsupial genome. We used these gene assignments to construct comparative maps between wallaby and opossum, which uncovered many intrachromosomal rearrangements, particularly for genes found on wallaby chromosomes X and 3. Expanding comparisons to include chicken and human permitted the putative ancestral marsupial (2n = 14) and therian mammal (2n = 19) karyotypes to be reconstructed.

Conclusions

Our physical mapping data for the tammar wallaby has uncovered the events shaping marsupial genomes and enabled us to predict the ancestral marsupial karyotype, supporting a 2n = 14 ancestor. Futhermore, our predicted therian ancestral karyotype has helped to understand the evolution of the ancestral eutherian genome.

【 授权许可】

   
2013 Deakin et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Phillips MJ, Bennett TH, Lee MS: Molecules, morphology, and ecology indicate a recent, amphibious ancestry for echidnas. Proc Natl Acad Sci USA 2009, 106:17089-17094.
• [2]Luo ZX, Yuan CX, Meng QJ, Ji Q: A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 2011, 476:442-445.
• [3]Beck RMD: A dated phylogeny of marsupials using a molecular supermatrix and multiple fossil constraints. J Mammal 2008, 89:175-189.
• [4]Meredith RW, Westerman M, Case JA, Springer MS: A Phylogeny and timescale for marsupial evolution based on sequences for five nuclear genes. J Mamm Evol 2008, 15:1-36.
• [5]Hayman DL: Marsupial cytogenetics. Aust J Zool 1990, 37:331-349.
• [6]Rens W, O’Brien PC, Fairclough H, Harman L, Graves JA, Ferguson-Smith MA: Reversal and convergence in marsupial chromosome evolution. Cytogenet Genome Res 2003, 102:282-290.
• [7]Rofe R, Hayman D: G-banding evidence for a conserved complement in the Marsupialia. Cytogenet Cell Genet 1985, 39:40-50.
• [8]Hayman DL, Martin PG: Marsupial Cytogenetics. Berlin: Gebruder Borntraeger; 1974.
• [9]Hayman DL, Martin PG: Mammalia I: Monotremata and Marsupialia . In Animal Cytogenetics. Volume 4: Chordata 4. Edited by John B. Gebruder Borntraeger: Berlin and Stuttgart; 1974.
• [10]Reig OA, Gardner AL, Bianchi NO, Patton JL: The chromosomes of the Didelphidae (Marsupialia) and their evolutionary significance. Biol J Linn Soc 1977, 9:191-216.
• [11]Sharman GB: The Chromosomes of non-Eutherian Mammals. In Cytotaxonomy and Vertebrate Evolution. Edited by Chiarelli AN, Capanna E. New York: Academic Press; 1973:485-530.
• [12]Svartman M, Vianna-Morgante AM: Karyotype evolution of marsupials: from higher to lower diploid numbers. Cytogenet Cell Genet 1998, 82:263-266.
• [13]Westerman M, Meredith RW, Springer MS: Cytogenetics meets phylogenetics: a review of karyotype evolution in diprotodontian marsupials. J Hered 2010, 101:690-702.
• [14]De Leo AA, Guedelha N, Toder R, Voullaire L, Ferguson-Smith MA, O’Brien PC, Graves JA: Comparative chromosome painting between marsupial orders: relationships with a 2n = 14 ancestral marsupial karyotype. Chromosome Res 1999, 7:509-517.
• [15]Rens W, O’Brien PC, Yang F, Solanky N, Perelman P, Graphodatsky AS, Ferguson MW, Svartman M, De Leo AA, Graves JA, Ferguson-Smith MA: Karyotype relationships between distantly related marsupials from South America and Australia. Chromosome Res 2001, 9:301-308.
• [16]Rens W, Ferguson-Smith M: The Conserved Marsupial Karyotype: Chromosome Painting and Evolution. In Marsupial Genetics and Genomics. Edited by Deakin JE, Waters PD, Graves JAM. Dordrecht, Heidlelberg, London, New York: Springer; 2010:37-53.
• [17]O’Neill RJ, Eldridge MD, Toder R, Ferguson-Smith MA, O’Brien PC, Graves JA: Chromosome evolution in kangaroos (Marsupialia: Macropodidae): cross species chromosome painting between the tammar wallaby and rock wallaby spp. with the 2n = 22 ancestral macropodid karyotype. Genome 1999, 42:525-530.
• [18]Meredith RW, Westerman M, Springer MS: A phylogeny of Diprotodontia (Marsupialia) based on sequences for five nuclear genes. Mol Phylogenet Evol 2009, 51:554-571.
• [19]Carvalho BD, Mattevi MS: (T2AG3)n telomeric sequence hybridization suggestive of centric fusion in karyotype marsupials evolution. Genetica 2000, 108:205-210.
• [20]Pagnozzi JM, De Jesus Silva MJ, Yonenaga-Yassuda Y: Intraspecific variation in the distribution of the interstitial telomeric (TTAGGG)n sequences in Micoureus demerarae (Marsupialia: Didelphidae). Chromosome Res 2000, 8:585-591.
• [21]Pagnozzi JM, Ditchfield AD, Yonenaga-Yassuda Y: Mapping the distribution of the interstitial telomeric (TTAGGG)n sequences in eight species of Brazilian marsupials (Didelphidae) by FISH and the correlation with constitutive heterochromatin. Do ITS represent evidence for fusion events in American marsupials? Cytogenet Genome Res 2002, 98:278-284.
• [22]Metcalfe CJ, Eldridge MD, Johnston PG: Mapping the distribution of the telomeric sequence (T2AG3)n in the 2n = 14 ancestral marsupial complement and in the macropodines (Marsupialia: Macropodidae) by fluorescence in situ hybridization. Chromosome Res 2004, 12:405-414.
• [23]Svartman M: American marsupials chromosomes: Why study them? Genet Mol Biol 2009, 32:675-687.
• [24]Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, Garber M, Gentles AJ, Goodstadt L, Heger A, et al.: Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 2007, 447:167-177.
• [25]Duke SE, Samollow PB, Mauceli E, Lindblad-Toh K, Breen M: Integrated cytogenetic BAC map of the genome of the gray, short-tailed opossum, Monodelphis domestica. Chromosome Res 2007, 15:361-370.
• [26]Murchison EP, Schulz-Trieglaff OB, Ning Z, Alexandrov LB, Bauer MJ, Fu B, Hims M, Ding Z, Ivakhno S, Stewart C, et al.: Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer. Cell 2012, 148:780-791.
• [27]Miller W, Hayes VM, Ratan A, Petersen DC, Wittekindt NE, Miller J, Walenz B, Knight J, Qi J, Zhao F, et al.: Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil). Proc Natl Acad Sci USA 2011, 108:12348-12353.
• [28]Deakin JE, Bender HS, Pearse AM, Rens W, O’Brien PC, Ferguson-Smith MA, Cheng Y, Morris K, Taylor R, Stuart A, et al.: Genomic restructuring in the Tasmanian devil facial tumour: chromosome painting and gene mapping provide clues to evolution of a transmissible tumour. PLoS Genet 2012, 8:e1002483.
• [29]Renfree MB, Papenfuss AT, Deakin JE, Lindsay J, Heider T, Belov K, Rens W, Waters PD, Pharo EA, Shaw G, et al.: Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. Genome Biol 2011, 12:R81. BioMed Central Full Text
• [30]Deakin JE, Koina E, Waters PD, Doherty R, Patel VS, Delbridge ML, Dobson B, Fong J, Hu Y, van den Hurk C, et al.: Physical map of two tammar wallaby chromosomes: a strategy for mapping in non-model mammals. Chromosome Res 2008, 16:1159-1175.
• [31]Clamp M, Andrews D, Barker D, Bevan P, Cameron G, Chen Y, Clark L, Cox T, Cuff J, Curwen V, et al.: Ensembl 2002: accommodating comparative genomics. Nucleic Acids Res 2003, 31:38-42.
• [32]Mohammadi A, Delbridge ML, Waters PD, Graves JA: Conservation of a chromosome arm in two distantly related marsupial species. Cytogenet Genome Res 2009, 124:147-150.
• [33]Trask BJ, Massa H, Kenwrick S, Gitschier J: Mapping of human chromosome Xq28 by two-color fluorescence in situ hybridization of DNA sequences to interphase cell nuclei. Am J Hum Genet 1991, 48:1-15.
• [34]Toder R, Wilcox SA, Smithwick M, Graves JA: The human/mouse imprinted genes IGF2, H19, SNRPN and ZNF127 map to two conserved autosomal clusters in a marsupial. Chromosome Res 1996, 4:295-300.
• [35]Edwards CA, Rens W, Clarke O, Mungall AJ, Hore T, Graves JA, Dunham I, Ferguson-Smith AC, Ferguson-Smith MA: The evolution of imprinting: chromosomal mapping of orthologues of mammalian imprinted domains in monotreme and marsupial mammals. BMC Evol Biol 2007, 7:157. BioMed Central Full Text
• [36]Lawton BR, Obergfell C, O’Neill RJ, O’Neill MJ: Physical mapping of the IGF2 locus in the South American opossum Monodelphis domestica. Cytogenet Genome Res 2007, 116:130-131.
• [37]Lewin HA, Larkin DM, Pontius J, O’Brien SJ: Every genome sequence needs a good map. Genome Res 2009, 19:1925-1928.
• [38]Wang C, Deakin JE, Rens W, Zenger KR, Belov K, Graves JAM, Nicholas FW: A first-generation integrated tammar wallaby map and its use in creating a tammar wallaby first-generation virtual map. BMC Genomicsin press
• [39]Warren WC, Hillier LW, Marshall Graves JA, Birney E, Ponting CP, Grutzner F, Belov K, Miller W, Clarke L, Chinwalla AT, et al.: Genome analysis of the platypus reveals unique signatures of evolution. Nature 2008, 453:175-183.
• [40]Ferguson-Smith MA, Trifonov V: Mammalian karyotype evolution. Nat Rev Genet 2007, 8:950-962.
• [41]Robinson TJ, Ruiz-Herrera A: Defining the ancestral eutherian karyotype: a cladistic interpretation of chromosome painting and genome sequence assembly data. Chromosome Res 2008, 16:1133-1141.
• [42]Bulazel KV, Ferreri GC, Eldridge MD, O’Neill RJ: Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol 2007, 8:R170. BioMed Central Full Text
• [43]Southern EM: Base sequence and evolution of guinea-pig alpha-satellite DNA. Nature 1970, 227:794-798.
• [44]Arnason U, Widegren B: Composition and chromosomal localization of cetacean highly repetitive DNA with special reference to the blue whale, Balaenoptera musculus. Chromosoma 1989, 98:323-329.
• [45]Deakin JE, Graves JA, Rens W: The evolution of marsupial and monotreme chromosomes. Cytogenet Genome Res 2012, 137:113-129.
• [46]Froenicke L, Caldes MG, Graphodatsky A, Muller S, Lyons LA, Robinson TJ, Volleth M, Yang F, Wienberg J: Are molecular cytogenetics and bioinformatics suggesting diverging models of ancestral mammalian genomes? Genome Res 2006, 16:306-310.
• [47]Ruiz-Herrera A, Farre M, Robinson TJ: Molecular cytogenetic and genomic insights into chromosomal evolution. Heredity (Edinb) 2012, 108:28-36.
• [48]Durinck S, Moreau Y, Kasprzyk A, Davis S, De Moor B, Brazma A, Huber W: BioMart and bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 2005, 21:3439-3440.
• [49]Derrien T, Andre C, Galibert F, Hitte C: AutoGRAPH: an interactive web server for automating and visualizing comparative genome maps. Bioinformatics 2007, 23:498-499.