1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Animal Biosciences
  4. Volume 9, 2021
  5. Article

Annual Review of Animal Biosciences

Volume 9, 2021

Programmed DNA Elimination in Vertebrates

Abstract

Over the last few decades, an increasing number of vertebrate taxa have been identified that undergo programmed genome rearrangement, or programmed DNA loss, during development. In these organisms, the genome of germ cells is often reproducibly different from the genome of all other cells within the body. Although we clearly have not identified all vertebrate taxa that undergo programmed genome loss, the list of species known to undergo loss now represents ∼10% of vertebrate species, including several basally diverging lineages. Recent studies have shed new light on the targets and mechanisms of DNA loss and their association with canonical modes of DNA silencing. Ultimately, expansion of these studies into a larger collection of taxa will aid in reconstructing patterns of shared/independent ancestry of programmed DNA loss in the vertebrate lineage, as well as more recent evolutionary events that have shaped the structure and content of eliminated DNA.

Keyword(s): evolution, genome, programmed DNA loss, programmed genome rearrangement, vertebrate
Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-061220-023220
2021-02-15
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/animal/9/1/annurev-animal-061220-023220.html?itemId=/content/journals/10.1146/annurev-animal-061220-023220&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Das S, Hirano M, Tako R, McCallister C, Nikolaidis N 2012. Evolutionary genomics of immunoglobulin-encoding loci in vertebrates. Curr. Genom. 13:95–102
     [Google Scholar]
  2. 2. 
    Hirano M, Das S, Guo P, Cooper MD 2011. The evolution of adaptive immunity in vertebrates. Adv. Immunol. 109:125–57
     [Google Scholar]
  3. 3. 
    Saha NR, Smith J, Amemiya CT 2010. Evolution of adaptive immune recognition in jawless vertebrates. Semin. Immunol. 22:25–33
     [Google Scholar]
  4. 4. 
    Boveri T. 1887. Über differenzierung der zellkerne während der furchung des eies von Ascaris megalocephala. Anat. Anz 2:288–693
     [Google Scholar]
  5. 5. 
    Bütschli O. 1876. Studien über die ersten Entwicklungsvorgänge der und die Konjugation der Infusorien. Abh. Senckenberg. Naturforschenden Ges. 10:1–250
     [Google Scholar]
  6. 6. 
    del Priore L, Pigozzi MI 2014. Histone modifications related to chromosome silencing and elimination during male meiosis in Bengalese finch. Chromosoma 123:293–302
     [Google Scholar]
  7. 7. 
    Scherbaum OH, Louderback AL, Jahn TL 1958. The formation of subnuclear aggregates in normal and synchronized protozoan cells. Biol. Bull. 115:269–75
     [Google Scholar]
  8. 8. 
    Yao MC, Gorovsky MA. 1974. Comparison of the sequences of macro- and micronuclear DNA of Tetrahymena pyriformis. Chromosoma 48:1–18
     [Google Scholar]
  9. 9. 
    Yao MC, Gall JG. 1979. Alteration of the Tetrahymena genome during nuclear differentiation. J. Protozool. 26:10–13
     [Google Scholar]
  10. 10. 
    Cleffmann G. 1980. Chromatin elimination and the genetic organisation of the macronucleus in Tetrahymena thermophila. Chromosoma 78:313–25
     [Google Scholar]
  11. 11. 
    Goday C, Pigozzi MI. 2010. Heterochromatin and histone modifications in the germline-restricted chromosome of the zebra finch undergoing elimination during spermatogenesis. Chromosoma 119:325–36
     [Google Scholar]
  12. 12. 
    Allis CD. 2018. Pursuing the secrets of histone proteins: an amazing journey with a remarkable supporting cast. Cell 175:18–21
     [Google Scholar]
  13. 13. 
    Allis CD, Glover CVC, Bowen JK, Gorovsky MA 1980. Histone variants specific to the transcriptionally active, amitotically dividing macronucleus of the unicellular eucaryote, Tetrahymena thermophila. Cell 20:609–17
     [Google Scholar]
  14. 14. 
    Inoue JG, Miya M, Lam K, Tay BH, Danks JA et al. 2010. Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Mol. Biol. Evol. 27:2576–86
     [Google Scholar]
  15. 15. 
    Smith JJ, Saha NR, Amemiya CT 2010. Genome biology of the cyclostomes and insights into the evolutionary biology of vertebrate genomes. Integr. Comp. Biol. 50:130–37
     [Google Scholar]
  16. 16. 
    Kitada J, Tagawa M. 1975. Somatic chromosomes of three species of Cyclostomata. Chrom. Inform. Serv. 18:10–12
     [Google Scholar]
  17. 17. 
    Kohno S, Nakai Y, Satoh S, Yoshida M, Kobayashi H 1986. Chromosome elimination in the Japanese hagfish, Eptatretus burgeri (Agnatha, Cyclostomata). Cytogenet. Cell Genet. 41:209–14
     [Google Scholar]
  18. 18. 
    Nogusa S. 1960. A comparative study of the chromosomes in fishes with particular considerations on taxonomy and evolution. Mem. Hyogo Univ. Agricult. 3:1–68
     [Google Scholar]
  19. 19. 
    Nakai Y, Kohno S. 1987. Elimination of the largest chromosome pair during differentiation into somatic cells in the Japanese hagfish, Myxine garmani (Cyclostomata, Agnatha). Cytogenet. Cell Genet. 45:80–83
     [Google Scholar]
  20. 20. 
    Nakai Y, Kubota S, Kohno S 1991. Chromatin diminution and chromosome elimination in four Japanese hagfish species. Cytogenet. Cell Genet. 56:196–98
     [Google Scholar]
  21. 21. 
    Kubota S, Nakai Y, Kuro-o M, Kohno S 1992. Germ line-restricted supernumerary (B) chromosomes in Eptatretus okinoseanus. Cytogenet. Cell Genet 60:224–28
     [Google Scholar]
  22. 22. 
    Kubota S, Nakai Y, Sato N, Kuro-o M, Kohno S 1994. Chromosome elimination in northeast Pacific hagfish, Eptatretus stoutii (Cyclostomata, Agnatha). J. Hered. 85:413–15
     [Google Scholar]
  23. 23. 
    Nakai Y, Kubota S, Goto Y, Ishibashi T, Davison W, Kohno S 1995. Chromosome elimination in three Baltic, south Pacific and north-east Pacific hagfish species. Chromosome Res 3:321–30
     [Google Scholar]
  24. 24. 
    Shichiri M, Kikuma Y, Kuo C-H, Liu L-L, Kubota S, Kohno S 1997. Chromosome elimination and germ line-restricted microchromosomes in Paramyxine sheni from Taiwan. Chromosome Sci 1:49–53
     [Google Scholar]
  25. 25. 
    Kohno S, Kubota S, Nakai Y 1998. Chromatin diminution and chromosome elimination in hagfishes. The Biology of Hagfishes81–100 Dordrecht, Neth: Springer
     [Google Scholar]
  26. 26. 
    Pigozzi MI, Solari AJ. 1998. Germ cell restriction and regular transmission of an accessory chromosome that mimics a sex body in the zebra finch, Taeniopygia guttata. Chromosome Res. 6:105–13
     [Google Scholar]
  27. 27. 
    Pigozzi MI, Solari AJ. 2005. The germ-line-restricted chromosome in the zebra finch: recombination in females and elimination in males. Chromosoma 114:403–9
     [Google Scholar]
  28. 28. 
    Kubota S, Kuro-o M, Mizuno S, Kohno S 1993. Germ line-restricted, highly repeated DNA sequences and their chromosomal localization in a Japanese hagfish (Eptatretus okinoseanus). Chromosoma 102:163–73
     [Google Scholar]
  29. 29. 
    Kubota S, Ishibashi T, Kohno S 1997. A germline restricted, highly repetitive DNA sequence in Paramyxine atami: an interspecifically conserved, but somatically eliminated, element. Mol. Gen. Genet. 256:252–56
     [Google Scholar]
  30. 30. 
    Goto Y, Kubota S, Kohno S 1998. Highly repetitive DNA sequences that are restricted to the germ line in the hagfish Eptatretus cirrhatus: a mosaic of eliminated elements. Chromosoma 107:17–32
     [Google Scholar]
  31. 31. 
    Kubota S, Takano J, Tsuneishi R, Kobayakawa S, Fujikawa N et al. 2001. Highly repetitive DNA families restricted to germ cells in a Japanese hagfish (Eptatretus burgeri): a hierarchical and mosaic structure in eliminated chromosomes. Genetica 111:319–28
     [Google Scholar]
  32. 32. 
    Nabeyama M, Kubota S, Kohno S 2000. Concerted evolution of a highly repetitive DNA family in Eptatretidae (Cyclostomata, Agnatha) implies specifically differential homogenization and amplification events in their germ cells. J. Mol. Evol. 50:154–69
     [Google Scholar]
  33. 33. 
    Kojima NF, Kojima KK, Kobayakawa S, Higashide N, Hamanaka C et al. 2010. Whole chromosome elimination and chromosome terminus elimination both contribute to somatic differentiation in Taiwanese hagfish Paramyxine sheni. Chromosome Res 18:383–400
     [Google Scholar]
  34. 34. 
    Jahn CL, Klobutcher LA. 2002. Genome remodeling in ciliated protozoa. Annu. Rev. Microbiol. 56:489–520
     [Google Scholar]
  35. 35. 
    Muller F, Tobler H. 2000. Chromatin diminution in the parasitic nematodes Ascaris suum and Parascaris univalens. Int. J. Parasitol 30:391–99
     [Google Scholar]
  36. 36. 
    Elder JFJr., Turner BJ. 1995. Concerted evolution of repetitive DNA sequences in eukaryotes. Q. Rev. Biol. 70:297–320
     [Google Scholar]
  37. 37. 
    Liao D. 1999. Concerted evolution: molecular mechanism and biological implications. Am. J. Hum. Genet. 64:24–30
     [Google Scholar]
  38. 38. 
    Kuraku S, Kuratani S. 2006. Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zool. Sci. 23:1053–64
     [Google Scholar]
  39. 39. 
    Thomson RC, Plachetzki DC, Mahler DL, Moore BR 2014. A critical appraisal of the use of microRNA data in phylogenetics. PNAS 111:E3659–68
     [Google Scholar]
  40. 40. 
    Smith JJ, Antonacci F, Eichler EE, Amemiya CT 2009. Programmed loss of millions of base pairs from a vertebrate genome. PNAS 106:11212–17
     [Google Scholar]
  41. 41. 
    Timoshevskiy VA, Timoshevskaya NY, Smith JJ 2019. Germline-specific repetitive elements in programmatically eliminated chromosomes of the sea lamprey (Petromyzon marinus). Genes 10:832
     [Google Scholar]
  42. 42. 
    Strange RM, Moore LL. 2019. Characterization and evolution of Germ1, an element that undergoes diminution in lampreys (Cyclostomata: Petromyzontidae). J. Mol. Evol. 87:298–308
     [Google Scholar]
  43. 43. 
    Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N et al. 2013. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat. Genet. 45:415–21
     [Google Scholar]
  44. 44. 
    Smith JJ, Stuart AB, Sauka-Spengler T, Clifton SW, Amemiya CT 2010. Development and analysis of a germline BAC resource for the sea lamprey, a vertebrate that undergoes substantial chromatin diminution. Chromosoma 119:381–89
     [Google Scholar]
  45. 45. 
    Smith JJ, Baker C, Eichler EE, Amemiya CT 2012. Genetic consequences of programmed genome rearrangement. Curr. Biol. 22:1524–29
     [Google Scholar]
  46. 46. 
    Bryant SA, Herdy JR, Amemiya CT, Smith JJ 2016. Characterization of somatically-eliminated genes during development of the sea lamprey (Petromyzon marinus). Mol. Biol. Evol. 33:2337–44
     [Google Scholar]
  47. 47. 
    Smith JJ, Timoshevskaya N, Ye C, Holt C, Keinath MC et al. 2018. The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution. Nat. Genet. 50:270–77
     [Google Scholar]
  48. 48. 
    Timoshevskiy VA, Herdy JR, Keinath MC, Smith JJ 2016. Cellular and molecular features of developmentally programmed genome rearrangement in a vertebrate (sea lamprey: Petromyzon marinus). PLOS Genet 12:e1006103
     [Google Scholar]
  49. 49. 
    Lachmann A, Xu H, Krishnan J, Berger SI, Mazloom AR, Ma'ayan A 2010. ChEA: transcription factor regulation inferred from integrating genome-wide ChIP-X experiments. Bioinformatics 26:2438–44
     [Google Scholar]
  50. 50. 
    Sachs M, Onodera C, Blaschke K, Ebata KT, Song JS, Ramalho-Santos M 2013. Bivalent chromatin marks developmental regulatory genes in the mouse embryonic germline in vivo. Cell Rep 3:1777–84
     [Google Scholar]
  51. 51. 
    Robinson ES, Potter IC, Atkin NB 1975. The nuclear DNA content of lampreys. Experientia 31:912–13
     [Google Scholar]
  52. 52. 
    Yan X, Meng W, Wu F, Xu A, Chen S, Huang S 2016. The nuclear DNA content and genetic diversity of Lampetra morii. PLOS ONE 11:e0157494
     [Google Scholar]
  53. 53. 
    Itoh Y, Arnold AP. 2005. Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res 13:47–56
     [Google Scholar]
  54. 54. 
    Biederman MK, Nelson MM, Asalone KC, Pedersen AL, Saldanha CJ, Bracht JR 2018. Discovery of the first germline-restricted gene by subtractive transcriptomic analysis in the zebra finch, Taeniopygia guttata. Curr. Biol. 28:1620–27.e5
     [Google Scholar]
  55. 55. 
    Smith JJ. 2018. Programmed DNA elimination: keeping germline genes in their place. Curr. Biol. 28:R601–R3
     [Google Scholar]
  56. 56. 
    Torgasheva AA, Malinovskaya LP, Zadesenets KS, Karamysheva TV, Kizilova EA et al. 2019. Germline-restricted chromosome (GRC) is widespread among songbirds. PNAS 116:11845–50
     [Google Scholar]
  57. 57. 
    Kinsella CM, Ruiz-Ruano FJ, Dion-Côté AM, Charles AJ, Gossmann TI et al. 2019. Programmed DNA elimination of germline development genes in songbirds. Nat. Commun. 10:5468
     [Google Scholar]
  58. 58. 
    Gall JG. 2012. Are lampbrush chromosomes unique to meiotic cells. Chromosome Res 20:905–9
     [Google Scholar]
  59. 59. 
    Hansson B. 2019. On the origin and evolution of germline chromosomes in songbirds. PNAS 116:11570–72
     [Google Scholar]
  60. 60. 
    Wang J, Gao S, Mostovoy Y, Kang Y, Zagoskin M et al. 2017. Comparative genome analysis of programmed DNA elimination in nematodes. Genome Res 27:2001–14
     [Google Scholar]
  61. 61. 
    Itoh Y, Kampf K, Pigozzi MI, Arnold AP 2009. Molecular cloning and characterization of the germline-restricted chromosome sequence in the zebra finch. Chromosoma 118:527–36
     [Google Scholar]
  62. 62. 
    Malinovskaya LP, Zadesenets KS, Karamysheva TV, Akberdina EA, Kizilova EA et al. 2020. Germline-restricted chromosome (GRC) in the sand martin and the pale martin (Hirundinidae, Aves): synapsis, recombination and copy number variation. Sci. Rep. 10:1058
     [Google Scholar]
  63. 63. 
    Schoenmakers S, Wassenaar E, Laven JS, Grootegoed JA, Baarends WM 2010. Meiotic silencing and fragmentation of the male germline restricted chromosome in zebra finch. Chromosoma 119:311–24
     [Google Scholar]
  64. 64. 
    Vigodner M, Morris PL. 2005. Testicular expression of small ubiquitin-related modifier-1 (SUMO-1) supports multiple roles in spermatogenesis: silencing of sex chromosomes in spermatocytes, spermatid microtubule nucleation, and nuclear reshaping. Dev. Biol. 282:480–92
     [Google Scholar]
  65. 65. 
    Metzler-Guillemain C, Depetris D, Luciani JJ, Mignon-Ravix C, Mitchell MJ, Mattei M-G 2008. In human pachytene spermatocytes, SUMO protein is restricted to the constitutive heterochromatin. Chromosome Res 16:761–82
     [Google Scholar]
  66. 66. 
    Greil F, van der Kraan I, Delrow J, Smothers JF, de Wit E et al. 2003. Distinct HP1 and Su(var)3–9 complexes bind to sets of developmentally coexpressed genes depending on chromosomal location. Genes Dev 17:2825–38
     [Google Scholar]
  67. 67. 
    Grewal SI, Jia S. 2007. Heterochromatin revisited. Nat. Rev. Genet. 8:35–46
     [Google Scholar]
  68. 68. 
    Giet R, Glover DM. 2001. Drosophila Aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152:669–82
     [Google Scholar]
  69. 69. 
    Gurley LR, D'Anna JA, Barham SS, Deaven LL, Tobey RA 1978. Histone phosphorylation and chromatin structure during mitosis in Chinese hamster cells. Eur. J. Biochem. 84:1–15
     [Google Scholar]
  70. 70. 
    Paulson JR, Taylor SS. 1982. Phosphorylation of histones 1 and 3 and nonhistone high mobility group 14 by an endogenous kinase in HeLa metaphase chromosomes. J. Biol. Chem. 257:6064–72
     [Google Scholar]
  71. 71. 
    Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD 1998. Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. PNAS 95:7480–84
     [Google Scholar]
  72. 72. 
    Sawicka A, Seiser C. 2012. Histone H3 phosphorylation—a versatile chromatin modification for different occasions. Biochimie 94:2193–201
     [Google Scholar]
  73. 73. 
    Li W, Wang P, Zhang B, Zhang J, Ming J et al. 2017. Differential regulation of H3S10 phosphorylation, mitosis progression and cell fate by Aurora Kinase B and C in mouse preimplantation embryos. Protein Cell 8:662–74
     [Google Scholar]
  74. 74. 
    Adams RR, Maiato H, Earnshaw WC, Carmena M 2001. Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J. Cell Biol. 153:865–80
     [Google Scholar]
  75. 75. 
    Lyon MF. 1962. Sex chromatin and gene action in the mammalian X-chromosome. Am. J. Hum. Genet. 14:135–48
     [Google Scholar]
  76. 76. 
    Brockdorff N, Duthie SM. 1998. X chromosome inactivation and the Xist gene. Cell. Mol. Life Sci. 54:104–12
     [Google Scholar]
  77. 77. 
    Richardson BJ, Czuppon AB, Sharman GB 1971. Inheritance of glucose-6-phosphate dehydrogenase variation in kangaroos. Nat. New Biol. 230:154–55
     [Google Scholar]
  78. 78. 
    Deakin JE, Chaumeil J, Hore TA, Marshall Graves JA 2009. Unravelling the evolutionary origins of X chromosome inactivation in mammals: insights from marsupials and monotremes. Chromosome Res 17:671–85
     [Google Scholar]
  79. 79. 
    Hayman DL, Martin PG. 1965. Sex chromosome mosaicism in the marsupial genera Isoodon and Perameles. Genetics 52:1201–6
     [Google Scholar]
  80. 80. 
    Close RL. 1979. Sex chromosome mosaicism in liver, thymus, spleen and regenerating liver of Perameles nasuta and Isoodon macrourus. Aust. J. Biol. Sci 32:615–24
     [Google Scholar]
  81. 81. 
    Close RL. 1984. Rates of sex chromosome loss during development in different tissues of the bandicoots Perameles nasuta and Isoodon macrourus (Marsupialia: Peramelidae). Aust. J. Biol. Sci. 37:53–61
     [Google Scholar]
  82. 82. 
    Watson CM, Margan SH, Johnston PG 1998. Sex-chromosome elimination in the bandicoot Isoodon macrourus using Y-linked markers. Cytogenet. Cell Genet. 81:54–59
     [Google Scholar]
  83. 83. 
    Hayman DL, Margan SH. 1969. Cytogenetics of marsupials. Comparative Mammalian Cytogenetics K Benirschke 191–217 Berlin, Heidelberg, Ger: Springer
     [Google Scholar]
  84. 84. 
    Hayman DL, Martin PG. 1974. Mammalia I: Monotremata and Marsupialia. Animal Cytogenetics 4. Chordata B John 19–84 Berlin, Stuttgart, Ger: Gebruder Borntraeger
     [Google Scholar]
  85. 85. 
    Sharman GB. 1974. Marsupial taxonomy and phylogeny. Aust. Mammal. 1:137–54
     [Google Scholar]
  86. 86. 
    Murray JD, McKay GM. 1979. Y chromosome mosaicism in pouch young of the marsupial, greater glider (Marsupialia: Petauridae). Chromosoma 72:329–34
     [Google Scholar]
  87. 87. 
    Guttenbach M, Koschorz B, Bernthaler U, Grimm T, Schmid M 1995. Sex chromosome loss and aging: in situ hybridization studies on human interphase nuclei. Am. J. Hum. Genet. 57:1143–50
     [Google Scholar]
  88. 88. 
    Bukvic N, Gentile M, Susca F, Fanelli M, Serio G et al. 2001. Sex chromosome loss, micronuclei, sister chromatid exchange and aging: a study including 16 centenarians. Mutat. Res. 498:159–67
     [Google Scholar]
  89. 89. 
    Johnston PG, Watson CM, Adams M, Paull DJ 2002. Sex chromosome elimination, X chromosome inactivation and reactivation in the southern brown bandicoot Isoodon obesulus (Marsupialia: Peramelidae). Cytogenet. Genome Res. 99:119–24
     [Google Scholar]
  90. 90. 
    Nazarenko SA, Timoshevskii VA. 2004. Analysis of the frequency of spontaneous aneuploidy in human somatic cells using interphase cytogenetic technology. Genetika 40:195–204
     [Google Scholar]
  91. 91. 
    McKay GM, McQuade JD, Murray JD, von Sturmer SR 1984. Sex-chromosome mosaicism in the lemur-like possum Hemibelideus lemuroides (Marsupialia: Petauridae). Aust. J. Biol. Sci. 37:131–36
     [Google Scholar]
  92. 92. 
    Bianchi NO, Contreras JR. 1967. The chromosomes of the field mouse Akodon azarae (Cricetidae, Rodentia) with special reference to sex chromosome anomalies. Cytogenetics 6:306–13
     [Google Scholar]
  93. 93. 
    Bianchi NO, Reig OA, Molina OJ, Dulout FN 1971. Cytogenetics of the South American akodont rodents (Cricetidae). I. A progress report of Argentinian and Venezuelan forms. Evolution 25:724–36
     [Google Scholar]
  94. 94. 
    Fredga K. 1983. Aberrant sex chromosome mechanisms in mammals: evolutionary aspects. Differentiation 23:Suppl.S23–30
     [Google Scholar]
  95. 95. 
    Vogel W, Jainta S, Rau W, Geerkens C, Baumstark A et al. 1998. Sex determination in Ellobius lutescens: the story of an enigma. Cytogenet. Cell Genet. 80:214–21
     [Google Scholar]
  96. 96. 
    Hoekstra HE, Edwards SV. 2000. Multiple origins of XY female mice (genus Akodon): phylogenetic and chromosomal evidence. Proc. Biol. Sci. 267:1825–31
     [Google Scholar]
  97. 97. 
    Arakawa Y, Nishida-Umehara C, Matsuda Y, Sutou S, Suzuki H 2002. X-chromosomal localization of mammalian Y-linked genes in two XO species of the Ryukyu spiny rat. Cytogenet. Genome Res. 99:303–9
     [Google Scholar]
  98. 98. 
    Just W, Baumstark A, Suss A, Graphodatsky A, Rens W et al. 2007. Ellobius lutescens: sex determination and sex chromosome. Sex Dev 1:211–21
     [Google Scholar]
  99. 99. 
    Castiglia R, Makundi R, Corti M 2007. The origin of an unusual sex chromosome constitution in Acomys sp. (Rodentia, Muridae) from Tanzania. Genetica 131:201–7
     [Google Scholar]
  100. 100. 
    Matthey R. 1958. New type of chromosomal sex determination in the mammals Ellobius lutescens Th. and Microtus (Chilotus) oregoni Bachm. (Muridae, Microtinae). Experientia 14:240–41
     [Google Scholar]
  101. 101. 
    Ohno S, Jainchill J, Stenius C 1963. The creeping vole (Microtus oregoni) as a gonosomic mosaic. I. The Oy/Xy constitution of the male. Cytogenetics 2:232–39
     [Google Scholar]
  102. 102. 
    Stanley HP, Kasinsky HE, Bols NC 1984. Meiotic chromatin diminution in a vertebrate, the holocephalan fish Hydrolagus collie (Chondrichthyes, Holocephali). Tissue Cell 16:203–15
     [Google Scholar]
  103. 103. 
    Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW et al. 2010. The genome of a songbird. Nature 464:757–62
     [Google Scholar]
  104. 104. 
    Korlach J, Gedman G, Kingan SB, Chin CS, Howard JT et al. 2017. De novo PacBio long-read and phased avian genome assemblies correct and add to reference genes generated with intermediate and short reads. GigaScience 6:gix085
     [Google Scholar]
  105. 105. 
    Chalker DL, Meyer E, Mochizuki K 2013. Epigenetics of ciliates. Cold Spring Harb. Perspect. Biol. 5:a017764
     [Google Scholar]
  106. 106. 
    Escriba MC, Goday C. 2013. Histone H3 phosphorylation and elimination of paternal X chromosomes at early cleavages in sciarid flies. J. Cell Sci. 126:3214–22
     [Google Scholar]
  107. 107. 
    Liu Y, Taverna SD, Muratore TL, Shabanowitz J, Hunt DF, Allis CD 2007. RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev 21:1530–45
     [Google Scholar]
  108. 108. 
    Duharcourt S, Yao MC. 2002. Role of histone deacetylation in developmentally programmed DNA rearrangements in Tetrahymena thermophila. Eukaryot. Cell 1:293–303
     [Google Scholar]
  109. 109. 
    Nikitina N, Bronner-Fraser M, Sauka-Spengler T 2009. Culturing lamprey embryos. Cold Spring Harb. Protoc. 2009. https://doi.org/10.1101/pdb.prot5122
    [Crossref] [Google Scholar]
  110. 110. 
    Sauka-Spengler T, Meulemans D, Jones M, Bronner-Fraser M 2007. Ancient evolutionary origin of the neural crest gene regulatory network. Dev. Cell 13:405–20
     [Google Scholar]
  111. 111. 
    Nikitina N, Sauka-Spengler T, Bronner-Fraser M 2008. Dissecting early regulatory relationships in the lamprey neural crest gene network. PNAS 105:20083–88
     [Google Scholar]
  112. 112. 
    Square T, Romasek M, Jandzik D, Cattell MV, Klymkowsky M, Medeiros DM 2015. CRISPR/Cas9-mediated mutagenesis in the sea lamprey Petromyzon marinus: a powerful tool for understanding ancestral gene functions in vertebrates. Development 142:4180–87
     [Google Scholar]
  113. 113. 
    York JR, Yuan T, Zehnder K, McCauley DW 2017. Lamprey neural crest migration is Snail-dependent and occurs without a differential shift in cadherin expression. Dev. Biol. 428:176–87
     [Google Scholar]
  114. 114. 
    Parker HJ, Sauka-Spengler T, Bronner M, Elgar G 2014. A reporter assay in lamprey embryos reveals both functional conservation and elaboration of vertebrate enhancers. PLOS ONE 9:e85492
     [Google Scholar]
  115. 115. 
    Parker HJ, De Kumar B, Green SA, Prummel KD, Hess C et al. 2019. A Hox-TALE regulatory circuit for neural crest patterning is conserved across vertebrates. Nat. Commun. 10:1189
     [Google Scholar]
  116. 116. 
    Dean B. 1899. On the Embryology of Bdellostoma stouti: A General Account of Myxinoid Development from the Egg and Segmentation to Hatching Jena, Ger: Verlag von Gustav Fischer
     [Google Scholar]
  117. 117. 
    Ota KG, Kuraku S, Kuratani S 2007. Hagfish embryology with reference to the evolution of the neural crest. Nature 446:672–75
     [Google Scholar]
  118. 118. 
    Pascual-Anaya J, Sato I, Sugahara F, Higuchi S, Paps J et al. 2018. Hagfish and lamprey Hox genes reveal conservation of temporal colinearity in vertebrates. Nat. Ecol. Evol. 2:859–66
     [Google Scholar]
  119. 119. 
    Hedges SB, Marin J, Suleski M, Paymer M, Kumar S 2015. Tree of life reveals clock-like speciation and diversification. Mol. Biol. Evol. 32:835–45
     [Google Scholar]
  120. 120. 
    Timoshevskiy VA, Lampman RT, Hess JE, Porter LL, Smith JJ 2017. Deep ancestry of programmed genome rearrangement in lampreys. Dev. Biol. 429:31–34
     [Google Scholar]
/content/journals/10.1146/annurev-animal-061220-023220
Loading
Programmed DNA Elimination in Vertebrates
Annual Review of Animal Biosciences 9, 173 (2021); https://doi.org/10.1146/annurev-animal-061220-023220
/content/journals/10.1146/annurev-animal-061220-023220
/content/journals/10.1146/annurev-animal-061220-023220
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error