Billions of basepairs of recently expanded, repetitive sequences are eliminated from the somatic genome during copepod development

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Sun, Cheng ^a   Wyngaard, Grace ^b   Walton, D B ^b   Wichman, Holly A ^c   Mueller, Rachel L ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b JAMES MADISON UNIVERSITY   (United States)

^c UNIVERSITY OF IDAHO   (United States)

Author keywords

Chromatin diminution; Copepod; Genome size; Germline soma differentiation; Transposable elements

Indexed keywords

DNA;

ADULT; ANIMAL CELL; ARTICLE; BASE PAIRING; CHROMATIN; DEVELOPMENT; EMBRYO; FEMALE; GENE SEQUENCE; HIGH THROUGHPUT SEQUENCING; MESOCYCLOPS; MESOCYCLOPS EDAX; NONHUMAN; NUCLEOTIDE REPEAT; POLYMERASE CHAIN REACTION; TRANSPOSON;

ANIMALS; CHROMATIN; COPEPODA; EVOLUTION, MOLECULAR; FEMALE; GENE DOSAGE; GENETIC VARIATION; GENOME; GENOMICS; GERM CELLS; REPETITIVE SEQUENCES, NUCLEIC ACID;

EID: 84897552380     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-186     Document Type: Article

References (44)

1. Coyne RS, Chalker DL, Yao MC. Genome downsizing during ciliate development: nuclear division of labor through chromosome restructuring. Annu Rev Genet 1996, 30(1):557-578. 10.1146/annurev.genet.30.1.557, 8982465.
2. Tobler H. The differentiation of germ and somatic cell lines in nematodes. Res Prob Cell Diff 1986, 13:1-69.
3. Beermann S. The diminution of heterochromatic chromosomal segments in Cyclops (Crustacea, Copepoda). Chromosoma 1977, 60(4):297. 10.1007/BF00292858, 870296.
4. Smith JJ, Antonacci F, Eichler EE, Amemiya CT. Programmed loss of millions of base pairs from a vertebrate genome. Proc Natl Acad Sci 2009, 106(27):11212-11217. 10.1073/pnas.0902358106, 2708698, 19561299.
5. Smith JJ, Baker C, Eichler EE, Amemiya CT. Genetic consequences of programmed genome rearrangement. Curr Biol 2012, 22(16):1524-1529. 10.1016/j.cub.2012.06.028, 3427415, 22818913.
6. Kubota S, Ishibashi T, Kohno S. A germline restricted, highly repetitive DNA sequence in Paramyxineatami: an interspecifically conserved, but somatically eliminated, element. Mol Gen Genet 1997, 256(3):252-256. 10.1007/s004380050567, 9393449.
7. Arnaiz O, Mathy N, Baudry C, Malinsky S, Aury J-M, Denby Wilkes C, Garnier O, Labadie K, Lauderdale BE, Le Mouël A, Marmignon A, Nowacki M, Poulain J, Prajer M, Wincker P, Meyer E, Duharcourt S, Duret L, Betermier M, Sperling L. The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences. PLoS Genet 2012, 8(10):e1002984. 10.1371/journal.pgen.1002984, 3464196, 23071448.
8. Rasch EM, Wyngaard GA. Genome sizes of cyclopoid copepods (Crustacea): evidence of evolutionary constraint. Biol J Linn Soc 2006, 87(4):625-635.
9. Wyngaard GA, Rasch EM, Connelly BA. Unusual augmentation of germline genome size in Cyclops kolensis (Crustacea, Copepoda): further evidence in support of a revised model of chromatin diminution. Chrom Res 2011, 19(7):911-923. 10.1007/s10577-011-9234-3, 21953028.
10. Wang J, Mitreva M, Berriman M, Thorne A, Magrini V, Koutsovoulos G, Kumar S, Blaxter Mark L, Davis Richard E. Silencing of germline-expressed genes by DNA elimination in somatic cells. Dev Cell 2012, 23(5):1072-1080. 10.1016/j.devcel.2012.09.020, 3620533, 23123092.
11. Etter A, Bernard V, Kenzelmann M, Tobler H, Muller F. Ribosomal heterogeneity from chromatin diminution in Ascaris lumbricoides. Science 1994, 265(5174):954. 10.1126/science.8052853, 8052853.
12. Hunter DJ, Williams K, Cartinhour S, Herrick G. Precise excision of telomere-bearing transposons during Oxytricha fallax macronuclear development. Genes Dev 1989, 3(12b):2101-2112. 10.1101/gad.3.12b.2101, 2560753.
13. Chalker DL, Yao MC. DNA elimination in ciliates: transposon domestication and genome surveillance. Annu Rev Genet 2011, 45:227-246. 10.1146/annurev-genet-110410-132432, 21910632.
14. Standiford DM. The development of a large nucleolus during oogenesis in Acanthocyclops vernalis (Crustacea, copepoda) and its possible relationship to chromatin diminution. Biol Cell 1988, 63(1):35-40. 10.1111/j.1768-322X.1988.tb00739.x, 2461240.
15. Zagoskin MV, Marshak TL, Mukha DV, Grishanin AK. Chromatin diminution process regulates rRNA gene copy number in freshwater copepods. Act Nat 2010, 2(4):52.
16. Drouin G. Chromatin diminution in the copepod Mesocyclops edax: diminution of tandemly repeated DNA families from somatic cells. Genome 2006, 49:657-665. 10.1139/G06-022, 16936845.
17. McKinnon C, Drouin G. Chromatin diminution in the copepod Mesocyclops edax: elimination of both highly repetitive and non-highly repetitive DNA. Genome 2013, doi:10.1139/gen-2012-0097.
18. Gregory TR, Hebert PD. The modulation of DNA content: proximate causes and ultimate consequences. Genome Res 1999, 9(4):317-324.
19. Gregory TR, Hebert PDN, Kolasa J. Evolutionary implications of the relationship between genome size and body size in flatworms and copepods. Heredity 2000, 84(2):201-208. 10.1046/j.1365-2540.2000.00661.x, 10762390.
20. Wyngaard GA, Gregory TR. Temporal control of DNA replication and the adaptive value of chromatin diminution in copepods. J Exp Zool 2001, 291(4):310-316. 10.1002/jez.1131, 11754011.
21. Wyngaard GA, Rasch EM, Manning NM, Gasser K, Domangue R. The relationship between genome size, development rate, and body size in copepods. Hydrobiologia 2005, 532(1):123-137.
22. Rasch EM, Wyngaard GA, Connelly BA. Heterochromatin endoreduplication prior to gametogenesis and chromatin diminution during early embryogenesis in Mesocyclops edax (Copepoda: Crustacea). J Morphol 2008, 269(4):387-397. 10.1002/jmor.10576, 17932949.
23. Sun C, Shepard DB, Chong RA, Arriaza JL, Hall K, Castoe TA, Feschotte C, Pollock DD, Mueller RL. LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders. Genome Biol Evol 2012, 4(2):168-183. 10.1093/gbe/evr139, 3318908, 22200636.
24. International Human Genome Sequencing Consortium Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921. 10.1038/35057062, 11237011, International Human Genome Sequencing Consortium.
25. Novick PA, Basta H, Floumanhaft M, McClure MA, Boissinot S. The evolutionary dynamics of autonomous non-LTR retrotransposons in the lizard Anolis carolinensis shows more similarity to fish than mammals. Mol Biol Evol 2009, 26(8):1811. 10.1093/molbev/msp090, 19420048.
26. Terpilowska B. Quantitative investigations of DNA in early embryogenesis of Acanthocyclops gigas (Claus). Zool Polon 1971, 21(2):163-175.
27. Blumenstiel JP. Evolutionary dynamics of transposable elements in a small RNA world. Trends Genet 2011, 27(1):23-31. 10.1016/j.tig.2010.10.003, 21074888.
28. Lynch M. The Origins of Genome Architecture 2007, Sunderland, MA: Sinauer Associates, Inc.
29. Lynch M, Bobay L-M, Catania F, Gout J-F, Rho M. The repatterning of eukaryotic genomes by random genetic drift. Annu Rev Genom Hum Genet 2011, 12(1):347-366.
30. Agren JA, Wright SI. Co-evolution between transposable elements and their hosts: a major factor in genome size evolution?. Chrom Res 2011, 19(6):777-786. 10.1007/s10577-011-9229-0, 21850458.
31. Petrov DA, Aminetzach YT, Davis J, Bensasson D, Hirsch AE. Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol Biol Evol 2003, 20(6):880-892. 10.1093/molbev/msg102, 12716993.
32. Nuzhdin SV. Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 1999, 107:129-137. 10.1023/A:1003957323876, 10952206.
33. De Gobbi M, Viprakasit V, Hughes JR, Fisher C, Buckle VJ, Ayyub H, Gibbons RJ, Vernimmen D, Yoshinaga Y, de Jong P, Cheng JF, Rubin EM, Wood WG, Bowden D, Higgs DR. A regulatory SNP causes a human genetic disease by creating a new transcriptional promoter. Science 2006, 26(312):1215-1217.
34. Cavalier-Smith T. Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Ann Bot 2005, 95:147-175. 10.1093/aob/mci010, 15596464.
35. Orgel LE. Selfish DNA: the ultimate parasite. Nature 1980, 284(5757):604. 10.1038/284604a0, 7366731.
36. Kataoka K, Mochizuki K. Programmed DNA elimination in Tetrahymena: a small RNA-mediated genome surveillance mechanism. RNA Infrastructure and Networks 2011, 156-173. New York: Springer, Collins L, vol. 722.
37. Baudry C, Malinsky S, Restituito M, Kapusta A, Rosa S, Meyer E, Bétermier M. PiggyMac, a domesticated piggyBac transposase involved in programmed genome rearrangements in the ciliate Paramecium tetraurelia. Genes Dev 2009, 23(21):2478-2483. 10.1101/gad.547309, 2779751, 19884254.
38. Hosono S, Faruqi AF, Dean FB, Du Y, Sun Z, Wu X, Du J, Kingsmore SF, Egholm M, Lasken RS. Unbiased whole-genome amplification directly from clinical samples. Genome Res 2003, 13(5):954-964. 10.1101/gr.816903, 430878, 12695328.
39. Gomez-Alvarez V, Teal TK, Schmidt TM. Systematic artifacts in metagenomes from complex microbial communities. ISME J 2009, 3:1314-1317. 10.1038/ismej.2009.72, 19587772.
40. Niu B, Fu L, Sun S, Li W. Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinforma 2010, 11:187.
41. Price AL, Jones NC, Pevzner PA. De novo identification of repeat families in large genomes. Bioinformatics 2005, 21(suppl 1):i351-i358. 10.1093/bioinformatics/bti1018, 15961478.
42. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999, 27(2):573-580. 10.1093/nar/27.2.573, 148217, 9862982.
43. Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, Tokishita S, Aerts A, Arnold GJ, Basu MK, Bauer DJ, Caceres CE, Carmel L, Casola C, Choi J, Detter JC, Dong Q, Dusheyko S, Eads BD, Frohlich T, Geiler-Samerotte KA, Gerlach D, Hatcher P, Jogdeo S, Krijgsveld J, Kriventseva EV, Kultz D, Laforsch C, Lindquist E, Lopez J, et al. The ecoresponsive genome of Daphnia pulex. Science 2011, 331(6017):555-561. 10.1126/science.1197761, 3529199, 21292972.
44. Casella G, Berger R. Statistical Inference 2002, Duxbury: Pacific Grove, CA.