Genome structure of bdelloid rotifers: Shaped by asexuality or desiccation?

Journal of Heredity

Volumn 101, Issue SUPPL. 1, 2010, Pages

  Gladyshev, Eugene A ^a,b   Arkhipova, Irina R ^a  

^a MARINE BIOLOGICAL LABORATORY   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Ancient asexuals; Anhydrobiosis; Horizontal gene transfer; Mobile DNA; Transposable elements

Indexed keywords

DNA; PRIMER DNA; TRANSPOSON;

ASEXUAL REPRODUCTION; CONFERENCE PAPER; CONTROLLED STUDY; DNA DAMAGE; GENE SEQUENCE; GENE STRUCTURE; GENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSPOSON; ANIMAL; DEHYDRATION; GENETICS; HORIZONTAL GENE TRANSFER; MOLECULAR CLONING; MOLECULAR EVOLUTION; PHYSIOLOGY; ROTIFERA;

ANIMALS; CLONING, MOLECULAR; DEHYDRATION; DNA DAMAGE; DNA PRIMERS; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENOME, HELMINTH; REPRODUCTION, ASEXUAL; ROTIFERA;

ANIMALIA; BDELLOIDA; INVERTEBRATA; ROTIFERA;

EID: 77952007577     PISSN: 00221503     EISSN: 14657333     Source Type: Journal    
DOI: 10.1093/jhered/esq008     Document Type: Conference Paper

References (59)

1. Aguilera JM, Karel M. 1997. Preservation of biological materials under desiccation. Crit Rev Food Sci Nutr. 37:287-309.
2. Argueso JL, Westmoreland J, Mieczkowski PA, Gawel M, Petes TD, Resnick MA. 2008. Double-strand breaks associated with repetitive DNA can reshape the genome. Proc Natl Acad Sci U S A. 105:11845-11850.
3. Arkhipova IR. 2006. Distribution and phylogeny of Penelope-like elements in eukaryotes. Syst Biol. 55:875-885.
4. Arkhipova I, Meselson M. 2000. Transposable elements in sexual and ancient asexual taxa. Proc Natl Acad Sci U S A. 97:14473-14477.
5. Arkhipova I, Meselson M. 2005a. Deleterious transposable elements and the extinction of asexuals. Bioessays. 27:76-85.
6. Arkhipova IR, Meselson M. 2005b. Diverse DNA transposons in rotifers of the class Bdelloidea. Proc Natl Acad Sci U S A. 102:11781-11786.
7. Bird DM, Williamson VM, Abad P, McCarter J, Danchin EG, Castagnone-Sereno P, Opperman CH. 2009. The genomes of root-knot nematodes. Annu Rev Phytopathol. 47:333-351.
8. Charlesworth B, Langley CH. 1989. The population genetics of Drosophila transposable elements. Annu Rev Genet. 23:251-287.
9. Clegg JS. 2001. Cryptobiosis: a peculiar state of biological organization. Comp Biochem Physiol B Biochem Mol Biol. 128:613-624.
10. Dolgin ES, Charlesworth B. 2008. The effects of recombination rate on the distribution and abundance of transposable elements. Genetics. 178:2169-2177.
11. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, et al. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature. 452:745-749.
12. Duret L, Marais G, Biemont C. 2000. Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans. Genetics. 156:1661-1669.
13. Gladyshev EA, Arkhipova IR. 2007. Telomere-associated endonucleasedeficient Penelope-like retroelements in diverse eukaryotes. Proc Natl Acad Sci U S A. 104:9352-9357.
14. Gladyshev EA, Arkhipova IR. 2009a. A single-copy IS5-like transposon in the genome of a bdelloid rotifer. Mol Biol Evol. 26:1921-1929.
15. Gladyshev EA, Arkhipova IR. 2009b. Rotifer rDNA-specific R9 retrotransposable elements generate an exceptionally long target site duplication upon insertion. Gene. 448:145-150.
16. Gladyshev EA, Arkhipova IR. Forthcoming. 2010. A subtelomeric non-LTR retrotransposon Hebe in the bdelloid rotifer Adineta vaga is subject to inactivation by deletions but not 5' truncations. Mob DNA (in press).
17. Gladyshev E, Meselson M. 2008. Extreme resistance of bdelloid rotifers to ionizing radiation. Proc Natl Acad Sci U S A. 105:5139-5144.
18. Gladyshev EA, Meselson M, Arkhipova IR. 2007. A deep-branching clade of retrovirus-like retrotransposons in bdelloid rotifers. Gene. 390:136-145.
19. Gladyshev EA, Meselson M, Arkhipova IR. 2008. Massive horizontal gene transfer in bdelloid rotifers. Science. 320:1210-1213.
20. Hickey DA. 1982. Selfish DNA: a sexually-transmitted nuclear parasite. Genetics. 101:519-531.
21. Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, et al. 2007. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science. 317:1753-1756.
22. Hsu WS. 1956a. Oogenesis in Habrotrocha tridens (Milne). Biol Bull. 111:364-374.
23. Hsu WS. 1956b. Oogenesis in the bdelloidea rotifer Philodina roseola (Ehrenberg). Cellule. 57:293-296.
24. Hudson CT, Gosse PH. 1886. The Rotifera or wheel-animalcules. London: Longmans, Green.
25. Hur JH, Van Doninck K, Mandigo ML, Meselson M. 2009. Degenerate tetraploidy was established before bdelloid rotifer families diverged. Mol Biol Evol. 26:375-383.
26. Jain R, Rivera MC, Lake JA. 1999. Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci U S A. 96:3801-3806.
27. Jordan IK, Matyunina LV, McDonald JF. 1999. Evidence for the recent horizontal transfer of long terminal repeat retrotransposon. Proc Natl Acad Sci U S A. 96:12621-12625.
28. Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, Patel S, Frise E, Wheeler DA, Lewis SE, Rubin GM, et al. 2002. The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol. 3: RESEARCH0084.
29. Keeling PJ, Palmer JD. 2008. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. 9:605-618.
30. Kim A, Terzian C, Santamaria P, Pélisson A, Purd'homme N, Bucheton A. 1994. Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 91:1285-1289.
31. Lapinski J, Tunnacliffe A. 2003. Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett. 553:387-390.
32. Leeuwenhoek A. 1677. Letter of October 9, 1676 to the Royal Society. Philos Trans R Soc Lond Ser B Biol Sci. 12:821-831.
33. Malik HS, Burke WD, Eickbush TH. 1999. The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol. 16:793-805.
34. Mark Welch DB. 2001. Early contributions of phylogenetics to understanding the evolution of Rotifera. Hydrobiologia. 446/447:315-322.
35. Mark Welch DB, Mark Welch JL, Meselson M. 2008. Evidence for degenerate tetraploidy in bdelloid rotifers. Proc Natl Acad Sci U S A. 105:5145-5149.
36. Mark Welch DB, Meselson M. 2000. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science. 288:1211-1215.
37. Mark Welch DB, Ricci C, Meselson M. 2009. In: Schön I, Martens K, Van Dijk P, editors. Lost sex: the evolutionary biology of parthenogenesis. Heidelberg (Germany): Springer. pp. 259-279.
38. Mark Welch JL, Mark Welch DB, Meselson M. 2004. Cytogenetic evidence for asexual evolution of bdelloid rotifers. Proc Natl Acad Sci U S A. 101:1618-1621.
39. Mark Welch JL, Meselson M. 1998. Karyotypes of bdelloid rotifers from three families. Hydrobiologia. 387/388:403-407.
40. Mattimore V, Battista JR. 1996. Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol. 178:633-637.
41. Meselson M, Mark Welch D. 2007. Evolution. Stable heterozygosity? Science. 101 (s1): 85-93.
42. Mitreva M, Smant G, Helder J. 2009. Role of horizontal gene transfer in the evolution of plant parasitism among nematodes. Methods Mol Biol. 532:517-535.
43. Muller HJ. 1964. The relation of recombination to mutational advance. Mutat Res. 106:2-9.
44. Pouchkina-Stantcheva NN, McGee BM, Boschetti C, Tolleter D, Chakrabortee S, Popova AV, Meersman F, Macherel D, Hincha DK, Tunnacliffe A. 2007. Functional divergence of former alleles in an ancient asexual invertebrate. Science. 318:268-271.
45. Ricci C. 1998. Anhydrobiotic capabilities of bdelloid rotifers. Hydrobiologia. 387/388:321-326.
46. Ricci C, Melone G, Santo N, Caprioli M. 2003. Morphological response of a bdelloid rotifer to desiccation. J Morphol. 257:246-253.
47. Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, Manhart JR. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc Natl Acad Sci U S A. 105:17867-17871.
48. Schön I, Arkhipova IR. 2006. Two families of non-LTR retrotransposons, Syrinx and Daphne, from the Darwinulid ostracod, Darwinula stevensoni. Gene. 371:296-307.
49. Schön I, Rossetti G, Martens K. 2009. Darwinulid ostracods: ancient asexual scandals or scandalous gossip? In: Schön I, Martens K, Van Dijk P, editors. Lost sex: the evolutionary biology of parthenogenesis. Heidelberg (Germany): Springer. pp. 217-240.
50. Segers H. 2007. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa. 1564:1-104.
51. Small KS, Brudno M, Hill MM, Sidow A. 2007. Extreme genomic variation in a natural population. Proc Natl Acad Sci U S A. 104:5698-5703.
52. Smith RJ, Kamiya T, Horne DJ. 2006. Living males of the 'ancient asexual' Darwinulidae (Ostracoda: Crustacea). Proc R Soc B Biol Sci. 273:1569-1578.
53. Song M, Boissinot S. 2007. Selection against LINE-1 retrotransposons results principally from their ability to mediate ectopic recombination. Gene. 390:206-213.
54. Vinson JP, Jaffe DB, O'Neill K, Karlsson EK, Stange-Thomann N, Anderson S, Mesirov JP, Satoh N, Satou Y, Nusbaum C, et al. 2005. Assembly of polymorphic genomes: algorithms and application to Ciona savignyi. Genome Res. 15:1127-1135.
55. Vlassov VV, Laktionov PP, Rykova EY. 2007. Extracellular nucleic acids. Bioessays. 29:654-667.
56. Wallace RL, Snell TW, Ricci C, Nogrady T. 2006. Rotifera: biology, ecology, and systematics. Vol. 1. Leiden (The Netherlands): Backhuys.
57. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, Kazazian HH, Boeke JD, Moran JV. 2001. Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol. 21:1429-1439.
58. Witek A, Herlyn H, Meyer A, Boell L, Bucher G, Hankeln T. 2008. EST based phylogenomics of Syndermata questions monophyly of Eurotatoria. BMC Evol Biol. 8:345.
59. Zahradka K, Slade D, Bailone A, Sommer S, Averbeck D, Petranovic M, Lindner AB, Radman M. 2006. Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature. 443:569-573.