#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Evolutionary history and classification of Micropia retroelements in Drosophilidae species


Autoři: Juliana Cordeiro aff001;  Tuane Letícia Carvalho aff002;  Vera Lúcia da Silva Valente aff003;  Lizandra Jaqueline Robe aff002
Působiště autorů: Departamento de Ecologia, Zoologia e Genética, Instituto de Biologia, Universidade Federal de Pelotas, Pelotas, RS, Brazil aff001;  Programa de Pós-Graduação em Biodiversidade Animal, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil aff002;  Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre; Rio Grande do Sul; Brazil aff003;  Departamento de Ecologia e Evolução, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0220539

Souhrn

Transposable elements (TEs) have the main role in shaping the evolution of genomes and host species, contributing to the creation of new genes and promoting rearrangements frequently associated with new regulatory networks. Support for these hypotheses frequently results from studies with model species, and Drosophila provides a great model organism to the study of TEs. Micropia belongs to the Ty3/Gypsy group of long terminal repeats (LTR) retroelements and comprises one of the least studied Drosophila transposable elements. In this study, we assessed the evolutionary history of Micropia within Drosophilidae, while trying to assist in the classification of this TE. At first, we performed searches of Micropia presence in the genome of natural populations from several species. Then, based on searches within online genomic databases, we retrieved Micropia-like sequences from the genomes of distinct Drosophilidae species. We expanded the knowledge of Micropia distribution within Drosophila species. The Micropia retroelements we detected consist of an array of divergent sequences, which we subdivided into 20 subfamilies. Even so, a patchy distribution of Micropia sequences within the Drosophilidae phylogeny could be identified, with incongruences between the species phylogeny and the Micropia phylogeny. Comparing the pairwise synonymous distance (dS) values between Micropia and three host nuclear sequences, we found several cases of unexpectedly high levels of similarity between Micropia sequences in divergent species. All these findings provide a hypothesis to the evolution of Micropia within Drosophilidae, which include several events of vertical and horizontal transposon transmission, associated with ancestral polymorphisms and recurrent Micropia sequences diversification.

Klíčová slova:

Amino acid sequence analysis – DNA sequence analysis – Drosophila melanogaster – Invertebrate genomics – Phylogenetic analysis – Sequence alignment – Sequence analysis – Sequence databases


Zdroje

1. Pardue M-L, DeBaryshe PG. Retrotransposons that maintain chromosome ends. Proceedings of the National Academy of Science. 2011; 108:20317–24.

2. Jangam D, Feschotte C, Betran E. Transposable element domestication as an adaptation to evolutionary conflicts. Trends in Genetics. 2017; 33:817–831 doi: 10.1016/j.tig.2017.07.011 28844698

3. Joly-Lopez Z, Bureau TE. Exaptation of transposable element coding sequences. Current Opinion in Genetics & Development. 2018; 49:34–42.

4. Bourque G, Burns KH, Gehring M, Gorbunova V, Seluanov A, Hammell M, et al. Ten things you should know about transposable elements. Genome Biology. 2018; 19(1), 199. doi: 10.1186/s13059-018-1577-z 30454069

5. Volff JN. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays. 2006; 28(9), 913–922. doi: 10.1002/bies.20452 16937363

6. Sinzelle L, Izsvak Z, Ivics Z. Molecular domestication of transposable elements: from detrimental parasites to useful host genes. Cellular and Molecular Life Sciences. 2009; 66(6), 1073–1093. doi: 10.1007/s00018-009-8376-3 19132291

7. Feschotte C. Transposable elements and the evolution of regulatory networks. Nature Reviews Genetics. 2008; 9(5), 397. doi: 10.1038/nrg2337 18368054

8. Lee HE, Ayarpadikannan S, Kim HS. Role of transposable elements in genomic rearrangement, evolution, gene regulation and epigenetics in primates. Genes & Genetic Systems. 2016; 15–00016.

9. Loreto ELS, Deprá M, Diesel JF, Panzera Y, Valente VLS. Drosophila relics hobo and hobo-MITEs transposons as raw material for new regulatory networks. Genetics and Molecular Biology. 2018; 41(1), 198–205.

10. Muotri AR, Marchetto MC, Coufal NG, Gage FH. The necessary junk: new functions for transposable elements. Human Molecular Genetics. 2007; 16(R2), R159–R167.

11. Tsushima A, Gan P, Kumakura N, Narusaka M, Takano Y, Narusaka Y, Shirasu K. Genomic plasticity mediated by transposable elements in the plant pathogenic fungus Colletotrichum higginsianum. Genome Biology and Evolution. 2019; 11(5): 1487–1500 doi: 10.1093/gbe/evz087 31028389

12. Kidwell MG. Transposable elements and the evolution of genome size in eukaryotes. Genetica. 2002; 115(1), 49–63. doi: 10.1023/a:1016072014259 12188048

13. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, et al. Initial sequencing and analysis of the human genome. Nature. 2001; 409, 860–921 doi: 10.1038/35057062 11237011

14. Schnable PS et al. The B73 maize genome: complexity, diversity, and dynamics. Science. 2009; 326, 1112–1115 doi: 10.1126/science.1178534 19965430

15. Bargues N, Lerat E. Evolutionary history of LTR retrotransposons among 20 Drosophila species Mobile DNA. 2017; 8:7. doi: 10.1186/s13100-017-0090-3 28465726

16. Peccoud J, Loiseau V, Cordaux R, Gilbert C. Massive horizontal transfer of transposable elements in insects. Proceedings of the National Academy of Sciences. 2017; 114(18), 4721–4726.

17. Schaack S, Gilbert C, Feschotte C. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends in Ecology & Evolution. 2010; 25(9), 537–546

18. Gilbert C, Feschotte C. Horizontal acquisition of transposable elements and viral sequences: patterns and consequences. Current Opinion in Genetics & Development. 2018; 49:15–24

19. Maumus F, Fiston-Lavier A-S, Quesneville H. Impact of transposable elements on insect genomes and biology. Current Opinion in Insect Science. 2015; 7, 1–7. doi: 10.1016/j.cois.2015.02.013

20. McDonald JF. Evolution and consequences of transposable elements. Current Opinion in Genetics and Development. 1993; 3: 855–864. doi: 10.1016/0959-437x(93)90005-a 8118210

21. Capy P, Gasperi G, Biémont C, Bazin C. Stress and transposable elements: co-evolution or useful parasites? Heredity. 2000; 85, 101–106. doi: 10.1046/j.1365-2540.2000.00751.x 11012710

22. Chuong EB, Elde NC, Feschotte C. Regulatory activities of transposable elements: from conflicts to benefits. Nature Reviews Genetics. 2017; 18, 71–86 doi: 10.1038/nrg.2016.139 27867194

23. El Baidouri M, Carpentier M-C, Cooke R, Gao D, Lasserre E, Llauro C, Mirouse M, Picault N, Jackson SA, Panaud O. Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res. 2014; 24:831–838 doi: 10.1101/gr.164400.113 24518071

24. Ivancevic AM, Walsh AM, Kortschak RD, Adelson DL. Jumping the fine LINE between species: Horizontal transfer of transposable elements in animals catalyses genome evolution. BioEssays. 2013; 35:1071–1082 doi: 10.1002/bies.201300072 24003001

25. Wallau GL, Capy P, Loreto E, Le Rouzic A, Hua-Van A. VHICA, a new method to discriminate between vertical and horizontal transposon transfer: Application to the mariner family within Drosophila. Mol Biol Evol. 2016; 33:1094–1109. doi: 10.1093/molbev/msv341 26685176

26. Loreto ELS, Carareto CM, Capy P. Revisiting horizontal transfer of transposable elements in Drosophila. Heredity. 2008; 100, 545–554 doi: 10.1038/sj.hdy.6801094 18431403

27. Silva JC et al. Factors that affect the horizontal transfer of transposable elements. Curr. Issues Mol. Biol. 2004; 6, 57–71 14632259

28. Wallau GL, Ortiz MF, Loreto ELS. Horizontal transposon transfer in eukarya: detection, bias, and perspectives. Genome Biology and Evolution. 2012; 4(8), 801–811.

29. Bartolomé C, Bello X, Maside X. Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes. Genome Biol. 2009; 10:R22 doi: 10.1186/gb-2009-10-2-r22 19226459

30. Capy P, Bazin C, Higuet D, Langin T. 1st ed. Dynamic and Evolution of Transposable Elements. RG Landes Company, Austin. 1997.

31. Kim A, Terzian C, Santamaria P, Pélisson A, Purd’homme N, Bucheton A. Retroviruses in invertebrates: the Gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc Natl Acad Sci. 1994; 91:1285–9. doi: 10.1073/pnas.91.4.1285 8108403

32. Song SU, Gerasimova T, Kurkulos M, Boeke JD, Corces VG. An env-like protein encoded by a Drosophila retroelement: evidence that Gypsy is an infectious retrovirus. Genes Dev. 1994; 8:2046–57 doi: 10.1101/gad.8.17.2046 7958877

33. Huijser P, Kirchhoff C, Lankenau D-H, Hennig W. Retrotransposon-like sequences are expressed in Y chromosomal lampbrush loops of Drosophila hydei. J Mol Biol. 1988; 203:689–697 doi: 10.1016/0022-2836(88)90202-1 2463366

34. Lankenau D-H, Huijser P, Jansen E, Miedema K, Hennig W. Micropia: a retrotransposon of Drosophila combining structural features of DNA viruses, retroviruses and non-viral transposable elements. J Mol Biol. 1988; 2:233–246

35. Lankenau D-H, Huijser P, Jansen E, Miedema K, Hennig W. DNA sequence comparison of Micropia transposable elements from Drosophila hydei and Drosophila melanogaster. Chromosoma. 1990; 99:111–117 doi: 10.1007/bf01735326 2162752

36. Almeida LM, Castro JP, Carareto CMA. Micropia transposable element occurrence in Drosophila species of the saltans group. DIS. 2001; 84:114–117

37. Almeida LM, Carareto CMA. Identification of two subfamilies of Micropia transposable element in species of the repleta group of Drosophila. Genetica. 2004; 121:155–164 doi: 10.1023/b:gene.0000040386.70086.71 15330115

38. Almeida LM, Carareto CMA. Sequence heterogeneity and phylogenetic relationships between the Copia retrotransposon in Drosophila species of the repleta and melanogaster groups. Genet Sel Evol. 2006; 38:535–550 doi: 10.1186/1297-9686-38-5-535 16954045

39. Cordeiro J, Robe LJ, Loreto EL, Valente VL. The LTR retrotransposon Micropia in the cardini group of Drosophila (Diptera: Drosophilidae): a possible case of horizontal transfer. Genetica. 2008; 134(3): 335–344. doi: 10.1007/s10709-008-9241-2 18259879

40. Setta N, Van-Sluys MA, Capy P, Carareto CM. Multiple invasions of Gypsy andMicropia retroelements in genus Zaprionus and melanogaster subgroup of the genus Drosophila. BMC Evolutionary Biology. 2009; 9(1), 279.

41. Lankenau D-H. The retrotransposon family Micropia in Drosophila species. In: McDonald J (eds) Transposable elements and evolution. 1993. Kluwer Publishers, Amsterdam pp 232–241

42. Lankenau S, Corces GV, Lankenau D-H. The Drosophila Micropia retrotransposon encodes a testis-specific antisense RNA complementary to reverse transcriptase. Mol Biol Evol. 1994. 17:1542–1557

43. Yassin A. Phylogenetic classification of the Drosophilidae Rondani (Diptera): the role of morphology in the postgenomic era. Sys. Entomol. 2013; 38: 349–364.

44. Sassi AK, Herédia FO, Loreto ELS, Valente VLS, Rohde C. Transposable elements P and gypsy in natural populations of Drosophila willistoni. Genet Mol Biol. 2005; 28:734–739

45. Staden R. The Staden sequence analysis package. Mol. Biotechnol. 1996; 5:233–241 8837029

46. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution. 2013; 30: 2725–2729. doi: 10.1093/molbev/mst197 24132122

47. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Research. 2004; 32(5), 1792–1797. doi: 10.1093/nar/gkh340 15034147

48. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nature Reviews Genetics. 2007; 8(12), 973. doi: 10.1038/nrg2165 17984973

49. Miller MA, Pfeiffer W, Schwartz T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA pp 1–8.

50. Brisson JA, Wilder J, Hollocher H. Phylogenetic analysis of the cardini group of Drosophila with respect to changes in pigmentation. Evolution. 2006; 60:1228–1241 16892973

51. Gao J, Watabe H, Aotsuka T, Pang J, Zang Y. Molecular phylogeny of the Drosophila obscura species group, with emphasis on the Old World species BMC Evolutionary Biology. 2007, 7:87 doi: 10.1186/1471-2148-7-7

52. Robe LJ, Loreto EL, Valente VL. Radiation of the Drosophila subgenus (Drosophilidae, Diptera) in the Neotropics. Journal of Zoological Systematics and Evolutionary Research. 2010; 48(4), 310–321.

53. Robe LJ, Valente VL, Loreto EL. Phylogenetic relationships and macro-evolutionary patterns within the Drosophila tripunctata “radiation” (Diptera: Drosophilidae). Genetica. 2010; 138(7), 725–735. doi: 10.1007/s10709-010-9453-0 20376692

54. Yang Y, Hou Z-C, Qian Y-H, Kang H, Zeng Q-T. Increasing the data size to accurately reconstruct the phylogenetic relationships between nine subgroups of the Drosophila melanogaster species group (Drosophilidae, Diptera). Molecular Phylogenetics and Evolution. 2012; 62: 214–223 doi: 10.1016/j.ympev.2011.09.018 21985965

55. Seetharam AS, Stuart GW. Whole genome phylogeny for 21 Drosophila species using predicted 2b-RAD fragments. PeerJ. 2013; 1:e226 doi: 10.7717/peerj.226 24432193

56. O’Grady PM, DeSalle R. Phylogeny of the genus Drosophila. Genetics. 2018; 209(1), 1–25. doi: 10.1534/genetics.117.300583 29716983

57. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986; 3:418–426 doi: 10.1093/oxfordjournals.molbev.a040410 3444411

58. R Core Team. R: A Language and Environment for Statistical Computing. 2018.

59. Sharp PM, Li WH. On the rate of DNA sequence evolution in Drosophila. Journal of Molecular Evolution. 1989; 28(5), 398–402. doi: 10.1007/bf02603075 2501501

60. Finnegan DJ. Eukaryotic transposable elements and genome evolution. Trends Genet. 1989; 5, 103–107. doi: 10.1016/0168-9525(89)90039-5 2543105

61. Piégu B, Bire S, Arensburger P, Bigot Y. A survey of transposable element classification systems–a call for a fundamental update to meet the challenge of their diversity and complexity. Molecular Phylogenetics and Evolution. 2015; 86, 90–109. doi: 10.1016/j.ympev.2015.03.009 25797922

62. Lohe AR, Moriyama EN, Lidholm DA, Hartl DL. Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Molecular Biology and Evolution. 1995; 12(1), 62–72. doi: 10.1093/oxfordjournals.molbev.a040191 7877497

63. Clark JB, Kidwell MG. A phylogenetic perspective on P transposable element evolution in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 1997; 94(21): 11428–11433. doi: 10.1073/pnas.94.21.11428 9326626

64. Herédia FO, Loreto ELS, Valente VLS. Complex evolution of gypsy in drosophilid species. Mol Biol Evol. 2004; 21:1–12 doi: 10.1093/molbev/msg223

65. Bao W, Kojima KK, Kohany O. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mobile DNA. 2015; 6: 11 doi: 10.1186/s13100-015-0041-9 26045719

66. Arkhipova IR. Using bioinformatic and phylogenetic approaches to classify transposable elements and understand their complex evolutionary histories. Mobile DNA. 2017; 8(1), 19.

67. Bächli G. Taxodros database: The database on taxonomy of Drosophilidae. URL: http://www.taxodros.unizh.ch/. Last accessed in April 2019

68. Heed WB, Russel JS. Phylogeny and population structure in island and continental species of the cardini group of Drosophila studied by inversion analysis. Univ Texas Publs. 1971; 7103:91–130

69. Souza CRG. Quaternário do Brasil. 1st ed. Holos Editora. 2005.

70. Franco FF, Manfrin MH. Recent demographic history of cactophilic Drosophila species can be related to Quaternary palaeoclimatic changes in South America. Journal of Biogeography. 2013; 40(1), 142–154.

71. Cenzi de Ré F, Gustani EC, Oliveira APF, Machado LP, Mateus RP, Loreto ELS, & Robe LJ. Brazilian populations of Drosophila maculifrons (Diptera: Drosophilidae): low diversity levels and signals of a population expansion after the Last Glacial Maximum. Biological Journal of the Linnean Society. 2014. 112(1), 55–66.


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#