Skip to main content

Advertisement

Log in

Changes of Osvaldo expression patterns in germline of male hybrids between the species Drosophila buzzatii and Drosophila koepferae

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Hybridization between different genomes is a source of genomic instability, sometimes associated with transposable element (TE) mobilization. Previous work showed that hybridization between the species Drosophila buzzatii and Drosophila koepferae induced mobilization of different (TEs), the Osvaldo retrotransposon being the most unstable. However, we ignore the mechanisms involved in this transposition release in interspecific hybrids. In order to disentangle the mechanisms involved in this process, we performed Osvaldo expression studies in somatic and germinal tissues from hybrids and parental species. There was a trend towards increased Osvaldo expression in the somatic tissues of hybrid females and males, which was always significant in males compared to the parental species D. buzzatii but, not in females compared to maternal species D. koepferae. There were massive changes of Osvaldo expression in the testes, which varied depending on the hybrid generation and family. Moreover, Osvaldo hybridization signals, restricted to the apical and primary spermatocyte regions in parents, occupied broader region in the hybrids. In ovaries, there were no significant differences in Osvaldo expression rates between hybrids and the maternal species D. koepferae. The transcript location was restricted to ovarian nurse cells in both parents and hybrids, undetectable in some hybrids. This research highlights first, the existence of putative complex deregulation mechanisms different between sexes and cell types and second, disruption of Osvaldo activity particularly evident in testes from sterile hybrid males. Deeper studies of the total transcriptome in hybrids and parental species are necessary to gain a better knowledge of the TE deregulation pathways in hybrids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Akkouche A, Grentzinger T, Fablet M, Armenise C, Burlet N, Braman V, Chambeyron S, Vieira C (2013) Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells. EMBO Rep 14:458–464

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arnault C, Dufournel I (1994) Genome and stresses: Reactions against aggressions, behavior of transposable elements. Genetica 93:149–160

    Article  CAS  PubMed  Google Scholar 

  • Arnold M (2006) Natural hybridization and Evolution. Oxford University Press

  • Barreau C, Benson E, Gudmannsdottir E, Newton F, White-Cooper H (2008) Post-meiotic transcription in Drosophila testes. Development 135:1897–1902

    Article  CAS  PubMed  Google Scholar 

  • Borie N, Maisonhaute C, Sarrazin S, Loevenbruck C, Biémont C (2002) Tissue-specificity of 412 retrotransposon expression in Drosophila simulans and D. melanogaster. Heredity 89:247–252

    Article  CAS  PubMed  Google Scholar 

  • Brennecke J, Aravin A, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ (2007a) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103

    Article  CAS  PubMed  Google Scholar 

  • Brennecke J, Aravin A, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ (2007b) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128

  • Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, Hannon GJ (2008) An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322:1387–1392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Capy P, Gasperi G, Biemont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites? Heredity (Edinb) 85:101–106

    Article  CAS  Google Scholar 

  • Carroll SB (2000) Endless Forms. Cell 101:577–580

    Article  CAS  PubMed  Google Scholar 

  • Cash AC, Andrews J (2012) Fine scale analysis of gene expression in Drosophila melanogaster gonads reveals programmed cell death 4 promotes the differentiation of female germline stem cells. BMC Dev Biol 12:4. doi:10.1186/1471-213X-12-4

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chambeyron S, Popkova A, Payen-Groschêne G, Brun C, Laouini D, Pelisson A, Bucheton A (2008) piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline. Proc Natl Acad Sci 105:14964–14969

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • de Almeida LM, Carareto CMA (2002) Gonadal hybrid dysgenesis in Drosophila sturtevanti (Diptera, Drosophilidae). Iheringia Série Zool 92:71–79

    Google Scholar 

  • Dion-Côté AM, Renaut S, Normandeau E, Bernatchez L (2014) RNA-seq reveals transcriptomic shock involving transposable elements reactivation in hybrids of young lake whitefish species. Mol Biol Evol 31:1188–1199

    Article  PubMed  Google Scholar 

  • Eickbush MT, Eickbush TH (2011) Retrotransposition of R2 elements in somatic nuclei during the early development of Drosophila. Mob DNA 2:11. doi:10.1186/1759-8753-2-11

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Filatov DA, Morozova TV, Pasyukova EG (1998) Age dependence of the copia transposition rate is positively associated with copia transcript abundance in a Drosophila melanogaster isogenic line. Mol Gen Genet 258:646–654

    Article  CAS  PubMed  Google Scholar 

  • Evgen’ev MB, Zelentsova H, Shostak N, Kozitsina M, Barskyi V, Lankenau DH, Corces VG (1997) Penelope, a new family of transposable elements and its possible role in hybrid dysgenesis in Drosophila virilis. Proc Natl Acad Sci 94:196–201

    Article  PubMed Central  PubMed  Google Scholar 

  • Fontdevila a (2005) Hybrid genome evolution by transposition. Cytogenet Genome Res 110:49–55

    Article  CAS  PubMed  Google Scholar 

  • García Guerreiro MP (2012) What makes transposable elements move in the Drosophila genome? Heredity 108:461–468

    Article  PubMed  Google Scholar 

  • García Guerreiro MP (2014) Interspecific hybridization as a genomic stressor inducing mobilization of transposable elements in Drosophila. Mob Genet Elements 4:e34394

    Article  Google Scholar 

  • García Guerreiro MP, Biémont C (1995) Changes of the copia element pattern during the process of making chromosomes homozygous in Drosophila melanogaster. Mol Gen Genet 246:206–211

    Article  PubMed  Google Scholar 

  • García Guerreiro MP, Fontdevila A (2001) Chromosomal distribution of the transposable elements Osvaldo and blanco in original and colonizer populations of Drosophila buzzatii. Genet Res 77:227–238

    Article  Google Scholar 

  • García Guerreiro MP, Fontdevila A (2007) Molecular characterization and genomic distribution of Isis: a new retrotransposon of Drosophila buzzatii. Mol Genet Genomics 277:83–95

    Article  PubMed  Google Scholar 

  • Girard A, Hannon GJ (2008) Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 18:136–148

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • González J, Petrov DA (2012) Evolution of genome content: population dynamics of transposable elements in flies and humans. Methods Mol Biol 855:361–383

    Article  PubMed  Google Scholar 

  • Granzotto A, Lopes FR, Vieira C, Carareto CMA (2011) Vertical inheritance and bursts of transposition have shaped the evolution of the BS non-LTR retrotransposon in Drosophila. Mol Genet Genomics 286:57–66

    Article  CAS  PubMed  Google Scholar 

  • Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC (2007) A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315:1587–1590

    Article  CAS  PubMed  Google Scholar 

  • Hamilton RS, Hartswood E, Vendra G, Jones C, Van De Bor V, Finnegan D, Davis I (2009) A bioinformatics search pipeline, RNA2DSearch, identifies RNA localization elements in Drosophila retrotransposons. RNA 15:200–207

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Josefsson C, Dilkes B, Comai L (2006) Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol 16:1322–1328

    Article  CAS  PubMed  Google Scholar 

  • Kalmykova AI, Klenov MS, Gvozdev VA (2005) Argonaute protein PIWI controls mobilization of retrotransposons in the Drosophila male germline. Nucleic Acids Res 33:2052–2059

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kano H, Godoy I, Courtney C, Vetter MR, Gerton GL, Ostertag EM, Kazazian HH (2009) L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev 23:1303–1312

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kelleher ES, Edelman NB, Barbash DA (2012) Drosophila interspecific hybrids phenocopy piRNA-pathway mutants. PLoS Biol. doi:10.1371/journal.pbio.1001428

    PubMed Central  PubMed  Google Scholar 

  • Kenan-Eichler M, Leshkowitz D, Tal L, Noor E, Melamed-Bessudo C, Feldman M, Levy AA (2011) Wheat hybridization and polyploidization results in deregulation of small RNAs. Genetics 188:263–272

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kidwell MG, Kidwell JF, Sved JA (1977) Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86:813–833

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kidwell MG, Lisch D (1997) Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci U S A 94:7704–7711

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kidwell MG, Lish D (2002) Transposable elements as sources of genomic variation. Washington DC

  • Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47:583–621

    Article  Google Scholar 

  • Laayouni H, Hasson E, Santos M, Fontdevila A (2003) The evolutionary history of Drosophila buzzatii. XXXV. Inversion polymorphism and nucleotide variability in different regions of the second chromosome. Mol Biol Evol 20:931–944

    Article  CAS  PubMed  Google Scholar 

  • Labrador M, Fontdevila A (1994) High transposition rates of Osvaldo, a new Drosophila buzzatii retrotransposon. Mol Gen Genet 245:661–674

    Article  CAS  PubMed  Google Scholar 

  • Labrador M, Seleme MC, Fontdevila A (1998) The evolutionary history of Drosophila buzzatii. XXXIV. The distribution of the retrotransposon Osvaldo in original and colonizing populations. Mol Biol Evol 15:1532–1547

    Article  CAS  PubMed  Google Scholar 

  • Labrador M, Riano Farré M, Utzet F, Fontdevila A (1999a) Interspecific hybridization increases transposition rates of Osvaldo. Mol Biol Evol 16:931–937

    Article  CAS  PubMed  Google Scholar 

  • Labrador M, Riano Farré M, Utzet F, Fontdevila A (1999b) Interspecific hybridization increases transposition rates of Osvaldo. Mol Biol Evol 16:931–937

    Article  CAS  PubMed  Google Scholar 

  • Lachaise D, Cariou M-L, David JR, Lemeunier F, Tsacas L, Ashburner M (1988) Historical biogeography of the Drosophila melanogaster species subgroup. Evol Biol 22:159–225

    Google Scholar 

  • Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, Hur JK, Aravin A, Tóth KF (2013) Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 27:390–399

    Article  PubMed Central  PubMed  Google Scholar 

  • Maside X, Assimacopoulos S, Charlesworth B (2000) Rates of movement of transposable elements on the second chromosome of Drosophila melanogaster. Genet Res 75:275–284

    Article  CAS  PubMed  Google Scholar 

  • Maside X, Bartolomé C, Assimacopoulos S, Charlesworth B (2001) Rates of movement and distribution of transposable elements in Drosophila melanogaster: in situ hybridization vs Southern blotting data. Genet Res 78:121–136. doi:10.1017/S0016672301005201

    Article  CAS  PubMed  Google Scholar 

  • Metcalfe CJ, Bulazel KV, Ferreri GC, Schroeder-Reiter E, Wanner G, Rens W, Obergfell C, Eldridge MDB, O’Neill RJ (2007) Genomic instability within centromeres of interspecific marsupial hybrids. Genet 177:2507–2517

    Article  CAS  Google Scholar 

  • Michalak P (2010) An eruption of mobile elements in genomes of hybrid sunflowers. Heredity (Edinb) 104:329–330

    Article  CAS  Google Scholar 

  • Mirkovic-Hösle M, Förstemann K (2014) Transposon defense by endo-siRNAs, piRNAs and somatic pilRNAs in Drosophila: contributions of Loqs-PD and R2D2. PLoS ONE 9:e84994. doi:10.1371/journal.pone.0084994

    Article  PubMed Central  PubMed  Google Scholar 

  • Moehring AJ, Teeter KC, Noor MAF (2007) Genome-wide patterns of expression in Drosophila pure species and hybrid males. II. Examination of multiple-species hybridizations, platforms, and life cycle stages. Mol Biol Evol. 24:137–145

    Article  CAS  PubMed  Google Scholar 

  • Morán T, Fontdevila A (2014) Genome-wide dissection of hybrid sterility in Drosophila confirms a polygenic threshold architecture. J Hered 105:381–396

    Article  PubMed  Google Scholar 

  • Muotri AR, Marchetto MCN, Coufal NG, Gage FH (2007) The necessary junk: new functions for transposable elements. Hum Mol Genet. doi:10.1093/hmg/ddm196 (16 Spec No:R159–67)

  • Nagao A, Mituyama T, Huang H, Chen D, Siomi MC, Siomi H (2010) Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis. RNA 16:2503–2515

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Naveira H, Fontdevila A (1991) The evolutionary history of D. buzzatii. XXII. Chromosomal and genic sterility in male hybrids of Drosophila buzzatii and Drosophila koepferae. Heredity 66:233–239

    Article  PubMed  Google Scholar 

  • Nishida KM, Saito K, Mori T, Kawamura Y, Nagami-Okada T, Inagaki S, Siomi H, Siomi MC (2007) Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad. RNA 13:1911–1922

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Noor MAF, Chang AS (2015) Evolutionary genetics: jumping into a new species. Curr Biol 16:R890–R892. doi:10.1016/j.cub.2006.09.022

    Article  Google Scholar 

  • Noor MAF, Grams KL, Bertucci LA, Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci 98:12084–12088

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nuzhdin SV, Mackay TF (1995) The genomic rate of transposable element movement in Drosophila melanogaster. Mol Biol Evol 12:180–181

    Article  CAS  PubMed  Google Scholar 

  • O’Neill RJW, O’Neill MJ, Graves JAM (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393:68–72

    Article  PubMed  Google Scholar 

  • Oliveira DCSG, Almeida FC, O’Grady PM, Armella MA, DeSalle R, Etges WJ (2012) Monophyly, divergence times, and evolution of host plant use inferred from a revised phylogeny of the Drosophila repleta species group. Mol Phylogenet Evol 64:533–544

    Article  PubMed  Google Scholar 

  • Pantazidis A, Laayouni H, Fontdevila A (1999) The retrotransposon Osvaldo from Drosophila buzzatiid is plays all structural features of a funcrional retrovirus. Mol Biol Evol 16:909–921

    Article  CAS  PubMed  Google Scholar 

  • Petrov DA, Schutzman JL, Hartl DL, Lozovskaya ER (1995) Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. Proc Natl Acad Sci U S A 92:8050–8054

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Picard G, Bregliano JC, Bucheton A, Lavige JM, Pelisson A, Kidwell MG (1978) Non-mendelian female sterility and hybrid dysgenesis in Drosophila melanogaster. Genet Res 32:275–287

    Article  CAS  PubMed  Google Scholar 

  • Rayburn AL, Biradar DP, Bullock DG, McMurphy LM (1993) Nuclear DNA content in F1 hybrids of maize. Heredity 70:294–300

    Article  CAS  Google Scholar 

  • Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H, Siomi MC (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20:2214–2222

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schulz C, Wood CG, Jones DL, Tazuke SI, Fuller MT (2002) Signaling from germ cells mediated by the rhomboid homolog stet organizes encapsulation by somatic support cells. Development 129:4523–4534

    CAS  PubMed  Google Scholar 

  • Shpiz S, Kwon D, Rozovsky Y, Kalmykova A (2009) rasiRNA pathway controls antisense expression of Drosophila telomeric retrotransposons in the nucleus. Nucleic Acids Res 37:268–278

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Siomi MC, Saito K, Siomi H (2008) How selfish retrotransposons are silenced in Drosophila germline and somatic cells. FEBS Lett 582:2473–2478

    Article  CAS  PubMed  Google Scholar 

  • Sokolova OA, Yakushev EY, Stolyarenko AD, Mikhaleva EA, Gvozdev VA, Klenov MS (2011) Interplay of transposon-silencing genes in the germline of Drosophila melanogaster. Mol Biol 45:582–590

    Article  CAS  Google Scholar 

  • Tenaillon MI, Hollister JD, Gaut BS (2010) A triptych of the evolution of plant transposable elements. Trends Plant Sci 15:471–478

    Article  CAS  PubMed  Google Scholar 

  • Turner LM, White MA, Tautz D, Payseur B a (2014) Genomic networks of hybrid sterility. PLoS Genet 10:e1004162. doi:10.1371/journal.pgen.1004162

    Article  PubMed Central  PubMed  Google Scholar 

  • Ungerer MC, Strakosh SC, Zhen Y (2006) Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. 16(20):R872–3. doi:10.1016/j.cub.2006.09.020

  • Vela D, Fontdevila A, Vieira C, García Guerreiro MP (2014) A genome-wide survey of genetic instability by transposition in Drosophila hybrids. PLoS One 9:e88992

    Article  PubMed Central  PubMed  Google Scholar 

  • Vela D, Garcia Guerreiro MP, Fontdevila A (2011) Adaptation of the AFLP technique as a new tool to detect genetic instability and transposition in interspecific hybrids. Biotechniques 50:247–250

    CAS  PubMed  Google Scholar 

  • Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8:206–216

    Article  CAS  PubMed  Google Scholar 

  • Xie W, Donohue RC, Birchler JA (2013) Quantitatively increased somatic transposition of transposable elements in Drosophila strains compromised for RNAi. PLoS One 8:e72163. doi:10.1371/journal.pone.0072163

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yuan JS, Reed A, Chen F, Stewart CN (2006) Statistical analysis of real-time PCR data. BMC Bioinform 7:85. doi:10.1186/1471-2105-7-85

    Article  Google Scholar 

Download references

Acknowledgments

I want to thank M. Peiró for her technical assistance; A. Akouche, R. Rebollo and C. Vieira for their valuable help with q-RTPCR and FISH techniques and A. Fontdevila for his comments and revision on the previous version of the manuscript. This work was supported by Spanish research grants CGL2013-42432-P from the Ministerio de Economía y Competitividad (Spain) and 2014 SGR 1346 from Generalitat de Catalunya to the Grup de Genòmica, Bioinformàtica i Biologia Evolutiva (GGBE).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Pilar García Guerreiro.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García Guerreiro, M.P. Changes of Osvaldo expression patterns in germline of male hybrids between the species Drosophila buzzatii and Drosophila koepferae . Mol Genet Genomics 290, 1471–1483 (2015). https://doi.org/10.1007/s00438-015-1012-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-015-1012-z

Keywords