Skip to main content

Advertisement

SpringerLink
Log in

Impact of repetitive DNA on sex chromosome evolution in plants

  • Review
  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Structurally and functionally diverged sex chromosomes have evolved in many animals as well as in some plants. Sex chromosomes represent a specific genomic region(s) with locally suppressed recombination. As a consequence, repetitive sequences involving transposable elements, tandem repeats (satellites and microsatellites), and organellar DNA accumulate on the Y (W) chromosomes. In this paper, we review the main types of repetitive elements, their gathering on the Y chromosome, and discuss new findings showing that not only accumulation of various repeats in non-recombining regions but also opposite processes form Y chromosome. The aim of this review is also to discuss the mechanisms of repetitive DNA spread involving (retro) transposition, DNA polymerase slippage or unequal crossing-over, as well as modes of repeat removal by ectopic recombination. The intensity of these processes differs in non-recombining region(s) of sex chromosomes when compared to the recombining parts of genome. We also speculate about the relationship between heterochromatinization and the formation of heteromorphic sex chromosomes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

TE:

Transposable element

LTR:

Long terminal repeat

RAYS :

Rumex acetosa Y chromosome-specific sequence

STAR-Y:

Silene tandem repeat accumulated on the Y chromosome

TRAYC:

Tandem Repeat Accumulated on the Y Chromosome

NUPT:

Nuclear insertions of plastid DNA

NUMT:

Nuclear insertions of mitochondrial DNA

HSY:

Hermaphrodite-specific region of the Yh chromosome

MSY:

Male-specific region of the Y chromosome

LINE:

Long interspersed nuclear element

References

  • Bachtrog D (2011) Plant sex chromosomes: a non-degenerated Y? Curr Biol 21:R685–R688

    Article  CAS  PubMed  Google Scholar 

  • Bachtrog D, Mank JE, Peichel CL et al (2014) Sex determination: why so many ways of doing it? PLoS Biol 12, e1001899

    Article  PubMed Central  PubMed  Google Scholar 

  • Bergero R, Qiu S, Charlesworth D (2015) Gene loss from a plant sex chromosome system. Curr Biol 25:1234–1240

    Article  CAS  PubMed  Google Scholar 

  • Blavet N, Blavet H, Muyle A et al (2015) Identifying new sex-linked genes through BAC sequencing in the dioecious plant Silene latifolia. BMC Genomics 16:546

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bridier-Nahmias A, Tchalikian-Cosson A, Baller JA et al (2015) An RNA polymerase III subunit determines sites of retrotransposon integration. Science 348:585–588

    Article  CAS  PubMed  Google Scholar 

  • Bushman FD (1994) Tethering human immunodeficiency virus 1 integrase to a DNA site directs integration to nearby sequences. Proc Natl Acad Sci U S A 91:9233–9237

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bushman F, Miller MD (1997) Tethering human immunodeficiency virus type 1 preintegration complexes to target DNA promotes integration at nearby sites. J Virol 71:458–464

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bushman F, Lewinski M, Ciuffi A et al (2005) Genome-wide analysis of retroviral DNA integration. Nat Rev Microbiol 3:848–858

    Article  CAS  PubMed  Google Scholar 

  • Calarco JP, Borges F, Donoghue MTA et al (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:194–205

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cegan R, Vyskot B, Kejnovsky E et al (2012) Genomic diversity in two related plant species with and without sex chromosomes—Silene latifolia and S. vulgaris. PLoS One 7, e31898

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cermak T, Kubat Z, Hobza R et al (2008) Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes. Chromosom Res 16:961–976

    Article  CAS  Google Scholar 

  • Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128

    Article  CAS  PubMed  Google Scholar 

  • Cherepanov P, Maertens GN, Hare S (2011) Structural insights into the retroviral DNA integration apparatus. Curr Opin Struct Biol 21:249–256

    Article  CAS  PubMed  Google Scholar 

  • Cherif E, Zehdi S, Castillo K et al (2013) Male-specific DNA markers provide genetic evidence of an XY chromosome system, a recombination arrest and allow the tracing of paternal lineages in date palm. New Phytol 197:409–415

    Article  CAS  PubMed  Google Scholar 

  • Cioffi MB, Kejnovsky E, Marquioni V et al (2012) The key role of repeated DNAs in sex chromosome evolution in two fish species with ZW sex chromosome system. Mol Cytogenet 5:28

    Article  CAS  Google Scholar 

  • Cohen S, Agmon N, Sobol O, Segal D (2010) Extrachromosomal circles of satellite repeats and 5S ribosomal DNA in human cells. Mob DNA 1:11

    Article  PubMed Central  PubMed  Google Scholar 

  • Creasey KM, Zhai J, Borges F et al (2014) miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature 508:411–415

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Hou Y, Ebina H, Levin HL, Voytas DF (2008) Chromodomains direct integration of retrotransposons to heterochromatin. Genome Res 18:359–363

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gehring M, Bubb KL, Henikoff S (2009) Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324:1447–1451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gschwend AR, Yu Q, Tong EJ et al (2012) Rapid divergence and expansion of the X chromosome in papaya. Proc Natl Acad Sci U S A 109:13716–13721

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Haldane JBS (1922) Sex ratio and unisexual sterility in hybrid animals. J Genet 12:101–109

    Article  Google Scholar 

  • Hobza R, Lengerova M, Svoboda J, Kubekova H, Kejnovsky E, Vyskot B (2006) An accumulation of tandem DNA repeats on the Y chromosome in Silene latifolia during early stages of sex chromosome evolution. Chromosoma 115:376–382

    Article  CAS  PubMed  Google Scholar 

  • Hobza R, Kejnovsky E, Vyskot B, Widmer A (2007) The role of chromosomal rearrangements in the evolution of Silene latifolia sex chromosomes. Mol Genet Genomics 278:633–638

    Article  CAS  PubMed  Google Scholar 

  • Hollister JD, Gaut BS (2009) Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 19:1419–1428

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hollister JD, Smith LM, Guo Y, Ott F, Weigel D, Gaut BS (2011) Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc Natl Acad Sci U S A 108:2322–2327

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hsieh TF, Ibarra CA, Silva P et al (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324:1451–1454

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ibarra CA, Feng X, Schoft VK et al (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337:1360–1364

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kejnovsky E, Kubat Z, Hobza R et al (2006a) Accumulation of chloroplast DNA sequences on the Y chromosome of Silene latifolia. Genetica 128:167–175

    Article  CAS  PubMed  Google Scholar 

  • Kejnovsky E, Kubat Z, Macas J, Hobza R, Mracek J, Vyskot B (2006b) Retand: a novel family of gypsy-like retrotransposon harboring an amplified tandem repeat. Mol Genet Genomics 276:254–263

    Article  CAS  PubMed  Google Scholar 

  • Kejnovsky E, Hobza R, Kubat Z, Widmer A, Marais GAB, Vyskot B (2007) High intrachromosomal similarity of retrotransposon long terminal repeats: evidence for homogenization by gene conversion on plant sex chromosomes? Gene 390:92–97

    Article  CAS  PubMed  Google Scholar 

  • Kejnovsky E, Hobza R, Kubat Z, Cermak T, Vyskot B (2009) The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity 102:533–541

    Article  CAS  PubMed  Google Scholar 

  • Kejnovsky E, Michalovova M, Steflova P et al (2013) Expansion of microsatellites on evolutionary young Y chromosome. PLoS One 8, e45519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kelkar YD, Eckert KA, Chiaromonte F, Makova KD (2011) A matter of life or death: how microsatellites emerge in and vanish from the human genome. Genome Res 21:2038–2048

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kijima TE, Innan H (2010) On the estimation of the insertion time of LTR retrotransposable elements. Mol Biol Evol 27:896–904

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick M (2010) How and why chromosome inversions evolve. PLoS Biol 8, e1000501

    Article  PubMed Central  PubMed  Google Scholar 

  • Kralova T, Cegan R, Kubat Z et al (2013) Identification of a novel retrotransposon with sex chromosome-specific distribution in Silene latifolia. Cytogenet Genome Res 143:87–95

    Article  Google Scholar 

  • Kubat Z, Zluvova J, Vogel I et al (2014) Possible mechanisms responsible for absence of retrotransposon family on a plant Y chromosome. New Phytol 202:662–678

    Article  CAS  PubMed  Google Scholar 

  • Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B (1988) On the role of unequal exchange in the containment of transposable element copy number. Genet Res 52:223–235

    Article  CAS  PubMed  Google Scholar 

  • Lewinski MK, Yamashita M, Emerman M et al (2006) Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog 2, e60

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu Z, Moore PH, Ma H et al (2004) A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427:348–352

    Article  CAS  PubMed  Google Scholar 

  • Mariotti B, Manzano S, Kejnovsky E, Vyskot B, Jamilena M (2009) Accumulation of Y-specific satellite DNAs during the evolution of Rumex acetosa sex chromosomes. Mol Genet Genomics 281:249–259

    Article  CAS  PubMed  Google Scholar 

  • Matsuo M, Ito Y, Yamauchi R, Obokata J (2005) The rice nuclear genome continuously integrates, shuffles, and eliminates the chloroplast genome to cause chloroplast-nuclear DNA flux. Plant Cell 17:665–675

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Michalovova M, Vyskot B, Kejnovsky E (2013) Analysis of plastid and mitochondrial DNA insertions in the nucleus (NUPTs and NUMTs) of six plant species: size, relative age and chromosomal localization. Heredity 111:314–320

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ming R, Bendahmane A, Renner SS (2011) Sex chromosomes in land plants. Ann Rev Plant Biol 62:485–514

  • Miyao A, Tanaka K, Murata K et al (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15:1771–1780

    Article  PubMed Central  PubMed  Google Scholar 

  • Na JK, Wang J, Ming R (2014) Accumulation of interspersed and sex-specific repeats in the non-recombining region of papaya sex chromosomes. BMC Genomics 15:335

    Article  PubMed Central  PubMed  Google Scholar 

  • Naito K, Zhang F, Tsukiyama T et al (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134

    Article  CAS  PubMed  Google Scholar 

  • Navajas-Pérez R, Herrán R, Jamilena M et al (2005) Reduced rate of sequence evolution of Y-linked satellite DNA in Rumex (Polygonaceae). J Mol Evol 60:391–399

    Article  PubMed  Google Scholar 

  • Navajas-Pérez R, Schwarzacher T, Rejón MR, Garrido-Ramos MA (2009) Molecular cytogenetic characterization of Rumex papillaris, a dioecious plant with an XX/XY1Y2 sex chromosome systém. Genetica 135:87–93

    Article  PubMed  Google Scholar 

  • Neumann P, Navrátilová A, Koblížková A et al (2011) Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mob DNA 2:4

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Plohl M, Luchetti A, Mestrovic N, Mantovani B (2008) Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene 409:72–82

    Article  CAS  PubMed  Google Scholar 

  • Reinders J, Mirouze M, Nicolet J, Paszkowski J (2013) Parent-of-origin control of transgenerational retrotransposon proliferation in Arabidopsis. EMBO Rep 14:823–828

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pokorna M, Kratochvil L, Kejnovsky E (2011) Microsatellite distribution on sex chromosomes at different stages of heteromorphism and heterochromatinization in two lizard species (Squamata: Eublepharidae: Coleonyx elegans and Laceridae: Eremias velox). BMC Genet 12:90

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sakamoto K, Ohmido N, Fukui K, Kamada H, Satoh S (2000) Site-specific accumulation of a LINE-like retrotransposon in a sex chromosome of the dioecious plant Cannabis sativa. Plant Mol Biol 44:723–732

    Article  CAS  PubMed  Google Scholar 

  • Shibata F, Hizume M, Kuroki Y (1999) Chromosome painting of Y chromosomes and isolation of a Y chromosome-specific repetitive sequences in the dioecious plant Rumex acetosa. Chromosoma 108:266–270

    Article  CAS  PubMed  Google Scholar 

  • Shibata F, Hizume M, Kuroki Y (2000) Differentiation and the polymorphic nature of the Y chromosomes revealed by repetitive sequences in the dioecious plant, Rumex acetosa. Chromosom Res 8:229–236

    Article  CAS  Google Scholar 

  • Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285

    Article  CAS  PubMed  Google Scholar 

  • Slotkin RK, Vaughn M, Borges F et al (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Steflova P, Tokan V, Vogel I et al (2013) Contrasting patterns of transposable element and satellite distribution on sex chromosomes (XY1Y2) in the dioecious plant Rumex acetosa. Genome Biol Evol 5:769–782

    Article  PubMed Central  PubMed  Google Scholar 

  • Steflova P, Hobza R, Vyskot B, Kejnovsky E (2014) Strong accumulation of chloroplast DNA in the Y chromosomes of Rumex acetosa and Silene latifolia. Cytogenet Genome Res 142:59–65

    Article  CAS  PubMed  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 

  • VanBuren R, Ming R (2013) Organelle DNA accumulation in the recently evolved papaya sex chromosomes. Mol Genet Genomics 288:277–284

    Article  CAS  PubMed  Google Scholar 

  • Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D (2013) Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol 11(8), e1001643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vyskot B, Hobza R (2015) The genomics of plant sex chromosomes. Plant Sci 236:126–135

    Article  CAS  PubMed  Google Scholar 

  • Wicker T, Sabot F, Hua-Van A et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982

    Article  CAS  PubMed  Google Scholar 

  • Yamato KT, Ishizaki K, Fujisawa M et al (2007) Gene organization of the liverworth Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proc Natl Acad Sci U S A 104:6472–6477

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang W, Wang X, Yu Q, Ming R, Jiang J (2008) DNA methylation and heterochromatinization in the male-specific region of the primitive Y chromosome of papaya. Genome Res 18:1938–1943

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Czech Science Foundation (grants P501/12/G090 to BV, P501/12/2220 to RH, 15-21523Y to ZK, and 15-02891S to EK). We would like to thank Alexander Oulton for the English corrections.

Author information

Authors and Affiliations

  1. Department of Plant Developmental Genetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, Brno, Czech Republic

    Roman Hobza, Zdenek Kubat, Radim Cegan, Wojciech Jesionek, Boris Vyskot & Eduard Kejnovsky

  2. Institute of Experimental Botany AS CR, Centre of the Region Hana for Biotechnological and Agricultural Research, Olomouc-Holice, Czech Republic

    Roman Hobza

Authors
  1. Roman Hobza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zdenek Kubat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Radim Cegan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wojciech Jesionek
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Boris Vyskot
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eduard Kejnovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Roman Hobza or Eduard Kejnovsky.

Additional information

Responsible Editors: Maria Assunta Biscotti, Pat Heslop-Harrison and Ettore Olmo

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hobza, R., Kubat, Z., Cegan, R. et al. Impact of repetitive DNA on sex chromosome evolution in plants. Chromosome Res 23, 561–570 (2015). https://doi.org/10.1007/s10577-015-9496-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-015-9496-2

Keywords

Search

Navigation