Skip to main content
Log in

Repetitive sequences and epigenetic modification: inseparable partners play important roles in the evolution of plant sex chromosomes

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The present review discusses the roles of repetitive sequences played in plant sex chromosome evolution, and highlights epigenetic modification as potential mechanism of repetitive sequences involved in sex chromosome evolution.

Sex determination in plants is mostly based on sex chromosomes. Classic theory proposes that sex chromosomes evolve from a specific pair of autosomes with emergence of a sex-determining gene(s). Subsequently, the newly formed sex chromosomes stop recombination in a small region around the sex-determining locus, and over time, the non-recombining region expands to almost all parts of the sex chromosomes. Accumulation of repetitive sequences, mostly transposable elements and tandem repeats, is a conspicuous feature of the non-recombining region of the Y chromosome, even in primitive one. Repetitive sequences may play multiple roles in sex chromosome evolution, such as triggering heterochromatization and causing recombination suppression, leading to structural and morphological differentiation of sex chromosomes, and promoting Y chromosome degeneration and X chromosome dosage compensation. In this article, we review the current status of this field, and based on preliminary evidence, we posit that repetitive sequences are involved in sex chromosome evolution probably via epigenetic modification, such as DNA and histone methylation, with small interfering RNAs as the mediator.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Akagi T, Henry IM, Tao R, Comai L (2014) A Y-chromosome-encoded small RNA acts as a sex determinant in persimmons. Science 346:646–650

    Article  CAS  PubMed  Google Scholar 

  • Akiyama K, Katakami H, Takata R (2007) Mobilization of a retrotransposon in 5-azacytidine-treated fungus Fusarium oxysporum. Plant Biotechnol 24:345–348

    Article  CAS  Google Scholar 

  • Armstrong SJ, Filatov DA (2008) A cytogenetic view of sex chromosome evolution in plants. Cytogenet Genome Res 120:241–246

    Article  CAS  PubMed  Google Scholar 

  • Arnaud P, Goubely C, Pélissier T, Deragon JM (2000) SINE retroposons can be used in vivo as nucleation centers for de novo methylation. Mol Cell Biol 20:3434–3441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bachtrog D (2005) Sex chromosome evolution: molecular aspects of Y chromosome degeneration in Drosophila. Genome Res 15:1393–1401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bachtrog D, Hom E, Wong KM, Maside X, de Jong P (2008) Genomic degradation of a young Y chromosome in Drosophila Miranda. Genome Biol 9:R30

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bellott DW, Skaletsky H, Pyntikova T, Mardis ER, Graves T, Kremitzki C, Brown LG, Rozen S, Warren WC, Wilson RK, Page DC (2010) Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466:612–616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergero R, Charlesworth D (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24:94–102

    Article  PubMed  Google Scholar 

  • Bergero R, Charlesworth D (2011) Preservation of the Y transcriptome in a 10-million-year-old plant sex chromosome system. Curr Biol 21:1470–1474

    Article  CAS  PubMed  Google Scholar 

  • Bergero R, Charlesworth D, Filatov D, Moore R (2008a) Defining regions and rearrangements of the Silene latifolia Y chromosome. Genetics 178:2045–2053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergero R, Forrest A, Charlesworth D (2008b) Active miniature transposons from a plant genome and its nonrecombining Y chromosome. Genetics 178:1085–1092

    Article  CAS  PubMed  PubMed Central  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, Käfer J, Cegan R, Deschamps C, Zemp N, Mousset S, Aubourg S, Bergero R, Charlesworth D, Hobza R, Widmer A, Marais GAB (2015) Identifying new sex-linked genes through BAC sequencing in the dioecious plant Silene latifolia. BMC Genom 16:546

    Article  CAS  Google Scholar 

  • Böhne A, Zhou QC, Darras A, Schmidt C, Schartl M, Galiana-Arnoux D, Volff JN (2012) Zisupton-a novel superfamily of DNA transposable elements recently active in fish. Mol Biol Evol 29:631–645

    Article  PubMed  CAS  Google Scholar 

  • Bůzek J, Koutníková H, Houben A, Ríha K, Janousek B, Siroký J, Grant S, Vyskot B (1997) Isolation and characterization of X chromosome-derived DNA sequences from a dioecious plant Melandrium album. Chromosome Res 5:57–65

    Article  PubMed  Google Scholar 

  • Cegan R, Marais GAB, Kubekova H, Blavet N, Widmer A, Vyskot B, Doležel J, Šafář J, Hobza R (2010) Structure and evolution of Apetala3, a sex-linked gene in Silene latifolia. BMC Plant Biol 10:180

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cermak T, Kubat Z, Hobza R, Koblizkova A, Widmer A, Macas J, Vyskot B, Kejnovsky E (2008) Survey of repetitive sequence in Silene latifolia with respect to their distribution on sex chromosome. Chromosome Res 16:961–976

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D (2013) Plant sex chromosome evolution. J Exp Bot 64:405–420

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D (2015) Plant contributions to our understanding of sex chromosome evolution. New Phytol 208:52–65

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D, Guttman DS (1999) The evolution of dioecy and plant sex chromosome systems. In: Ainsworth C (ed) Sex determination in plants. Bios Scientific Publisher press, Oxford, pp 25–49

    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 

  • Chinnusamy V, Dalal M, Zhu JK (2013) Epigenetic regulation of abiotic stress responses in plants. In: Jenks MA, Hasegawa PM (eds) Plant abiotic stress, 2nd edn. Wiley, Hoboken, pp 203–229

    Google Scholar 

  • Cioffi MB, Kejnovský E, Marquioni V, Poltronieri J, Molina WF, Diniz D, Bertollo LA (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 

  • Cioffi MB, Bertollo LAC, Villa MA, de Oliveira EA, Tanomtong A, Yano CF, Supiwong W, Chaveerach A (2015) Genomic organization of repetitive DNA elements and its implications for the chromosomal evolution of channid fishes (Actinopterygii, Perciformes). PLoS One 10:e0130199

    Article  PubMed Central  Google Scholar 

  • Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Contreras B, Vives C, Castells R, Casacuberta JM (2015) The impact of transposable elements in the evolution of plant genomes: from selfish elements to key players. In: Pontarotti P (ed) Evolutionary biology: Biodiversification from genotype to phenotype. Switzerland, pp 93–105

  • Cui X, Cao X (2014) Epigenetic regulation and functional exaptation of transposable elements in higher plants. Curr Opin Plant Biol 21:83–88

    Article  CAS  PubMed  Google Scholar 

  • Divashuk MG, Alexandrov OS, Kroupin PY, Karlov GI (2011) Molecular cytogenetic mapping of Humulus lupulus sex chromosomes. Cytogenet Genome Res 134:213–219

    Article  CAS  PubMed  Google Scholar 

  • Divashuk MG, Alexandrov OS, Razumova OV, Kirov IV, Karlov GI (2014) Molecular cytogenetic characterization of the dioecious Cannabis sativa with an XY chromosome sex determination system. PLoS One 9:e85118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Eichten SR, Dllis NA, Makarevitch I, Yeh CT, Gent JI, Guo L, McGinnis KM, Zhang X, Schnable PS, Vaughn MW, Dawe RK, Springer NM (2012) Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet 8:e1003127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellison CE, Bachtrog D (2013) Dosage compensation via transposable element mediated rewiring of a regulatory network. Science 342:846–850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erlandsson R, Wilson JF, Paabo S (2000) Sex chromosomal transposable element accumulation and male-driven substitutional evolution in humans. Mol Biol Evol 17:804–812

    Article  CAS  PubMed  Google Scholar 

  • Faber-Hammond JJ, Phillips RB, Brown KH (2015) Comparative analysis of the shared sex-determination region (SDR) among salmonid fishes. Genome Biol Evol 7:1972–1987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng W, Michaels SD (2015) Accessing the inaccessible: the organization, transcription, replication, and repair of heterochromatin in plants. Annu Rev Genet 49:439–459

    Article  CAS  PubMed  Google Scholar 

  • Gent JI, Ellis NA, Guo L, Harkess AE, Yao Y, Zhang X, Dawe RK (2013) CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res 23:628–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geraldes A, Hefer CA, Capron A, Kolosova N, Martinez-Nuñez F, Soolanayakanahally RY, Stanton B, Guy RD, Mansfield SD, Douglas CJ, Cronk QCB (2015) Recent Y chromosome divergence despite ancient origin of dioecy in poplars (Populus). Mol Ecol 24:3243–3256

    Article  CAS  PubMed  Google Scholar 

  • Grabowska-Joachimiak A, Mosiolek M, Lech A, Góralski G (2011) C-banding/DAPI and in situ hybridization reflect karyotype structure and sex chromosome differentiation in Humulus japonicas Siebold & Zucc. Cytogenet Genome Res 132:203–211

    Article  CAS  PubMed  Google Scholar 

  • Graves JAM (2006) Sex chromosome specialization and degeneration in mammals. Cell 124:901–914

    Article  PubMed  CAS  Google Scholar 

  • Gschwend A, Yu Q, Tong E, Zeng F, Han J, VanBuren R, Aryal R, Charlesworth D, Moore PH, Paterson AH, Ming R (2012) Rapid divergence and expansion of the X chromosome in papaya. Proc Natl Acad Sci USA 109:13716–13721

    Article  CAS  PubMed  PubMed Central  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 

  • Hobza R, Kubat Z, Cegan R, Jesionek W, Vyskot B, Kejnovsky B (2015) Impact of repetitive DNA on sex chromosome evolution in plants. Chromosome Res 23:561–570

    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  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishizaki K, Shimizu-Ueda Y, Okada S, Yamamoto M, Fujisawa M, Tamato KT, Fukuzawa H, Ohyama K (2002) Multicopy genes uniquely amplified in the Y chromosome-specific repeats of the liverwort Marchantia polymorpha. Nucleic Acids Res 30:4675–4681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jablonka E (2004) The evolution of the peculiarities of mammalian sex chromosomes: an epigenetic view. BioEssays 26:1327–1332

    Article  PubMed  Google Scholar 

  • Jamsari A, Nitz I, Reamon-Büttner SM, Jung C (2004) BAC-derived diagnostic markers for sex determination in Asparagus. Theor Appl Genet 108:1140–1146

    Article  CAS  PubMed  Google Scholar 

  • Janoušek B, Široký J, Vyskot B (1996) Epigenetic control of sexual phenotype in a dioecious plant Melandrium album. Mol Gen Genet 250:483–490

    Article  PubMed  Google Scholar 

  • Kawashima T, Berger F (2014) Epigenetic reprogramming in plant sexual reproduction. Nat Rev Genet 15:613–624

    Article  CAS  PubMed  Google Scholar 

  • Kejnovsky E, Kubat Z, Macas J, Hobza R, Mracek J, Vyskot B (2006) 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, Cermak T, Kubat Z, 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 

  • Kejnovský E, Michalovova M, Steflova P, Kejnovska I, Manzano S, Hobza R, Kubát Z, Kovařík J, Jamilena M, Vyskot B (2013) Expansion of microsatellites on evolutionary young Y chromosome. PLoS One 8:e45519

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kralova T, Cegan R, Kubat Z, Vrana J, Vyskot B, Vogel I, Kejnovsky E, Hobza R (2014) Identification of a novel retrotransposon with sex chromosome-specific distribution in Silene latifolia. Cytogenet Genome Res 143:87–95

    Article  CAS  PubMed  Google Scholar 

  • Kubat Z, Hobza R, Vyskot B (2008) Microsatellite accumulation on the Y chromosome in Silene latifolia. Genome 51:350–356

    Article  CAS  PubMed  Google Scholar 

  • Kubat Z, Zluvova J, Vogel I, Kovacova V, Cermak T, Cegan R, Hobza R, Vyskot B, Kejnovsky E (2014) Possible mechanisms responsible for absence of a retrotransposon family on a plant Y chromosome. New Phytol 202:662–678

    Article  CAS  PubMed  Google Scholar 

  • Kuroki S, Matoba S, Akiyoshi M, Matsumura Y, Miyachi H, Mise N, Abe K, Ogura A, Wilhelm D, Koopman P, Nozaki M, Kanai Y, Shinkai Y, Tachibana M (2013) Epigenetic regulation of mouse sex determination by the histone demethylase Jmjd1a. Science 341:1106–1109

    Article  CAS  PubMed  Google Scholar 

  • Li SF, Gao WJ, Zhao XP, Dong TY, Deng CL, Lu LD (2014) Analysis of transposable elements in the genome of Asparagus officinalis from high coverage sequence data. PLoS One 9:e97189

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li SF, Zhang GJ, Yuan JH, Deng CL, Lu LD, Gao WJ (2015a) Effect of 5-azaC on the growth, flowering time and sexual phenotype in spinach. Russ J Plant Physiol 62:670–675

    Article  CAS  Google Scholar 

  • Li Y, Mukherjee I, Thum KE, Tanurdzic M, Katari MS, Obertello M, Edwards MB, McCombie WR, Martienssen RA, Coruzzi GM (2015b) The histone methyltransferase SDG8 mediates the epigenetic modification of light and carbon responsive genes in plants. Genome Biol 16:79

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66

    Article  CAS  PubMed  Google Scholar 

  • Lisch D, Bennetzen JL (2011) Transposable element origins of epigenetic gene regulation. Curr Opin Plant Biol 14:156–161

    Article  CAS  PubMed  Google Scholar 

  • Liu ZY, Moore PH, Ma H, Ackerman CM, Ragiba M, Yu Q, Pearl HM, Kim MS, Charlton JW, Stiles JI, Zee FT, Paterson AH, Ming R (2004) A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427:348–352

    Article  CAS  PubMed  Google Scholar 

  • Ma H, Moore PH, Liu Z, Kim MS, Yu Q, Fitch MMM, Sekioka T, Paterson AH, Ming R (2004) High-density linkage mapping revealed suppression of recombination at the sex determination locus in papaya. Genetics 166:419–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408

    Article  CAS  PubMed  Google Scholar 

  • Marais GAB, Nicolas M, Bergero R, Chambrier P, Kejnovsky E, Monéger F, Hobza R, Widmer A, Charlesworth D (2008) Evidence for degeneration of the Y chromosome in the dioecious plant Silene latifolia. Curr Biol 18:545–549

    Article  CAS  PubMed  Google Scholar 

  • Mariotti B, Manzano S, Kejnovský 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 

  • Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, Pitrat M, Dogimont C, Bendahmane A (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nature 461:1135–1138

    Article  CAS  PubMed  Google Scholar 

  • Matsubara K, O’Meally D, Azad B, Georges A, Sarre SD, Graves JAM, Matsuda Y, Ezaz T (2015) Amplification of microsatellite repeat motifs is associated with the evolutionary differentiation and heterochromatinization of sex chromosome in Sauropsida. Chromosoma Adv. doi:10.1007/s00412-015-0531-z

    Google Scholar 

  • Matsunaga S, Yagisawa F, Yamamoto M, Uchida W, Nakao S, Kawano S (2002) LTR retrotransposons in the dioecious plant Silene latifolia. Genome 45:745–751

    Article  CAS  PubMed  Google Scholar 

  • McClintock B (1948) Mutable loci in maize. Carnegie Inst Wash Year Book 47:155–169

    Google Scholar 

  • Mehrotra S, Goyal V (2014) Repetitive sequences in plant nuclear DNA: types, distribution, evolution and function. Genomics Proteomics Bioinformatics 12:164–171

    Article  PubMed  PubMed Central  Google Scholar 

  • Menon DU, Coarfa C, Xiao W, Gunaratne PH, Meller VH (2014) siRNAs from an X-linked satellite repeat promote X chromosome recognition in Drosophila melanogaster. Proc Natl Acad Sci USA 111:16460–16465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ming R, Hou SB, Feng Y et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Morales ME, Servant G, Ade C, Roy-Engel AM (2015) Altering genomic integrity: heavy metal exposure promotes transposable element-mediated damage. Biol Trace Elem Res 16:24–33

    Article  CAS  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 Genom 15:335

    Article  Google Scholar 

  • Navajas-Pérez R, de la Herrán R, González GL, Jamilena M, Lozano R, Rejón CR, Rejón MR, Garrido-Ramos MA (2005) The evolution of reproductive systems and sex-determining mechanisms within Rumex (Polygonaceae) inferred from nuclear and plastidial sequence data. Mol Biol Evol 22:1929–1939

    Article  PubMed  CAS  Google Scholar 

  • Nicolas M, Marais G, Hykelova V, Janousek B, Laporte V, Vyskot B, Mouchiroud D, Negrutiu I, Charlesworth D, Monéger F (2005) A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol 3:e4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ohno S (1967) Sex Chromosomes and Sex linked Genes. New York

  • Okada S, Sone T, Fujisawa M, Nakayama S, Takenaka M, Ishizaki K, Shimizu-Ueda Kono K, Hanajiri T, Yamato KT, Fukuzawa H, Brennicke A, Ohyama K (2001) The Y chromosome in the liverwort Marchantia polymorpha was accumulated unique repeat sequences harboring a male-specific gene. Proc Natl Acad Sci USA 98:9454–9459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oyama RK, Silber MV, Renner SS (2010) A specific insertion of a solo-LTR characterizes the Y-chromosome of Bryonia dioica (Cucurbitaceae). BMC Res Notes 3:166

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Piferrer F (2013) Epigenetics of sex determination and gonadogenesis. Dev Dyn 242:360–370

    Article  CAS  PubMed  Google Scholar 

  • Pontes O, Costa-Nunes P, Vithayathil P, Pikaard CS (2009) RNA polymerase V functions in Arabidopsis interphase heterochromatin organization independently of the 24-nt siRNA-directed DNA methylation pathway. Mol Plant 2:700–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rejón CR, Jamilena M, Ramos MG, Parker JS, Rejón MR (1994) Cytogenetic and molecular analysis of the multiple sex chromosome system of Rumex acetosa. Heredity 72:209–215

    Article  Google Scholar 

  • Renner SS (2014) The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am J Bot 101:1588–1596

    Article  PubMed  Google Scholar 

  • Repping S, Daalen SKMv, Brown LG, Korver CM, Lange J, Marszalek JD, Pyntikova T, van der Veen F, Skaletsky H, Rozen S (2006) High mutation rates have driven extensive structural polymorphism among human Y chromosomes. Nat Genet 38:463–467

    Article  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 

  • Sakamoto K, Abe T, Matsuyama T, Yoshida S, Ohmido N, Fukui K, Satoh S (2005) RAPD markers encoding retrotransposable elements are linked to the male sex in Cannabis sativa L. Genome 48:931–936

    Article  CAS  PubMed  Google Scholar 

  • Schaack S, Pritham EJ, Wolf A, Lynch M (2010) DNA transposon dynamics in population of Daphnia pulex with and without sex. Proc Biol Sci 277:2381–2387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Secco D, Wang C, Shou H, Schultz MD, Chiarenza S, Nussaume L, Ecker JR, Whelan J, Lister R (2015) Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 4: e09343

  • Sentmanat MF, Elgin SCR (2012) Ectopic assembly of heterochromatin in Drosophila melanogaster triggered by transposable elements. Proc Natl Acad Sci USA 109:14104–14109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shibata F, Hizume M, Kuroki Y (1999) Chromosome painting of Y chromosomes and isolation of a Y chromosome-specific repetitive sequence 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. Chromosome Res 8:229–236

    Article  CAS  PubMed  Google Scholar 

  • Skaletsky H, Kuroda-Kawaguchi T, Minx PJ et al (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837

    Article  CAS  PubMed  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, Tanurdžić M, Becker JD, Feijó JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soppe WJJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, Jacobsen SE, Schubert I, Fransz PF (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21:6549–6559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sousa A, Fuchs J, Renner SS (2013) Molecular cytogenetics (FISH, GISH) of Coccinia grandis: a ca. 3 myr-old species of cucurbitaceae with the largest Y/autosome divergence in flowering plants. Cytogenet Genome Res 139:107–118

    Article  CAS  PubMed  Google Scholar 

  • Steflova P, Tokan V, Vogel I, Lexa M, Macas J, Novak P, Hobza R, Vyskot B, Kejnovsky E (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  PubMed Central  CAS  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 

  • Steinemann M, Steinemann S (1992) Degenerating Y chromosome of Drosophila miranda: a trap for retrotransposons. Proc Natl Acad Sci USA 89:7591–7595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinemann S, Steinemann M (2005a) Retroelements: tools for sex chromosome evolution. Cytogenet Genome Res 110:134–143

    Article  CAS  PubMed  Google Scholar 

  • Steinemann S, Steinemann M (2005b) Y chromosomes: born to be destroyed. BioEssays 27:1076–1083

    Article  CAS  PubMed  Google Scholar 

  • Takata M, Kiyohara A, Takasu A, Kishima Y, Ohtsubo H, Sano Y (2007) Rice transposable elements are characterized by various methylation environments in the genome. BMC Genom 8:469

    Article  Google Scholar 

  • Telgmann-Rauber A, Jamsari A, Kinney MS, Pires JC, Jung C (2007) Genetic and physical maps around the sex-determining M-locus of the dioecious plant asparagus. Mol Genet Genomics 278:221–234

    Article  CAS  PubMed  Google Scholar 

  • Tenaillon MI, Hufford MB, Gaut BS, Ross-Ibarra J (2012) Genome size and transposable element content as determined by high-throughput sequencing in maize and Zea luxurians. Genome Biol Evol 3:219–229

    Article  CAS  Google Scholar 

  • Tian Z, Rizzon C, Du J, Zhu L, Bennetzen JL, Jackson SA, Gaut BS, Ma J (2009) Do genetic recombination and gene density shape the pattern of DNA elimination in rice long terminal repeat retrotransposons? Genome Res 19:2221–2230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toups M, Veltsos P, Pannell JR (2015) Plant sex chromosomes: lost genes with little compensation. Curr Biol 25:R427–R430

    Article  CAS  PubMed  Google Scholar 

  • VanBuren R, Ming R (2013a) Dynamic transposable element accumulation in the nascent sex chromosomes of papaya. Mob Genet Elements 3:e23462

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • VanBuren R, Zeng F, Chen C et al (2015) Origin and domestication of papaya Yh chromosome. Genome Res 25:524–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vyskot B (2005) The role of DNA methylation in plant reproductive development. In: Ainsworth CC (ed) Sex determination in plants. Oxford, UK, pp 101–121

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang JP, Na JK, Yu QY, Gschwend AR, Han J, Zeng F, Aryal R, VanBuren R, Murray JE, Zhang W, Navajas-Pérez R, Feltus FA, Lemke C, Tong EJ, Chen C, Wai CM, Singh R, Wang ML, Min XJ, Alam M, Charlesworth D, Moore PH, Jiang J, Paterson AH, Ming R (2012) Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc Natl Acad Sci USA 109:13710–13715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westergaard M (1958) The mechanism of sex determination in dioecious flowering plants. Adv Genet 9:217–281

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson MF (2015) Evidence that DNA methylation engenders dynamic gene regulation. Proc Natl Acad Sci USA 112:E2116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wollmann H, Berger F (2012) Epigenetic reprogramming during plant reproduction and seed development. Curr Opin Plant Biol 15:63–69

    Article  CAS  PubMed  Google Scholar 

  • Xuan YH, Piao HL, Je BI, Park SJ, Park SH, Huang J, Zhang JB, Peterson T, Han C (2011) Transposon Ac/Ds-induced chromosomal rearrangements at the rice OsRLG5 locus. Nucleic Acids Res 39:e149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matzke MA, Kanno T, Matzke AJM (2015) RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu Rev Plant Biol 66:91–925

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yano CF, Bertollo LAC, Molina WF, Liehr T, Cioffi MB (2014) Genomic organization of repetitive DNAs and its implications for male karyotype and the neo-Y chromosome differentiation in Erythrinus erythrinus (Characiformes, Erythrinidae). Comp Cytogenet 8:139–151

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu QY, Hou SB, Hobza R, Feltus FA, Wang X, Jin WW, Skelton RL, Blas A, Lemke C, Saw JH, Moore PH, Alam M, Jiang JM, Paterson AH, Vyskot B, Ming R (2007) Chromosomal location and gene paucity of the male specific region on papaya Y chromosome. Mol Genet Genomics 278:177–185

    Article  CAS  PubMed  Google Scholar 

  • Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:193–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng F, Cheng B (2014) Transposable element insertion and epigenetic modification cause the multiallelic variation in the expression of FAE1 in Sinapis alba. Plant Cell 26:2648–2659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X (2008) The epigenetic landscape of plants. Science 320:489–492

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhu JK (2011) RNA-directed DNA methylation. Curr Opin Plant Biol 14:142–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Wang X, Yu QY, 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Q, Ellison CE, Kaiser VB, Alekseyenko AA, Gorchakov AA, Bachtrog D (2013) The epigenome of evolving Drosophila neo-sex chromosomes: dosage compensation and heterochromatin formation. PLoS Biol 11:e1001711

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, Jarvis ED, Gilbert MTP, Zhang G (2014) Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346:1332–1340

    Article  CAS  Google Scholar 

  • Zhu Y, Dai J, Fuerst PG, Voytas DF (2003) Controlling integration specificity of a yeast retrotransposon. Proc Natl Acad Sci USA 100:5891–5895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zluvova J, Georgiev S, Janousek B, Charlesworth D, Vyskot B, Negrutiu I (2007) Early events in the evolution of the Silene latifolia Y chromosome: male specialization and recombination arrest. Genetics 177:375–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Natural Science foundation of China (31300202, 30970211 and 31470334). We are grateful to Dr. Yongfang Li (Department of Biochemistry and Molecular Biology, Oklahoma State University) for her reviewing of this manuscript and constructive comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wu-Jun Gao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, SF., Zhang, GJ., Yuan, JH. et al. Repetitive sequences and epigenetic modification: inseparable partners play important roles in the evolution of plant sex chromosomes. Planta 243, 1083–1095 (2016). https://doi.org/10.1007/s00425-016-2485-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-016-2485-7

Keywords

Navigation