Sex chromosomes are an ideal system to study processes connected with suppressed recombination. We found evidence of microsatellite expansion, on the relatively young Y chromosome of the dioecious plant sorrel (Rumex acetosa, XY1Y2 system), but no such expansion on the more ancient Y chromosomes of liverwort (Marchantia polymorpha) and human. The most expanding motifs were AC and AAC, which also showed periodicity of array length, indicating the importance of beginnings and ends of arrays. Our data indicate that abundance of microsatellites in genomes depends on the inherent expansion potential of specific motifs, which could be related to their stability and ability to adopt unusual DNA conformations. We also found that the abundance of microsatellites is higher in the neighborhood of transposable elements (TEs) suggesting that microsatellites are probably targets for TE insertions. This evidence suggests that microsatellite expansion is an early event shaping the Y chromosome where this process is not opposed by recombination, while accumulation of TEs and chromosome shrinkage predominate later.

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

Zobrazit více v PubMed

Ellegren H (2004) Microsatellites: Simple sequences with complex evolution. Nature Rev Genet 5: 435–445. PubMed

Schotterer C (2000) Evolutionary dynamics of microsatellite DNA. Chromosoma 109: 365–371. PubMed

Koren Z, Trifonov EN (2011) Role of everlasting triplet expansion in protein evolution. J Mol Evol 72: 232–239. PubMed

Tautz D, Trick M, Dover GA (1986) Cryptic simplicity in DNA is a major source of genetic variation. Nature 322: 652–656. PubMed

Matula M, Kypr J (1999) Nucleotide sequences flanking dinucleotide microsatellites in the human, mouse and Drosophila genomes. J Biomol Struct Dyn 17: 275–280. PubMed

Shinde D, Lai Y, Sun F, Arnheim N (2003) Taq DNA polymerase slippage mutation rates measured by PCR and quasi-likelihood analysis: (CA/GT)n and (A/T)n microsatellites. Nucleic Acids Res 31: 974–980. PubMed PMC

Varela MA, Sanmiguel S, Gonzales-Tizon A, Martinez-Lage A (2008) Heterogeneous nature and distribution of interruptions in dinucleotides may indicate the existence of biased substitutions underlying microsatellite evolution. J Mol Evol 66: 575–580. PubMed

Pearson CE, Sinden RR (1998) Trinucleotide repeat DNA structures: dynamic mutations from dynamic DNA. Curr OpinStruct Biol 8: 321–330. PubMed

Kejnovska I, Tumova M, Vorlickova M (2001) (CGA)4: Parallel, anti-parallel, right-handed and left-handed homoduplexes of a trinucleotide repeat DNA. Biochim Biophys Acta 1527: 73–80. PubMed

Renciuk D, Kypr J, Vorlickova M (2011) CGG repeats associated with fragileXchromosome form left-handed Z-DNA. Biopolymers 95: 174–181. PubMed

Vorlickova M, Kypr J, Stokrova S, Sponar J (1982) A Z-like form of poly(dA-dC).poly(dG-dT) in solution? Nucleic Acids Res 10: 1071–1080. PubMed PMC

Bacolla A, Wells RD (2004) Non-B DNA conformations, genomic rearrangements, and human disease. J Biol Chem 279: 47411–47414. PubMed

Majewski J, Ott J (2000) GT repeats are associated with recombination on human chromosome 22. Genome Res 10: 1108–1114. PubMed PMC

Wahls WP, Moore PD (1990) Homologous recombination enhancement conferred by the Z-DNA motif d(TG)30 is abrogated by simian virus 40 T antigen binding to adjacent DNA sequences. Mol Cell Biol 10: 794–800. PubMed PMC

Wahls WP, Wallace LJ, Moore PD (1990) The Z-DNA motif d(TG)30 promotes reception of information during gene conversion events while stimulating homologous recombination in human cells in culture. Mol Cell Biol 10: 785–793. PubMed PMC

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 103: 533–541. PubMed

Bachtrog D, Weiss S, Zangerl B, Brem G, Schlotterer C (1999) Distribution of dinucleotide microsatellites in the Drosophila melanogaster genome. Mol Biol Evol 16: 602–610. PubMed

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. PubMed

Cermak T, Kubat Z, Hobza R, Koblizkova A, Widmer A, et al. (2008) Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes. Chromosome Research 16: 961–976. PubMed

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

Nadir E, Margalit H, Gallily T, Ben-Sasson S (1996) Microsatellite spreading in the human genome: Evolutionary mechanisms and structural implications. Proc Natl Acad Sci USA 93: 6470–6475. PubMed PMC

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. PubMed PMC

Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nature Genet 30: 194–200. PubMed

Temnykh S, DeClerk G, Lukashova A, Lipovich L, Cartinhour S, et al. (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): Frequency, length variation, transposon association, and genetic marker potential. Genome Res 11: 1441–1452. PubMed PMC

Ramsay L, Macaulay M, Cardie L, Morgante M, degli Ivanissevich S, et al. (1999) Intimate association of microsatellite repeats with retrotransposons and other dispersed repetitive elements in barley. Plant J 17: 415–425. PubMed

Wilder J, Hollocher H (2001) Mobile elements and the genesis of microsatellites in dipterans. Mol Biol Evol 18: 384–392. PubMed

Arcot SS, Wang Z, Weber JL, Deininger PL, Batzer MA (1995) Alu repeats: A source for the genesis of primate microsatellites. Genomics 29: 136–144. PubMed

Navajas-Perez R, de la Herran R, Lopez G, Jamilena M, Lozano R, et al. (2005) The evolution of reproductive systems and sex-determining mechanisms within Rumex (Polygonaceae) inferred from nuclear and chloroplastidial sequence data. Mol Biol Evol 22: 1929–1939. PubMed

Graves JAM (2002) The rise and fall of SRY. Trends Genetics 18: 259–264. PubMed

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

Vyskot B, Hobza R (2004) Gender in plants: sex chromosomes are emerging from the fog. Trends Genet 20: 432–438. PubMed

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

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

Yant SR, Wu X, Huang Y, Garrison B, Burgess SM, et al. (2005) High-resolutioni genome-wide mapping of transposon integration in mammals. Mol Cell Biol 25: 2085–2094. PubMed PMC

Pruss D, Bushman FD, Wolffe AP (1994) Human immunodeficiency virus integrase directs integration to sites of severe DNA distortion within the nucleosome core. Proc Natl Acad Sci USA 91: 5913–5917. PubMed PMC

Zayed H, Izsvak Z, Khare D, Heinemann U, Ivics Z (2003) The DNA-bending protein HMGB1 is a cellular cofactor of Sleeping Beauty transposition. Nucleic Acids Res 31: 2313–2322. PubMed PMC

Ulanovsky L, Bodner M, Trifonov EN, Choder M (1986) Curved DNA: Design, synthesis, and circularization. Proc Natl Acad Sci USA 83: 862–866. PubMed PMC

Crothers DM, Haran TE, Nadeau JG (1990) Intrinsically bent DNA. J Biol Chem 265: 7093–7096. PubMed

Gangadharan S, Mularoni L, Fain-Thorton J, Wheelan SJ, Craig NL (2010) DNA transposon Hermes inserts into DNA in nucleosome-free regions in vivo. Proc Natl Acad Sci USA 107: 21966–21972. PubMed PMC

Baller JA, Gao J, Voytas DF (2011) Access to DNA establishes a secondary target site bias for the yeast retrotransposon Ty5. Proc Natl Acad Sci USA 108: 203561–29356. PubMed PMC

Hrabcova I, Kypr J (2003) Genomic occurrence of microsatellites containing integral and non-integral repeat numbers. Biochem Biophys Res Commun 300: 824–831. PubMed

Rizzon C, Marais G, Gouy M, Biemont C (2002) Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res 12: 400–407. PubMed PMC

Marais GAB, Nicolas M, Bergero R, Chambrier P, Kejnovsky E, et al. (2008) Evidence for degeneration of the Y chromosome in the dioecious plant Silene latifolia. Current Biology 18: 1–5. PubMed

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

Mariotti B, Manzano S, Kejnovsky E, Vyskot B, Jamilena M (2008) Accumulation of Y-specific satellite DNAs during the evolution of Rumex acetosa sex chromosomes. Mol. Genet. Genomics 281: 249–259. PubMed

The 1000 Genome Project Consortium (2010) A map of human genome variation from population/scale sequencing. Nature 467: 1061–1073. PubMed PMC

Mayer C (2006–2010) Phobos 3.3.11. Available: http://www.rub.de/spezzoo/cm/cm_phobos.htm. Accessed 2012 Dec 17.

Smit AFA, Hubley R, Green (1996–2010) RepeatMasker Open-3.0. Available: http://www.repeatmasker.org. Accessed 2012 Dec 17.

Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 26: 841–842. PubMed PMC

Gray DM, Hung SH, Johnson KH (1995) Absorption and circular dichroism spectroscopy of nucleic acid duplexes and triplexes. Methods Enzymol 246: 19–34. PubMed

Small Body, Large Chromosomes: Centric Fusions Shaped the Karyotype of the Amazonian Miniature Fish Nannostomus anduzei (Characiformes, Lebiasinidae)

A step forward in the genome characterization of the sugarcane borer, Diatraea saccharalis: karyotype analysis, sex chromosome system and repetitive DNAs through a cytogenomic approach

Fundamentally different repetitive element composition of sex chromosomes in Rumex acetosa

Transposons and satellite DNA: on the origin of the major satellite DNA family in the Chenopodium genome

The Formation of Sex Chromosomes in Silene latifolia and S. dioica Was Accompanied by Multiple Chromosomal Rearrangements

Karyotypes and Sex Chromosomes in Two Australian Native Freshwater Fishes, Golden Perch (Macquaria ambigua) and Murray Cod (Maccullochella peelii) (Percichthyidae)

Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae)

Natural History of a Satellite DNA Family: From the Ancestral Genome Component to Species-Specific Sequences, Concerted and Non-Concerted Evolution

Sex and the flower - developmental aspects of sex chromosome evolution

Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2 system in Hoplias malabaricus (Teleostei, Characiformes)

The slowdown of Y chromosome expansion in dioecious Silene latifolia due to DNA loss and male-specific silencing of retrotransposons

Impact of Repetitive Elements on the Y Chromosome Formation in Plants

Chromosomal Evolution in Lower Vertebrates: Sex Chromosomes in Neotropical Fishes

Transposable elements and G-quadruplexes

Impact of repetitive DNA on sex chromosome evolution in plants

Multiple sex chromosomes in the light of female meiotic drive in amniote vertebrates

Contrasting patterns of transposable element and satellite distribution on sex chromosomes (XY1Y2) in the dioecious plant Rumex acetosa