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

. 2013 ; 5 (4) : 769-82.

Jazyk angličtina Země Velká Británie, Anglie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid23542206

Rumex acetosa is a dioecious plant with the XY1Y2 sex chromosome system. Both Y chromosomes are heterochromatic and are thought to be degenerated. We performed low-pass 454 sequencing and similarity-based clustering of male and female genomic 454 reads to identify and characterize major groups of R. acetosa repetitive DNA. We found that Copia and Gypsy retrotransposons dominated, followed by DNA transposons and nonlong terminal repeat retrotransposons. CRM and Tat/Ogre retrotransposons dominated the Gypsy superfamily, whereas Maximus/Sireviruses were most abundant among Copia retrotransposons. Only one Gypsy subfamily had accumulated on Y1 and Y2 chromosomes, whereas many retrotransposons were ubiquitous on autosomes and the X chromosome, but absent on Y1 and Y2 chromosomes, and others were depleted from the X chromosome. One group of CRM Gypsy was specifically localized to centromeres. We also found that majority of previously described satellites (RAYSI, RAYSII, RAYSIII, and RAE180) are accumulated on the Y chromosomes where we identified Y chromosome-specific variant of RAE180. We discovered two novel satellites-RA160 satellite dominating on the X chromosome and RA690 localized mostly on the Y1 chromosome. The expression pattern obtained from Illumina RNA sequencing showed that the expression of transposable elements is similar in leaves of both sexes and that satellites are also expressed. Contrasting patterns of transposable elements (TEs) and satellite localization on sex chromosomes in R. acetosa, where not only accumulation but also depletion of repetitive DNA was observed, suggest that a plethora of evolutionary processes can shape sex chromosomes.

Zobrazit více v PubMed

Altschul SF, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–3402. PubMed PMC

Benson DA, et al. GenBank. Nucleic Acids Res. 2012;40(Database issue):D32–D37. PubMed PMC

Blocka-Wandas M, Slivinska E, Grabowska-Joachimiak A, Musial K, Joachimiak AJ. Male gametophyte development and two different DNA classes of pollen grains in Rumex acetosa L., a plant with an XX/XY1Y2 sex chromosome system and female-biased sex ratio. Sexual Plant Reprod. 2007;20:171–180.

Camacho C, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421. PubMed PMC

Cermak T, et al. Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes. Chromosome Res. 2008;16:961–976. PubMed

Cioffi MB, Kejnovsky E, Bertollo LAC. The chromosomal distribution of microsatellite repeats in the genome of the wolf fish Hoplias malabaricus, focusing on the sex chromosomes. Cytogenet Genome Res. 2011;132:289–296. PubMed

Charlesworth B. The evolution of sex chromosomes. Science. 1991;251:1030–1033. PubMed

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

Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14:1188–1190. PubMed PMC

Cunado N, et al. The evolution of sex chromosomes in the genus Rumex (Polygonaceae): identification of a new species with heteromorphic sex chromosomes. Chromosome Res. 2007;15:825–832. PubMed

Drummond AJ, et al. Geneious v5.5. 2011. Available from: http://www.geneious.com.

Frickey T, Lupas A. CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics. 2004;20:3702–3704. PubMed

Gvozdev VA, Kogan GL, Usakin LA. The Y chromosome as a target for acquired and amplified genetic material in evolution. Bioessays. 2005;27:1256–1262. PubMed

Heslop-Harrison JS, Schwarzacher T. Organization of the plant genome in chromosomes. Plant J. 2011;66:18–33. PubMed

Hobza R, et al. An accumulation of a tandem DNA repeats on the Y chromosome in an early stages of sex chromosome evolution. Chromosoma. 2006;115:376–382. PubMed

Kejnovsky E, et al. Expansion of microsatellites on evolutionary young Y chromosome. PLoS One. 2013;8:e45519. PubMed PMC

Kejnovsky E, Hawkins JS, Feschotte C. Plant transposable elements: biology and evolution. In: Wendel JF, Greilhuber J, Dolezel J, Leitch IJ, editors. Plant genome diversity. Volume 1: Plant genomes, their residents and their evolutionary dynamics. Wien: Springer; 2012. pp. 17–34.

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

Kejnovsky E, Leitch I, Leitch A. Contrasting evolutionary dynamics between angiosperm and mammalian genomes. Trends Ecol Evol. 2009;24:572–582. PubMed

Kent WJ. BLAT—the BLAST-like alignment tool. Genome Res. 2002;12:656–664. PubMed PMC

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

Lahn BT, Page DC. Four evolutionary strata on the human X chromosome. Nature. 1999;286:964–967. PubMed

Lengerova M, Vyskot B. Sex chromatin and nucleolar analysis in Rumex acetosa L. Protoplasma. 2001;217:147–153. PubMed

Llorens C, et al. The Gypsy Database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res. 2011;39(1 Suppl):D70–D74. PubMed PMC

Macas J, et al. Next generation sequencing-based analysis of repetitive DNA in the model dioceous plant Silene latifolia. PLoS One. 2011;6:e27335. PubMed PMC

Macas J, Neumann P, Novak P, Jiang J. Global sequence characterization of rice centromeric satellite based on oligomer frequency analysis in large-scale sequencing data. Bioinformatics. 2010;26:2101–2108. PubMed

Macas K, Meszaros T, Nouzova M. PlantSat: a specialized database for plant satellite repeats. Bioinformatics. 2002;18:28–35. PubMed

Mariotti B, et al. Cloning and characterization of dispersed repetitive DNA derived from microdissected sex chromosomes of Rumex acetosa. Genome. 2005;49:114–121. PubMed

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

McMillan D, et al. Characterizing the chromosomes of the platypus (Ornithorhynchus anatinus) Chromosome Res. 2007;15:961–974. PubMed

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

Navajas-Pérez R, et al. The evolution of reproductive systems and sex-determining mechanisms within Rumex (Polygonaceae) inferred from nuclear and chloroplastidial sequence data. Mol Biol Evol. 2005a;22:1929–1939. PubMed

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

Navajas-Pérez R, Quesada del Bosque ME, Garrido-Ramos MA. Effect of localization, organization, and repeat-copy number in satellite-DNA evolution. Mol Genet Genomics. 2009;282:395–406. PubMed

Navajas-Pérez R, et al. The origin and evolution of the variability in a Y-specific satellite-DNA of Rumex acetosa and its relatives. Gene. 2005c;368:61–71. PubMed

Neumann P, et al. Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mob DNA. 2011;2:4. PubMed PMC

Neumann P, Koblízková A, Navrátilová A, Macas J. Significant expansion of Vicia pannonica genome size mediated by amplification of a single type of giant retroelement. Genetics. 2006;173:1047–1056. PubMed PMC

Novak P, Neumann P, Macas J. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics. 2010;11(1):378–389. PubMed PMC

Pokorna M, Kratochvil L, Kejnovsky E. 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. 2011;12:90. PubMed PMC

Rice P, Longden I, Bleasby A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 2000;16:276–277. PubMed

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

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

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

Schiex T, Gouzy J, Moisan A, de Oliveira Y. FrameD: a flexible program for quality check and gene prediction in prokaryotic genomes and noisy matured eukaryotic sequences. Nucleic Acids Res. 2003;31:3738–3741. PubMed PMC

Skaletsky H, et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature. 2003;423:825–837. PubMed

Steinemann M, Steinemann S. Degenerating Y chromosome of Drosophila miranda: a trap for retrotransposons. Proc Natl Acad Sci U S A. 1992;89:7591–7595. PubMed PMC

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25:4876–4882. PubMed PMC

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

Xu Z, Wang H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007;35(Web Server issue):W265–W268. PubMed PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Detection and classification of long terminal repeat sequences in plant LTR-retrotransposons and their analysis using explainable machine learning

. 2024 Dec 18 ; 17 (1) : 57. [epub] 20241218

Sexy ways: approaches to studying plant sex chromosomes

. 2024 Sep 11 ; 75 (17) : 5204-5219.

X Chromosome-Specific Repeats in Non-Domestic Bovidae

. 2024 Jan 25 ; 15 (2) : . [epub] 20240125

Fundamentally different repetitive element composition of sex chromosomes in Rumex acetosa

. 2021 Jan 01 ; 127 (1) : 33-47.

Sex and the flower - developmental aspects of sex chromosome evolution

. 2018 Dec 31 ; 122 (7) : 1085-1101.

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

. 2018 Feb 20 ; 19 (1) : 153. [epub] 20180220

Impact of Repetitive Elements on the Y Chromosome Formation in Plants

. 2017 Nov 01 ; 8 (11) : . [epub] 20171101

Satellite DNA and Transposable Elements in Seabuckthorn (Hippophae rhamnoides), a Dioecious Plant with Small Y and Large X Chromosomes

. 2017 Jan 01 ; 9 (1) : 197-212.

Impact of repetitive DNA on sex chromosome evolution in plants

. 2015 Sep ; 23 (3) : 561-70.

Fully automated pipeline for detection of sex linked genes using RNA-Seq data

. 2015 Mar 11 ; 16 (1) : 78. [epub] 20150311

Zobrazit více v PubMed

GENBANK
KC310863, KC310864, KC310865, KC310866, KC310867, KC310868, KC310869, KC310870, KC310871, KC310872

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...