Seabuckthorn (Hippophae rhamnoides) is a dioecious shrub commonly used in the pharmaceutical, cosmetic, and environmental industry as a source of oil, minerals and vitamins. In this study, we analyzed the transposable elements and satellites in its genome. We carried out Illumina DNA sequencing and reconstructed the main repetitive DNA sequences. For data analysis, we developed a new bioinformatics approach for advanced satellite DNA analysis and showed that about 25% of the genome consists of satellite DNA and about 24% is formed of transposable elements, dominated by Ty3/Gypsy and Ty1/Copia LTR retrotransposons. FISH mapping revealed X chromosome-accumulated, Y chromosome-specific or both sex chromosomes-accumulated satellites but most satellites were found on autosomes. Transposable elements were located mostly in the subtelomeres of all chromosomes. The 5S rDNA and 45S rDNA were localized on one autosomal locus each. Although we demonstrated the small size of the Y chromosome of the seabuckthorn and accumulated satellite DNA there, we were unable to estimate the age and extent of the Y chromosome degeneration. Analysis of dioecious relatives such as Shepherdia would shed more light on the evolution of these sex chromosomes.

All Russia Research Institute of Agricultural Biotechnology Moscow Russia

Centre for Molecular Biotechnology Russian State Agrarian University Moscow Timiryazev Agricultural Academy Moscow Russia

Department of Information Systems Faculty of Information Technology Brno University of Technology Brno Czech Republic

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

Institute of Experimental Botany Center of the Region Haná for Biotechnological and Agricultural Research Olomouc Czech Republic

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Alexandrov OS, Divashuk MG, Yakovin NA, Karlov GI. 2012. Sex chromosome differentiation in Humulus japonicus Siebold & Zuccarini, 1846 (Cannabaceae) revealed by fluorescence in situ hybridization of subtelomeric repeat. Comp Cytogenet. 47:239–247. PubMed PMC

Alexandrov OS, Karlov GI. 2016. Molecular cytogenetic analysis and genomic organization of major DNA repeats in castor bean (Ricinus communis L.). Mol Genet Genomics 291:775–787. PubMed

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403–410. PubMed

Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. 2009. GenBank. Nucleic Acids Res. 38:D46–D51. PubMed PMC

Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. PubMed PMC

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

Campell BR, Song Y, Posch TE, Cullis CA, Town CD. 1992. Sequence and organization of 5S ribosomal RNA-encoding genes of Arabidopsis thaliana. Gene 112:225–228. PubMed

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

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

Charlesworth D. 2016. Plant sex chromosomes. Annu Rev Plant Biol. 67:397–420. PubMed

Chen L, Yu Z, Jin H. 2010. Comparison of ribosomal DNA ITS regions among Hippophae rhamnoides ssp. sinensis from different geographical area in China. Plant Mol Biol Rep. 28:635–645.

Crooks G, Hon G, Chandonia J, Brenner S. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188–1190. PubMed PMC

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

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. PubMed PMC

Doležel J, Bartoš J, Voglmayr H, Greilhuber J. 2003. Nuclear DNA content and genome size of trout and human. Cytom Part A 51:127–128. PubMed

Doyle JJ, Doyle JL. 1990. Isolation of plant DNA from fresh tissue. Focus 12:13–15.

Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797. PubMed PMC

Fruchterman TMJ, Reingold EM. 1991. Graph drawing by force-directed placement. Softw Pract Exp. 21:1129–1164.

Ghangal R, Chaudhary S, Jain M, Purty RS, Sharma PC. 2013. Optimization of de novo short read assembly of seabuckthorn (Hippophae rhamnoides L.) transcriptome. PLoS One 8:e72516. PubMed PMC

Gerlach WL, Bedbrook JR. 1979. Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res. 7:1869–1885. PubMed PMC

Hobza R, Lengerova M, Cernohorska H, Rubes J, Vyskot B. 2004. FAST-FISH with laser beam microdissected DOP-PCR probe distinguishes the sex chromosomes of Silene latifolia . Chromosome Res. 12:245–250. PubMed

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

Hobza R, et al. 2015. Impact of repetitive DNA on sex chromosome evolution in plants. Chromosome Res. 23:561–570. PubMed

Hough J, Hollister JD, Wang W, Barrett SCH, Wright SI. 2014. Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus . Proc Natl Acad Sci U S A. 111:7713–7718. PubMed PMC

Kearse M, et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. PubMed PMC

Karlov GI, Danilova TV, Horlemann C, Weber G. 2003. Molecular cytogenetic in hop (Humulus lupulus L.) and identification of sex chromosomes by DAPI banding. Euphytica 132:185–190.

Kejnovsky E, et al. 2006. Retand: A novel family of gypsy-like retrotransposon harboring an amplified tandem repeat. Mol Genet Genomics 276:254–263. PubMed

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. PubMed

Kejnovsky E, Vyskot B. 2010. Silene latifolia: the classical model to study heteromorphic sex chromosomes. Cytogenet Genome Res. 129:250–262. PubMed

Kirov I, Divashuk M, Van Laere K, Soloviev A, Khrustaleva L. 2014. An easy “SteamDrop” method for high quality plant chromosome preparation. Mol Cytogenet. 7:21. PubMed PMC

Kubat Z, et al. 2014. Possible mechanisms responsible for absence of retrotransposon family on a plant Y chromosome. New Phytol. 202:662–678. PubMed

Langmead B, Salzberg S. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. PubMed PMC

Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv 1303.3997.

Li SF, Zhang GJ, Yuan JH, Deng CL, Gao WJ. 2016a. Repetitive sequences and epigenetic modification: inseparable partners play important roles in the evolution of plant sex chromosomes. Planta 243:1083–1095. PubMed

Li SF, et al. 2016b. DPTEdb, an integrative database of transposable elements in dioecious plants. Database 2016:1–10. PubMed PMC

Lim KY, et al. 2007. Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol. 175:756–763. PubMed

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

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

Macas J, et al. 2015. In depth characterization of repetitive DNA in 23 plant genomes reveals sources of genome size variation in the legume tribe fabeae. PLoS One 10:e0143424. PubMed PMC

Marchler-Bauer A, et al. 2015. CDD: NCBI's conserved domain database. Nucleic Acids Res. 43:222–226. PubMed PMC

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. PubMed

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

Miller JT, Dong F, Jackson SA, Song J, Jiang J. 1998. Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics 150:1615–1623. PubMed PMC

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

Navajas-Perez 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

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

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

Novak P, Neumann P, Pech J, Steinhaisl J, Macas J. 2013. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29:792–793. PubMed

Rousi A, Arohonka T. 1980. C-band and ploidy level of Hippophae rhamnoides . Hereditas 92:327–330.

Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 4:406–425. PubMed

Segawa M, Kishi S, Tatuno S. 1971. Sex chromosomes of Cycas revoluta . Jpn J Genet. 46:33–39.

Sharma A, Zinta G, Rana S, Shirko P. 2010. Molecular identification of sex in Hippophae rhamnoides L. using isozyme and RAPD markers. For Stud China 12:62–66.

Shchapov NS. 1979. On the karyology of Hippophaë rhamnoides L. Tsitol Genet. 13:45–47.

Shephard HL, Parker JS, Darby P, Ainsworth CC. 2000. Sexual development and sex chromosomes in hop. New Phytol. 148:397–411. PubMed

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. PubMed

Souza A, Bellot S, Fuchs J, Houben A, Renner SS. 2016. Analysis of transposable elements and organellar DNA in male and female genomes of a species with a huge Y-chromosome reveals distinct Y-centromeres. Plant J. 88:387–396. PubMed

Steflova P, 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. PubMed PMC

Truta E, et al. 2011. Morphometric pattern of somatic chromosomes in three Romanian seabuckthorn genotypes. Caryologia 64:189–196.

Untergasser A, et al. 2012. Primer3–new capabilities and interfaces. Nucleic Acids Res. 40:1–12. PubMed PMC

Veldkamp JF. 1986. Elaeagnaceae In: Van Steenis CGGJ, de Wilde WJJO, editors . Flora Malesiana 10 (2), Martinus Nijhoff. Boston, London: The Hague, p. 151–156.

Wicker T, Matthews DE, Keller B. 2002. TREP: A database for Triticeae repetitive elements. Trends Plant Sci. 7:561–562.

Yamato KT, et al. 2007. Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proc Natl Acad Sci U S A. 104:6472–6477. PubMed PMC

Zhang X, Wessler SR. 2004. Genome-wide comparative analysis of the transposable elements in the related species Arabidopsis thaliana and Brassica oleracea . Proc Natl Acad Sci U S A. 101:5589–5594. PubMed PMC

Zhou X, et al. 2010. Genome size of the diploid hybrid species Hippophae goniocarpa and its parental species, H. rhamnoides ssp. sinensis and H. neurocarpa ssp. neurocarpa (Elaeagnaceae). Acta Biol Cracoviensia Ser Bot. 52:12–16.

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