Comparative Dissection of Three Giant Genomes: Allium cepa, Allium sativum, and Allium ursinum

. 2019 Feb 09 ; 20 (3) : . [epub] 20190209

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30744119

Grantová podpora
SYMBIT reg. number: CZ.02.1.01/0.0/0.0/15_003/0000477 European Regional Development Fund
17-09644S Grantová Agentura České Republiky

Knowledge of the fascinating world of DNA repeats is continuously being enriched by newly identified elements and their hypothetical or well-established biological relevance. Genomic approaches can be used for comparative studies of major repeats in any group of genomes, regardless of their size and complexity. Such studies are particularly fruitful in large genomes, and useful mainly in crop plants where they provide a rich source of molecular markers or information on indispensable genomic components (e.g., telomeres, centromeres, or ribosomal RNA genes). Surprisingly, in Allium species, a comprehensive comparative study of repeats is lacking. Here we provide such a study of two economically important species, Allium cepa (onion), and A. sativum (garlic), and their distantly related A. ursinum (wild garlic). We present an overview and classification of major repeats in these species and have paid specific attention to sequence conservation and copy numbers of major representatives in each type of repeat, including retrotransposons, rDNA, or newly identified satellite sequences. Prevailing repeats in all three studied species belonged to Ty3/gypsy elements, however they significantly diverged and we did not detect them in common clusters in comparative analysis. Actually, only a low number of clusters was shared by all three species. Such conserved repeats were for example 5S and 45S rDNA genes and surprisingly a specific and quite rare Ty1/copia lineage. Species-specific long satellites were found mainly in A. cepa and A. sativum. We also show in situ localization of selected repeats that could potentially be applicable as chromosomal markers, e.g., in interspecific breeding.

Zobrazit více v PubMed

Li Q.Q., Zhou S.D., He X.J., Yu Y., Zhang Y.C., Wei X.Q. Phylogeny and biogeography of Allium (Amaryllidaceae: Allieae) based on nuclear ribosomal internal transcribed spacer and chloroplast rps16 sequences, focusing on the inclusion of species endemic to China. Ann. Bot. 2010;106:709–733. doi: 10.1093/aob/mcq177. PubMed DOI PMC

Bennett M.D., Smith J.B. Nuclear-DNA Amounts in Angiosperms. Philos. Trans. R. Soc. B. 1976;274:227–274. doi: 10.1098/rstb.1976.0044. PubMed DOI

Bennett M.D., Leitch I.J. Nuclear DNA amounts in angiosperms—583 new estimates. Ann. Bot. 1997;80:169–196. doi: 10.1006/anbo.1997.0415. DOI

Bennett M.D., Bhandol P., Leitch I.J. Nuclear DNA amounts in angiosperms and their modern uses—807 new estimates. Ann. Bot. 2000;86:859–909. doi: 10.1006/anbo.2000.1253. DOI

Novak P., Neumann P., Pech J., Steinhaisl J., Macas J. RepeatExplorer: A Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics. 2013;29:792–793. doi: 10.1093/bioinformatics/btt054. PubMed DOI

Novak P., Robledillo L.A., Koblizkova A., Vrbova I., Neumann P., Macas J. TAREAN: A computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Res. 2017;45:e111. doi: 10.1093/nar/gkx257. PubMed DOI PMC

Peska V., Sitova Z., Fajkus P., Fajkus J. BAL31-NGS approach for identification of telomeres de novo in large genomes. Methods. 2017;114:16–27. doi: 10.1016/j.ymeth.2016.08.017. PubMed DOI

Saladino R., Sponer J.E., Sponer J., Di Mauro E. Rewarming the Primordial Soup: Revisitations and Rediscoveries in Prebiotic Chemistry. ChemBioChem. 2018;19:22–25. doi: 10.1002/cbic.201700534. PubMed DOI PMC

Srivastava A.K., Schlessinger D. Structure and Organization of Ribosomal DNA. Biochimie. 1991;73:631–638. doi: 10.1016/0300-9084(91)90042-Y. PubMed DOI

Kawai H., Nakayama T., Inouye I., Kato A. Linkage of 5S ribosomal DNA to other rDNAs in the chromophytic algae and related taxa. J. Phycol. 1997;33:505–511. doi: 10.1111/j.0022-3646.1997.00505.x. DOI

Sone T., Fujisawa M., Takenaka M., Nakagawa S., Yamaoka S., Sakaida M., Nishiyama R., Yamato K.T., Ohmido N., Fukui K., et al. Bryophyte 5S rDNA was inserted into 45S rDNA repeat units after the divergence from higher land plants. Plant Mol. Biol. 1999;41:679–685. doi: 10.1023/A:1006398419556. PubMed DOI

Garcia S., Lim K.Y., Chester M., Garnatje T., Pellicer J., Valles J., Leitch A.R., Kovarik A. Linkage of 35S and 5S rRNA genes in Artemisia (family Asteraceae): First evidence from angiosperms. Chromosoma. 2009;118:85–97. doi: 10.1007/s00412-008-0179-z. PubMed DOI

Garcia S., Kovarik A. Dancing together and separate again: Gymnosperms exhibit frequent changes of fundamental 5S and 35S rRNA gene (rDNA) organisation. Heredity. 2013;111:23–33. doi: 10.1038/hdy.2013.11. PubMed DOI PMC

Garcia S., Galvez F., Gras A., Kovarik A., Garnatje T. Plant rDNA database: Update and new features. Database J. Biol. Databases Curation. 2014;2014:bau063. doi: 10.1093/database/bau063. PubMed DOI PMC

Rosato M., Alvarez I., Feliner G.N., Rossello J.A. High and uneven levels of 45S rDNA site-number variation across wild populations of a diploid plant genus (Anacyclus, Asteraceae) PLoS ONE. 2017;12 doi: 10.1371/journal.pone.0187131. PubMed DOI PMC

Fajkus P., Peska V., Sitova Z., Fulneckova J., Dvorackova M., Gogela R., Sykorova E., Hapala J., Fajkus J. Allium telomeres unmasked: The unusual telomeric sequence (CTCGGTTATGGG)(n) is synthesized by telomerase. Plant J. 2016;85:337–347. doi: 10.1111/tpj.13115. PubMed DOI

Ricroch A., Peffley E.B., Baker R.J. Chromosomal location of rDNA in Allium: In situ hybridization using biotin- and fluorescein-labelled probe. Theor. Appl. Genet. 1992;83:413–418. doi: 10.1007/BF00226528. PubMed DOI

Hizume M. Allodiploid Nature of Allium-Wakegi Araki Revealed by Genomic in-Situ Hybridization and Localization of 5s and 18s Rdnas. Jpn. J. Genet. 1994;69:407–415. doi: 10.1266/jjg.69.407. PubMed DOI

Do G.S., Seo B.B. Phyiogenetic relationships among allium subg. rhizirideum species based on the molecular variation of 5S rRNA genes. Korean J. Biol. Sci. 2000;4:77–85. doi: 10.1080/12265071.2000.9647527. DOI

Lee S.H., Do G.S., Seo B.B. Chromosomal localization of 5S rRNA gene loci and the implications for relationships within the Allium complex. Chromosom. Res. 1999;7:89–93. doi: 10.1023/A:1009222411001. PubMed DOI

Neumann P., Navratilova A., Schroeder-Reiter E., Koblizkova A., Steinbauerova V., Chocholova E., Novak P., Wanner G., Macas J. Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains. PLoS Genet. 2012;8 doi: 10.1371/journal.pgen.1002777. PubMed DOI PMC

Nagaki K., Yamamoto M., Yamaji N., Mukai Y., Murata M. Chromosome dynamics visualized with an anti-centromeric histone H3 antibody in Allium. PLoS ONE. 2012;7:e51315. doi: 10.1371/journal.pone.0051315. PubMed DOI PMC

Barnes S.R., James A.M., Jamieson G. The Organization, Nucleotide-Sequence, and Chromosomal Distribution of a Satellite DNA from Allium-Cepa. Chromosoma. 1985;92:185–192. doi: 10.1007/BF00348692. DOI

Do G.S., Seo B.B., Yamamoto M., Suzuki G., Mukai Y. Identification and chromosomal location of tandemly repeated DNA sequences in Allium cepa. Genes Genet. Syst. 2001;76:53–60. doi: 10.1266/ggs.76.53. PubMed DOI

Pich U., Fritsch R., Schubert I. Closely related Allium species (Alliaceae) share a very similar satellite sequence. Plant Syst. Evol. 1996;202:255–264. doi: 10.1007/BF00983386. DOI

Irifune K., Hirai K., Zheng J., Tanaka R., Morikawa H. Nucleotide-Sequence of a Highly Repeated DNA-Sequence and Its Chromosomal Localization in Allium-Fistulosum. Theor. Appl. Genet. 1995;90:312–316. doi: 10.1007/BF00221970. PubMed DOI

Fesenko I.A., Khrustaleva L.I., Karlov G.I. Organization of the 378-bp satellite repeat in terminal heterochromatin of Allium fistulosum. Russ. J. Genet. 2002;38:745–753. doi: 10.1023/A:1016379319030. PubMed DOI

Kirov I.V., Kiseleva A.V., Van Laere K., Van Roy N., Khrustaleva L.I. Tandem repeats of Allium fistulosum associated with major chromosomal landmarks. Mol. Genet. Genom. 2017;292:453–464. doi: 10.1007/s00438-016-1286-9. PubMed DOI

Pearce S.R., Pich U., Harrison G., Flavell A.J., HeslopHarrison J.S.P., Schubert I., Kumar A. The Ty1-copia group retrotransposons of Allium cepa are distributed throughout the chromosomes but are enriched in the terminal heterochromatin. Chromosom. Res. 1996;4:357–364. doi: 10.1007/BF02257271. PubMed DOI

Pich U., Schubert I. Terminal heterochromatin and alternative telomeric sequences in Allium cepa. Chromosom. Res. 1998;6:315–321. doi: 10.1023/A:1009227009121. PubMed DOI

Kiseleva A.V., Kirov I.V., Khrustaleva L.I. Chromosomal organization of centromeric Ty3/gypsy retrotransposons in Allium cepa L. and Allium fistulosum L. Genetika. 2014;50:670–676. doi: 10.1134/S102279541404005X. PubMed DOI

Sykorova E., Fajkus J., Meznikova M., Lim K.Y., Neplechova K., Blattner F.R., Chase M.W., Leitch A.R. Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am. J. Bot. 2006;93:814–823. doi: 10.3732/ajb.93.6.814. PubMed DOI

Sykorova E., Lim K.Y., Kunicka Z., Chase M.W., Bennett M.D., Fajkus J., Leitch A.R. Telomere variability in the monocotyledonous plant order Asparagales. Proc. R. Soc. B-Biol. Sci. 2003;270:1893–1904. doi: 10.1098/rspb.2003.2446. PubMed DOI PMC

Witte C.P., Le Q.H., Bureau T., Kumar A. Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc. Natl. Acad. Sci. USA. 2001;98:13778–13783. doi: 10.1073/pnas.241341898. PubMed DOI PMC

Hertweck K.L. Assembly and comparative analysis of transposable elements from low coverage genomic sequence data in Asparagales. Genome. 2013;56:487–494. doi: 10.1139/gen-2013-0042. PubMed DOI

Benson G. Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Res. 1999;27:573–580. doi: 10.1093/nar/27.2.573. PubMed DOI PMC

Fajkus J., Kovarik A., Kralovics R., Bezdek M. Organization of Telomeric and Subtelomeric Chromatin in the Higher-Plant Nicotiana-Tabacum. Mol. Gen. Genet. 1995;247:633–638. doi: 10.1007/BF00290355. PubMed DOI

Kovarik A., Fajkus J., Koukalova B., Bezdek M. Species-specific evolution of telomeric and rDNA repeats in the tobacco composite genome. Theor. Appl. Genet. 1996;92:1108–1111. doi: 10.1007/BF00224057. PubMed DOI

Maillet G., White C.I., Gallego M.E. Telomere-length regulation in inter-ecotype crosses of Arabidopsis. Plant Mol. Biol. 2006;62:859–866. doi: 10.1007/s11103-006-9061-7. PubMed DOI

Shakirov E.V., Shippen D.E. Length regulation and dynamics of individual telomere tracts in wild-type Arabidopsis. Plant Cell. 2004;16:1959–1967. doi: 10.1105/tpc.104.023093. PubMed DOI PMC

Kelly L.J., Renny-Byfield S., Pellicer J., Macas J., Novak P., Neumann P., Lysak M.A., Day P.D., Berger M., Fay M.F., et al. Analysis of the giant genomes of Fritillaria (Liliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size. New Phytol. 2015;208:596–607. doi: 10.1111/nph.13471. PubMed DOI PMC

Ambrozova K., Macas J., Neumann P., Leitch I.J., Lysak M.A. Molecular and cytogenetic analysis of the giant genomes of Fritillaria lilies. Chromosom. Res. 2009;17:558–559.

Chester M., Sykorova E., Fajkus J., Leitch A.R. Single Integration and Spread of a Copia-Like Sequence Nested in rDNA Intergenic Spacers of Allium cernuum (Alliaceae) Cytogenet. Genome Res. 2010;129:35–46. doi: 10.1159/000312959. PubMed DOI

Babraham Bioinformatics, FastQC. [(accessed on 10 November 2018)]; Available online: https://www.bioinformatics.babraham.ac.uk/projects/fastqc/

Singh R., Ming R., Yu Q.Y. Comparative Analysis of GC Content Variations in Plant Genomes. Trop. Plant Biol. 2016;9:136–149. doi: 10.1007/s12042-016-9165-4. DOI

Smarda P., Bures P., Smerda J., Horova L. Measurements of genomic GC content in plant genomes with flow cytometry: A test for reliability. New Phytol. 2012;193:513–521. doi: 10.1111/j.1469-8137.2011.03942.x. PubMed DOI

Ricroch A., Brown S.C. DNA base composition of Allium genomes with different chromosome numbers. Gene. 1997;205:255–260. doi: 10.1016/S0378-1119(97)00395-8. PubMed DOI

Dolezel J., Bartos J., Voglmayr H., Greilhuber J. Nuclear DNA content and genome size of trout and human. Cytom. Part A J. Int. Soc. Anal. Cytol. 2003;51:127–128. PubMed

Dellaporta S.L., Wood J., Hicks J.B. A plant DNA minipreparation: Version II. Plant Mol. Biol. Rep. 1983;1:19–21. doi: 10.1007/BF02712670. DOI

Peska V., Fajkus P., Fojtova M., Dvorackova M., Hapala J., Dvoracek V., Polanska P., Leitch A.R., Sykorova E., Fajkus J. Characterisation of an unusual telomere motif (TTTTTTAGGG)(n) in the plant Cestrum elegans (Solanaceae), a species with a large genome. Plant J. 2015;82:644–654. doi: 10.1111/tpj.12839. PubMed DOI

RepeatExplorer-GALAXY, Repeat de novo Assembly. [(accessed on 10 November 2018)]; Available online: https://galaxy-elixir.cerit-sc.cz/galaxy/

Mandáková T., Lysak M.A. Painting of Arabidopsis Chromosomes with Chromosome-Specific BAC Clones. Curr. Protoc. Plant Biol. 2017;1:359–371. PubMed

Mandáková T., Lysak M.A. Chromosome Preparation for Cytogenetic Analyses in Arabidopsis. Curr. Protoc. Plant Biol. 2016;1:43–51. PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...