Abstract
Tandem repeats are often associated with important chromosomal landmarks, such as centromeres, telomeres, subtelomeric, and other heterochromatic regions, and can be good candidates for molecular cytogenetic markers. Tandem repeats present in many plant species demonstrate dramatic differences in unit length, proportion in the genome, and chromosomal organization. Members of genus Allium with their large genomes represent a challenging task for current genetics. Using the next generation sequencing data, molecular, and cytogenetic methods, we discovered two tandemly organized repeats in the Allium fistulosum genome (2n = 2C = 16), HAT58 and CAT36. Together, these repeats comprise 0.25% of the bunching onion genome with 160,000 copies/1 C of HAT58 and 93,000 copies/1 C of CAT36. Fluorescent in situ hybridization (FISH) and C-banding showed that HAT58 and CAT36 associated with the interstitial and pericentromeric heterochromatin of the A. fistulosum chromosomes 5, 6, 7, and 8. FISH with HAT58 and CAT36 performed on A. cepa (2n = 2C = 16) and A. wakegi (2n = 2C = 16), a natural allodiploid hybrid between A. fistulosum and A. cepa, revealed that these repeats are species specific and produced specific hybridization patterns only on A. fistulosum chromosomes. Thus, the markers can be used in interspecific breeding programs for monitoring of alien genetic material. We applied Non-denaturing FISH that allowed detection of the repeat bearing chromosomes within 3 h. A polymorphism of the HAT58 chromosome location was observed. This finding suggests that the rapid evolution of the HAT58 repeat is still ongoing.
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Abbreviations
- FISH:
-
Fluorescence in situ hybridization
- ND-FISH:
-
Non-denaturing Fluorescence in situ hybridization
- TRs:
-
Tandem repeats
- TAMRA:
-
6-Carboxytetramethylrhodamine
- DAPI:
-
4,6-Diamidino-2-phenylindole
- PMCs:
-
Pollen mother cells
References
Albert PS, Gao Z, Danilova TV, Birchler JA (2010) Diversity of chromosomal karyotypes in maize and its relatives. Cytogenet Genome Res 129(1–3):6–16. doi:10.1159/000314342
Albini SM, Jones GH (1990) Synaptonemal complex spreading in Allium cepa and Allium fistulosum. III. The F1 hybrid. Genome 38:854–866. doi:10.1139/g90-129
Alkhimova OG, Mazurok NA, Potapova TA, Zakian SM, Heslop-Harrison JS, Vershinin AV (2004) Diverse patterns of the tandem repeats organization in rye chromosomes. Chromosoma 113(1):42–52. doi:10.1007/s00412-004-0294-4
Ananiev EV, Phillips RL, Rines HW (1998) Chromosome specific molecular organization of maize (Zea mays L.) centromeric regions. Proc Natl Acad Sci USA 95(22):13073–13078. doi:10.1073/pnas.95.22.13073
Barnes SR, James AM, Jamiesson G (1985) The organization, nucleotide sequence, and chromosomal distribution of a satellite DNA from A. cepa. Chromosoma 92:185–192. doi:10.1007/BF00348692
Barros A, Guerra S (2010) The meaning of DAPI bands observed after C-banding and FISH procedures. Biotech Histochem 85(2):115–125. doi:10.3109/10520290903149596
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucl Acids Res 27(2):573–580
Blackburn EH (2001) Switching and signaling at the telomere. Cell 106(6):661–673. doi:10.1016/S0092-8674(01)00492-5
Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371(6494):215–220. doi:10.1038/371215a0
Cohen S, Houben A, Segal D (2008) Extrachromosomal circular DNA derived from tandemly repeated genomic sequences in plants. Plant J 53(6):1027–1034. doi:10.1111/j.1365-313X.2007.03394.x
Cohen AL, Jia S (2014) Noncoding RNAs and the borders of heterochromatin. Wiley Interdiscip Rev RNA 5(6):835–847. doi:10.1002/wrna.1249
Cuadrado A, Jouve N (2010) Chromosomal detection of simple sequence repeats (SSRs) using nondenaturing FISH (ND-FISH). Chromosoma 119(5):495–503. doi:10.1007/s00412-010-0273-x
de Vries JN and MC Jongerius (1988) Interstitial C-bands on the chromosomes of Allium-species from section Cepa. In: Proc. 4th Eucarpia Allium Symp, pp 71–78
Do GS, Seo BB, Yamamoto M, SuzukiG, Mukai Y (2001) Identification and chromosomal location of tandemly repeated DNA sequences in Allium cepa. Genes Genet Syst 76:53–60
Emadzade K, Jang TS, Macas J, Kovařík A, Novák P, Parker J, Weiss-Schneeweiss H (2014) Differential amplification of satellite PaB6 in chromosomally hypervariable Prospero autumnale complex (Hyacinthaceae). Ann Bot 114:1597–1608. doi:10.1093/aob/mcu178
Fajkus P, Peška V, Sitová Z et al (2016) Allium telomeres unmasked: the unusual telomeric sequence (CTCGGTTATGGG) n is synthesized by telomerase. Plant J 85 (3): 337–347. doi:10.1111/tpj.13115
Ferree PM, Barbash DA (2009) Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol 7(10):e1000234. doi:10.1371/journal.pbio.1000234
Fesenko IA, Khrustaleva LI, Karlov GI (2002) Organization of the 378 bp satellite repeat in terminal heterochromatin of Allium fistulosum. Rus J Genet 38(7):745–753. doi:10.1023/A:1016379319030
Fransz PF, de Jong JH (2002) Chromatin dynamics in plants. Curr Opin Plant Biol 5(6):560–567. doi:10.1016/S1369-5266(02)00298-4
Friesen N, Fritsch RM, Blattner FR (2006) Phylogeny and new intrageneric classification of Allium (Alliaceae) based on nuclear ribosomal DNA ITS sequences. Aliso 22:372–395
Garrido-Ramos MA (2015) Satellite DNA in plants: more than just rubbish. Cytogenet Genome Res 146:153–170. doi:10.1159/000437008
Grabowska-Joachimiak A, Mosiolek M, Lech A, Gуralski 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. doi:10.1159/000321584
Grewal SI, Moazed D (2003) Heterochromatin and epigenetic control of gene expression. Science 8:301(5634):798–802. doi:10.1126/science.1086887
He Q, Cai Z, Hu T et al (2015) Repetitive sequence analysis and karyotypingreveals centromere-associated DNA sequences in radish (Raphanussativus L.). BMC Plant Biol 15:105. doi:10.1186/s12870-015-0480-y
Hemleben V, Kovarik A, Torres-Ruiz RA, Volkov RA, Beridze T (2007) Plant highly repeated satellite DNA: molecular evolution, distribution, and use for identification of hybrids. Syst Biodivers 5 (3): 277–289. doi:10.1017/S147720000700240X
Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293(5532):1098–1102. doi:10.1126/science.1062939
Hizume M (1994) Allodiploid nature of Allium wakegi Araki revealed by genomic in situ hybridization and localization of 5S and 18S rDNAs. Jpn J Genet 69(4):407–415. doi:10.1266/jjg.69.407
Holoch D, Moazed D (2015) RNA-mediated epigenetic regulation of gene expression. Nat Rev Genet 16(2):71–84. doi:10.1038/nrg3863
Inada I, Endo M (1994) C-banded karyotype analysis of Allium fistulosum and A. altaicum and their phylogenetic relationship. J Jpn Soc Hortic Sci 63(3):593–602
Inden H, Asahira T (1990) Japanese bunching onion (Allium fistulosum L.). In: Brewster JL, Rabinowitch HD (eds) Onions and allied crops, vol III. Biochemistry, food science, and minor crops, pp 159–178. CRC Press, Boca Raton
Irifune K, Hirai K, Zheng J, Tanaka R, Morikawa H (1995) Nucleotide sequences of a highly repeated DNA sequences and its chromosomal localization in Allium fistulosum. Theor Appl Genet 90(3–4):312–316. doi:10.1007/BF00221970
Iwasa S (1964) Cytogenetic studies in the Wakegi, Allium fistulosum var. caespitosum. J Fac Agric Kyushu Univ 13(1):165–177
Jiang J, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8(12):570–575. doi:10.1016/j.tplants.2003.10.011
Jones RN, Rees H (1968) Nuclear DNA variation in Allium. Heredity 23:591–605
Khrustaleva L, Kik C (2000) Introgression of A. fistulosum into A. cepa mediated by A. roylei. Theor Appl Genet 100:17–26. doi:10.1007/s001220050003
Khrustaleva L, Kik C (2001) Localization of single copy T-DNA insertion in transgenic shallots (Allium cepa L.) by using ultra-sensitive FISH with tyramide signal amplification. Plant J 25:699–707. doi:10.1046/j.1365-313x.2001.00995.x
Kim S, Park JY, Yang TJ (2014) Characterization of three active transposable elements recently inserted in three independent DFR-A alleles and one high-copy DNA transposon isolated from the Pink allele of the ANS gene in onion (Allium cepa L. Mol Genet Genom 290(3):1027–1037. doi:10.1007/s00438-014-0973-7
King JJ, Bradeen JM, Bark O, McCallum JA, Havey MJ (1998) A low-density genetic map of onion reveals a role for tandem duplication in the evolution of an extremely large diploid genome. Theor Appl Genet 96(1):52–62. doi:10.1007/s001220050708
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(1):21. doi:10.1186/1755-8166-7-21
Kiseleva AV, Kirov IV, Khrustaleva LI (2014) Chromosomal organization of centromeric Ty3/gypsy retrotransposons in Allium cepa L. and Allium fistulosum L. Rus. J Genet 50(6):586–592. doi:10.1134/S102279541404005X
Komuro S, Endo R, Shikata K, Kato A (2013) Genomic and chromosomal distribution patterns of various repeated DNA sequences in wheat (Triticum aestivum L.) revealed by a fluorescence in situ hybridization procedure. Genome 56(3):131–137. doi:10.1139/gen-2013-0003
Koo D-H, Hong CP, Batley J, Chung YS, Edwards D, Bang J-W, Hur Y, Lim YP (2011) Rapid divergence of repetitive DNAs in Brassica relatives. Genomics 97(3):173–185. doi:10.1016/j.ygeno.2010.12.002
Lai Z, Nakazato T, Salmaso M, Burk JM, Tang S, Knapp SJ, Reiseberg LH (2005) Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171:291–303. doi:10.1534/genetics.105.042242
Lawrence GJ, Appels R (1986) Mapping the nucleolar organizer region, seed protein loci and isozyme loci on chromosome 1R in rye. Theor Appl Genet 71:742–749
Li Q-Q, Zhou S-D, He X-J, Yu Y, Zhang Y-C, Wei X-Q (2010) Phylogeny and biogeography of Allium (Amarylidaceae: Alliaceae) based on nucleolar ribosomal internal transcribed spacer and chloroplast rps16, focusing on the inclusion of species endemic to China. Ann Bot 106:709–733. doi:10.1093/aob/mcq177
Macas J, Kejnovský E, Neumann P, Novák P, Koblížková A, Vyskot B (2011) Next generation sequencing-based analysis of repetitive DNA in the model dioecious plant Silenelatifolia. PLoS One 6(11):e27335. doi:10.1371/journal.pone.0027335
McClintock B (1951) Chromosome organization and genic expression. In: Cold Spring Harb Symp Quant Biol, vol 16, pp 13–47
Mehrotra S, Goyal V (2014) Repetitive sequences in plant nuclear DNA: types, distribution, evolution and function. Genom Proteom Bioinform 12(4):164–171. doi:10.1016/j.gpb.2014.07.003
Nagaki K, Yamamoto M, Yamaji N, Mukai Y, Murata M (2012) Chromosome dynamics visualized with an anti-centromeric histone H3 antibody in allium. PLoS One 7(12):e51315. doi:10.1371/journal.pone.0051315
Neumann P, Navratilova A, KoblizkovaA et al. (2011) Plant centromericretrotransposons: a structural and cytogenetic perspective. Mobile DNA 2:4. doi:10.1186/1759-8753-2-4
Novák P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform 11:378. doi:10.1186/1471-2105-11-378
Novák 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(6):792–793. doi:10.1093/bioinformatics/btt054
Ohri D (1998) Genome size variation and plant systematics. Ann Bot 82:75–83
Oliveira RA, Kotadia S, Tavares A et al. (2014) Centromere-independent accumulation of cohesin at ectopic heterochromatin sites induces chromosome stretching during anaphase. PLoS Biol 12(10):e1001962. doi:10.1371/journal.pbio.1001962
Pearce SR, Pich U, Harrison G, Flavell AJ, Heslop-Harrison JS, Schubert I, Kumar A (1996) The Ty1-copia group retrotransposons of Allium cepa are distributed throughout the chromosomes but are enriched in the terminal heterochromatin. Chromosome Res 4(5):357–364. doi:10.1007/BF02257271
Pich U, Fritsch R, Shubert I (1996) Closely related Allium species (Alliaceae) share a very similar satellite sequence. Plant Syst Evol 202:255–264
Reeves A, Tear J (2000) MicroMeasure for Windows. Version 3.3. http://www.colostate.edu/Depts/Biology/MicroMeasure. Accessed 25 May 2016
Reinhart BJ, Bartel DP (2002) Small RNAs correspond to centromere heterochromatic repeats. Science 297(5588):1831. doi:10.1126/science.1077183
Renny-Byfield S, Kovařík A, Chester M, Nichols RA, Macas J, Novák P, Leitch AR (2012) Independent, rapid and targeted loss of highly repetitive dna in natural and synthetic allopolyploids of Nicotiana. PLoS One 7(5):e36963. doi:10.1371/journal.pone.0036963
Ricroch A, Yockteng R, Brown SC, Nadot S (2005) Evolution of genome size across some cultivated Allium species. Genome 48(3):511–520. doi:10.1139/g05-017
Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5(2):69–76. doi:10.1007/BF00020088
Schmidt T, Heslop-Harrison JS (1993) Variability and evolution of highly repeated DNA sequences in the genus Beta. Genome 36(6):1074–1079. doi:10.1139/g93-142
Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large-scale organization of plant chromosomes. Trends Plant Sci 3(5):195–199. doi:10.1016/S1360-1385(98)01223-0
Seo BB, Do GS, Lee SH (1999) Identification of a tandemly repeated DNA sequence using combined RAPD and FISH in welsh onion (Allium fistulosum). Kor J Biol Sci 3(1): 69–72. doi:10.1080/12265071.1999.9647467
Sharma S, Raina SN (2005) Organization and evolution of highly repeated satellite DNA sequences in plant chromosomes. Cytogenet Genome Res 109(1–3):15–26. doi:10.1159/000082377
Shibata F, Hizume M (2002) The identification and analysis of the sequences that allow the detection of Allium cepa chromosomes by GISH in the allodiploid A. wakegi. Chromosoma 111(3):184–191. doi:10.1007/s00412-002-0197-1
Tashiro Y (1980) Cytogenetic studies on the origin in Allium wakegi Araki and the interspecific hybrid between A. fistulosum L. and A. ascalonicum L. Bull Fac Agric Saga Univ 49:47–57
Tashiro Y (1984) Genome analysis of Allium wakegi Araki. J Jpn Soc Hort Sci 52:399–407
Treangen TJ, Salzberg SL (2011) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 13(1):36–46. doi:10.1038/nrg3117
Verstrepen KJ, Jansen A, Lewitter F, Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37(9):986–990. doi:10.1038/ng1618
Vitte C, Estep MC, Leebens-Mack J, Bennetzen JL (2013) Young, intact and nested retrotransposons are abundant in the onion and asparagus genomes. Ann Bot 112(5):881–889. doi:10.1093/aob/mct155
Wallrath LL (1998) Unfolding the mysteries of heterochromatin. Curr Opin Genet Dev 8(2):147–153. doi:10.1016/S0959-437X(98)80135-4
Wang C, Liu C, Roqueiro D, Grimm D, Schwab R, Becker C, Lanz C, Weigel D (2014) Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res 25:246–256. doi:10.1101/gr.170332.113
Zhang H, Koblížková A, Wang K et al (2014) Boom-bust turnovers of megabase-sized centromeric DNA in Solanum species: rapid evolution of DNA sequences associated with centromeres. Plant Cell 26(4):1436–1447. doi:10.1105/tpc.114.123877
Acknowledgements
We are grateful to Ruth Newman for correction of English in this paper. We thank our students Nataliya Kudryavtseva, Pavel Kornienkov, and Sergey Odintsov for technical assistance. This study was financially supported by a research Grant No. 16-16-10031 from the Russian Science Foundation.
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Kirov, I.V., Kiseleva, A.V., Van Laere, K. et al. Tandem repeats of Allium fistulosum associated with major chromosomal landmarks. Mol Genet Genomics 292, 453–464 (2017). https://doi.org/10.1007/s00438-016-1286-9
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DOI: https://doi.org/10.1007/s00438-016-1286-9