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Molecular Genetics and Genomics

, Volume 292, Issue 2, pp 453–464 | Cite as

Tandem repeats of Allium fistulosum associated with major chromosomal landmarks

  • Ilya V. Kirov
  • Anna V. Kiseleva
  • Katrijn Van Laere
  • Nadine Van Roy
  • Ludmila I. Khrustaleva
Original Article

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.

Keywords

Allium fistulosum Allium wakegi FISH Heterochromatin Pachytene Pericentromeric region Satellite DNA 

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

Notes

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.

References

  1. 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 CrossRefPubMedGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  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 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucl Acids Res 27(2):573–580CrossRefPubMedPubMedCentralGoogle Scholar
  8. Blackburn EH (2001) Switching and signaling at the telomere. Cell 106(6):661–673. doi: 10.1016/S0092-8674(01)00492-5 CrossRefPubMedGoogle Scholar
  9. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371(6494):215–220. doi: 10.1038/371215a0 CrossRefPubMedGoogle Scholar
  10. 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 CrossRefPubMedGoogle Scholar
  11. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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 CrossRefPubMedGoogle Scholar
  13. 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 71–78Google Scholar
  14. 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 76:53–60CrossRefPubMedGoogle Scholar
  15. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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 CrossRefPubMedGoogle Scholar
  17. 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
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefPubMedGoogle Scholar
  20. Friesen N, Fritsch RM, Blattner FR (2006) Phylogeny and new intrageneric classification of Allium (Alliaceae) based on nuclear ribosomal DNA ITS sequences. Aliso 22:372–395Google Scholar
  21. Garrido-Ramos MA (2015) Satellite DNA in plants: more than just rubbish. Cytogenet Genome Res 146:153–170. doi: 10.1159/000437008 CrossRefPubMedGoogle Scholar
  22. 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 CrossRefPubMedGoogle Scholar
  23. Grewal SI, Moazed D (2003) Heterochromatin and epigenetic control of gene expression. Science 8:301(5634):798–802. doi: 10.1126/science.1086887 CrossRefPubMedGoogle Scholar
  24. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 CrossRefPubMedGoogle Scholar
  27. 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 CrossRefPubMedGoogle Scholar
  28. Holoch D, Moazed D (2015) RNA-mediated epigenetic regulation of gene expression. Nat Rev Genet 16(2):71–84. doi: 10.1038/nrg3863 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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):593–602CrossRefGoogle Scholar
  30. 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 RatonGoogle Scholar
  31. 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 PubMedGoogle Scholar
  32. Iwasa S (1964) Cytogenetic studies in the Wakegi, Allium fistulosum var. caespitosum. J Fac Agric Kyushu Univ 13(1):165–177Google Scholar
  33. 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 CrossRefPubMedGoogle Scholar
  34. Jones RN, Rees H (1968) Nuclear DNA variation in Allium. Heredity 23:591–605CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefPubMedGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 Google Scholar
  41. 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 CrossRefPubMedGoogle Scholar
  42. 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 CrossRefPubMedGoogle Scholar
  43. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Lawrence GJ, Appels R (1986) Mapping the nucleolar organizer region, seed protein loci and isozyme loci on chromosome 1R in rye. Theor Appl Genet 71:742–749CrossRefPubMedGoogle Scholar
  45. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  47. McClintock B (1951) Chromosome organization and genic expression. In: Cold Spring Harb Symp Quant Biol, vol 16, pp 13–47Google Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefPubMedGoogle Scholar
  53. Ohri D (1998) Genome size variation and plant systematics. Ann Bot 82:75–83CrossRefGoogle Scholar
  54. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 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 CrossRefPubMedGoogle Scholar
  56. Pich U, Fritsch R, Shubert I (1996) Closely related Allium species (Alliaceae) share a very similar satellite sequence. Plant Syst Evol 202:255–264CrossRefGoogle Scholar
  57. Reeves A, Tear J (2000) MicroMeasure for Windows. Version 3.3. http://www.colostate.edu/Depts/Biology/MicroMeasure. Accessed 25 May 2016
  58. Reinhart BJ, Bartel DP (2002) Small RNAs correspond to centromere heterochromatic repeats. Science 297(5588):1831. doi: 10.1126/science.1077183 CrossRefPubMedGoogle Scholar
  59. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 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 CrossRefPubMedGoogle Scholar
  61. 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 CrossRefPubMedGoogle Scholar
  62. 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 CrossRefPubMedGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. 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 CrossRefGoogle Scholar
  65. 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 CrossRefPubMedGoogle Scholar
  66. 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 CrossRefPubMedGoogle Scholar
  67. 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 49:47–57Google Scholar
  68. Tashiro Y (1984) Genome analysis of Allium wakegi Araki. J Jpn Soc Hort Sci 52:399–407CrossRefGoogle Scholar
  69. 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 PubMedPubMedCentralGoogle Scholar
  70. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Wallrath LL (1998) Unfolding the mysteries of heterochromatin. Curr Opin Genet Dev 8(2):147–153. doi: 10.1016/S0959-437X(98)80135-4 CrossRefPubMedGoogle Scholar
  73. 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 CrossRefPubMedGoogle Scholar
  74. 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 CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Center of Molecular BiotechnologyRussian State Agrarian University-Moscow Timiryazev Agricultural AcademyMoscowRussia
  2. 2.Department of Genetics, Biotechnology and Plant BreedingRussian State Agrarian University-Moscow Timiryazev Agricultural AcademyMoscowRussia
  3. 3.Plant Sciences Unit, Applied Genetics and Breeding, Institute for Agricultural and Fisheries Research (ILVO)MelleBelgium
  4. 4.Faculty of Medicine and Health Sciences, Center of Medical GeneticsGhent UniversityGhentBelgium

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