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Comparative triple-color FISH mapping in eleven Senna species using rDNA and telomeric repeat probes

Abstract

Senna is a diverse and paraphyletic genus in the subfamily Caesalpinioideae (Fabaceae Lindl.) comprising various species of industrial and medicinal value. To date, the genome-based taxonomic relationship among several Senna species remains enigmatic. Cytogenetic information is invaluable in deciphering phylogenetic relationships and evolutionary history. However, insufficient chromosomal research for many Senna species impedes comparative cytotaxonomic analyses aimed at understanding their genomic evolution. To provide additional Senna-related molecular cytogenetic information, we karyotyped 11 Senna species by employing triple-color fluorescence in situ hybridization using 5S rDNA, 45S rDNA, and Arabidopsis thaliana-type telomeric pre-labeled oligonucleotide probes. Chromosome numbers were predominantly 2n = 28, but 2n = 22 (S. marilandica) and 2n = 24 (S. uniflora) were also observed. While most species revealed only one interstitial 5S rDNA locus, except for S. uniflora which has two loci, a range of one to three 45S rDNA loci were detected at distal chromosomal regions. Additionally, we observed a hemizygous 45S rDNA locus in S. auriculata. In addition to chromosome termini, weak signals for telomeric repeats were found in interstitial regions in S. hirsuta, S. corymbosa, and S. alexandrina. These cytogenetic data can be integrated with molecular phylogenetic data for more comprehensive Senna cytotaxonomic analyses.

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References

  1. Aksenova AY, Mirkin SM (2019) At the beginning of the end and in the middle of the beginning: structure and maintenance of telomeric DNA repeats and interstitial telomeric sequences. Genes 10:118. https://doi.org/10.3390/genes10020118

    CAS  Article  PubMed Central  Google Scholar 

  2. Al-Turki TA, Filfilan SA, Mehmood SF (2000) A cytological study of flowering plants from Saudi Arabia. Willdenowia 30:339–358. https://doi.org/10.3372/wi.30.30211

    Article  Google Scholar 

  3. Baskin JM, Nan X, Baskin CC (1998) A comparative study of seed dormancy and germination in an annual and a perennial species of Senna (Fabaceae). Seed Sci Res 8:501–512. https://doi.org/10.1017/s0960258500004475

    Article  Google Scholar 

  4. Biondo E, Miotto S, Schifino-Wittmann M, Castro B (2012) Cytogenetics and cytotaxonomy of Brazilian species of Senna Mill. (Cassieae–Caesalpinioideae–Leguminosae). Caryologia 58:152–163. https://doi.org/10.1080/00087114.2005.10589445

    Article  Google Scholar 

  5. Chen L, Su D, Sun J, Li Z, Han Y (2020) Development of a set of chromosome-specific oligonucleotide markers and karyotype analysis in the Japanese morning glory Ipomoea nil. Sci Hortic 273:109633. https://doi.org/10.1016/j.scienta.2020.109633

    CAS  Article  Google Scholar 

  6. Cordeiro JMP, Felix LP (2018) Intra- and interspecific karyotypic variations of the genus Senna Mill. (Fabaceae, Caesalpinioideae). Acta Bot Bras 32:128–134. https://doi.org/10.1590/0102-33062017abb0274

    Article  Google Scholar 

  7. Freyman WA, Höhna S (2018) Cladogenetic and anagenetic models of chromosome number evolution: a Bayesian model averaging approach. Syst Biol 67:195–215. https://doi.org/10.1093/sysbio/syx065

    Article  PubMed  Google Scholar 

  8. Fuchs J, Brandes A, Schubert I (1995) Telomere sequence localization and karyotype evolution in higher-plants. Oesterr Bot Wochenbl 196:227–241. https://doi.org/10.1007/BF00982962

    CAS  Article  Google Scholar 

  9. Guerra M (2008) Chromosome numbers in plant cytotaxonomy: concepts and implications. Cytogenet Genome Res 120:339–350. https://doi.org/10.1159/000121083

    CAS  Article  PubMed  Google Scholar 

  10. He L, Liu J, Torres GA, Zhang H, Jiang J, Xie C (2013) Interstitial telomeric repeats are enriched in the centromeres of chromosomes in Solanum species. Chromosome Res 21:5–13. https://doi.org/10.1007/s10577-012-9332-x

    CAS  Article  PubMed  Google Scholar 

  11. Irwin HS, Turner BL (1960) Chromosomal relationships and taxonomic considerations in the genus Cassia. Am J Bot 47:309–318. https://doi.org/10.1002/j.1537-2197.1960.tb07130.x

    Article  Google Scholar 

  12. Jo YK, Mazharul IMD, Kim CK, Kim HY, Lim KB (2019) Morphological characteristics and FISH analysis of Hibiscus F1 hybrids and parental lines. Hortic Sci Technol 37:630–639. https://doi.org/10.7235/HORT.20190063

    Article  Google Scholar 

  13. Kang SH, Pandey RP, Lee CM, Sim JS, Jeong JT, Choi BS, Jung M, Ginzburg D, Zhao K, Won SY et al (2020) Genome-enabled discovery of anthraquinone biosynthesis in Senna tora. Nat Commun 11:5875. https://doi.org/10.1038/s41467-020-19681-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Koo DH, Nam YW, Choi D, Bang JW, De Jong H, Hur Y (2010) Molecular cytogenetic mapping of Cucumis sativus and C. melo using highly repetitive DNA sequences. Chromosome Res 18:325–336. https://doi.org/10.1007/s10577-010-9116-0

    CAS  Article  PubMed  Google Scholar 

  15. Lan T, Albert VA (2011) Dynamic distribution patterns of ribosomal DNA and chromosomal evolution in Paphiopedilum, a lady’s slipper orchid. BMC Plant Biol 11:126. https://doi.org/10.1186/1471-2229-11-126

    Article  PubMed  PubMed Central  Google Scholar 

  16. Levan A, Fredga K, Sandberg AA (2009) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220. https://doi.org/10.1111/j.1601-5223.1964.tb01953.x

    Article  Google Scholar 

  17. Maluszynska J, Heslop-Harrison JS (1993) Physical mapping of rDNA loci in Brassica species. Genome 36:774–781. https://doi.org/10.1139/g93-102

    CAS  Article  PubMed  Google Scholar 

  18. Mancia FH, Sohn S-H, Ahn YK, Kim D-S, Kim JS, Kwon Y-S, Kim C-W, Lee T-H, Hwang Y (2015) Distribution of various types of repetitive DNAs in Allium cepa L. based on dual color FISH. Hortic Environ Biotechnol 56:793–799. https://doi.org/10.1007/s13580-015-1100-3

    CAS  Article  Google Scholar 

  19. Mantovani M, Abel LD, Moreira-Filho O (2005) Conserved 5S and variable 45S rDNA chromosomal localisation revealed by FISH in Astyanax scabripinnis (Pisces, Characidae). Genetica 123:211–216. https://doi.org/10.1007/s10709-004-2281-3

    CAS  Article  PubMed  Google Scholar 

  20. Marazzi B, Endress PK, De Queiroz LP, Conti E (2006) Phylogenetic relationships within Senna (Leguminosae, Cassiinae) based on three chloroplast DNA regions: patterns in the evolution of floral symmetry and extrafloral nectaries. Am J Bot 93:288–303. https://doi.org/10.3732/ajb.93.2.288

    CAS  Article  PubMed  Google Scholar 

  21. Ohri D, Kumar A, Pal M (1986) Correlations between 2C DNA values and habit in Cassia (Leguminosae:Caesalpinioideae). Plant Syst Evol 153:223–227. https://doi.org/10.1007/BF00983689

    CAS  Article  Google Scholar 

  22. Pellerin RJ, Waminal NE, Belandres HR, Kim HH (2018a) Karyotypes of three exotic Cucurbit species based on triple-color FISH analysis. Hortic Sci Technol 36:417–425. https://doi.org/10.12972/kjhst.20180041

    Article  Google Scholar 

  23. Pellerin RJ, Waminal NE, Kim HH (2018b) Triple-color FISH karyotype analysis of four Korean wild Cucurbitaceae species. Hortic Sci Technol 36:98–107. https://doi.org/10.12972/kjhst.20180011

    CAS  Article  Google Scholar 

  24. Pellerin RJ, Waminal NE, Kim HH (2019) FISH mapping of rDNA and telomeric repeats in 10 Senna species. Hortic Environ Biotechnol 60:253–260. https://doi.org/10.1007/s13580-018-0115-y

    CAS  Article  Google Scholar 

  25. Peniton E, Waminal NE, Kim T-H, Kim HH (2019) FISH karyotype comparison between wild and cultivated perilla species using 5S and 45S rDNA probes. Plant Breed Biotechnol 7:237–244. https://doi.org/10.9787/PBB.2019.7.3.237

    Article  Google Scholar 

  26. Peska V, Garcia S (2020) Origin, diversity, and evolution of telomere sequences in plants. Front Plant Sci 11:117. https://doi.org/10.3389/fpls.2020.00117

    Article  PubMed  PubMed Central  Google Scholar 

  27. Rahman MO, Rahman MZ, Begum A (2013) Numerical taxonomy of the genus Senna Mill. from Bangladesh. Bangladesh J Plant Taxon 20:77–83. https://doi.org/10.3329/bjpt.v20i1.15467

    Article  Google Scholar 

  28. Randell B (1970) Adaptations in the genetic system of Australian arid zone Cassia species (Leguminosae, Caesalpinioideae). Aust J Bot 18:77–97. https://doi.org/10.1071/BT9700077

    Article  Google Scholar 

  29. Resende K, Prado C, Davide L, Torres G (2014) Polyploidy and apomixis in accessions of Senna rugosa (G.Don) H.S.Irwin & Barneby. Turk J Biol 38:510–515. https://doi.org/10.3906/biy-1312-66

    Article  Google Scholar 

  30. Rice A, Glick L, Abadi S, Einhorn M, Kopelman NM, Salman-Minkov A, Mayzel J, Chay O, Mayrose I (2015) The chromosome counts database (CCDB) - a community resource of plant chromosome numbers. New Phytol 206:19–26. https://doi.org/10.1111/nph.13191

    Article  PubMed  Google Scholar 

  31. Roa F, Guerra M (2012) Distribution of 45S rDNA sites in chromosomes of plants: structural and evolutionary implications. BMC Evol Biol 12:225. https://doi.org/10.1186/1471-2148-12-225

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Roa F, Guerra M (2015) Non-random distribution of 5S rDNA sites and its association with 45S rDNA in plant chromosomes. Cytogenet Genome Res 146:243–249. https://doi.org/10.1159/000440930

    CAS  Article  PubMed  Google Scholar 

  33. Rosato M, Álvarez I, Feliner GN, Rosselló JA (2018) Inter- and intraspecific hypervariability in interstitial telomeric-like repeats (TTTAGGG)n in Anacyclus (Asteraceae). Ann Bot 122:387–395. https://doi.org/10.1093/aob/mcy079

    Article  PubMed  PubMed Central  Google Scholar 

  34. Ruiz-Herrera A, Nergadze SG, Santagostino M, Giulotto E (2008) Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet Genome Res 122:219–228. https://doi.org/10.1159/000167807

    CAS  Article  PubMed  Google Scholar 

  35. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Schubert I, Lysak MA (2011) Interpretation of karyotype evolution should consider chromosome structural constraints. Trends Genet 27:207–216. https://doi.org/10.1016/j.tig.2011.03.004

    CAS  Article  PubMed  Google Scholar 

  37. Schubert I, Rieger R, Fuchs J (1995) Alteration of basic chromosome numberby fusion–fission cycles. Genome 38:1289–1292. https://doi.org/10.1139/g95-170

    CAS  Article  PubMed  Google Scholar 

  38. Seijo JG, Fernández A (2003) Karyotype analysis and chromosome evolution in South American species of Lathyrus (Leguminosae). Am J Bot 90:980–987. https://doi.org/10.3732/ajb.90.7.980

    Article  PubMed  Google Scholar 

  39. Shchapova AI (2013) The diversity of lifecycles and their role in the evolution of basic chromosome numbers in various living species. Russ J Genet Appl Res 3:239–245. https://doi.org/10.1134/S2079059713040102

    Article  Google Scholar 

  40. Silvestri MC, Ortiz AM, Robledo GA, Lavia GI (2020) Chromosome diversity in species of the genus Arachis, revealed by FISH and CMA/DAPI banding, and inferences about their karyotype differentiation. An Acad Bras Cienc 92:e20191364. https://doi.org/10.1590/0001-3765202020191364

    Article  PubMed  Google Scholar 

  41. Sousa A, Cusimano N, Renner SS (2014) Combining FISH and model-based predictions to understand chromosome evolution in Typhonium (Araceae). Ann Bot 113:669–680. https://doi.org/10.1093/aob/mct302

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Souza M, Iseppon A (2004) Cytogenetics and chromosome banding patterns in Caesalpinioideae and Papilionioideae species of Pará, Amazonas, Brazil. Bot J Linn Soc 144:181–191. https://doi.org/10.1111/j.1095-8339.2003.00230.x

    Article  Google Scholar 

  43. Souza G, Vanzela ALL, Crosa O, Guerra M (2016) Interstitial telomeric sites and Robertsonian translocations in species of Ipheion and Nothoscordum (Amaryllidaceae). Genetica 144:157–166. https://doi.org/10.1007/s10709-016-9886-1

    CAS  Article  PubMed  Google Scholar 

  44. Ta TD, Waminal NE, Nguyen TH, Pellerin RJ, Kim HH (2021) Comparative FISH analysis of Senna tora tandem repeats revealed insights into the chromosome dynamics in Senna. Genes Genom. https://doi.org/10.1007/s13258-021-01051-w

    Article  Google Scholar 

  45. Uchida W, Matsunaga S, Sugiyama R, Kawano S (2002) Interstitial telomere-like repeats in the Arabidopsis thaliana genome. Genes Genet Syst 77:63–67. https://doi.org/10.1266/ggs.77.63

    CAS  Article  PubMed  Google Scholar 

  46. Vrána J, Simková H, Kubaláková M, Cíhalíková J, Doležel J (2012) Flow cytometric chromosome sorting in plants: the next generation. Methods 57:331–337. https://doi.org/10.1016/j.ymeth.2012.03.006

    CAS  Article  PubMed  Google Scholar 

  47. Waminal NE, Kim HH (2012) Dual-color FISH karyotype and rDNA distribution analyses on four Cucurbitaceae species. Hortic Environ Biotechnol 53:49–56. https://doi.org/10.1007/s13580-012-0105-4

    Article  Google Scholar 

  48. Waminal NE, Perumal S, Lee J, Kim HH, Yang T-J (2016) Repeat evolution in Brassica rapa (AA), B. oleracea (CC), and B. napus (AACC) genomes. Plant Breed Biotech 4:107–122. https://doi.org/10.9787/PBB.2016.4.2.107

    Article  Google Scholar 

  49. Waminal NE, Pellerin RJ, Kim N, Jayakodi M, Park JY, Yang TJ, Kim HH (2018) Rapid and efficient FISH using pre-labeled oligomer probes. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-018-26667-z

    CAS  Article  Google Scholar 

  50. Waminal NE, Pellerin RJ, Kang S-H, Kim HH (2021) Chromosomal mapping of tandem repeats revealed massive chromosomal rearrangements and insights into Senna tora dysploidy. Front Plant Sci. https://doi.org/10.3389/fpls.2021.629898

    Article  PubMed  PubMed Central  Google Scholar 

  51. Watanabe K, King RM, Yahara T, Ito M, Yokoyama J, Suzuki T, Crawford DJ (1995) Chromosomal cytology and evolution in Eupatorieae (Asteraceae). Ann Missouri Bot Gard 82:581–592. https://doi.org/10.2307/2399838

    Article  Google Scholar 

  52. Watson J, Riha K (2010) Comparative biology of telomeres: where plants stand. FEBS Lett 584:3752–3759. https://doi.org/10.1016/j.febslet.2010.06.017

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Winterfeld G, Ley A, Hoffmann MH, Paule J, Röser M (2020) Dysploidy and polyploidy trigger strong variation of chromosome numbers in the prayer-plant family (Marantaceae). Plant Syst Evol. https://doi.org/10.1007/s00606-020-01663-x

    Article  Google Scholar 

  54. Wölk A, Winterfeld G, Röser M (2015) Genome evolution in a Mediterranean species complex: phylogeny and cytogenetics of Helictotrichon (Poaceae) allopolyploids based on nuclear DNA sequences (rDNA, topoisomerase gene) and FISH. Syst Biodivers 13:326–345. https://doi.org/10.1080/14772000.2015.1023867

    Article  Google Scholar 

  55. Youn SM, Kim HH (2018) Chromosome karyotyping of Senna covesii and S. floribunda based on triple-color FISH mapping of rDNAs and telomeric repeats. Plant Breed Biotech 6:51–56. https://doi.org/10.9787/PBB.2018.6.1.51

    Article  Google Scholar 

  56. Zhou HC, Pellerin RJ, Waminal NE, Yang T-J, Kim HH (2019a) Pre-labelled oligo probe-FISH karyotype analyses of four Araliaceae species using rDNA and telomeric repeat. Genes Genom 41:839–847. https://doi.org/10.1007/s13258-019-00786-x

    CAS  Article  Google Scholar 

  57. Zhou HC, Waminal NE, Kim HH (2019b) In silico mining and FISH mapping of a chromosome-specific satellite DNA in Capsicum annuum L. Genes Genom 41:1001–1006. https://doi.org/10.1007/s13258-019-00832-8

    CAS  Article  Google Scholar 

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Acknowledgements

This study was funded by projects (NRF 2017R1A2B2004778 and NRF 2020K1A3A1A39112373) from grants of the National Research Foundation of Korea.

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HHK is the supervisor and project administrator. THN and NEW carried out the experiments, analyzed the data, and wrote the original draft, reviewed, and edited the manuscript. DSL and RJP carried out the experiments, and reviewed and edited the manuscript. TDT, NBC, and BYK reviewed and edited the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Hyun Hee Kim.

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Nguyen, T.H., Waminal, N.E., Lee, D.S. et al. Comparative triple-color FISH mapping in eleven Senna species using rDNA and telomeric repeat probes. Hortic. Environ. Biotechnol. (2021). https://doi.org/10.1007/s13580-021-00364-9

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Keywords

  • Cytogenetic markers
  • FISH
  • Genome
  • Karyotype
  • Senna