DOI QR코드

DOI QR Code

Chromosome numbers and polyploidy events in Korean non-commelinids monocots: A contribution to plant systematics

  • JANG, Tae-Soo (Department of Biological Science, College of Bioscience and Biotechnology, Chungnam National University) ;
  • WEISS-SCHNEEWEISS, Hanna (Department of Botany and Biodiversity Research, University of Vienna)
  • Received : 2018.06.04
  • Accepted : 2018.12.16
  • Published : 2018.12.30

Abstract

The evolution of chromosome numbers and the karyotype structure is a prominent feature of plant genomes contributing to or at least accompanying plant diversification and eventually leading to speciation. Polyploidy, the multiplication of whole chromosome sets, is widespread and ploidy-level variation is frequent at all taxonomic levels, including species and populations, in angiosperms. Analyses of chromosome numbers and ploidy levels of 252 taxa of Korean non-commelinid monocots indicated that diploids (ca. 44%) and tetraploids (ca. 14%) prevail, with fewer triploids (ca. 6%), pentaploids (ca. 2%), and hexaploids (ca. 4%) being found. The range of genome sizes of the analyzed taxa (0.3-44.5 pg/1C) falls well within that reported in the Plant DNA C-values database (0.061-152.33 pg/1C). Analyses of karyotype features in angiosperm often involve, in addition to chromosome numbers and genome sizes, mapping of selected repetitive DNAs in chromosomes. All of these data when interpreted in a phylogenetic context allow for the addressing of evolutionary questions concerning the large-scale evolution of the genomes as well as the evolution of individual repeat types, especially ribosomal DNAs (5S and 35S rDNAs), and other tandem and dispersed repeats that can be identified in any plant genome at a relatively low cost using next-generation sequencing technologies. The present work investigates chromosome numbers (n or 2n), base chromosome numbers (x), ploidy levels, rDNA loci numbers, and genome size data to gain insight into the incidence, evolution and significance of polyploidy in Korean monocots.

Keywords

References

  1. Babcock, E. B. and J. A. Jenkins. 1943. Chromosomes and phylogeny in Crepis. III. The relationships of one hundred and thirteen species. University of California Publications in Botany 18: 241-292.
  2. Bennett, M. D. 1972. Nuclear DNA content and minimum generation time in herbaceous plants. Proceedings of the Royal Society of London Series B-Biological Sciences 181: 109-135. https://doi.org/10.1098/rspb.1972.0042
  3. Bennett, M. D. 1998. Plant genome values: how much do we know? Proceedings of the National Academy of Sciences of the United States of America 95: 2011-2016. https://doi.org/10.1073/pnas.95.5.2011
  4. Bennett, M. D. and I. J. Leitch. 2012. Angiosperm DNA C-values database (release 8.0, Dec. 2012). Royal Botanic Gardens, Kew.
  5. Bloch, C., H. Weiss-Schneeweiss, G. M. Schneeweiss, M. H. J. Barfuss, C. A. Rebernig, J. L. Villasenor and T. F. Stuessy. 2009. Molecular phylogenetic analyses of nuclear and plastid DNA sequences support dysploid and polyploid chromosome number changes and reticulate evolution in the diversification of Melampodium (Millerieae, Asteraceae). Molecular Phylogenetics and Evolution 53: 220-233. https://doi.org/10.1016/j.ympev.2009.02.021
  6. Bowers, J. E., B. A. Chapman, J. Rong and A. H. Paterson. 2003. Unraveling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438. https://doi.org/10.1038/nature01521
  7. Choi, H.-W., J.-S. Kim, S.-H. Lee and J.-W. Bang. 2008. Physical mapping by FISH and GISH of rDNA loci and discrimination of genomes A and B in Scilla scilloides complex distributed in Korea. Journal of Plant Biology 51: 408-412. https://doi.org/10.1007/BF03036061
  8. Chumova, Z., J. Krejcikova, T. Mandakova, J. Suda and P. Travnicek. 2015. Evolutionary and taxonomic implications of variation in nuclear genome size: lesson from the grass genus Anthoxanthum (Poaceae). PLoS ONE 10: e0133748. https://doi.org/10.1371/journal.pone.0133748
  9. Deng, C.-L., R.-Y. Qin, N.-N. Wang, Y. Cao, J. Gao, W.-J. Gao and L.-D. Lu. 2012. Karyotype of Asparagus by physical mapping of 45S and 5S rDNA by FISH. Journal of Genetics 91: 209-212. https://doi.org/10.1007/s12041-012-0159-1
  10. Do, G.-S., B.-B. Seo, J.-M. Ko, S.-H. Lee, J.-H. Pak, I.-S. Kim and S.-D. Song. 1999. Analysis of somaclonal variation through tissue culture and chromosomal localization of rDNA sites by fluorescent in situ hybridization in wild Allium tuberosum and a regenerated variant. Plant Cell, Tissue and Organ Culture 57: 113-119. https://doi.org/10.1023/A:1006377415723
  11. Do, G. S., B. B. Seo, M. Yamamoto, G. Suzuki and Y. Mukai. 2001. Identification and chromosomal location of tandemly repeated DNA sequences in Allium cepa. Genes and Genetic Systems 76: 53-60. https://doi.org/10.1266/ggs.76.53
  12. Dodsworth, S., M. W. Chase, L. J. Kelly, I. J. Leitch, J. Macas, P. Novak, M. Piednoël, H. Weiss-Schneeweiss and A. R. Leitch. 2015. Genomic repeat abundances contain phylogenetic signal. Systematic Biology 64: 112-126. https://doi.org/10.1093/sysbio/syu080
  13. Dodsworth, S., T.-S. Jang, M. Struebig, M. W. Chase, H. Weiss-Schneeweiss and A. R. Leitch. 2017. Genome-wide repeat dynamics reflect phylogenetic distance in closely related allotetraploid Nicotiana (Solanaceae). Plant Systematics and Evolution 303: 1013-1020. https://doi.org/10.1007/s00606-016-1356-9
  14. Emadzade, K., T.-S. Jang, J. Macas, A. Kovarik, P. Novak, J. Parker and H. Weiss-Schneeweiss. 2014. Differential amplification of satellite PaB6 in chromosomally hypervariable Prospero autumnale complex (Hyacinthaceae). Annals of Botany 114: 1597-1608. https://doi.org/10.1093/aob/mcu178
  15. Fleischmann, A., T. P. Michael, F. Rivadavia, A. Sousa, W. Wang, E. M. Temsch, J. Greilhuber, K. F. Müller and G. Heubl. 2014. Evolution of genome size and chromosome number in the carnivorous plant genus Genlisea (Lentibulariaceae), with a new estimate of the minimum genome size in angiosperms. Annals of Botany 114: 1651-1663. https://doi.org/10.1093/aob/mcu189
  16. Goldblatt, P. 1980. Polyploidy in angiosperms: monocotyledons. In Polyploidy: Biological Relevance. Lewis, W. H. (ed.), Plenum Press, New York. Pp. 219-239.
  17. Gong, Z., Y. Wu, A. Koblizkova, G. A. Torres, K. Wang, M. Iovene, P. Neumann, W. Zhang, P. Novak, C. R. Buell, J. Macas and J. Jiang. 2012. Repeatless and repeat-based centromeres in potato: implications for centromere evolution. The Plant Cell 24: 3559-3574. https://doi.org/10.1105/tpc.112.100511
  18. Grant, V. 1982. Chromosome number patterns in primitive angiosperms. Botanical Gazette 143: 390-394. https://doi.org/10.1086/337314
  19. Grant, W. F. 1991. Chromosomal evolution and aneuploidy in Lotus. In Chromosome Engineering in Plant Genetics: Genetics, Breeding, Evolution. Part B. Tsuchiya, T. and P. K. Gupta (eds.), Elsevier, Amsterdam. Pp. 429-447.
  20. Guerra, M. 2008. Chromosome numbers in plant cytotaxonomy: concepts and implications. Cytogenetic and Genome Research 120: 339-350. https://doi.org/10.1159/000121083
  21. Hayashi, A., T. Saito, T. Mukai, S. Kurita and T. Hori. 2005. Genetic variation in Lycoris radiata var. radiata in Japan. Genes and Genetic Systems 80: 199-212. https://doi.org/10.1266/ggs.80.199
  22. Hizume, M. 1994. Allodiploid nature of Allium wakegi Araki revealed by genomic in situ hybridization and localization of 5S and 18S rDNAs. Japanese Journal of Genetics 69: 407-415. https://doi.org/10.1266/jjg.69.407
  23. Hizume, M. and H. Araki. 1994. Chromosomal localization of rRNA genes in six cytotypes of Scilla scilloides Druce. Cytologia 59: 35-42. https://doi.org/10.1508/cytologia.59.35
  24. Husband, B. C., S. J. Baldwin and J. Suda. 2013. The incidence of polyploidy in natural plant populations: major patterns and evolutionary processes. In Plant Genome Diversity. Vol. 2. Physical Structure, Behaviour and Evolution of Plant Genomes. Leitch, I. J., J. Greilhuber, J. Dolezel and J. F. Wendel (eds.), Springer, Vienna. Pp. 255-276.
  25. Jang, T.-S. 2013. Chromosomal evolution in Prospero autumnale complex. Ph.D. dissertation, University of Vienna, Vienna, Austria, 165 pp.
  26. Jang, T.-S., K. Emadzade, J. Parker, E. M. Temsch, A. R. Leitch, F. Speta and H. Weiss-Schneeweiss. 2013. Chromosomal diversification and karyotype evolution of diploids in the cytologically diverse genus Prospero (Hyacinthaceae). BMC Evolutionary Biolology 13: 136. https://doi.org/10.1186/1471-2148-13-136
  27. Jang, T.-S., J. McCann, J. S. Parker, K. Takayama, S.-P. Hong, G. M. Schneeweiss and H. Weiss-Schneeweiss. 2016a. rDNA loci evolution in the genus Glechoma (Lamiaceae). PLoS ONE 11: e0167177. https://doi.org/10.1371/journal.pone.0167177
  28. Jang, T.-S., J. S. Parker, K. Emadzade, E. M. Temsch, A. R. Leitch and H. Weiss-Schneeweiss. 2018. Multiple origins and nested cycles of hybridization result in high tetraploid diversity in the monocot Prospero. Frontiers in Plant Science 9: 433. https://doi.org/10.3389/fpls.2018.00433
  29. Jang, T.-S., J. S. Parker and H. Weiss-Schneeweiss. 2016b. Structural polymorphisms and distinct genomic composition suggest recurrent origin and ongoing evolution of B chromosome in the Prospero autumnale complex (Hyacinthaceae). New Phytologist 210: 669-679. https://doi.org/10.1111/nph.13778
  30. Jang, T.-S. and H. Weiss-Schneeweiss. 2015. Formamide-free genomic in situ hybridization allows unambiguous discrimination of highly similar parental genomes in diploid hybrids and allopolyploids. Cytogenetic and Genome Research 146: 325-331. https://doi.org/10.1159/000441210
  31. Kim, S. Y., H. W. Choi and J. W. Bang. 2004. Physical mapping of rDNAs using McFISH in Anemarrhena asphodeloides Bunge. Korean Journal of Medicinal and Crop Sciences 12: 515-518 (in Korean).
  32. Ko, E.-M., H.-J. Choi and B.-U. Oh. 2009. A cytotaxonomic study of Allium (Alliaceae) sect. Sacculiferum in Korea. Korean Journal of Plant Taxonomy 39: 170-180 (in Korean). https://doi.org/10.11110/kjpt.2009.39.3.170
  33. Lee, S. H., G. S. Do and B. B. Seo. 1999. Chromosomal localization of 5S rRNA gene loci and the implications for relationship within the Allium complex. Chromosome Research 7: 89-93. https://doi.org/10.1023/A:1009222411001
  34. Leitch, A. R. and I. J. Leitch. 2008. Genome plasticity and the diversity of polyploid plants. Science 320: 481-483. https://doi.org/10.1126/science.1153585
  35. Leitch, I. J. and A. R. Leitch. 2013. Genome size diversity and evolution in land plants. In Plant Genome Diversity. Vol. 2. Physical Structure, Behaviour and Evolution of Plant Genomes. Leitch, I. J., J. Greilhuber, J. Dolezel and J. F. Wendel (eds.), Springer, Vienna. Pp. 307-322.
  36. Levin, D. A. and A. C. Wilson. 1976. Rates of evolution in seed plants: net increase in diversity of chromosome numbers and species numbers through time. Proceedings of the National Academy of Sciences of the United States of America 73: 2086-2090. https://doi.org/10.1073/pnas.73.6.2086
  37. Lim, K. Y., R. Matyasek, A. Kovarik and A. Leitch. 2007. Parental origin and genome evolution in the allopolyploid Iris versicolor. Annals of Botany 100: 219-224. https://doi.org/10.1093/aob/mcm116
  38. Liu, B. and J. F. Wendel. 2003. Epigenetic phenomena and the evolution of plant allopolyploids. Molecular Phylogenetics and Evolution 29: 365-379. https://doi.org/10.1016/S1055-7903(03)00213-6
  39. Mandakova, T., A. Kovarik, J. Zozomova-Lihova, R. Shimizu-Inatsugi, K. K. Shimizu, K. Mummenhoff, K. Marhold and M. A. Lysak. 2013. The more the merrier: recent hybridization and polyploidy in Cardamine. The Plant Cell 25: 3280-3295. https://doi.org/10.1105/tpc.113.114405
  40. Mandakova, T., M. Pouch, K. Harmanova, S. H. Zhan, I. Mayrose and M. A. Lysak. 2017. Multispeed genome diploidization and diversification after an ancient allopolyploidization. Molecular Ecology 26: 6445-6462. https://doi.org/10.1111/mec.14379
  41. Masterson, J. 1994. Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264: 421-424. https://doi.org/10.1126/science.264.5157.421
  42. Mayrose, I., M. S. Barker and S. P. Otto. 2010. Probabilistic models of chromosome number evolution and the inference of polyploidy. Systematic Biology 59: 132-144. https://doi.org/10.1093/sysbio/syp083
  43. McCann, J., T.-S. Jang, J. Macas, G. M. Schneeweiss, N. J. Matzke, P. Novak, T. F. Stuessy, J. L. Villasenor and H. Weiss-Schneeweiss. 2018. Dating the species network: allopolyploidy and repetitive DNA evolution in American daisies (Melampodium sect. Melampodium, Asteraceae). Systematic Biology 67:1010-1024. https://doi.org/10.1093/sysbio/syy024
  44. McCann, J., G. M. Schneeweiss, T. F. Stuessy, J. L. Villasenor and H. Weiss-Schneeweiss. 2016. The impact of reconstruction methods, phylogenetic uncertainty and branch lengths on inference of chromosome number evolution in American daisies (Melampodium, Asteraceae). PLoS ONE 11: e0162299. https://doi.org/10.1371/journal.pone.0162299
  45. Novak, P., E. Hribova, P. Neumann, A. Koblizkova, J. Dolezel and J. Macas. 2014. Genome-wide analysis of repeat diversity across the family Musaceae. PLoS ONE 9: e98918. https://doi.org/10.1371/journal.pone.0098918
  46. Novak, P., P. Neumann and J. Macas. 2010. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11: 378. https://doi.org/10.1186/1471-2105-11-378
  47. Osborn, T. C., J. C. Pires, J. A. Birchler, D. L. Auger, Z. J. Chen, H.-S. Lee, L. Comai, A. Madlung, R. W. Doerge, V. Colot and R. A. Martienssen. 2003. Understanding mechanisms of novel gene expression in polyploids. Trends in Genetics 19: 141-147. https://doi.org/10.1016/S0168-9525(03)00015-5
  48. Otto, S. P. and J. Whitton. 2000. Polyploid incidence and evolution. Annual Review of Genetics 34: 401-437. https://doi.org/10.1146/annurev.genet.34.1.401
  49. Parisod, C., R. Holderegger and C. Brochmann. 2010. Evolutionary consequences of autopolyploidy. New Phytologist 186: 5-17. https://doi.org/10.1111/j.1469-8137.2009.03142.x
  50. Pellicer, J., M. F. Fay and I. J. Leitch. 2010. The largest eukaryotic genome of them all? Botanical Journal of the Linnean Society 164: 10-15. https://doi.org/10.1111/j.1095-8339.2010.01072.x
  51. Ramsey, J. and D. W. Schemske. 2002. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33: 589-639. https://doi.org/10.1146/annurev.ecolsys.33.010802.150437
  52. Rapp, R. A. and J. F. Wendel. 2005. Epigenetics and plant evolution. New Phytologist 168: 81-91. https://doi.org/10.1111/j.1469-8137.2005.01491.x
  53. Remon-Büttner, S. M., T. Schmidt and C. Jung. 1999. AFLPs represent highly repetitive sequences in Asparagus officinalis L. Chromosome Research 7: 279-304.
  54. Renny-Byfield, S., M. Ainouche, I. J. Leitch, K. Y. Lim, S. C. Le Comber and A. R. Leitch. 2010. Flow cytometry and GISH reveal mixed ploidy populations and Spartina nonaploids with genomes of S. alterniflora and S. maritima origin. Annals of Botany 105: 527-533. https://doi.org/10.1093/aob/mcq008
  55. Renny-Byfield, S., A. Kovarik, L. J. Kelly, J. Macas, P. Novak, M. W. Chase, R. A. Nichols, M. R. Pancholi, M.-A. Grandbastien and A. R. Leitch. 2013. Diploidization and genome size change in allopolyploids is associated with differential dynamics of low- and high-copy sequences. The Plant Journal 74: 829-839. https://doi.org/10.1111/tpj.12168
  56. Rice, A., L. Glick, S. Abadi, M. Einhorn, N. M. Kopelman, A. Salman-Minkov, J. Mayzel, O. Chay and I. Mayrose. 2015. The chromosome counts database (CCDB): a community resource of plant chromosome numbers. New Phytologist 206: 19-26. https://doi.org/10.1111/nph.13191
  57. Roberto, C. 2005. Low chromosome number angiosperms. Caryologia 58: 403-409. https://doi.org/10.1080/00087114.2005.10589480
  58. Schubert, I. and M. A. Lysak. 2011. Interpretation of karyotype evolution should consider chromosome structural constraints. Trends in Genetics 27: 207-216. https://doi.org/10.1016/j.tig.2011.03.004
  59. Soltis, P. S. and D. E. Soltis. 2009. The role of hybridization in plant speciation. Annual Review of Plant Biology 60: 561-588. https://doi.org/10.1146/annurev.arplant.043008.092039
  60. Soltis, D. E., P. S. Soltis, D. W. Schemske, J. F. Hancock, J. N. Thompson, B. C. Husband and W. S. Judd. 2007. Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56: 13-30.
  61. Soltis, D. E., C. J. Visger, D. B. Marchant and P. S. Soltis. 2016. Polyploidy: pitfalls and paths to a paradigm. American Journal of Botany 103: 1146-1166. https://doi.org/10.3732/ajb.1500501
  62. Son, J.-H., K.-C. Park, S.-I. Lee, E.-J. Jeon, H.-H. Kim and N.-S. Kim. 2012. Sequence variation and comparison of the 5S rRNA sequences in Allium species and their chromosomal distribution in four Allium species. Journal of Plant Biology 55: 15-25. https://doi.org/10.1007/s12374-011-9185-4
  63. Stebbins, G. L. 1971. Chromosomal Evolution in Higher Plants. Edward Arnold, London, 216 pp.
  64. Stuessy, T. F. 1971. Chromosome numbers and phylogeny in Melampodium (Compositae). American Journal of Botany 58: 732-736. https://doi.org/10.1002/j.1537-2197.1971.tb10027.x
  65. Sultana, S., S.-H. Lee, J.-W. Bang and H.-W. Choi. 2010. Physical mapping of rRNA gene loci and inter-specific relationships in wild Lilium distributed in Korea. Journal of Plant Biology 53: 433-443. https://doi.org/10.1007/s12374-010-9133-8
  66. The Angiosperm Phylogeny Group. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20. https://doi.org/10.1111/boj.12385
  67. Uhl, C. H. 1978. Chromosomes of Mexican Sedum II. Section Pachysedum. Rhodora 80: 491-512.
  68. Vanzela, A. L. L., M. Guerra and M. Luceno. 1996. Rhynchospora tenuis Link (Cyperaceae), a species with the lowest number of holocentric chromosomes. Cytobios 88: 219-228.
  69. Vitales, D., U. D’Ambrosio, F. Galvez, A. Kovarik and S. Garcia. 2017. Third release of the plant rDNA database with updated content and information on telomere composition and sequenced plant genomes. Plant Systematics and Evolution 303: 1115-1121. https://doi.org/10.1007/s00606-017-1440-9
  70. Wan, T., X. Zhang, J. Gregan, Y. Zhang, P. Guo and Y. Guo. 2012. A dynamic evolution of chromosome in subgenus Potamogeton revealed by physical mapping of rDNA loci detection. Plant Systematics and Evolution 298: 1195-1210. https://doi.org/10.1007/s00606-012-0621-9
  71. Weiss-Schneeweiss, H., K. Emadzade, T.-S. Jang and G. M. Schneeweiss. 2013. Evolutionary consequences, constraints and potential of polyploidy in plants. Cytogenetic and Genome Research 140: 137-150. https://doi.org/10.1159/000351727
  72. Weiss-Schneeweiss, H., A. R. Leitch, J. McCann, T.-S. Jang and J. Macas. 2015. Employing next generation sequencing to explore the repeat landscape of the plant genome. In Next Generation Sequencing in Plant Systematics. Regnum Vegetabile. Horandl, E. and M. Appelhans (eds.), Koeltz Scientific Books, Konigstein. Pp. 155-179.
  73. Weiss-Schneeweiss, H. and G. M. Schneeweiss. 2013. Karyotype diversity and evolutionary trends in angiosperms. In Plant Genome Diversity. Vol. 2. Physical Structure, Behaviour and Evolution of Plant Genomes. Leitch, I. J., J. Greilhuber, J. Dolezel and J. F. Wendel (eds.), Springer, Vienna. Pp. 209-230.
  74. Weiss-Schneeweiss, H., T. F. Stuessy and J. L. Villasenor. 2009. Chromosome numbers, karyotypes, and evolution in Melampodium (Asteraceae). International Journal of Plant Sciences 170: 1168-1182. https://doi.org/10.1086/605876
  75. Zhang, H., A. Koblizkova, K. Wang, Z. Gong, L. Oliveira, G. A. Torres, Y. Wu, W. Zhang, P. Novak, C. R. Buell, J. Macas and J. Jiang. 2014. Boom-bust turnovers of megabase-sized centromeric DNA in Solanum species: rapid evolution of DNA sequences associated with centromeres. The Plant Cell 26: 1436-1447. https://doi.org/10.1105/tpc.114.123877

Cited by

  1. Symplocarpus koreanus (Araceae; Orontioideae), a new species based on morphological and molecular data vol.51, pp.1, 2021, https://doi.org/10.11110/kjpt.2021.51.1.1