Abstract
The genus Festuca L. (subtribe Loliinae), which encompasses about 500 species, is one of the largest genera of the Poeae tribe and is distributed worldwide. The taxonomy of the genus Festuca and the subtribe Loliinae remains a subject of debate until now. Taking into account that the comparison of the 5S rDNA intergenic spacer (IGS) sequences is successfully used to estimate genetic distances between closely related plant taxa, we evaluated the possibility of its application in the study of the phylogeny of the Loliinae subtribe. Accordingly, we cloned and sequenced this region of F. ovina (subgenus Festuca) and F. carpatica (subgenus Leucopoa) genomes and compared them with the 5S rDNA of Lolium perenne and other members of the tribe Poeae. It was found that the genomes of F. ovina and F. carpatica contain only one structural class of 5S rDNA repeats. The level of IGS similarity between the two studied Festuca species ranges from 80.2 to 81.7%, and between these species and L. perenne—from 62.5 to 70.1%. Species of the genera Festuca and Lolium form a highly-supported monophyletic group on the phylodendrogram, which indicates their origin from a common ancestor. The high rate of the IGS evolution allows using of this nuclear genome region in studies on the molecular taxonomy of the subtribe Loliinae.
Similar content being viewed by others
REFERENCES
Andreev, I.O., Spiridonova, E.V., Kyryachenko, S.S., et al., Population-genetic analysis of Deschampsia antarctica from two regions of Maritime Antarctica, Moscow Univ. Biol. Sci. Bull., 2010, vol. 65, no. 4, pp. 208–210. https://doi.org/10.3103/S0096392510040243
Barberá, P., Soreng, R.J., Peterson, P.M., et al., Molecular phylogenetic analysis resolves Trisetum (Poaceae: Pooideae: Koeleriinae) polyphyletic: evidence for a new genus, Sibirotrisetum and resurrection of Acrospelion, J. Syst. Evol., 2019, vol. 58, pp. 517–526.https://doi.org/10.1111/jse.12523
Baum, B.R. and Johnson, D.A., Lophopyrum Á. Löve (1980), Thinopyrum Á. Löve (1980), Trichopyrum Á. Löve (1986): one, two or three genera? A study based on the nuclear 5S DNA, Genet. Resour. Crop. Evol., 1986, vol. 65, pp. 161–186. https://doi.org/10.1007/s10722-017-0519-z
Catalán, P., Torrecilla, P., and Olmstead, R.G., Phylogeny of the festucoid grasses of subtribe Loliinae and allies (Poeae, Pooideae) inferred from ITS and trnL-F sequences, Mol. Phylogenet. Evol., 2004, vol. 31, pp. 517–542.https://doi.org/10.1016/j.ympev.2003.08.025
Catalán, P., Torrecilla, P., Lypez-Rodríguez, J.A., et al., A systematic approach to subtribe Loliinae (Poaceae: Pooideae) based on phylogenetic evidence, Aliso, 2007, vol. 23, no. 1, pp. 380–405. https://doi.org/10.5642/aliso.20072301.31
Cheng, Y., Zhou, K., Humphreys, M.W., et al., Phylogenetic relationships in the Festuca-Lolium complex (Loliinae; Poaceae): new insights from chloroplast sequences, Front. Ecol. Evol., 2016, vol. 4, p. 89. https://doi.org/10.3389/fevo.2016.00089
Clayton, W.D. and Renvoize, S.A., Genera Graminum, in Grasses of the World, Kew Bull. Add. Ser., 1986, vol. 13, pp. 1–389.
Cloix, C., Tutois, S., Mathieu, O., et al., Analysis of 5S rDNA arrays in Arabidopsis thaliana: physical mapping and chromosome-specific polymorphisms, Genome Res., 2000, vol. 10, no. 5, pp. 679–690. https://doi.org/10.1101/gr.10.5.679
Darbyshire, S.J., Realignment of Festuca subgenus Schedonorus with the genus Lolium (Poaceae), Novon, 1993, vol. 3, pp. 239–343.
Davis, J.I. and Soreng, R.J., A preliminary phylogenetic analysis of the grass subfamily Pooideae (Poaceae), with attention to structural features of the plastid and nuclear genomes, including an intron loss in GBSSI, Aliso, 2007, vol. 23, pp. 335—348.
Devesa, J.A., Catalán P, Muller, J., et al., Checklist de Festuca L. (Poaceae) en la Península Ibérica, Lagascalia, 2013, vol. 33, no. 1, pp. 183–274.
Duvall, M.R., Burke, S.V., and Clark, D.C., Plastome phylogenomics of Poaceae: alternate topologies depend on alignment gaps, Bot. J. Linn. Soc., 2020, vol. 192, no. 1, pp. 9–20. https://doi.org/10.1093/botlinnean/boz060
Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res., 2004, vol. 32, no. 5, pp. 1792–1797. https://doi.org/10.1093/nar/gkh340
Foggi, B., Scholz, H., and Valdés, B., The Euro Med treatment of Festuca (Gramineae)—new names and new combinations in Festuca and allied genera, Willdenowia, 2005, vol. 35, no. 2, pp. 241–244.https://doi.org/10.3372/wi.35.35202
Garcia, S., Garnatje, T., and Kovarik, A., Plant rDNA database: ribosomal DNA loci information goes online, Chromosoma, 2012, vol. 121, no. 4, pp. 389–394. https://doi.org/10.1007/s00412-012-0368-7
Garcia, S., Wendel, J.F., Borowska-Zuchowska, N., et al., The utility of graph clustering of 5S ribosomal DNA homoeologs in plant allopolyploids, homoploid hybrids, and cryptic introgressants, Front. Plant Sci., 2020, vol. 11, p. 41. https://doi.org/10.3389/fpls.2020.00041
Gaut, B.S., Tredway, L.P., Kubik, C., et al., Phylogenetic relationships and genetic diversity among members of the Festuca-Lolium complex (Poaceae) based on ITS sequence data, Plant Syst. Evol., 2000, vol. 224, pp. 33–53. https://doi.org/10.1007/BF00985265
Givnish, T.J., Ames, M., McNeal, J.R., et al., Assembling the tree of the monocotyledons: Plastome sequence phylogeny and evolution of Poales, Ann. Missouri Bot. Gard., 2010, vol. 97, no. 4, pp. 584–616. https://doi.org/10.3417/2010023
Hodkinson, T.R., Evolution and taxonomy of the grasses (Poaceae): a model family for the study of species-rich groups, Ann. Rev. Plant Biol., 2018, vol. 1, no. 1, pp. 255—294. https://doi.org/10.1002/9781119312994.apr0622
Inda, L.A., Sanmartín, I., Buerki, S., et al., Mediterranean origin and Miocene-Holocene Old World diversification of meadow fescues and ryegrasses (Festuca subgenus Schedonorus and Lolium), J. Biogeogr., 2014, vol. 41, no. 3, pp. 600–614. https://doi.org/10.1111/jbi.12211
Ishchenko, O.O., Panchuk, I.I., Andreev, I.O., et al., Molecular organization of 5S ribosomal DNA of Deschampsia antarctica, Cytol. Genet., 2018a, vol. 52, no. 6, pp. 416–421. https://doi.org/10.3103/S0095452719010146
Ishchenko, O.O., Derevenko, T.O., and Panchuk, I.I., 5S rDNA of Timothy-grass Phleum pratense L., Sci. Her. Chernivtsi Univ. Biol. (Biol. Systems), 2018b, vol. 10, no. 2, pp. 107–112. https://doi.org/10.3186l/biosystems2018.02.107
Ishchenko, O.O. and Panchuk, I.I., Molecular organization of 5S rDNA of perennial ryegrass Lolium perenne L., Bull. Vavilov Soc. Genet. Breed. Ukr., 2018c, vol. 16, no. 2, pp. 166–173.https://doi.org/10.7124/visnyk.utgis.16.2.1054
Ishchenko, O.O., Mel’nyk, V.M., Parnikoza, I.Y., et al., Molecular organization of 5S ribosomal DNA and taxonomic status of Avenella flexuosa (L.) Drejer (Poaceae), Cytol. Genet., 2020, vol. 54, no. 6, pp. 505–513. https://doi.org/10.3103/S0095452720060055
Kolano, B.M., Cann, J., Oskedra, M., et al., Parental origin and genome evolution of several Eurasian hexaploid species of Chenopodium (Chenopodiaceae), Phytotaxa, 2019, vol. 392, no. 3, pp. 163–185. https://doi.org/10.11646/phytotaxa.392.3.1
Kopecký, D., Lukaszewski, A.J., and Doledžel, J., Cytogenetics of festulolium (Festuca x Lolium hybrids), Cytogen. Genom. Res., 2008, vol. 120, nos. 3–4, pp. 370–383. https://doi.org/10.1186/s12864-019-5766-2
Krawczyk, K., Nobis, M., Nowak, A., et al., Phylogenetic implications of nuclear rRNA IGS variation in Stipa L. (Poaceae), Sci. Rep., 2017, vol. 7, no. 1, pp. 1–11. https://doi.org/10.1038/s41598-017-11804-x
Nani, T.F., Cenzi, G., Pereira, D.L., et al., Ribosomal DNA in diploid and polyploid Setaria (Poaceae) species: number and distribution, Comp. Cytogenet., 2015, vol. 9, no. 4, pp. 645–660. https://doi.org/10.3897/CompCytogen.v9i4.5456
Peng, Y.Y., Wei, Y.M., Baum, B.R., et al., Molecular diversity of the 5S rRNA gene and genomic relationships in the genus Avena (Poaceae: Aveneae), Genome, 2008, vol. 51, no. 2, pp. 137–154. https://doi.org/10.1139/G07-111
Peterson, P.M., Romaschenko, K., Arrieta, Y.H., et al., A molecular phylogeny of the subtribe Sporobolinae and a classification of the subfamily Chloridoideae (Poaceae), Mem. NY Bot. Gard., 2017, vol. 118, pp. 127–151. https://doi.org/10.21135/893275341.003
Porebski, S., Bailey, L.G., and Baum, B.R., Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components, Plant Mol. Biol. Rep., 1997, vol. 15, no. 1, pp. 8–15.https://doi.org/10.1007/BF02772108
Rodrigues, J., Viegas, W., and Silva, M., 45S rDNA external transcribed spacer organization reveals new phylogenetic relationships in Avena genus, PLoS One, 2017, vol. 12, no. 4, e0176l70. https://doi.org/10.1371/journal.pone.0176 170
Röser, M., Winterfeld, G., Grebenstein, B., et al., Molecular diversity and physical mapping of 5S rDNA in wild and cultivated oat grasses (Poaceae: Aveneae), Mol. Phylogen. Evol., 2001, vol. 21, no. 2, pp. 198–217. https://doi.org/10.1006/mpev.2001.1003
Saarela, J.M., Liu, Q., Peterson, P.M., et al., Phylogenetics of the grass ‘Aveneae-type plastid DNA clade’ (Poaceae: Pooideae, Poeae) based on plastid and nuclear ribosomal DNA sequence data, in Diversity, Phylogeny, and Evolution in the Monocotyledons, Aarhus: Aarhus Univ. Press, 2010.
Saini, A. and Jawali, N., Molecular evolution of 5S rDNA region in Vigna subgenus Ceratotropis and its phylogenetic implications, Plant Syst. Evol., 2009, vol. 280, nos. 3–4, pp. 187–206. https://doi.org/10.1007/s00606-009-0178-4
Sambrook, J., Fritsch, E., and Maniatis, T., Molecular Cloning, New York: Cold Spring Harbor Laboratory, 1989.
Scoppola, A., Cardoni, S., Pellegrino, M., et al., Genetic diversity and taxonomic issues in Gastridium P. Beauv (Poaceae) inferred from plastid and nuclear DNA sequence analysis, BioRxiv, 2019, 817965. https://doi.org/10.1101/817965
Shelyfist, A.Y., Tynkevich, Y.O., and Volkov, R.A., Molecular organization of 5S rDNA of Brunfelsia uniflora (Pohl.) D. Don, Bull. Vavilov. Soc. Genet. Breed. Ukr., 2018, vol. 16, no. l, pp. 6l–68. https://doi.org/10.7124/visnyk.utgis.16.1.903
Shelyfist, A.Y., Yakobyshen, D.V., and Volkov, R.A., Molecular structure of 5S rDNA of Mandragora autumnalis Bertol., Bull. Vavilov. Soc. Genet. Breed. Ukr., 2019, vol. 17, no. 2, pp. 187–195. https://doi.org/10.7124/visnyk.utgis.17.2.1220
Simeone, M.C., Cardoni, S., Piredda, R., et al., Comparative systematics and phylogeography of Quercus section Cerris in western Eurasia: inferences from plastid and nuclear DNA variation, Peer J., 2018, vol. 6, e5793. https://doi.org/10.7717/peerj.5793
Simon, L., Rabanal, F.A., Dubos, T., et al., Genetic and epigenetic variation in 5S ribosomal RNA genes reveals genome dynamics in Arabidopsis thaliana, Nucleic Acids Res., 2018, vol. 46, no. 6, pp. 3019–3033. https://doi.org/10.1093/nar/ gkyl63
Soreng, R.J., Davis, J.I., and Voionmaa, M.A., A phylogenetic analysis of Poaceae tribe Poeae sensu lato based on morphological characters and sequence data from three plastid-encoded genes: evidence for reticulation, and a new classification for the tribe, Kew Bull., 2007, vol. 62, no. 3, pp. 425–454.
Soreng, R.J., Peterson, P.M., Romschenko, K., et al., A worldwide phylogenetic classification of the Poaceae (Gramineae), J. Syst. Evol., 2015, vol. 53, no. 2, pp. 117–137. https://doi.org/10.1111/jse.12150
Stamatakis, A., RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies, Bioinformatics, 2014, vol. 30, no. 9, pp. 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Thomas, H. and Humphreys, M.O., Progress and potential of interspecific hybrids of Lolium and Festuca, J. Agric. Sci., 1991, vol. 117, no. 1, pp. 1–8.
Thomas, H.M., Morgan, W.G., and Humphreys, M.W., Designing grasses with a future-combining the attributes of Lolium and Festuca, Euphytica, 2003, vol. 133, no. 1, pp. 19–26. https://doi.org/10.1023/A:1025694819031
Tkach, N., Schneider, J., Döring, E., et al., Phylogeny, morphology and the role of hybridization as driving force of evolution in grass tribes Aveneae and Poeae (Poaceae), BioRxiv, 2019, 707588. https://doi.org/10.1101/707588
Torrecilla, P. and Catalán, P., Phylogeny of broad-leaved and fine-leaved Festuca lineages (Poaceae) based on nuclear ITS sequences, Syst. Bot., 2002, vol. 27, no. 2, pp. 241–251. https://doi.org/10.1043/0363-6445-27.2.241
Tynkevich, Y.O. and Volkov, R.A., Structural organization of 5S ribosomal DNA in Rosa rugosa, Cytol. Genet., 2014, vol. 48, no. 1, pp. 1–6. https://doi.org/10.3103/S0095452714010095
Tynkevich, Y.O. and Volkov, R.A., 5S Ribosomal DNA of distantly related Quercus species: molecular organization and taxonomic application, Cytol. Genet., 2019, vol. 53, no. 6, pp. 459–466. https://doi.org/10.3103/S0095452719060100
Tynkevich, Y.O., Nevelska, A.O., et al., Organization and variability of the 5S rDNA intergenic spacer of Lathyrus venetus, Bull. Vavilov Soc. Genet. Breed. Ukr., 2015, vol. 13, no. 1, pp. 81–87.
Vaio, M., Mazzella, C., et al., Effects of the diploidisation process upon the 5S and 35S rDNA sequences in the allopolyploid species of the Dilatata group of Paspalum (Poaceae, Paniceae), Austral. J. Bot., 2019, vol. 67, no. 7, pp. 521–530. https://doi.org/10.1071/BT18236
Volkov, A.R. and Panchuk, I.I., 5S rDNA of Dactylis glomerata (Poaceae): molecular organization and taxonomic application, Bull. Vavilov. Soc. Genet. Breed. Ukr., 2014, vol. 12, no. 1, pp. 3–11.
Volkov, R.A., Panchuk, I.I., et al., Plant rDNA: organization, evolution, and using, Cytol. Genet., 2003, vol. 37, no. 1, pp. 68–72.
Volkov, R.A., Kozeretska, I.A., Kyryachenko, S.S., et al., Molecular evolution and variability of ITS1 and ITS2 in populations of Deschampsia antarctica from two regions of the Maritime Antarctic, Polar Sci., 2010, vol. 4, no. 3, pp. 469–478. https://doi.org/10.1016/j.polar.2010.04.011
Wang, W., Chen, S., Guo, W., et al., Tropical plants evolve faster than their temperate relatives: a case from the bamboos (Poaceae: Bambusoideae) based on chloroplast genome data, Biotech. Biotech. Equip., 2020, vol. 34, no. 1, pp. 482–493. https://doi.org/10.1080/13102818.2020.1773312
Yamada, T., Festuca, in Wild Crop Relatives: Genomic and Breeding Resources, Kole, C., Ed., Berlin: Springer, 2011, pp. 153–164.
ACKNOWLEDGMENTS
The authors express their sincere gratitude to prof. Roman A. Volkov (Chernivtsi National University) for participating in the discussion of the results.
Funding
The research was supported by the Ministry of Education and Science of Ukraine (grant no. 0118U000137).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
About this article
Cite this article
Ishchenko, O.O., Bednarska, I.O. & Panchuk, І.І. Application of 5S Ribosomal DNA for Molecular Taxonomy of Subtribe Loliinae (Poaceae). Cytol. Genet. 55, 10–18 (2021). https://doi.org/10.3103/S0095452721010096
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.3103/S0095452721010096