Skip to main content
Log in

Polyphyly of the grass tribe Hainardieae (Poaceae: Pooideae): identification of its different lineages based on molecular phylogenetics, including morphological and cytogenetic characteristics

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

The small pooid grass tribe Hainardieae comprises six genera with approximately ten species; however, this tribe was not accepted by all previous taxonomic treatments. To study the relationships among these genera and to infer the phylogeny and evolutionary patterns, we used sequence variation of the internal transcribed spacers (ITS) of nuclear ribosomal and chloroplast (cp) matK DNA and morphology. Many genera of the Aveneae/Poeae tribe complex additionally were included. Both molecular datasets showed Hainardieae to be highly polyphyletic, and its genera to branch with different groups of the Aveneae/Poeae. Parapholis and Hainardia are corroborated as being closely related, and belonging to a firmly supported Eurasian clade together with Catapodium incl. Scleropoa, Cutandia, Desmazeria, Sphenopus, Vulpiella (subtribe Parapholiinae) and with Cynosurus as sister to this assemblage. The other genera of traditionally recognised Hainardieae are positioned phylogenetically distant: Mediterranean Narduroides is verified as more or less related to Festuca and relatives (subtribe Loliinae), whereas the west Eurasian Pholiurus is close to the lineage of Poa and relatives (subtribe Poinae). North American Scribneria is sister to Deschampsia and both genera should be unified under a common subtribe (Aristaveninae or Holcinae). The phylogenetic position of the Algerian genus Agropyropsis (close to Narduroides and within the Loliinae) is suggested on morphology only, because no molecular data was obtained for it. Considering classification, we support the abandonment of tribe Hainardieae and argue to abandon Poeae subtribe Scribneriinae. Poeae subtribe Parapholiinae is redefined with a novel genus content, due to the exclusion of Agropyropsis and Pholiurus and the inclusion of Vulpiella.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Albers, F., & Butzin, F. (1977). Taxonomie and Nomenklatur der Subtriben Aristaveninae und Airinae (Gramineae-Aveneae). Willdenowia, 8, 81–84.

    Google Scholar 

  • Baum, B. R., & Appels, R. (1992). Evolutionary change at the 5S DNA loci of species in the Triticeae. Plant Systematics and Evolution, 183, 195–208.

    Article  CAS  Google Scholar 

  • Blattner, F. R., Weising, K., Baenfer, G., Maschwitz, U., & Fiala, B. (2001). Molecular analysis of phylogenetic relationships among myrmecophytic Macaranga species (Euphorbiaceae). Molecular Phylogenetics and Evolution, 19, 331–344.

    Article  PubMed  CAS  Google Scholar 

  • Bor, N. L. (1970). Gramineae. In K. H. Rechinger (Ed.), Flora iranica, vol. 70 (pp. 1–573). Graz: Akademische Druck- und Verlagsanstalt.

  • Bouchenak-Khelladi, Y., Salamin, N., Savolainen, V., Forest, V., van der Bank, M., Chase, M. W., & Hodkinson, T. R. (2008). Large multi-gene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. Molecular Phylogenetics and Evolution, 47, 488–505.

    Article  PubMed  CAS  Google Scholar 

  • Brysting, A. K., Fay, M. F., Leitch, I. J. & Aiken S. G. (2004). One or more species in the artic grass genus Dupontia?—A contribution to the Panarctic Flora project. Taxon, 53, 365–382.

    Article  Google Scholar 

  • Catalán, P., Kellogg, E. A., & Olmstead, R. G. (1997). Phylogeny of Poaceae subfamily Pooideae based on chloroplast ndhF gene sequences. Molecular Phylogenetics and Evolution, 8, 150–166.

    Article  PubMed  Google Scholar 

  • Catalán, P., Torrecilla, P., López-Rodríguez, J. A., & Olmstead, R. G. (2004). Phylogeny of the festucoid grasses of subtribe Loliinae and allies (Poeae, Pooideae) inferred from ITS and trnL–F sequences. Molecular Phylogenetics and Evolution, 31, 517–541.

    Article  PubMed  Google Scholar 

  • Catalán, P., Torrecilla, P., López-Rodríguez, J. A., Müller, J., & Stace, C. A. (2007). A systematic approach to subtribe Loliinae (Poaceae: Pooideae) based on phylogenetic evidence. Aliso, 23, 380–405.

    Google Scholar 

  • Clayton, W. D., & Renvoize, S. A. (1986). Genera graminum. Grasses of the world. London: Her Majesty’s Stationary Office.

    Google Scholar 

  • Clayton, W. D., Vorontsova, M. S., Harman, K. T., & Williamson, H. (2006 onwards). GrassBase - The online world grass flora. Available at http://www.kew.org/data/grasses-db.html (accessed 1 March 2011).

  • Conert, H. J. (1979–1998). Poaceae (Echte Gräser oder Süßgräser). In H. J. Conert, E. J. Jäger, W. Schultze-Motel, G. Wagenitz, H. E. Weber & G. Hegi (Eds.), Illustrierte Flora von Mitteleuropa (3rd ed.), vol. 1, part 3 (pp. 1–898). Berlin: Parey.

  • Davis, J. I., & Soreng, R. J. (2007). A preliminary phylogenetic analysis of the grass subfamily Pooideae subfamily Pooideae (Poaceae), with attention to structural features of the plastid and nuclear genomes, including an intron loss in GBSSI. Aliso, 23, 335–348.

    Google Scholar 

  • Davis, J. I., & Soreng, R. J. (2010). Migration of endpoints of two genes relative to boundaries between regions of the plastid genome in the grass family (Poaceae). American Journal of Botany, 97, 874–892.

    Article  PubMed  CAS  Google Scholar 

  • Devesa, J. A. (1987). Narduroides Rouy. In B. Valdés, S. Talavera, & E. Fernández-Galiano (Eds.), Flora vascular de Andalucía occidental, vol. 3 (pp. 292–293). Barcelona: Ketres Editora.

    Google Scholar 

  • Döring, E. (2009). Molekulare Phylogenie der Hafer-Gräser (Poaceae: Pooideae: Aveneae). PhD dissertation. Halle/Saale: Martin Luther University Halle-Wittenberg. Available at http://digital.bibliothek.uni-halle.de/hs/content/titleinfo/177571.

  • Döring, E., Schneider, J., Hilu, K. W., & Röser, M. (2007). Phylogenetic relationships in the Aveneae/Poeae complex (Pooideae, Poaceae). Kew Bulletin, 62, 407–424.

    Google Scholar 

  • Duvall, M., Davis, J. I., Clark, L. G., Noll, J. D., Goldman, D. H., & Sánchez Ken, J. G. (2007). Phylogeny of the grasses (Poaceae) revisited. Aliso, 23, 237–247.

    Google Scholar 

  • Fedorov, A. A. (Ed.). (1969). Chromosome numbers of flowering plants. Leningrad: Nauka.

    Google Scholar 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.

    Article  Google Scholar 

  • Garcia-Suárez, R., Alonso-Blanco, C., Fernández-Carvajal, M. C., Fernández-Prieto, J. A., Roca, A., & Giraldez, R. (1997). Diversity and systematics of Deschampsia sensu lato (Poaceae) inferred from karyotypes, protein electrophoresis, total genomic DNA hybridization and chloroplast DNA analysis. Plant Systematics and Evolution, 205, 99–110.

    Article  Google Scholar 

  • Gillespie, L. J., Archambault, A., & Soreng, R. J. (2007). Phylogeny of Poa (Poaceae) based on trnT–trnF sequence data: major clades and basal relationships. Aliso, 23, 420–434.

    Google Scholar 

  • Gillespie, L. J., Soreng, R. J., Bull, R. D., Jacobs, S. W. L., & Refulio-Rodriguez, N. F. (2008). Phylogenetic relationships in subtribe Poinae (Poaceae, Poeae) based on nuclear ITS and plastid trnT–trnF sequences. Botany, 86, 938–967.

    Article  CAS  Google Scholar 

  • Gillespie, L. J., Soreng, R. J., & Jacobs, S. W. L. (2009). Phylogenetic relationships of Australian Poa (Poaceae: Poinae): molecular evidence for two new genera, Saxipoa and Sylvipoa. Australian Systematic Botany, 22, 413–436.

    Article  Google Scholar 

  • Gillespie, L. J., Soreng, R. J., Paradis, L. M., & Bull, R. D. (2010). Phylogeny and reticulation in Poinae subtribal complex based on nrITS, ETS, and trnTLF data. In O. Seberg, G. Petersen, A. S. Barford, & J. I. Davis (Eds.), Diversity, phylogeny, and evolution in the monocotyledons (pp. 589–617). Aarhus: Aarhus University Press.

    Google Scholar 

  • GPWG [The Grass Phylogeny Working Group]. (2001). Phylogeny and subfamilial classification of the grasses (Poaceae). Annals of the Missouri Botanical Garden, 88, 373–457.

    Article  Google Scholar 

  • Grebenstein, B., Röser, M., Sauer, W., & Hemleben, V. (1998). Molecular phylogenetic relationships in Aveneae (Poaceae) species and other grasses as inferred from ITS1 and ITS2 rDNA sequeneces. Plant Systematics and Evolution, 213, 233–250.

    Article  Google Scholar 

  • Guinochet, M., & de Vilmorin, R. (1978). Flore de France (Vol. 3). Paris: Éditions du Centre National de la Recherche Scientifique.

    Google Scholar 

  • Hilu, K. W. (2004). Phylogenetics and chromosomal evolution in the Poaceae (grasses). Australian Journal of Botany, 52, 13–22.

    Article  CAS  Google Scholar 

  • Hilu, K. W., Alice, L. A., & Liang, H. (1999). Phylogeny of the Poaceae inferred from matK sequences. Annals of the Missouri Botanical Garden, 86, 835–851.

    Article  Google Scholar 

  • Hsiao, C., Chatterton, N. J., & Asay, K. H. (1995a). Molecular phylogeny of the Pooideae (Poaceae) based on nuclear rDNA (ITS) sequences. Theoretical and Applied Genetics, 90, 389–398.

    Article  CAS  Google Scholar 

  • Hsiao, C., Chatterton, N. J., Asay, K. H., & Jensen, K. B. (1995b). Phylogenetic relationship of the monogenomic species of the wheat tribe, Triticeae (Poaceae), inferred from nuclear rDNA (internal transcribed spacer) sequences. Genome, 38, 211–223.

    Article  PubMed  CAS  Google Scholar 

  • Hsiao, C., Jacobs, S. W. L., Chatterton, N. J., & Asay, K. H. (1999). A molecular phylogeny of the grass family (Poaceae) based on the sequences of nuclear ribosomal DNA (ITS). Australian Journal of Botany, 11, 667–688.

    Google Scholar 

  • Hunter, A. M., Orlovich, D. A., Lloyd, K. M., Lee, W. G., & Murphy, D. J. (2004). The generic position of Austrofestuca littoralis and the reinstatement of Hookerochloa and Festucella (Poaceae) based on evidence from nuclear (ITS) and chloroplast (trnL–trnF) DNA sequences. New Zealand Journal of Botany, 42, 253–262.

    Article  Google Scholar 

  • Hunziker, J. M., & Stebbins, G. L. (1987). Chromosomal evolution in the Gramineae. In T. R. Soderstrom, K. W. Hilu, C. S. Campell, & M. E. Barkworth (Eds.), Grass systematics and evolution (pp. 179–187). Washington: Smithsonian Institution Press.

    Google Scholar 

  • IPCN [Index to Plant Chromosome Numbers]. (2010). Available at http://mobot.mobot.org/W3T/Search/ipcn.html (accessed 25 May 2010).

  • Kellogg, E. A., Appels, R., & Mason-Gamer, R. J. (1996). When gene trees tell different stories: The diploid genera of Triticeae (Gramineae). Systematic Botany, 21, 312–347.

    Article  Google Scholar 

  • Kim, E. S., Bolsheva, N. L., Samatadze, T. E., Nosov, N. N., Nosova, I. V., Zelenin, A. V., Punina, E. O., Muravenko, O. V., & Rodionov, A. V. (2009). The unique genome of two-chromosome grasses Zingeria and Colpodium, its origin, and evolution. Russian Journal of Genetics, 45, 1329–1337.

    Article  CAS  Google Scholar 

  • Kotseruba, V., Gernand, D., Meister, A., & Houben, A. (2003). Uniparental loss of ribosomal DNA in the allotetraploid grass Zingeria trichopoda (2n = 8). Genome, 46, 156–163.

    Article  PubMed  CAS  Google Scholar 

  • Kotseruba, V., Pistrick, K., Gernand, D., Meister, A., Ghukasyan, A., Gabrielyan, I., et al. (2005). Characterisation of the low-chromosome number grass Colpodium versicolor (Stev.) Schmalh. (2n = 4) by molecular cytogenetics. Caryologia, 58, 241–245.

    Google Scholar 

  • Kotseruba, V., Pistrick, K., Blattner, F. R., Kumke, K., Weiss, O., Rutten, T., et al. (2010). The evolution of the hexaploid grass Zingeria kochii (Mez) Tzvel. (2n = 12) was accompanied by complex hybridization and uniparental loss of ribosomal DNA. Molecular Phylogenetics and Evolution, 56, 146–155.

    Google Scholar 

  • Macfarlane, T. D. (1987). Poaceae subfamily Pooideae. In T. R. Soderstrom, K. W. Hilu, C. S. Campbell, & M. E. Barkworth (Eds.), Grass systematics and evolution (pp. 265–276). Washington: Smithsonian Institution Press.

    Google Scholar 

  • Maire, R. (1955). Flore de l’Afrique du Nord, vol. 3, Monocotyledonae: Glumiflorae (Gramineae: sf. Pooideae p.p.). Paris: Lechevalier.

    Google Scholar 

  • Mason-Gamer, R. J. (2005). The β-amylase genes of grasses and a phylogenetic analysis of the Triticeae (Poaceae). American Journal of Botany, 92, 1045–1058.

    Article  PubMed  CAS  Google Scholar 

  • Mason-Gamer, R. J., & Kellogg, E. A. (2000). Phylogenetic analysis of the Triticeae using the starch synthase gene, and a preliminary analysis of some North American Elymus species. In S. W. L. Jacobs & J. Everett (Eds.), Grasses: Systematics and evolution (pp. 102–109). Melbourne: CSIRO.

    Google Scholar 

  • Mathews, S., Tsai, R. C., & Kellogg, E. A. (2000). Phylogenetic structure in the grass family (Poaceae): Evidence from the nuclear gene phytochrome B. American Journal of Botany, 87, 96–107.

    Article  PubMed  CAS  Google Scholar 

  • Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. Uppsala: Evolutionary Biology Centre, Uppsala University.

    Google Scholar 

  • Quintanar, A., Castroviejo, S., & Catalán, P. (2007). Phylogeny of the tribe Aveneae (Pooideae, Poaceae) inferred from plastid trnT–F and nuclear ITS sequences. American Journal of Botany, 94, 1554–1569.

    Article  PubMed  CAS  Google Scholar 

  • Rodionov, A. V., Kim, E. S., Punina, E. O., Machs, E. M., Tyupa, N. B., & Nosov, N. N. (2007). Evolution of chromosome numbers in the tribes Aveneae and Poeae inferred from the comparative analysis of the internal transcribed spacers ITS1 and ITS2 of nuclear 45S rDNA genes (in Russian). Botanicheskii Zhurnal (Moscow & Leningrad), 92, 57–71.

    Google Scholar 

  • Romero, A. T. (2009). Narduroides Rouy. In G. Blanca, B. Cabezudo, M. Cueto, C. Fernández López, & C. Morales Torres (Eds.), Flora vascular de Andalucía oriental, vol. 1 (pp. 319–320). Sevilla: Consejería de Medio Ambiente.

    Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Article  PubMed  CAS  Google Scholar 

  • Ronquist, F., Huelsenbeck, J., & Teslenko, M. (2011). Draft MrBayes version 3.2 manual: tutorials and model summaries. Version 15 November 2011. Available at http://mrbayes.sourceforge.net/mb3.2_manual.pdf.

  • Röser, M., Winterfeld, G., Grebenstein, B., & Hemleben, V. (2001). Molecular diversity and physical mapping of 5S rDNA in wild and cultivated oat grasses (Poaceae: Aveneae). Molecular Phylogenetics and Evolution, 21, 198–217.

    Article  PubMed  Google Scholar 

  • Saarela, J. M., Peterson, P. M., Keane, R. M., Cayouette, J., & Graham, S. W. (2007). Molecular phylogenetics of the genus Bromus (Poaceae: Pooideae) based on nuclear and chloroplast DNA sequence data. Aliso, 23, 450–467.

    Google Scholar 

  • Saarela, J. M., Liu, Q., Peterson, P. M., Soreng, R. J., & Paszko, B. (2010). Phylogenetics of the grass ‘Aveneae-type plastid DNA clade’ (Poaceae: Pooideae, Poeae) based on plastid and nuclear ribosomal DNA sequence data. In O. Seberg, G. Petersen, A. S. Barford, & J. I. Davis (Eds.), Diversity, phylogeny, and evolution in the monocotyledons (pp. 557–587). Aarhus: Aarhus University Press.

    Google Scholar 

  • Schneider, J., Döring, E., Hilu, K. W., & Röser, M. (2009). Phylogenetic structure of the grass subfamily Pooideae based on comparison of plastid matK gene–3′trnK exon and nuclear ITS sequences. Taxon, 58, 405–424.

    Google Scholar 

  • Schneider, J., Winterfeld, G., Hoffmann, M. H., & Röser, M. (2011). Duthieeae, a new tribe of grasses (Poaceae) identified among the early diverging lineages of subfamily Pooideae: molecular phylogenetics, morphological delineation, cytogenetics, and biogeography. Systematics and Biodiversity, 9, 27–44.

    Article  Google Scholar 

  • Schwarzacher, T., Ambros, P., & Schweizer, D. (1980). Application of Giemsa banding to orchid karyotype analysis. Plant Systematics and Evolution, 134, 293–297.

    Article  Google Scholar 

  • Seberg, O., & Petersen, G. (2007). Phylogeny of Triticeae (Poaceae) based on three organelle genes, two single-copy nuclear genes, and morphology. In O. Seberg, G. Petersen, A. S. Barfod, & J. I. Davis (Eds.), Diversity, phylogeny, and evolution in the monocotyledons (pp. 362–371). Aarhus: Aarhus University Press.

    Google Scholar 

  • Smith, J. P. (2007). Scribneria Hack. In M. E. Barkworth, K. M. Capels, S. Long, L. K. Anderton, & M. B. Piep (Eds.), Flora of North America North of Mexico (Vol. 24, p. 689). New York: Oxford University Press.

    Google Scholar 

  • Soreng, R. J., & Davis, J. I. (1998). Phylogenetics and character evolution in the grass family (Poaceae): Simultaneous analysis of morphological and chloroplast DNA restriction site character sets. The Botanical Review, 64, 1–85.

    Article  Google Scholar 

  • Soreng, R. J., & Davis, J. I. (2000). Phylogenetic structure in Poaceae subfamily Pooideae as inferred from molecular and morphological characters: misclassification versus reticulation. In S. W. L. Jacobs & J. Everett (Eds.), Grasses: systematics and evolution (pp. 61–74). Melbourne: CSIRO.

    Google Scholar 

  • Soreng, R. J., Peterson, P. M., Davidse, G., Judziewicz, E. J., Zuloaga, F. O., Filgueras, T. S., et al. (2003). Catalogue of New World grasses (Poaceae): IV. subfamily Pooideae. Contributions from the United States National Herbarium, 48, 1–730.

  • Soreng, R. J., Davis, J. I., & Voionmaa, M. A. (2007). 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 of the tribe. Kew Bulletin, 62, 425–454.

    Google Scholar 

  • Stace, C. (1980). Narduroides Rouy. In T. G. Tutin, V. H., Heywood, N. A. Burges, D. M. Moore, D. H., Valentine, S. M. Walters & D. A. Webb (Eds.), Flora europaea, vol. 5 (pp. 157–158). Cambridge: Cambridge University Press.

  • Stebbins, G. L. (1956). Cytogenetics and evolution of the grass family. American Journal of Botany, 43, 890–905.

    Article  Google Scholar 

  • Stebbins, G. L. (1985). Polyploidy, hybridization and the invasion of new habitats. Annals of the Missouri Botanical Garden, 72, 824–832.

    Article  Google Scholar 

  • Stebbins, G. L., & Crampton, B. (1961). A suggested revision of the grass genera of temperate North America. Recent Advances in Botany, 1, 133–145.

    Google Scholar 

  • Swofford, D. L. (2002). PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sunderland: Sinauer.

  • Torrecilla, P., López-Rodriguez, J. A., & Catalán, P. (2004). Phylogenetic relationships of Vulpia and related genera (Poeae, Poaceae) based on analysis of ITS and trnL–F sequences. Annals of the Missouri Botanical Garden, 91, 124–158.

    Google Scholar 

  • Tzvelev, N. N. (1976). Grasses of the Soviet Union, parts 1 and 2. Leningrad: Nauka. [Cited from the English translation 1984. Rotterdam: A. A. Balkema.]

  • Tzvelev, N. N. (1982). Poryadok zlaki (Poales). Semeystvo zlaki (Poaceae, ili Gramineae). In A. L. Takhtajan (Ed.), Zhizn rasteniy v shesti tomakh, vol. 6 (pp. 341–378). Moskva: Izdatelstvo Prosveshchenie.

  • Tzvelev, N. N. (1989). The system of grasses (Poaceae) and their evolution. The Botanical Review, 55, 141–203.

    Article  Google Scholar 

  • Watson, L., & Dallwitz, M. J. (1992). The Grass genera of the world (revised ed.). Wallingford: CAB International.

    Google Scholar 

  • Watson, L., & Dallwitz, M. J. (1992 onwards). The grass genera of the world: descriptions, illustrations, identification, and information retrieval; including synonyms, morphology, anatomy, physiology, phytochemistry, cytology, classification, pathogens, world and local distribution, and references. Version 23 October 2005. Available at http://delta-intkey.com (Accessed 13 January 2010).

  • Winterfeld, G. (2006). Molekular-cytogenetische Untersuchungen an Hafergräsern (Aveneae) und anderen Poaceae. Stapfia, 86, 1–170.

    Google Scholar 

  • Winterfeld, G., & Röser, M. (2007). Disposition of ribosomal DNAs in the chromosomes of perennial oats (Poaceae: Aveneae). Botanical Journal of the Linnean Society, 155, 193–210.

    Article  Google Scholar 

Download references

Acknowledgements

We wish to thank Natalia V. Tkach and all herbaria listed in the Appendix for providing plant material for our molecular and morphological work. Further, we are very grateful to Bärbel Hildebrandt for technical support in our lab and thank the State Saxony-Anhalt for a fellowship to J.S., and the Deutsche Forschungsgemeinschaft for a research grant (RO 865/8-1).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Röser.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schneider, J., Winterfeld, G. & Röser, M. Polyphyly of the grass tribe Hainardieae (Poaceae: Pooideae): identification of its different lineages based on molecular phylogenetics, including morphological and cytogenetic characteristics. Org Divers Evol 12, 113–132 (2012). https://doi.org/10.1007/s13127-012-0077-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-012-0077-3

Keywords

Navigation