Cryptic invasion suggested by a cytogeographic analysis of the halophytic Puccinellia distans complex (Poaceae) in Central Europe
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
37929170
PubMed Central
PMC10620967
DOI
10.3389/fpls.2023.1249292
Knihovny.cz E-zdroje
- Klíčová slova
- Puccinellia distans agg., cryptic invasion, cytogeography, flow cytometry, genetic pollution, halophyte, polyploidy,
- Publikační typ
- časopisecké články MeSH
INTRODUCTION: Despite the wealth of studies dealing with the invasions of alien plants, invasions of alien genotypes of native species (cryptic invasions) have been vastly neglected. The impact of cryptic invasions on the biodiversity of plant communities can, however, be significant. Inland saline habitats and halophytes (i.e., salt-tolerant plant species) are especially threatened by this phenomenon as they inhabit fragmented remnants of largely destroyed habitats, but at the same time some of these halophytic species are rapidly spreading along salt-treated roads. To study potential cryptic invasion of halophytes, the patterns of genome size and ploidy variation in the Puccinellia distans complex (Poaceae), the most rapidly spreading roadside halophyte in Central Europe, were investigated. METHODS: DNA flow cytometry with confirmatory chromosome counts were employed to assess ploidy levels of 1414 individuals from 133 populations of the P. distans complex. In addition, climatic niche modelling was used to predict the distributions of selected cytotypes. RESULTS: Eight groups differing in ploidy level and/or genome size were discovered, one diploid (2x; 2n = 14), two tetraploid (4xA, 4xB; 2n = 28), one pentaploid (5x; 2n = 35), three hexaploid (6xA, 6xB, 6xC; 2n = 42), and one heptaploid (7x; 2n = 49). The hexaploids (mostly the 6xC cytotype) were widespread through the study area, spreading intensively in both anthropogenic and natural habitats and probably hybridizing with the natural habitat dwelling tetraploids. In contrast, the non-hexaploid cytotypes rarely spread and were predominantly confined to natural habitats. DISCUSSION: The extensive spread of the hexaploid cytotypes along roadsides has most likely facilitated their incursion into natural habitats. The colonization of new natural habitats by the hexaploids may pose a threat to the indigenous Puccinellia populations by compromising their genetic integrity and/or by outcompeting them.
Botanischer Garten und Botanisches Museum Berlin Freie Universität Berlin Berlin Germany
Department of Botany and Biodiversity Research University of Vienna Vienna Austria
Department of Botany Faculty of Science Charles University Prague Czechia
Department of Botany Faculty of Science University of South Bohemia České Budějovice Czechia
Department of Botany National Museum Prague Czechia
Independent Researcher Celldömölk Hungary
Institute of Botany Czech Academy of Sciences Průhonice Czechia
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Ainouche M. L., Gray A. (2016). Invasive Spartina: lessons and challenges. Biol. Invasions 18, 2119–2122.
Amarell U., Gregor T. (2021). Puccinellia fontana (Portal) Amarell & T. Gregor comb. et stat. nov. – ein halophytisches Gras Mittel- und Westeuropas. Kochia 14, 61–73.
Anonymous (2008). Rote Liste der Farn- und Blütenpflanzen des Saarlandes (Saarbrúcken: Ministerium für Umwelt und Verbraucherschutz; ).
Avdulow N. P. (1931). Karyosystematische untersuchungen der familie gramineen. Bull. Appl. botany Genet. plant-breeding 43, 353–425.
Bellstedt R., Bettinger A., Böttcher H., Gőri S., Grimm H., Hartenauer K., et al. . (2005). Binnensalzstellen mitteleuropas (Bad Frankenhausen: Thüringer Ministerium für Landwirtschaft, Naturschutz und Umwelt; ).
Belyayev A., Paštová L., Fehrer J., Josefiová J., Chrtek J., Mráz P. (2018). Mapping of Hieracium (Asteraceae) chromosomes with genus-specific satDNA elements derived from next generation sequencing data. Plant Syst. Evol. 304, 387–396.
Bozdogan H. (1987). Model selection and Akaike’s Information Criterion (AIC): The general theory and its analytical extensions. Psychometrika 52, 345–370.
Chapman G. P. (1996). The biology of grasses (Wallingford, Oxon, UK: CAB International; ).
Conert H. J. (1994). “ Puccinellia ,” in Illustrierte Flora von Mitteleuropa. Begründet von Gustav Hegi. Spermatophyta: Angiospermae: Monocotyledones 1(2). Poaceae (Echte Gräser oder Süßgräser). Eds. Hegi G., Conert J. (Berlin: Parey Buchverlag; ), 488–501.
Conway J. R., Lex A., Gehlenborg N. (2017). UpSetR: an R package for the visualization of intersecting sets and their properties. Bioinformatics 33, 2938–2940. PubMed PMC
Daneshgar P., Jose S., Collins A., Ramsey C. (2008). Cogongrass (Imperata cylindrica), an alien invasive grass, reduces survival and productivity of an establishing pine forest. For. Sci. 54, 579–587.
Deák B., Valkó O., Tóthmérész B., Török P. (2014). “Alkali marshes of Central-Europe: ecology, management and nature conservation,” in Salt marshes: ecosystem vegetation and restoration strategies. Ed. Shao H.-B. (New York: Nova Science Publishers; ), 1–11.
Dítě D., Eliáš P., Šuvada R. (2009). The current distribution and status of community Puccinellietum limosae in Slovakia. Thaiszia – J. Bot. 19, 63–70.
Doležel J., Greilhuber J., Suda J. (2007). Estimation of nuclear DNA content in plants using flow cytometry. Nat. Protoc. 2, 2233–2244. PubMed
Ehl S., Mildenberger K., Frankenberg T., Ries C. (2019). Halophytes in roadside habitats: a survey of salt-tolerant vascular plant species along roads in Luxembourg. B. Soc Nat. Lux. 121, 37–51.
Eliáš P., Sopotlieva D., Dítě D., Hájková P., Apostolova I., Senko D., et al. . (2013). Vegetation diversity of salt-rich grasslands in Southeast Europe. Appl. Veg. Sci. 16, 521–537.
Englmaier P. (1982). Gliederung der Puccinellia distans-Gruppe (Poaceae) in Österreich. Stapfia 10, 81–94.
Fick S., Hijmans R. (2017). WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315.
Grulich V. (2012). Red List of vascular plants of the Czech Republic: 3rd edition. Preslia 84, 631–645.
Hackel E. (1902). Atropis pannonica nov. spec. Magyar Botanikai Lapok 1, 41–43.
Hardion L., Verlaque R., Saltonstall K., Leriche A., Vila B. (2014). Origin of the invasive Arundo donax (Poaceae): a trans-Asian expedition in herbaria. Ann. Bot. 114, 455–462. PubMed PMC
Harris S. A. (2014). Grasses (London: Reaktion Books; ).
Hetzel G. (2006). Die neophyten oberfrankens. Floristik, standortcharakteristik, vergesellschaftung, verbreitung, dynamik (Würzburg: Bayerischen Julius-Maximilians-Universität; ).
Hodkinson T. R. (2018). Evolution and taxonomy of the grasses (Poaceae): a model family for the study of species-rich groups. Ann. Plant Rev. 1, 1–39.
Holmberg O. R. (1920). Einige puccinellia-arten und -hybriden. Bot. Notiser 3, 103–112.
Hughes W. E. (1976). The taxonomy of the genus Puccinellia Parl. (Gramineae) (Leicester: University of Leicester; ).
Kass J., Vilela B., Aiello-Lammens M., Muscarella R., Merow C., Anderson R. (2018). WALLACE: A flexible platform for reproducible modeling of species niches and distributions built for community expansion. Methods Ecol. Evol. 9, 1151–1156.
Keeler K. J. (1998). “Population biology of intraspecific polyploidy in grasses,” in Population biology of biology of grasses. Ed. Cheplick G. (Cambridge: Cambridge University Press; ), 183–207.
Kúr P., Gregor T., Jandová M., Mesterházy A., Paule J., Píšová S., et al. . (2023). Cryptic invasion suggested by cytogeographic analysis of the halophytic Puccinellia distans complex (Poaceae) in Central Europe. doi: 10.5281/zenodo.8077314. Data from: Kúr. PubMed DOI PMC
Kúr P., Píšová S., Tremetsberger K., Dřevojan P., Kacki Z., Böckelmann J., et al. . (2021). Ecology and genetics of Cyperus fuscus in Central Europe-a model for ephemeral wetland plant research and conservation. Water 13 (9), 1277.
Levin D., Ortega F. J., Jansen R. (1996). Hybridization and the extinction of rare plant species. Conserv. Biol. 10, 10–16.
Link C. T. (1992). Untersuchungen zur Polymorphie des Puccinellia-distans-complex (Marburg: Philipps Universität; ).
Marcinkowska-Ochtyra A., Jarocinska A., Bzdega K., Tokarska-Guzik B. (2018). Classification of expansive grassland species in different growth stages based on hyperspectral and LiDAR data. Remote Sens. 10 (12), 2019.
McCaw Z. (2021). MGMM: missingness aware gaussian mixture models (Ver. 1.0.0). Available at: https://CRAN.R-project.org/package=MGMM (Accessed June 12, 2021).
Merow C., Smith M., Silander J. (2013). A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36, 1058–1069.
Měsíček J., Javůrková-Jarolímová V. (1992). List of chromosome numbers of the Czech vascular plants (Praha: Academia; ).
Montserrat G., Montserrat J. M. (1988). Puccinellia caespitosa (Poaceae) a new species from Spain. Collectanea Botanica 17, 79–82.
Mooij W. M., Hulsmann S., Domis L. N. S., Nolet B. A., Bodelier P. L. E., Boers P. C. M., et al. . (2005). The impact of climate change on lakes in the Netherlands: a review. Aquat. Ecol. 39, 381–400.
Moravcová L., Jarolímová V., Zákravský P. (2001). Morphological differences and chromosome numbers in Puccinellia distans and P. limosa populations from Central Europe. Preslia 73, 161–172.
Moura R., Queiroga D., Vilela E., Moraes A. (2021). Polyploidy and high environmental tolerance increase the invasive success of plants. J. Plant Res. 134, 105–114. PubMed
Oliveira G. C., Arruda D. M., Fernandes F. E. I., Veloso G. V., Francelino M. R., Schaefer C. E. G. R. (2021). Soil predictors are crucial for modelling vegetation distribution and its responses to climate change. Sci. Total Environ. 780, 146680. PubMed
Opitz A. (2019). Rote Liste der Farn- und Samenpflanzen Hessens (Wiesbaden: Hessisches Landesamt für Naturschutz, Umwelt und Geologie; ).
Otto F. (1990). “DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA,” in Methods in cell biology. Eds. Crissman H. A., Darzynkiewicz Z. (New York: Academic Press; ), 105–110. PubMed
Pandit M., Pocock M., Kunin W. (2011). Ploidy influences rarity and invasiveness in plants. J. Ecol. 99, 1108–1115.
Paule J., Gregor T., Schmidt M., Gerstner E.-M., Dersch G., Dressler S., et al. . (2017). Chromosome numbers of the flora of Germany—a new online database of georeferenced chromosome counts and flow cytometric ploidy estimates. Plant Syst. Evol. 303, 1123–1129.
Petsch D. (2016). Causes and consequences of biotic homogenization in freshwater ecosystems. Int. Rev. Hydrobiol. 101, 113–122.
Phillips S., Anderson R., Schapire R. (2006). Maximum entropy modelling of species geographic distributions. Ecol. Model. 190, 231–259.
Phillips S., Dudik M. (2008). Modelling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31, 161–175.
Pignatti S., Guarino R., Rosa M. L. (2017). Flora d’Italia (Bologna: Edagricole; ).
Pijnacker L. P., Ferwerda M. A. (1984). Giemsa C-banding of potato chromosomes. Can. J. Genet. Cytol. 26, 415–419.
Ramsey J., Schemske D. W. (2002). Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33, 589–639.
R Development Core Team (2022) R: a language and environment for statistical computing (Vienna: R Foundation for Statistical Computing; ). Available at: http://cran.r-project.org (Accessed May 22, 2022).
Rice A., Glick L., Abadi S., Einhorn M., Kopelman N. M., Salman-Minkov A., et al. . (2015). The Chromosome Counts Database (CCDB) – a community resource of plant chromosome numbers. New Phytol. 206, 19–26. PubMed
Saltonstall K. (2002). Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. P. Natl. Acad. Sci. U.S.A. 99, 2445–2449. PubMed PMC
Schur P. J. F. (1866). Enumeratio plantarum Transsilvaniae: exhibens: stirpes phanerogamas sponte crescentes atque frequentius cultas, cryptogamas vasculares, characeas, etiam muscos hepaticasque (Vienna: Sumptibus C. Graeser; ).
Šerá B. (2008). Road vegetation in Central Europe - an example from the Czech Republic. Biologia 63, 1085–1088.
Šerá B. (2010). Road-side herbaceous vegetation: life history groups and habitat preferences. Pol. J. Ecol. 58, 69–79.
Šerá B. (2011). Stress tolerant plant species spread in the road-net. Ecol. Questions 14, 45–46.
Simon L., Rühl D. (2007). Rote listen von rheinland-pfalz. (Meinz: Landesamt für Umwelt, Gewässer und Gewerbeaufsicht; ).
Šmarda P., Bureš P. (2010). Understanding intraspecific variation in genome size in plants. Preslia 82, 41–61.
Šumberová K., Vild O., Duchacek M., Fabsicova M., Potuzak J., Frankova M. (2021). Drivers of macrophyte and diatom diversity in a shallow hypertrophic lake. Water 13 (11), 1569.
Sutherland B. L., Galloway L. F. (2017). Postzygotic isolation varies by ploidy level within a polyploid complex. New Phytol. 213, 404–412. PubMed
te Beest M., Le Roux J. J., Richardson D. M., Brysting A. K., Suda J., Kubesová M., et al. . (2012). The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109, 19–45. PubMed PMC
Temsch E. M., Koutecký P., Urfus T., Šmarda P., Doležel J. (2021). Reference standards for flow cytometric estimation of absolute nuclear DNA content in plants. Cytometry Part A 2021, 1–15. PubMed PMC
Trávníček P., Eliášová A., Suda J. (2010). The distribution of cytotypes of Vicia cracca in Central Europe: the changes that have occurred over the last four decades. Preslia 82, 149–163.
Walczyk A. (2018). Evaluating the interactive roles of soil nutrients and polyploidy on competitive outcomes of Chamerion angustifolium. (Houghton: Michigan Technological University; ).
Herbarium specimens reveal a cryptic invasion of polyploid Centaurea stoebe in Europe