Frequent occurrence of triploid hybrids Festuca pratensis × F. apennina in the Swiss Alps

Abstract

The occurrence of triploid hybrids in nature is scarce due to the so-called triploid block representing formation of nonviable progeny after mating diploid with tetraploid. Here we describe frequent presence of triploids originating from hybridization of diploid Festuca pratensis with tetraploid F. apennina in the Swiss Alps. F. pratensis is a forage grass grown in lowlands and up to 1800 m a.s.l., while F. apennina is a mountain grass found in elevations from 1100 to 2000 m a.s.l. In the overlapping zone these species often grow sympatrically and triploid hybrids have been observed. We show that elevation is the main factor in the distribution of plants with various ploidy levels. Diploids occupy lower elevations, while triploids predominate in the mid-elevation zones and tetraploids are the most frequent in higher elevations. Other factors, such as topography and soil composition probably have only marginal effects on the distribution of the plants with different ploidy levels. Triploids seem to be frequently formed in the Swiss Alps and crosses in both directions are involved in the formation of triploid hybrids. As shown by chloroplast DNA analysis, F. apennina more frequently serves as female. Our analysis suggests that in the mid-elevation zones, triploids have a higher level of competitiveness than both parents. Triploids can overgrow microhabitats to a much higher extent than tetraploids. Such frequent occurrence and local dominance of triploids can at least be partially explained by asexual reproduction. Using DNA markers, we show that triploids can disperse ramets of a single clone over a distance of at least 14.4 m.

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References

  1. Agroscope (2015) Schweizerische Referenzmethoden der For­schungsanstalten Agroscope, Band 1: bodenuntersuchungen zur Düngeberatung, Ausgabe 2015. Agroscope, Zürich

    Google Scholar 

  2. Aleza P, Juarez J, Hernandez M, Ollitrault P, Navarro L (2012) Implementation of extensive citrus triploid breeding programs based on 4X × 2X sexual hybridisations. Tree Genet Genom 8:1293–1306

    Article  Google Scholar 

  3. Alix K, Gerard PR, Schwarzacher T, Heslop-Harrison JS (2017) Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Ann Bot 120:183–194

    Article  Google Scholar 

  4. Augustine DJ, McNaughton SJ (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J Wildl Manage 62:1165–1183

    Article  Google Scholar 

  5. Baird JH, Kopecký D, Lukaszewski AJ, Green RL, Bartoš J, Doležel J (2012) Genetic diversity of turf-type tall fescue using diversity arrays technology. Crop Sci 52:408–412

    Article  Google Scholar 

  6. Barrett SCH, Richardson BJ (1986) Genetic attributes of invading species. In: Groves R, Burdon JJ (eds) Ecology of biological invasions, an Australian perspective. Australian Academy of Sciences, Canberra, pp 21–33

    Google Scholar 

  7. Boller B, Felder T, Kopecký D (2018) Tetraploid Festuca apennina is prone to produce triploid hybrid progeny when crossed with diploid Festuca pratensis. In: Brazauskas G et al (eds) Breeding grasses and protein crops in the era of genomics. Springer, Cham. https://doi.org/10.1007/978-3-319-89578-9

    Google Scholar 

  8. Borrill M, Tyler BF, Morgan WG (1976) Studies in Festuca. 7. Chromosome atlas. 2. Appraisal of chromosome race distribution and ecology, including Festuca pratensis var. apennina (DeNot) Hack.—tetraploid. Cytologia 41:219–236

    Article  Google Scholar 

  9. Budzakova M, Hodalova I, Mereda P, Somlyay L, Bisbing SM, Sibik J (2014) Karyological, morphological and ecological differentiation of Sesleria caerulea and S. tatrae in the Western Carpathians and adjacent regions. Preslia 86:245–277

    Google Scholar 

  10. Clarke J, Chandrasekharan P, Thomas H (1976) Studies in Festuca. 9. Cytological studies of Festuca pratensis var. apennina (DeNot.) Hack. (2n = 28). Z Pflanzenzuchtg 77:205–214

    Google Scholar 

  11. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    CAS  Article  Google Scholar 

  12. Cushman KE, Snyder RG, Nagel DH, Gerard PD (2003) Yield and quality of triploid watermelon cultivars and experimental hybrids grown in Mississippi. Horttechnology 13:375–380

    Google Scholar 

  13. Dolezel J, Greilhuber J, Lucretti S, Meister A, Lysak MA, Nardi L et al (1998) Plant genome size estimation by flow cytometry: inter-laboratory comparison. Ann Bot 82:17–26

    CAS  Article  Google Scholar 

  14. Dolezel J, Greilhuber J, Suda J (2007) Estimation of nuclear DNA content in plants using flow cytometry. Nat Protoc 2:2233–2244

    CAS  Article  Google Scholar 

  15. Eckert CG (2002) Effect of geographical variation in pollinator fauna on the mating system of Decodon verticillatus (Lythraceae). Int J Plant Sci 163:123–132

    Article  Google Scholar 

  16. Fjellheim S, Rognli OA, Fosnes K, Brochmann C (2006) Phylogeographical history of the widespread meadow fescue (Festuca pratensis Huds.) inferred from chloroplast DNA sequences. J Biogeogr 33:1470–1478

    Article  Google Scholar 

  17. Grabherr G (2003) Alpine vegetation dynamics and climate change: a synthesis of long-term studies and observations. Alpine Divers Europe 167:399–409

    Article  Google Scholar 

  18. Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009

    Article  Google Scholar 

  19. Gusmeroli F, Della Marianna G, Fava F, Monteiro A, Bocchi S, Parolo G (2013) Effects of ecological, landscape and management factors on plant species composition, biodiversity and forage value in Alpine meadows. Grass Forage Sci 68:437–447

    Article  Google Scholar 

  20. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  21. Harberd DJ, Owen M (1969) Some experimental observations on clone structure of a natural population of Festuca rubra L. New Phytol 68:93–104

    Article  Google Scholar 

  22. Hoshino Y, Miyashita T, Thomas TD (2011) In vitro culture of endosperm and its application in plant breeding: approaches to polyploidy breeding. Sci Hortic 130:1–8

    CAS  Article  Google Scholar 

  23. Jaccoud D, Peng K, Feinstein D, Kilian A (2001) Diversity arrays: a solid state technology for sequence information independent genotyping. Nucl Acids Res 29:e25

    CAS  Article  Google Scholar 

  24. Jiao YN, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–113

    CAS  Article  Google Scholar 

  25. Jonsdottir IS, Augner M, Fagerstrom T, Persson H, Stenstrom A (2000) Genet age in marginal populations of two clonal Carex species in the Siberian Arctic. Ecography 23:402–412

    Article  Google Scholar 

  26. Kleijn D, Steinger T (2002) Contrasting effects of grazing and hay cutting on the spatial and genetic population structure of Veratrum album, an unpalatable, long-lived, clonal plant species. J Ecol 90:360–370

    Article  Google Scholar 

  27. Kopecký D, Bartoš J, Lukaszewski AJ, Baird JH, Černoch V, Kölliker R, Rognli OA, Blois H, Caig V, Lübberstedt T, Studer B, Shaw P, Doležel J, Kilian A (2009) Development and mapping of DArT markers within the FestucaLolium complex. BMC Genom 10:473–483

    Article  Google Scholar 

  28. Kopecký D, Bartoš J, Christelová P, Černoch V, Kilian A, Doležel J (2011) Genomic constitution of Festuca × Lolium hybrids revealed by the DArTFest array. Theor Appl Genet 122:355–363

    Article  Google Scholar 

  29. Kopecký D, Harper J, Bartoš J, Gasior D, Vrána J, Hřibová E, Boller B, Ardenghi NMG, Šimoníková D, Doležel J, Humphreys MW (2016) An increasing need for productive and stress resilient Festulolium amphiploids: what can be learnt from the stable genomic composition of Festuca pratensis subsp. apennina (De Not.) Hegi? Frontiers Env Sci 4:66

    Article  Google Scholar 

  30. Lakshmi Sita G (1987) Triploids. In: Bonga JM, Durzan DJ (eds) Cell and tissue culture in forestry. Forestry sciences. Springer, Dordrecht, vol 24–26

    Google Scholar 

  31. Lammerts WE (1931) Interspecific hybridization in Nicotiana. XII. The amphidiploid rustica-paniculata hybrid; its origin and cytogenetic behavior. Genetics 16:191–211

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Lohaus R, Van de Peer Y (2016) Of dups and dinos: evolution at the K/Pg boundary. Curr Opin Plant Biol 30:62–69

    CAS  Article  Google Scholar 

  33. Loureiro I, Escorial MC, Chueca MC (2016) Pollen-mediated movement of herbicide resistance genes in Lolium rigidum. Plos One 11:6

    Article  Google Scholar 

  34. Madlung A (2013) Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110:99–104

    CAS  Article  Google Scholar 

  35. Markgraf-Dannenberg I (1980) 4. Festuca L. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea, vol 5. Cambridge University Press, Cambridge, pp 125–153

    Google Scholar 

  36. Marques I, Draper D, López-Herranz ML, Garnatje T, Segarra-Moragues JG, Catalán P (2016) Past climate changes facilitated homoploid speciation in three mountain spiny fescues (Festuca, Poaceae). Sci Rep 6:36283

    CAS  Article  Google Scholar 

  37. Masterson J (1994) Stomatal size in fossil plants—evidence for polyploidy in majority of angiosperms. Science 264:421–424

    CAS  Article  Google Scholar 

  38. Novak SJ, Welfley AY (1997) Genetic diversity in the introduced clonal grass Poa bulbosa (Bulbous bluegrass). Northwest Sci 71:271–280

    Google Scholar 

  39. Pandit MK, Pocock MJO, Kunin WE (2011) Ploidy influences rarity and invasiveness in plants. J Ecol 99:1108–1115

    Article  Google Scholar 

  40. Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501

    Article  Google Scholar 

  41. Rognli OA, Nilsson NO, Nurminiemi M (2000) Effects of distance and pollen competition on gene flow in the wind-pollinated grass Festuca pratensis Huds. Heredity 85:550–560

    CAS  Article  Google Scholar 

  42. Rognli OA, Saha MC, Bhamidimarri S, van der Heijden S (2010) Fescues. Fodd Crops Amenity Grass 5:261–292

    Article  Google Scholar 

  43. Saint-Yves A (1913) Les Festuca de la Section Eu-Festuca et leurs variations. Georg, Geneva. https://doi.org/10.5962/bhl.title.15432

    Google Scholar 

  44. Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588

    CAS  Article  Google Scholar 

  45. Soltis PS, Soltis DE (2016) Ancient WGD events as drivers of key innovations in angiosperms. Curr Opin Plant Biol 30:159–165

    Article  Google Scholar 

  46. Stebbins GL (1940) The significance of polyploidy in plant evolution. Am Nat 74:54–66

    Article  Google Scholar 

  47. Stebbins GL (1957) Self fertilization and population variability in the higher plants. Am Nat 91(861):337–354

    Article  Google Scholar 

  48. Stebler FG (1904) Jahresbericht der Schweizerischen Samenuntersuchungs- und Kontrollstation Zürich. Schweiz Landw Jahrbuch 18:43–46

    Google Scholar 

  49. Suda J (2002) New DNA ploidy level in Empetrum (Empetraceae) revealed by flow cytometry. Ann Bot Fenn 39(2):133–141

    Google Scholar 

  50. Suzuki J-U, Herben T, Krahulec F, Štorchová H, Hara T (2006) Effects of neighbourhood structure and tussock dynamics on genet demography of Festuca rubra in a mountain meadow. J Ecol 94:66–76

    Article  Google Scholar 

  51. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of 3 noncoding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109

    CAS  Article  Google Scholar 

  52. Tamura K, Uwatoko N, Yamashita H, Fujimori M, Akiyama Y, Shoji A et al (2016) Discovery of natural interspecific hybrids between Miscanthus Sacchariflorus and Miscanthus Sinensis in Southern Japan: morphological characterization, genetic structure, and origin. Bioenerg Res 9:315–325

    Article  Google Scholar 

  53. te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubesova M et al (2012) The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot 109:19–45

    Article  Google Scholar 

  54. Torrecilla P, Acedo C, Marques I, Díaz-Pérez AJ, López-Rodríguez JA, Mirones V, Sus A, Llamas F, Alonso A, Pérez-Collazos E, Viruel J, Sahuquillo E, Del Carmen Sancho M, Komac B, Manso JA, Segarra-Moragues JG, Draper D, Villar L, Catalán P (2013) Morphometric and molecular variation in concert: taxonomy and genetics of the reticulate Pyrenean and Iberian alpine spiny fescues (Festuca eskia complex, Poaceae). Bot J Linn Soc 173:676–706

    Article  Google Scholar 

  55. Tyler BF (1988) Description and distribution of natural variation in forage grasses. In: Proceedings of the Eucarpia fodder crops section meeting, (Lusignan, France), pp 13–22

  56. Tyler B, Borrill M, Chorlton K (1978) Studies in Festuca. 10. Observations on germination and seedling cold tolerance in diploid Festuca pratensis and tetraploid F. pratensis var. apennina in relation to their altitudinal distribution. J Appl Ecol 15:219–226

    Article  Google Scholar 

  57. Uwatoko N, Tamura K, Yamashita H, Gau M (2016) Naturally occurring triploid hybrids between Miscanthus sacchariflorus and M. sinensis in Southern Japan, show phenotypic variation in agronomic and morphological traits. Euphytica 212:355–370

    CAS  Article  Google Scholar 

  58. Wagenaar EB (1968) Meiotic restitution and origin of polyploidy. 2. Influence of genotype on polyploid seedset in a Triticum crissum × T. turgidum hybrid. Can J Genet Cyt 10:836–843

    Article  Google Scholar 

  59. WallisDeVries MF, Laca EA, Demment MW (1999) The importance of scale of patchiness for selectivity in grazing herbivores. Oecologia 121:355–363

    CAS  Article  Google Scholar 

  60. Wang ZY, Ge YX, Scott M, Spangenberg G (2004) Viability and longevity of pollen from transgenic and nontransgenic tall fescue (Festuca arundinacea) (Poaceae) plants. Am J Bot 91:523–530

    Article  Google Scholar 

  61. Wang XL, Cheng ZM, Zhi S, Xu FX (2016) Breeding triploid plants: a review. Czech J Genet Plant 52:41–54

    CAS  Article  Google Scholar 

  62. Watrud LS, Lee EH, Fairbrother A, Burdick C, Reichman JR, Bollman M et al (2004) Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. P Natl Acad Sci USA 101:14533–14538

    CAS  Article  Google Scholar 

  63. Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends Plant Sci 7:270–277

    CAS  Article  Google Scholar 

  64. Zhang CH, Zhang SL, Shen SX, Wang M, Wang YH (2001) Observation on obtaining the triploid by 4X × 2X and its cytoembryology in false pakchoi. Acta Hortic Sinica 28:317–322

    Google Scholar 

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Acknowledgements

We would like to express our thanks to Prof. Adam J. Lukaszewski for critical reading and valuable comments on the manuscript. Special thanks belong to the team of Diversity Arrays Ltd. lead by Dr. Andrzej Kilian for their help in processing the data on analysis of clonality and Dr. Jan Vrána and Eva Jahnová for technical assistance on flow cytometry measurements. We greatly appreciated the support of Dr. Manuel Schneider in identifying suitable sampling locations, and we wish to thank Cheng Zhao for technical assistance.

Funding

This study was partially funded by the grant award LO1204 from the National Program of Sustainability I. and the Czech Academy of Sciences Long-Term Research Development Project RVO 67985939.

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TF, FXS and BB sampled the specimens, DK and JD conducted flow cytometry measurements, VM performed chloroplast DNA analysis, DK and JB analyzed clonality using Diversity Arrays Technology, TF, FXS and BB realized soil analysis, DK drafted the manuscript, BB and JD revised manuscript critically for important intellectual content.

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Correspondence to David Kopecký.

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Kopecký, D., Felder, T., Schubiger, F.X. et al. Frequent occurrence of triploid hybrids Festuca pratensis × F. apennina in the Swiss Alps. Alp Botany 128, 121–132 (2018). https://doi.org/10.1007/s00035-018-0204-7

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Keywords

  • Asexual reproduction
  • Triploid
  • Grass
  • Festuca
  • Hybrid
  • Clonality
  • Fescue