Advertisement

Plant Systematics and Evolution

, Volume 301, Issue 1, pp 279–290 | Cite as

Sexual reproduction as a source of ploidy level variation in the model agamic complex of Pilosella bauhini and P. officinarum (Asteraceae: Lactuceae)

  • Radka RosenbaumováEmail author
  • František Krahulec
Original Article

Abstract

We studied the significance of sexual reproduction as a source of ploidy level variation in a model system consisting of hexaploid, facultatively apomictic Pilosella bauhini and tetraploid, sexual P. officinarum. As the maternal parent, apomictic P. bauhini generated higher ploidy level variation than sexual P. officinarum. Ploidy levels of its progeny ranged from triploid to octoploid under experimental conditions and even to decaploid in the field. This progeny diversity resulted from the breeding system in P. bauhini, which included haploid parthenogenesis and sexual reproduction through both reduced and unreduced gametes besides prevailing apomixis; these particular reproductive pathways have been quantified. Sexual P. officinarum, on the other hand, reproduced exclusively through fusion of reduced gametes and produced only pentaploid hybrids or tetraploid progeny from autogamy, allogamy or both. Surprisingly, sexual P. officinarum was also the species showing stronger reproductive isolation, especially under the field conditions where intra-specific fertilization was highly favoured, most probably through competition between conspecific and heterospecific pollen. Apomictic P. bauhini thus appeared to be a significant source of ploidy level variation in the model population even though most of its progeny was formed clonally through apomixis. Only part of this variation was manifested in the field.

Keywords

Facultative apomixis Haploid parthenogenesis Hybridization Pilosella Residual sexuality Unreduced gametes 

Notes

Acknowledgments

We thank to Anna Krahulcová for many critical and useful comments. This work was financially supported by the Ministry of Culture of the Czech Republic (DKRVO 2013/09, National Museum, 00023272 to RR) and by the long-term institutional research plan No. AVOZ60050516 from the Academy of Sciences of the Czech Republic (to FK).

References

  1. Asker SE, Jerling L (1992) Apomixis in plants. CRC Press, Boca RatonGoogle Scholar
  2. Bayer RJ, Chandler GT (2007) Evolution of polyploid agamic complexes: a case study using the Catipes group of Antennaria, including the A. rosea complex (Asteraceae: Gnaphalieae). In: Grossniklaus U, Hörandl E, Sharbel T, van Dijk P (eds) Apomixis: evolution, mechanisms and perspectives. Regnum Vegetabile 147, Koelz Scientific Books, Koenigstein, pp 317–336Google Scholar
  3. Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16:228–245CrossRefGoogle Scholar
  4. Bicknell RA, Lambie SC, Butler RC (2003) Quantification of progeny classes in two facultatively apomictic accessions of Hieracium. Hereditas 138:11–20PubMedCrossRefGoogle Scholar
  5. Bräutigam S, Greuter W (2007) A new treatment of Pilosella for the Euro-Mediterranean flora [Notulae ad floram euro-mediterraneam pertinentes 24]. Willdenowia 37(1):123–137CrossRefGoogle Scholar
  6. Brock MT (2004) The potential for genetic assimilation of a native dandelion species, Taraxacum ceratophorum (Asteraceae), by the exotic congener T. officinale. Amer J Bot 91:656–663CrossRefGoogle Scholar
  7. Chapman HM, Parh D, Oraguzie N (2000) Genetic structure and colonizing success of a clonal, weedy species, Pilosella officinarum (Asteraceae). Heredity 84:401–409PubMedCrossRefGoogle Scholar
  8. Darlington CD (1939) The evolution of genetic systems. Cambridge University Press, CambridgeGoogle Scholar
  9. de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants, 2nd edn. Springer, BerlinCrossRefGoogle Scholar
  10. Desroches AM, Rieseberg LH (1998) Mentor effects in wild species of Helianthus (Asteraceae). Amer J Bot 85:770–775CrossRefGoogle Scholar
  11. Dickinson TA (1998) Taxonomy of agamic complexes in plants: a role for metapopulation thinking. Folia Geobot 33:327–332CrossRefGoogle Scholar
  12. Fehrer J, Šimek R, Krahulcová A, Krahulec F, Chrtek J, Bräutigam E, Bräutigam S (2005) Evolution, hybridisation, and clonal distribution of apo- and amphimictic species of Hieracium subgen. Pilosella (Asteraceae, Lactuceae) in a Central European mountain range. In: Bakker FT, Chatrou LW, Gravendeel B, Pelser PB (eds) Plant species-level systematics: new perspectives on pattern and process. Regnum Vegetabile 143, Koelz Scientific Books, Koenigstein, pp 175–201Google Scholar
  13. Fehrer J, Krahulcová A, Krahulec F, Chrtek J Jr, Rosenbaumová R, Bräutigam S (2007) Evolutionary aspects in Hieracium subgenus Pilosella. In: Grossniklaus U, Hörandl E, Sharbel T, van Dijk P (eds) Apomixis: evolution, mechanisms and perspectives. Regnum Vegetabile 147, Koelz Scientific Books, Koenigstein, pp 359–390Google Scholar
  14. Gadella ThWJ (1982) Cytology and reproduction of Hieracium pilosella L. and some related diploid species. Acta Bot Neerl 31:140–141Google Scholar
  15. Gadella ThWJ (1984) Cytology and the mode of reproduction of some taxa of Hieracium subgenus Pilosella. Proc K Ned Akad Wet 87:387–399Google Scholar
  16. Gadella ThWJ (1987) Sexual tetraploid and apomictic pentaploid populations of Hieracium pilosella (Compositae). Plant Syst Evol 157:219–246CrossRefGoogle Scholar
  17. Gadella ThWJ (1988) Some notes on the origin of polyploidy in Hieracium pilosella aggr. Acta Bot Neerl 37:515–522Google Scholar
  18. Gadella ThWJ (1991) Variation, hybridization and reproductive biology of Hieracium pilosella L. Proc K Ned Akad Wet 94(4):455–488Google Scholar
  19. Gadella ThWJ (1992) Notes of some triple and inter-sectional hybrids in Hieracium L. subgenus Pilosella (Hill) S. F. Gray. Proc K Ned Akad Wet 95:51–63Google Scholar
  20. Grossniklaus U (2001) From sexuality to apomixis: molecular and genetic approaches. In: Savidan Y, Carman JG, Dresselhaus T (eds) The flowering of apomixis: from mechanisms to genetic engineering. CIMMYT, IRD, EC, Mexico, pp 168–211Google Scholar
  21. Grossniklaus U, Nogler GA, van Dijk PJ (2001) How to avoid sex: the genetic control of gametophytic apomixis. The Plant Cell 13(7):1491–1497PubMedCentralPubMedCrossRefGoogle Scholar
  22. Harlan JR, de Wet JMJ (1975) On Ö. Winge and a prayer: the origins of polyploidy. Bot Rev 41:361–390CrossRefGoogle Scholar
  23. Hörandl E (1998) Species concepts in agamic complexes: applications in the Ranunculus auricomus complex and general perspectives. Folia Geobot 33:335–348CrossRefGoogle Scholar
  24. Koltunow AM (1993) Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. The Plant Cell 5:1425–1437PubMedCentralPubMedCrossRefGoogle Scholar
  25. Koltunow AM, Bicknell RA, Chaudhury AM (1995) Apomixis: molecular strategies for the generation of genetically identical seeds without fertilization. Plant Physiol 108:1345–1352PubMedCentralPubMedGoogle Scholar
  26. Koltunow AM, Johnson SD, Bicknell RA (1998) Sexual and apomictic development in Hieracium. Sex Plant Reprod 11:213–230CrossRefGoogle Scholar
  27. Koutecký P, Baďurová T, Štech M, Košiar J, Karásek J (2011) Hybridization between diploid Centaurea pseudophrygia and tetraploid C. jacea (Asteraceae): the role of mixed pollination, unreduced gametes, and mentor effects. Biol J Linn Soc 104:93–106CrossRefGoogle Scholar
  28. Krahulcová A, Krahulec F (2000) Offspring diversity in Hieracium subgen. Pilosella (Asteraceae): new cytotypes from hybridization experiments and from open pollination. Fragm Florist Geobot 45(1–2):239–255Google Scholar
  29. Krahulcová A, Chrtek J, Krahulec F (1999) Autogamy in Hieracium subgen. Pilosella Folia Geobot 34:373–376CrossRefGoogle Scholar
  30. Krahulcová A, Krahulec F, Chapman HM (2000) Variation in Hieracium subgen. Pilosella (Asteraceae): what do we know about its sources? Folia Geobot 35:319–338CrossRefGoogle Scholar
  31. Krahulcová A, Papoušková S, Krahulec F (2004) Reproduction mode in the allopolyploid facultatively apomictic hawkweed Hieracium rubrum (Asteraceae, H. subgen. Pilosella). Hereditas 141:19–30PubMedCrossRefGoogle Scholar
  32. Krahulcová A, Rotreklová O, Krahulec F, Rosenbaumová R, Plačková I (2009) Enriching ploidy level diversity: the role of apomictic and sexual biotypes of Hieracium subgen. Pilosella (Asteraceae) that coexist in polyploid populations. Folia Geobot 44:281–306CrossRefGoogle Scholar
  33. Krahulcová A, Krahulec F, Rosenbaumová R (2011) Expressivity of apomixis in 2n + n hybrids from an apomictic and a sexual parent: insights into variation detected in Pilosella (Asteraceae: Lactuceae). Sex Plant Reprod 24:63–74PubMedCrossRefGoogle Scholar
  34. Krahulcová A, Raabe U, Krahulec F (2012) Prozesse innerhalb hybridisierender Pilosella-Populationen: P. aurantiaca und P. officinarum in Hagen (Nordrhein-Westfalen). Kochia 6:123–142Google Scholar
  35. Krahulcová A, Rotreklová O, Krahulec F (2014) The detection, rate and manifestation of residual sexuality in apomictic populations of Pilosella (Asteraceae, Lactuceae). Folia Geobot 49(2). doi: 10.1007/s12224-013-9166-0
  36. Krahulec F, Krahulcová A, Fehrer J, Bräutigam S, Plačková I, Chrtek J Jr (2004) The Sudetic group of Hieracium subgen. Pilosella from the Krkonoše Mts: a synthetic view. Preslia 76:223–243Google Scholar
  37. Krahulec F, Krahulcová A, Papoušková S (2006) Ploidy level selection during germination and early stages of seedling growth in the progeny of allohexaploid facultative apomict, Hieracium rubrum (Asteraceae). Folia Geobot 41:407–416CrossRefGoogle Scholar
  38. Krahulec F, Krahulcová A, Fehrer J, Bräutigam S, Schuhwerk F (2008) The structure of the agamic complex of Hieracium subgen. Pilosella in the Šumava Mts and its comparison with other regions in Central Europe. Preslia 80:1–26Google Scholar
  39. Krahulec F, Krahulcová A, Rosenbaumová R, Plačková I (2011) Production of polyhaploids by facultatively apomictic Pilosella can result in formation of new genotypes via genome doubling. Preslia 83:471–490Google Scholar
  40. Leong-Škorničková J, Šída O, Jarolímová V et al (2007) Chromosome numbers and genome size variation in Indian species of Curcuma (Zingiberaceae). Ann of Bot 100:505–526CrossRefGoogle Scholar
  41. Loomis ES, Fishman L (2009) A continent wide clone: population genetic variation of the invasive plant Hieracium aurantiacum (orange hawkweed; Asteraceae) in North America. Int J Plant Sci 170(6):759–765CrossRefGoogle Scholar
  42. Mártonfiová L (2006) Possible pathways of the gene flow in Taraxacum Sect. Ruderalia. Folia Geobot 41:183–201CrossRefGoogle Scholar
  43. Matzk F, Meister A, Brutovska R, Schubert I (2001) Reconstruction of reproductive diversity in Hypericum perforatum L. opens novel strategies to manage apomixis. Plant J 26:275–282PubMedCrossRefGoogle Scholar
  44. Matzk F, Hammer K, Schubert I (2003) Co-evolution of apomixis and genome size within the genus Hypericum. Sex Plant Reprod 16:51–58CrossRefGoogle Scholar
  45. Morita T, Menken SBJ, Sterk AA (1990) Hybridization between European and Asian dandelions (Taraxacum section Ruderalia and section Mongolica). 1. Crossability and breakdown of self-incompatibility. New Phytol 114:519–529CrossRefGoogle Scholar
  46. Mráz P (2003) Mentor effects in the genus Hieracium s.str. (Compositae, Lactuceae). Folia Geobot 38(3):345–350CrossRefGoogle Scholar
  47. Nägeli C, Peter A (1885) Die Hieracien Mittel–Europas. Monographische Bearbeitung der Piloselloiden mit besonderer Berücksichtigung der mitteleuropäischen Sippen. R. Oldenbourg, MünchenGoogle Scholar
  48. Naumova TN (2008) Apomixis and amphimixis in flowering plants. Cytol Genet 42:51–53CrossRefGoogle Scholar
  49. Naumova TN, van der Laak J, Osadtchiy J, Matzk F, Kravtchenko A, Bergervoet J, Ramulu KS, Boutilier K (2001) Reproductive development in apomictic populations of Arabis holboellii (Brassicaceae). Sex Plant Reprod 14:195–200PubMedCrossRefGoogle Scholar
  50. Nogler GA (1984) Gametophytic apomixis. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, pp 475–518CrossRefGoogle Scholar
  51. Noyes RD, Rieseberg LH (2000) Two independent loci control agamospermy (apomixis) in the triploid flowering plant Erigeron annuus. Genet 155:379–390Google Scholar
  52. Ostenfeld CH (1906) Experimental and cytological studies in the Hieracia. I. Castration and hybridization experiments with some species of Hieracia. Bot Tidsskr 27:225–248Google Scholar
  53. Otto F (1990) DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. Methods in Cell Biol 33:105–110CrossRefGoogle Scholar
  54. Richards AJ (2003) Apomixis in flowering plants: an overview. Philos Trans R Soc Lond Series B Biological Sciences 358:1085–1093CrossRefGoogle Scholar
  55. Rieseberg LH, Desrochers AM, Youn SJ (1995) Interspecific pollen competition as a reproductive barrier between sympatric species of Helianthus (Asteraceae). Amer J Bot 82(4):515–519CrossRefGoogle Scholar
  56. Rieseberg LH, Baird SJE, Desrochers AM (1998) Patterns of mating in wild sunflower hybrid zones. Evolution 52(3):713–726CrossRefGoogle Scholar
  57. Rosenbaumová R, Krahulcová A, Krahulec F (2012) The intriguing complexity of parthenogenesis inheritance in Pilosella rubra (Asteraceae, Lactuceae). Sex Plant Reprod 25(3):185–196PubMedCrossRefGoogle Scholar
  58. Rotreklová O (2008) Hieracium subgen. Pilosella: pollen stainability in sexual, apomictic and sterile plants. Biol 63(1):61–66CrossRefGoogle Scholar
  59. Rotreklová O, Krahulcová A, Vaňková D, Peckert T, Mráz P (2002) Chromosome numbers and breeding systems in some species of Hieracium subgen. Pilosella from Central Europe. Preslia 74:27–44Google Scholar
  60. Sharbel TF, Mitchell-Olds T (2001) Recurrent polyploid origins and chloroplast phylogeography in the Arabis holboellii complex (Brassicaceae). Heredity 87:59–68PubMedCrossRefGoogle Scholar
  61. Skalińska M (1971a) Experimental and embryological studies in Hieracium aurantiacum L. Acta Biol Cracov Ser Bot 14:139–159Google Scholar
  62. Skalińska M (1971b) Further studies in apomixis of Hieracium aurantiacum L. Genet Pol 12:209–212Google Scholar
  63. Skalińska M (1971c) Further studies in twins of Hieracium aurantiacum L. Acta Biol Cracov Ser Bot 14:43–53Google Scholar
  64. Skalińska M (1973) Further studies in facultative apomixis of Hieracium aurantiacum L. Acta Biol Cracov Ser Bot 16:121–133Google Scholar
  65. Skalińska M (1976) Cytological diversity in the progeny of octoploid facultative apomicts of Hieracium aurantiacum. Acta Biol Cracov Ser Bot 19:39–46Google Scholar
  66. Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New YorkGoogle Scholar
  67. Suda J, Krahulcová A, Trávníček P, Rosenbaumová R, Peckert T, Krahulec F (2007) Genome size variation and species relationships in Hieracium sub-genus Pilosella (Asteraceae) as inferred by flow cytometry. Ann of Bot 100:1323–1335CrossRefGoogle Scholar
  68. Tas ICQ, van Dijk PJ (1999) Crosses between sexual and apomictic dandelions (Taraxacum). I. The inheritance of apomixis. Heredity 83:707–714PubMedCrossRefGoogle Scholar
  69. Urfus T, Krahulec F, Krahulcová A. (2014) Hybridization within a Pilosella population: a morphometric analysis. Folia Geobot 49(2). doi: 10.1007/s12224-013-9179-8
  70. van Dijk PJ, Vijverberg K (2005) The significance of apomixis in the evolution of the angiosperms: a reappraisal. In: Bakker FT, Chatrou LW, Gravendeel B, Pelser PB (eds) Plant species-level systematics: new perspectives on pattern and process. Regnum Vegetabile 143, Koelz Scientific Books, Koenigstein, pp 175–201Google Scholar
  71. van Dijk PJ, van Baarlen P, de Jong JH (2003) The occurrence of phenotypically complementary apomixis-recombinants in crosses between sexual and apomictic dandelions (Taraxacum officinale). Sex Plant Reprod 16:71–76CrossRefGoogle Scholar
  72. Verduijn MH, Van Dijk PJ, Van Damme JMM (2004) The role of tetraploids in the sexual–asexual cycle in dandelions (Taraxacum). Heredity 93:390–398PubMedCrossRefGoogle Scholar
  73. Whitton J, Sears CJ, Baack EJ, Otto SP (2008) The dynamic nature of apomixis in the angiosperms. Int J Plant Sci 169(1):169–182CrossRefGoogle Scholar
  74. Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15(4):1039–1053CrossRefGoogle Scholar
  75. Zahn KH (1922–1930) Hieracium. In: Ascherson P, Graebner P (eds) Synopsis der mitteleuropäischen Flora 12(1). Gebrüder Bornträger, Leipzig, pp 1–492Google Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  1. 1.Department of BotanyNational MuseumPrague 9 - Horní PočerniceCzech Republic
  2. 2.Institute of BotanyAcademy of SciencesPrůhoniceCzech Republic

Personalised recommendations