Skip to main content
Log in

Enriching Ploidy Level Diversity: the Role of Apomictic and Sexual Biotypes of Hieracium subgen. Pilosella (Asteraceae) that Coexist in Polyploid Populations

  • Published:
Folia Geobotanica Aims and scope Submit manuscript

Abstract

The capacity to generate variation in ploidy and reproductive mode was compared in facultatively apomictic versus sexual maternal plants that coexist in two model populations. The population structure was studied in polyploid hybrid swarms comprised of Hieracium pilosella (usually sexual, less commonly apomictic), H. bauhini (apomictic), and their hybrids (sexual, apomictic, or sterile). Relationships among established biotypes were proposed on the basis of their DNA ploidy level/chromosome number, reproductive mode and morphology. Isozyme phenotypes and chloroplast DNA haplotypes were assayed in the population that was richer in hybrids. The reproductive origin of seed progeny was identified in both sexual and apomictic mothers, using alternative methods: the karyological, morphological and reproductive characters of the cultivated progeny were compared with those of respective mothers, or flow cytometric seed screening was used. In both populations, the progeny of sexual mothers mainly retained a rather narrow range of ploidy level/chromosome number, while the progeny of facultatively apomictic mothers was more variable. The high-polyploid hybrids, which had arisen from the fertilization of unreduced egg cells of apomicts, mainly produced aberrant non-maternal progeny (either sexually and/or via haploid parthenogenesis). Apparently, such versatile reproduction resulted in genomic instability of the recently formed high-polyploid hybrids. While the progeny produced by both true apomictic and sexual mothers mostly maintained the maternal reproductive mode, the progeny of those ‘versatile’ mothers was mainly sexual. Herein, we argue that polyploid facultative apomicts can considerably increase population diversity.

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

  • Asker S, Jerling L (1992) Apomixis in plants. CRC Press, Boca Raton

    Google Scholar 

  • Barcaccia G, Arzenton F, Sharbel TF, Varotto S, Parrini P, Lucchin M (2006) Genetic diversity and reproductive biology in ecotypes of the facultative apomict Hypericum perforatum L. Heredity 96:322–334

    Article  CAS  PubMed  Google Scholar 

  • Bengtsson O, Ceplitis A (2000) The balance between sexual and asexual reproduction in plants living in variable environments. J Evol Biol 13:415–422

    Article  Google Scholar 

  • Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. Pl Cell 16:228–245

    Article  Google Scholar 

  • Bicknell RA, Lambie SC, Butler RC (2003) Quantification of progeny classes in two facultatively apomictic accessions of Hieracium. Hereditas (Lund) 138:11–20

    Article  CAS  Google Scholar 

  • Chapman HM, Houliston GJ, Robson B, Iline J (2003) A case of reversal: the evolution and maintenance of sexuals from parthenogenetic clones in Hieracium pilosella. Int J Pl Sci 164:719–728

    Article  Google Scholar 

  • Chrtek J (2004) Hieracium L. – jestřábník. In Slavík B, Štěpánková J (eds) Květena České republiky (Flora of the Czech Republic) 7. Academia, Praha, pp 540–701

    Google Scholar 

  • Czapik R (1994) How to detect apomixis in Angiospermae. Polish Bot Stud 8:13–21

    Google Scholar 

  • de Kovel CGF, de Jong G (2000) Selection on apomictic lineages of Taraxacum at establishment in a mixed sexual-apomictic population. J Evol Biol 13:561–568

    Article  Google Scholar 

  • Durand J, Garnier L, Dajoz I, Mousset S, Veuille M (2000) Gene flow in a facultative apomictic Poaceae, the savanna grass Hyparrhenia diplandra. Genetics 156:823–831

    CAS  PubMed  Google Scholar 

  • Fehrer J, Šimek R, Krahulcová A, Krahulec F, Chrtek J Jr, 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 P (eds) Plant species-level systematics: new perspectives on pattern & process. Regnum Veg 143, Koeltz, Königstein, pp 175–201

  • Fehrer J, Gemeinholzer B, Chrtek J Jr, Bräutigam S (2007a) Incongruent plastid and nuclear DNA phylogenies reveal ancient intergeneric hybridization in Pilosella hawkweeds (Hieracium, Cichorieae, Asteraceae). Molec Phylogenet Evol 42:347–361

    Article  CAS  PubMed  Google Scholar 

  • Fehrer J, Krahulcová A, Krahulec F, Chrtek J Jr, Rosenbaumová R, Bräutigam S (2007b) Evolutionary aspects in Hieracium subgenus Pilosella. In Hörandl E, Grossniklaus U, van Dijk P, Sharbel T (eds) Apomixis: evolution, mechanisms and perspectives. Regnum Veg 147, A. R. G. Gantner Verlag, Rugell, pp 359–390

  • Fitze D, Fehrer J (2000) PCR-RFLP studies of non-coding chloroplast DNA in European Hieracium subgen. Pilosella. Abh Ber Naturkundemus Görlitz 72 (suppl.):4

    Google Scholar 

  • Gadella TWJ (1984) Cytology and the mode of reproduction of some taxa of Hieracium subgenus Pilosella. Proc Kon Ned Akad Wetensch C 87:387–399

    Google Scholar 

  • Gadella TWJ (1987) Sexual tetraploid and apomictic pentaploid populations of Hieracium pilosella (Compositae). Pl Syst Evol 157:219–246

    Article  Google Scholar 

  • Harlan JR, de Wet JMJ (1975) On Ö. Winge and a prayer: the origins of polyploidy. Bot Rev (Lancaster) 41:361–390

    Article  Google Scholar 

  • Houliston GJ, Chapman HM (2004) Reproductive strategy and population variabitity in the facultative apomict Hieracium pilosella (Asteraceae). Amer J Bot 91:37–44

    Article  Google Scholar 

  • Jeffreys AJ, MacLeod A, Neumann R, Povey S, Royle NJ (1990) “Major minisatellite loci” detected by minisatellite clones 33.6 and 33.15 correspond to the cognate loci D1S111 and D7S437. Genomics 7:449–452

    Article  CAS  PubMed  Google Scholar 

  • Kao RH (2007) Asexuality and the coexistence of cytotypes. New Phytol 175:764–772

    Article  PubMed  Google Scholar 

  • Koltunow AM (1993) Apomixis: Embryo sacs and embryos formed without meiosis or fertilization in ovules. Pl Cell 5:1437–1452

    Google Scholar 

  • Koltunow AM, Johnson SD, Bicknell RA (1998) Sexual and apomictic development in Hieracium. Sexual Pl Reprod 11:213–220

    Article  Google Scholar 

  • Krahulcová A, Krahulec F (1999) Chromosome numbers and reproductive systems in selected representatives of Hieracium subgen. Pilosella in the Krkonoše Mts (the Sudeten Mts). Preslia 71:217–234

    Google Scholar 

  • Krahulcová A, Suda J (2006) A modified method of flow cytometric seed screen simplifies the quantification of progeny classes with different ploidy levels. Biol Pl 50:457–460

    Article  Google Scholar 

  • Krahulcová A, Chrtek J Jr, Krahulec F (1999) Autogamy in Hieracium subgen. Pilosella. Folia Geobot 34:373–376

    Article  Google Scholar 

  • Krahulcová A, Krahulec F, Chapman HM (2000) Variation in Hieracium subgen. Pilosella (Asteraceae): what do we know about its sources? Folia Geobot 35:319–338

    Article  Google Scholar 

  • Krahulcová A, Papoušková S, Krahulec F (2004) Reproduction mode in the allopolyploid facultatively apomictic hawkweed Hieracium rubrum (Asteraceae, H. subgen. Pilosella). Hereditas (Lund) 141:19–30

    Article  Google Scholar 

  • 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 76:223–243

    Google Scholar 

  • Krahulec F, Krahulcová A, Papoušková S (2006) Ploidy level selection during germination and early stage of seedling growth in the progeny of allohexaploid facultative apomict, Hieracium rubrum (Asteraceae). Folia Geobot 41:407–416

    Article  Google Scholar 

  • 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 80:1–26

    Google Scholar 

  • Lepage E (1967) Étude de quelques hybrides chez nos Épèrvieres (Hieracium) adventices. Naturaliste Canad 94:609–619

    Google Scholar 

  • Loomis ES (2007) Sex and diversity in the invasive plant Hieracium aurantiacum. M.S. Thesis, The University of Montana, Missoula. Available at: http://etd.lib.umt.edu/theses/available/etd-05302007-121438/unrestricted/EliThesis.pdf. Accessed 21 Nov 2008

  • Mártonfiová L (2006) Possible pathways of the gene flow in Taraxacum sect. Ruderalia. Folia Geobot 41:183–201

    Article  Google Scholar 

  • Mártonfiová L, Majeský L, Mártonfi P (2007) Polyploid progeny from crosses between diploid sexuals and tetraploid apomictic pollen donors in Taraxacum sect. Ruderalia. Acta Biol Cracov, Ser Bot 49:47–54

    Google Scholar 

  • Matzk F, Meister A, Schubert I (2000) An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Pl J 21:97–108

    Article  CAS  Google Scholar 

  • Meirmans PG, Vlot EC, den Nijs JCM, Menken SBJ (2003) Spatial ecological and genetic structure of a mixed population of sexual diploid and apomictic triploid dandelions. J Evol Biol 16:343–352

    Article  CAS  PubMed  Google Scholar 

  • Menken SBJ, Smit E, den Nijs JCM (1995) Genetical population structure in plants: gene flow between diploid sexual and triploid asexual dandelions (Taraxacum sect. Ruderalia). Evolution 49:1108–1118

    Article  Google Scholar 

  • Morgan-Richards M, Trewick SA, Chapman HM, Krahulcová A (2004) Interspecific hybridization among Hieracium species in New Zealand: evidence from flow cytometry. Heredity 93:34–42

    Article  CAS  PubMed  Google Scholar 

  • Mráz P, Šingliarová B, Urfus T, Krahulec F (2008) Cytogeography of Pilosella officinarum (Compositae): Altitudinal and longitudinal differences in ploidy level distribution in the Czech Republic and Slovakia and the general pattern in Europe. Ann Bot (Oxford) 101:59–71

    Article  Google Scholar 

  • Nogler GA (1984) Gametophytic apomixis. In Johri BM (ed) Embryology of Angiosperms. Springer-Verlag, Berlin & Heidelberg, pp 475–518

    Google Scholar 

  • Otto F (1990) DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. In Crissman HA, Darzynkiewicz Z (eds) Methods in cell biology 33. Academic Press, San Diego, pp 105–110

    Google Scholar 

  • Richards AJ (1997) Plant breeding systems. Ed. 2, Chapman & Hall, London

    Google Scholar 

  • Richards AJ (2003) Apomixis in flowering plants: an overview. Philos Trans, Ser B 358:1085–1093

    Article  CAS  Google Scholar 

  • Rotreklová O (2004) Hieracium bauhini group in Central Europe: chromosome numbers and breeding systems. Preslia 76:313–330

    Google Scholar 

  • Rotreklová O (2008) Hieracium subgen. Pilosella: pollen stainability in sexual, apomictic and sterile plants. Biologia (Bratislava) 63:61–65

    Google Scholar 

  • 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 74:27–44

    Google Scholar 

  • Rotreklová O, Krahulcová A, Mráz P, Mrázová V, Mártonfiová L, Peckert T, Šingliarová B (2005) Chromosome numbers and breeding systems of some European species of Hieracium subgen. Pilosella. Preslia 77:177–195

    Google Scholar 

  • Savidan Y, Pernès J (1982) Diploid-tetraploid-dihaploid cycles and the evolution of Panicum maximum Jacq. Evolution 36:596–600

    Article  Google Scholar 

  • Savidan Y, Carman JG, Dresselhaus T (eds) (2001) The flowering of apomixis: from mechanisms to genetic engineering. CIMMIT, IRD, European Commission DG VI (FAIR), Mexico, D.F.

    Google Scholar 

  • Schranz ME, Dobeš Ch, Koch MA, Mitchell-Olds T (2005) Sexual reproduction, hybridization, apomixis, and polyploidization in the genus Boechera (Brassicaceae). Amer J Bot 92:1797–1810

    Article  CAS  Google Scholar 

  • Štorchová H, Hrdličková R, Chrtek J Jr, Tetera M, Fitze D, Fehrer J (2000) An improved method of DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon 49:79–84

    Article  Google Scholar 

  • Suda J, Krahulcová A, Trávníček P, Krahulec F (2006) Ploidy level versus DNA ploidy level: an appeal for consistent terminology. Taxon 55:447–450

    Article  Google Scholar 

  • Trewick SA, Morgan-Richards M, Chapman HM (2004) Chloroplast DNA diversity of Hieracium pilosella (Asteraceae) introduced to New Zealand: reticulation, hybridization and invasion. Amer J Bot 91:73–85

    Article  CAS  Google Scholar 

  • 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 P (eds) Plant species-level systematics: new perspectives on pattern & process. Regnum Veg 143, Koeltz, Königstein, pp 101–116

  • Verduijn MH, van Dijk PJ, van Damme JMM (2004) The role of tetraploids in the sexual-asexual cycle in dandelions (Taraxacum). Heredity 93:390–398

    Article  CAS  PubMed  Google Scholar 

  • Whitton J, Sears ChJ, Baack EJ, Otto SP (2008) The dynamic nature of apomixis in the angiosperms. Int J Pl Sci 169:169–182

    Article  Google Scholar 

  • Wilson LM, Fehrer J, Bräutigam S, Grosskopf G (2006) A new invasive hawkweed, Hieracium glomeratum (Lactuceae, Asteraceae), in the Pacific Northwest. Canad J Bot 84:133–142

    Article  CAS  Google Scholar 

  • Zahn KH (1922–30) Hieracium. In Ascherson P, Graebner P (eds) Synopsis der mitteleuropäischen Flora 12 (1), Gebrüder Bornträger, Leipzig

    Google Scholar 

Download references

Acknowledgements

We would like to thank H. Jedličková, the director of the Experimental Garden of the Faculty of Education, Masaryk University of Brno-Kejbaly. V. Křišťálová (Košťálová) is acknowledged for assistance in the field and for help in early reproductive system studies. We are grateful to J. Fehrer for kindly revising the first draft of this paper. This collective study was supported by the Czech Science Foundation (projects no. 206/07/0059 and 206/08/0890), by the Academy of Sciences of the Czech Republic (AVOZ60050516) to A.K., F.K., R.R. and I.P. and by the Ministry of Education, Youth and Sports (projects MSM 0021622416 and LC 06073) to O.R.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna Krahulcová.

Appendix

Appendix

Overview of chromosome numbers, ploidy levels and genotypes of maternal plants (sexual and apomictic) of the studied Hieracium subgen. Pilosella and their seed progeny, spontaneously arisen at localities Praha-Vysočany (locality 1) and Brno-Kamenný kopec (locality 2). The labels (BA – Hieracium bauhini, PI – H. pilosella, HYB – hybrid) refer to individual maternal plants and genotypes symbolized by lowercase letters. The supposed origin of the progeny was inferred i) by comparing their own and the maternal ploidy level, and from the morphology of cultivated progeny plants (all progeny from locality 1, part of the progeny of plants 2-3763 PI and 2-3734 PI from locality 2); or ii) by FCSS analysis (the other progeny from locality 2). Symbols of progeny origins follow Harlan and de Wet (1975).

Apomictic maternal plants

Progeny

Sexual maternal plants

Progeny

Cytotype

Plant label

Genotype

2n / ploidy (x = 9)

No. of individuals

Origin

Cytotype

Plant

Genotype

2n / ploidy (x = 9)

No. of individuals

Origin

Locality 1: 13 individuals

 

Locality 1: 12 individuals

 

2n = 4x = 36

1-656 BA

BA b

4x

23

2n + 0

2n = 4x = 36

1-296 PI

 

36

1

n + n

2n = 5x = 45

1-292 BA

BA c

5x

6

2n + 0

1-505 PI

PI i

36

6

n + n

1-644 BA

BA d

2n = 39

1

n + n

  

44

1

n + n

  

5x

15

2n + 0

1-511 PI

PI l

36

7

n + n

1-649 BA

BA d

5x

2

2n + 0

1-646 PI

PI m

35

2

n + n

  

2n = 7x = 63

1

2n + n

  

36

6

n + n

1-652 BA

BA d

5x

10

2n + 0

1-654 PI

PI n

36

5

n + n

  

2n = 7x = 63

1

2n + n

1-643 HYB

HYB c

36

5

n + n

1-655 BA

BA e

5x

5

2n + 0

1-642 HYB

HYB c

36

1

n + n

  

2n = 7x = 63

1

2n + n

2n = 5x = 45

1-506 PI

PI p

36

1

n + n

1-647 HYB

HYB l

5x

7

2n + 0

  

37

2

n + n

1-661 HYB

HYB l

2n = 41

1

n + n

  

39

2

n + n

  

5x

19

2n + 0

  

40

2

n + n

  

2n = 7x = 63

2

2n + n

  

41

2

n + n

1-653 HYB

HYB l

4x

1

n + n

  

42

2

n + n

  

5x

7

2n + 0

  

45

2

n + n

  

2n = 7x = 63

2

2n + n

2n = 6x = 54

1-660 HYB

 

43

2

n + n

2n = 7x = 63

1-508 HYB

HYB o

2n = 28

1

n + 0

  

44

6

n + n

1-513 HYB

HYB p

2n = 29

1

n + 0

  

45

3

n + n

  

2n = 45

1

n + n

  

46

3

n + n

  

2n = 48–50

1

n + n

2n = 48 (aneuploid)

1-295 HYB

 

40

3

n + n

1-515 HYB

HYB p

2n = 32

1

n + 0

  

41

8

n + n

  

2n = 36

1

n + 0

  

42

4

n + n

  

2n = 47

5

n + n

  

43

1

n + n

  

2n = 48

1

n + n

  

44

1

n + n

  

2n = 49

2

n + n

2n = 49 (aneuploid)

1-648 HYB

 

40

1

n + n

  

2n = 50

2

n + n

  

41

5

n + n

1-651 HYB

HYB r

2n = 28

1

n + 0

  

42

2

n + n

  

2n = 46

1

n + n

  

43

1

n + n

  

2n = 48

1

n + n

2n = 58 (aneuploid)

1-641 HYB

 

44

1

n + n

  

2n = 51

1

n + n

  

45

1

n + n

  

Total

124

   

46

5

n + n

       

46/47

1

n + n

       

47

2

n + n

       

48

1

n + n

       

48/49

1

n + n

       

Total

99

 

Locality 2: 12 individuals

   

Locality 2: 9 individuals

   

2n = 5x

2-3672 BA

 

5x

9

2n + 0

2n = 6x

2-3659 PI

 

6x

15

n + n

  

5x

1

n + n

2-3693 PI

 

6x

2

n + n

2-3701 BA

 

5x

32

2n + 0

2-3694 PI

 

6x

17

n + n

2-3706 BA

 

5x

12

2n + 0

2-3763 PI

 

6x

6

n + n

  

5x

1

n + n

  

8x

1

2n + n

2-3707 BA

 

5x

29

2n + 0

2-3734 PI

 

6x

64

n + n

2-3703 BA

 

5x

3

2n + 0

2-3735 PI

 

6x

30

n + n

  

5x

2

n + n

2-3772 PI

 

6x

71

n + n

2-3782 BA

 

5x

8

2n + 0

2-3774 PI

 

6x

62

n + n

  

5x

1

n + n

2-3775 PI

 

6x

49

n + n

  

8x

1

2n + n

  

Total

317

 

2-3784 BA

 

5x

33

2n + 0

     
  

3x

2

n + 0

     

2n = 6x

2-3669 BA

 

6x

77

2n + 0

     

2-3702 BA

 

6x

15

2n + 0

     

2-3730 PI

 

6x

14

2n + 0

     

2-3733 PI

 

6x

38

2n + 0

     

2-3737 PI

 

6x

58

2n + 0

     
  

Total

336

      

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krahulcová, A., Rotreklová, O., Krahulec, F. et al. Enriching Ploidy Level Diversity: the Role of Apomictic and Sexual Biotypes of Hieracium subgen. Pilosella (Asteraceae) that Coexist in Polyploid Populations. Folia Geobot 44, 281–306 (2009). https://doi.org/10.1007/s12224-009-9041-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12224-009-9041-1

Keywords

Navigation