The Hieracium and Pilosella (Lactuceae, Asteraceae) genera of closely related hawkweeds contain species with two different modes of gametophytic apomixis (asexual seed formation). Both genera contain polyploid species, and in wild populations, sexual and apomictic species co-exist. Apomixis is known to co-exist with sexuality in apomictic Pilosella individuals, however, apomictic Hieracium have been regarded as obligate apomicts. Here, a developmental analysis of apomixis within 16 Hieracium species revealed meiosis and megaspore tetrad formation in 1 to 7% of ovules, for the first time indicating residual sexuality in this genus. Molecular markers linked to the two independent, dominant loci LOSS OF APOMEIOSIS (LOA) and LOSS OF PARTHENOGENESIS (LOP) controlling apomixis in Pilosella piloselloides subsp. praealta were screened across 20 phenotyped Hieracium individuals from natural populations, and 65 phenotyped Pilosella individuals from natural and experimental cross populations, to examine their conservation, inheritance and association with reproductive modes. All of the tested LOA and LOP-linked markers were absent in the 20 Hieracium samples irrespective of their reproductive mode. Within Pilosella, LOA and LOP-linked markers were essentially absent within the sexual plants, although they were not conserved in all apomictic individuals. Both loci appeared to be inherited independently, and evidence for additional genetic factors influencing quantitative expression of LOA and LOP was obtained. Collectively, these data suggest independent evolution of apomixis in Hieracium and Pilosella and are discussed with respect to current knowledge of the evolution of apomixis.

] Institute of Botany Academy of Sciences of the Czech Republic Zámek 1 Průhonice Czech Republic [2] Department of Botany Faculty of Science Charles University Prague Benátská 2 Prague Czech Republic

Commonwealth Scientific and Industrial Research Organization Plant Industry Waite Campus Glen Osmond SA Australia

Institute of Botany Academy of Sciences of the Czech Republic Zámek 1 Průhonice Czech Republic

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Bergman B. (1941). Studies on the embryo sac mother cell and its development in Hieracium subg. Archieracium. Svensk Bot Tidskr 35: 1–41.

Bicknell RA, Koltunow AM. (2004). Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16: S228–S245. PubMed PMC

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

Bräutigam S. (2012) Pilosella. In: Greuter W, Raus T (eds) Med-Checklist Notulae, 31. Willdenowia. Vol 42, pp 290.

Bräutigam S, Greuter W. (2007). A new treatment of Pilosella for the Euro-Mediterranean flora. Willdenowia 37: 123–137.

Carman JG. (1997). Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biol J Linn Soc 61: 51–94.

Catanach AS, Erasmuson SK, Podivinsky E, Jordan BR, Bicknell R. (2006). Deletion mapping of genetic regions associated with apomixis in Hieracium. Proc Natl Acad Sci USA 103: 18650–18655. PubMed PMC

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

Fehrer J, Krahulcová A, Krahulec F, Chrtek J, Rosenbaumová R, Bräutigam S. (2007. b). Evolutionary aspects in Hieracium subgenus Pilosella. In: Hörandl E, Grossniklaus U, van Dijk P, Sharbel T (eds) Apomixis: Evolution, Mechanisms and Perspectives. Koeltz: Königstein. pp 359–390.

Fehrer J, Krak K, Chrtek J. (2009). Intra-individual polymorphism in diploid and apomictic polyploid hawkweeds (Hieracium, Lactuceae, Asteraceae): disentangling phylogenetic signal, reticulation, and noise. BMC Evol Biol 9: 239. PubMed PMC

Fehrer J, Šimek R, Krahulcová A, Krahulec F, Chrtek J, 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 F, Chatrou L, Gravendeel B, Pelser P (eds) Plant Species-Level Systematics: New Perspectives on Pattern & Process. Regnum Vegetabile. A. R. G. Gantner Verlag:: Rugellvol 143, pp 175–201.

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

Gentcheff G, Gustafsson A. (1940). The balance system of meiosis in Hieracium. Hereditas 26: 209–249.

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

Hörandl E, Hojsgaard D. (2012). The evolution of apomixis in angiosperms: a reappraisal. Plant Biosyst 146: 681–693.

Huson DH, Bryant D. (2006). Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254–267. PubMed

Koltunow AM, Johnson SD, Bicknell RA. (1998). Sexual and apomictic development in Hieracium. Sex Plant Reprod 11: 213–230.

Koltunow AM, Johnson SD, Bicknell RA. (2000). Apomixis is not developmentally conserved in related, genetically characterized Hieracium plants of varying ploidy. Sex Plant Reprod 12: 253–266.

Koltunow AMG, Johnson SD, Rodrigues JCM, Okada T, Hu Y, Tsuchiya T et al. (2011). Sexual reproduction is the default mode in apomictic Hieracium subgenus Pilosella, in which two dominant loci function to enable apomixis. Plant J 66: 890–902. PubMed

Koltunow AM, Ozias-Akins P, Siddiqi I. (2013). Apomixis. In: Becraft PW (ed.) Seed Genomics. John Wiley & Sons, pp 83–110.

Kotani Y, Henderson ST, Suzuki G, Johnson SD, Okada T, Siddons H et al. (2014). The LOSS OF APOMEIOSIS (LOA) locus in Hieracium praealtum can function independently of the associated large-scale repetitive chromosomal structure. New Phytol 201: 973–981. PubMed

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.

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: 63–74. PubMed

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

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: 281–306.

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.

Krak K, Caklová P, Chrtek J, Fehrer J. (2013). Reconstruction of phylogenetic relationships in a highly reticulate group with deep coalescence and recent speciation (Hieracium, Asteraceae). Heredity 110: 138–151. PubMed PMC

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

Mráz P. (2003). Mentor effects in the genus Hieracium s.str. (Compositae, Lactuceae). Folia Geobot 38: 345–350.

Mráz P, Chrtek J, Fehrer J. (2011). Interspecific hybridization in the genus Hieracium s. str.: evidence for bidirectional gene flow and spontaneous allopolyploidization. Plant Syst Evol 293: 237–245.

Mráz P, Chrtek J, Fehrer J, Plačková I. (2005). Rare recent natural hybridization in Hieracium s. str.—evidence from morphology, allozymes and chloroplast DNA. Plant Syst Evol 255: 177–192.

Mráz P, Paule J. (2006). Experimental hybridization in the genus Hieracium s. str. (Asteraceae): crosses between selected diploid taxa. Preslia 78: 1–26.

Nägeli C, Peter A. (1885) Die Hieracien Mittel-Europas, Piloselloiden. R. Oldenbourg: München.

Ogawa D, Johnson SD, Henderson ST, Koltunow AM. (2013). Genetic separation of autonomous endosperm formation (AutE) from two other components of apomixis in Hieracium. Plant Reprod 26: 113–123. PubMed

Okada T, Ito K, Johnson SD, Oelkers K, Suzuki G, Houben A et al. (2011). Chromosomes carrying meiotic avoidance loci in three apomictic eudicot Hieracium subgenus Pilosella species share structural features with two monocot apomicts. Plant Physiol 157: 1327–1341. PubMed PMC

Ozias-Akins P. (2006). Apomixis: developmental characteristics and genetics. Crit Rev Plant Sci 25: 199–214.

Rosenberg O. (1927). Die semiheterotypische Teilung und ihre Bedeutung für die Entstehung verdoppelter Chromosomenzahlen. Hereditas 8: 305–338.

Skawińska R. (1963). Apomixis in Hieracium alpinum L. Acta Biol Cracov 5: 7–14.

Slade K, Rich TCG. (2007). Pollen studies in British Hieracium sect. Alpina (Asteraceae). Watsonia 26: 443–450.

Tucker MR, Koltunow AMG. (2009). Sexual and asexual (apomictic) seed development in flowering plants: molecular, morphological and evolutionary relationships. Funct Plant Biol 36: 490–504. PubMed

Tucker MR, Okada T, Johnson SD, Takaiwa F, Koltunow AMG. (2012). Sporophytic ovule tissues modulate the initiation and progression of apomixis in Hieracium. J Exp Bot 63: 3229–3241. PubMed PMC

Van Dijk P, Vijverberg K. (2005). The significance of apomixis in the evolution of the angiosperms: a reappraisal. In: Bakker F, Chatrou L, Gravendeel B, Pelser P (eds) Plant Species-Level Systematics: New Perspectives on Pattern and Process. Gantner Verlag: Ruggell, Liechtenstein. pp 101–116.

Zahn KH. (1921–1923). Hieracium. In: Engler A (ed.) Das Pflanzenreich. Wilhelm Engelmann: LeipzigVol 4.

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A Multigene Phylogeny of Native American Hawkweeds (Hieracium Subgen. Chionoracium, Cichorieae, Asteraceae): Origin, Speciation Patterns, and Migration Routes

Reproductive pathways in Hieracium s.s. (Asteraceae): strict sexuality in diploids and apomixis in polyploids

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