Towards a better understanding of the Taraxacum evolution (Compositae–Cichorieae) on the basis of nrDNA of sexually reproducing species

ORIGINAL ARTICLE

Towards a better understanding of the Taraxacum evolution(Compositae–Cichorieae) on the basis of nrDNA of sexuallyreproducing species

Jan Kirschner • Lenka Zaveska Drabkova •

Jan Stepanek • Ingo Uhlemann

Received: 10 October 2013 / Accepted: 14 July 2014 / Published online: 31 July 2014

� Springer-Verlag Wien 2014

Abstract The genus Taraxacum is characterized by pre-

vailing complex multiple hybridity, frequent polyploidy

and widespread agamospermous reproduction, which

makes the phylogenetic analysis difficult. On the basis of

the previous analysis of the variation of nrDNA in Taraxa-

cum taxa with different ploidy levels and modes of repro-

duction, to mitigate consequences of the reticulate com-

plexity of the genus, a phylogenetic study of 52 samples of

sexually reproducing dandelions of 26 sections (and another

13 agamospermous representatives of other sections known

to include sexuals) was carried out. Both sexual and ag-

amospermous samples were analysed using maximum

parsimony and neighbour network. Exclusively sexual

dandelions were analysed using the same approaches. In

spite of the general agreement among various types of

analyses, there is a limited overall congruence between

results of nrDNA analyses and the established taxonomic

system of the genus Taraxacum. The analyses shed light on

the relationships among the most primitive groups. A stable

clade is formed by representatives of the sections Primi-

genia, Orientalia, Sonchidium, Piesis and T. cylleneum.

Another case of stable relationships is that of the members

of the sect. Dioszegia. Relationships between the sects.

Erythrosperma and Erythrocarpa were supported, and the

relatedness of the members of sect. Australasica was con-

firmed. Rather unexpectedly, the agamospermous samples

of the sect. Oligantha (T. minutilobum) are shown to be

closely related with the sect. Macrocornuta. The latter

section is generally considered to be close to sect. Cera-

toidea (T. koksaghyz) on morphological grounds but this

presumption is not corroborated by the results of nrDNA

analyses. Analyses of 72 samples of sexual dandelions were

also performed using the trnL–trnF region of the chloro-

plast DNA. The maximum parsimony analysis of this region

reveals intraspecific variation in a number of ancestral

diploid sexual species, all present in the two main branches

of the cladogram. This phenomenon is attributed to the

ancient gene flow and possibly to the persistence of

ancestral cpDNA polymorphism. The strict consensus

cpDNA tree information content and interpretability is quite

low. The maximum parsimony analysis of combined

nrDNA and cpDNA data sets was also performed with

expectably low interpretability of the results.

Keywords Maximum parsimony � Neighbour network �nrDNA � Sexuality � Taxonomy � Taraxacum

Introduction

The genus Taraxacum

The genus Taraxacum (Compositae–Cichorieae) undoubt-

edly represents an example of evolutionary and taxonomic

complexity. Reasons for the complicated nature of the

variation in the genus were summarised by Kirschner et al.

(2003) and Zaveska Drabkova et al. (2009): (i) a low level

of morphological structural differentiation, (ii) predomi-

nant agamospermy and common coexistence of agamo-

sperms with sexuals, (iii) old and complex hybridity, and

(iv) common polyploidy (with the exception of three

J. Kirschner (&) � L. Zaveska Drabkova � J. Stepanek

Institute of Botany, Academy of Sciences, Zamek 1,

252 43 Pruhonice, 25243 Prague, Czech Republic

e-mail: [email protected]; [email protected]

L. Zaveska Drabkova

e-mail: [email protected]

I. Uhlemann

Teichstraße 61, 01778 Liebenau, Germany

123

Plant Syst Evol (2015) 301:1135–1156

DOI 10.1007/s00606-014-1139-0

tetraploid sexual species in the sect. Piesis, all known

polyploid taxa are agamospermous). In particular, the

complex hybridity, i.e., repeated, multiple hybridization

events in the evolutionary history of the majority of taxa,

poses great difficulties in the interpretation of supraspecific

and specific variation in Taraxacum.

The genus, predominantly north-temperate to subarctic,

includes about 60 sections with about 2,800 species. Thus,

another hindrance in phylogenetic studies is the very number

of taxonomic units to be dealt with. The unequal levels of

exploration of the main diversity centres (NE Europe, the

Mediterranean and Near East, Middle Asia, the Himalayas,

the Far East) also result in an inevitably incomplete sampling.

Distribution of sexuality in the genus Taraxacum

Sexuality has a strikingly uneven distribution, both in terms

of geography and taxonomy. Purely sexual sections are few.

The Southern Hemisphere sections, sect. Australasica and

sect. Antarctica (monotypic) is purely sexual. If we disre-

gard the monotypic sect. Biennial Beinnia (T. nutans) and

sect. Glacialia (T. glaciale), there are only three exclusively

sexual sections in the Northern Hemisphere, sect. Primi-

genia, sect. Dioszegia and sect. Piesis. Several, mostly

derived sections, so far as our material goes, consist of

agamospermous species only (e.g., sect. Naevosa—NW

Europe, sect. Celtica—NW Europe, sect. Hamata—NW

Europe, sect. Crocea (Arcto-Alpine), sect. Spectabilia (NW

Europe), sect. Obovata—W and C Mediterranean, sect.

Porphyrantha—the Caucasus, sect. Cucullata—the Alps,

sect. Boreigena—N Europe, sect. Stenoloba—NC Asia).

The most remarkable phenomenon in the genus is the

common existence of geographical parthenogenesis (Ho-

randl 2006): the sexual member is confined to a small

southern or local mountain geographical range while aga-

mospermous derivatives migrated or evolved northwards

and/or along mountain ranges. This concerns, for instance,

the group of T. nigricans and T. alpestre of the sect. Al-

pestria (Stepanek et al. 2011), sect. Obliqua with its only

sexual T. pyrenaicum in the Pyrenees, sect. Leucantha with

sexuals confined to a relatively small areas in Transbaicalia

and Mongolia, or sect. Sonchidium with a local sexual

diploid in C Anatolia (T. farinosum).

The last situation to be described shows several geo-

graphically restricted complexes of sympatric young diploid

sexuals and closely related and similar triploid and tetraploid

obligate and facultative agamosperms; they exhibit a high

variation and dynamics, including a 29–39–49cycle. The

most well-known case is that of Taraxacum sect. Taraxacum

(T. officinale Wigg.) in southern, south-central, southwest-

ern and partly also western Europe (e.g., Verduijn and al.

2004, van Dijk and Bakx-Schotman 2004), other cases are

represented by T. sect. Erythrosperma in SE Europe

(Martonfiova et al. 2010), T. sect. Macrocornuta in southern

Middle Asia, NW India, Pakistan, Afghanistan and Iran, and

probably also T. sect. Mongolica in SE China and Japan.

Previous studies of Taraxacum evolution using DNA

markers

As a consequence of the complicated hybridogenous evo-

lutionary history of Taraxacum species, the previous

molecular and phylogenetic studies of dandelions did not

provide any deeper insight into the processes that formed

the existing species and sections. However, some basic

principles were confirmed or newly established, which

represents a certain basis for future studies. For the sake of

convenience, we give a brief review of the results of pre-

vious molecular studies of the genus.

Reticulation/hybridity as a common phenomenon

in dandelions

In the early analysis of the origin of genotypic variation in

North American dandelions, King (1993), using a combi-

nation of cpDNA and nrDNA markers, revealed multiple

hybridization events as the main phenomenon responsible

for the variation among dandelion samples. Van der Hulst

et al. (2000, 2003) show that sexual reproduction must

have contributed to genetic variation at sampled sites

(which probably can be accounted for as a result of ancient

reticulation). It is clear from their results that recombina-

tion phenomena play a substantially more important role in

the evolutionary history of dandelions than somatic muta-

tions in clonal apomicts. Relatively frequent somatic

mutations reported by King (1993) may be a consequence

of an enormous intraindividual nrDNA variation within

polyploid agamospermous individuals (see also Zaveska

Drabkova et al. 2009).

cpDNA analyses

Chloroplast DNA, as a uniparentally inherited source of

phylogenetic information, was found a disputable tool in

the genus characterized by multiple hybridization history.

Moreover, Mes et al. (2000) showed that phylogenetic

information from non-coding cpDNA in Taraxacum is

disturbed by homoplasious indels. On the other hand, the

very different timing of the hybridization events made it

possible to discern ancient haplotypes in morphologically

more primitive taxa from those of derived groups (Wittzell

1999; Kirschner et al. 2003). The latter two works also

identified common reticulations as a source of incongru-

ence among different data sets in Taraxacum. The absence

of data on direct parents of the extant hybridogenous taxa

and the repeated multiple hybridization events in the

1136 J. Kirschner et al.

123

https://www.researchgate.net/publication/12338470_Hairpins_involving_both_inverted_an_direct_repeats_are_associated_with_homoplasious_indels_in_non-coding_chloroplast_DNA_of_Taraxacum_Lactuceae_Asteraceae?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

https://www.researchgate.net/publication/272530958_Origins_of_Genotypic_Variation_in_North_American_Dandelions_Inferred_from_Ribosomal_DNA_and_Chloroplast_DNA_Restriction_Enzyme_Analysis?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

https://www.researchgate.net/publication/272530958_Origins_of_Genotypic_Variation_in_North_American_Dandelions_Inferred_from_Ribosomal_DNA_and_Chloroplast_DNA_Restriction_Enzyme_Analysis?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

https://www.researchgate.net/publication/225460429_Analysis_of_nrDNA_polymorphism_in_closely_related_diploid_sexual_tetraploid_sexual_and_polyploid_agamospermous_species?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

history of most taxa make the exploitation of cpDNA for

phylogenetic inference in Taraxacum problematic. In spite

of that, we make a comparison of the cpDNA analysis in

Taraxacum sexuals with the nrDNA ITS results (see

below), and also exploit the previously published results.

nrDNA attributes and phylogeny

The basic methodological analysis of the nrDNA poly-

morphism in dandelions with different modes of repro-

duction and ploidy levels (Zaveska Drabkova et al. 2009)

showed that the ITS1-5.8S-ITS2 variation principally is not

a consequence of pseudogene incidence. The intra-indi-

vidual ITS variation in polyploids corresponds in its extent

to that among species. Therefore, most importantly for the

present paper, concerted evolution of nrDNA is substan-

tially suppressed in agamospermous polyploids in Taraxa-

cum while in sexually reproducing diploids and polyploids

the nrDNA ITS regions are homogenised. This qualifies the

nrDNA of sexual dandelions as a region suitable for phy-

logenetic analysis even without cloning.

The plausible historical effect in the ITS variation of

Taraxacum sect. Naevosa was pointed out by Mes et al.

(2002): nucleotide polymorphisms in nrDNA were

incompatible with the clonal structure of the Norwegian

individuals, probably due to persistent ancestral polymor-

phisms that pre-date the origin of the Naevosa clones.

The first phylogenetic utilisation of the nrDNA poly-

morphism dealt with the recently described Southern

Hemisphere section Australasica and justified its position

among taxa close to the sect. Arctica (Uhlemann et al. 2004,

2009).

The early nrDNA study of the among-sibling variation

in apomictic dandelions (King and Schaal 1990) seemingly

showed the polyclonal structure of several apomicts but the

results may be a consequence of the overlooked intraindi-

vidual variation in nrDNA in polyploid apomicts (lacking

homogenization).

Population analyses and the individuality of clones

Before DNA markers were made available for routine

population studies, many studies used products of low-

copy nuclear and organelle genes (allozymes) for the

identification of multilocus genotypes of dandelion clones.

The main results were only confirmed by similar DNA

studies: Local populations of agamospermous dandelions

are composed of several to many common clones, usually

corresponding to morphological units (often called micro-

species). Selected microspecies were subjected to a repre-

sentative allozyme analysis and widespread taxa often were

found almost uniclonal, or more rarely oligoclonal. On the

other hand, polyclonal agamospermous units were also

revealed. Other works used DNA markers to identify

genotypes in ecological and competition experiments. The

most important selected works showing the above results,

chronologically, are Menken and Morita (1989, but see

also Sato et al. 2011), Kirschner et al. (1994), Falque et al.

(1998), Van der Hulst et al. (2000), Vasut et al. (2004),

Collier and Rogstad (2004), Reisch (2004), Keane et al.

(2005), Vellend et al. (2009).

Exploitation of nrDNA sequences in Taraxacum

sexuals and objectives of the present study

It follows from the study of the sequence variation of the

ITS1-5.8S-ITS2 region of nrDNA (Zaveska Drabkova et al.

2009) that ‘‘raw’’ nrDNA (i.e., not sequences of randomly

selected clones of the nrDNA of agamospermous polyploids)

is not very suitable for phylogenetic analyses in Taraxacum.

The enormously high sequence variation within agamosper-

mous polyploid individuals (amounting to 1–17 %) is in

contrast with the perfectly homogenised sequences of sexual

diploids and sexual tetraploids. As more than a half of the ca

60 sections recognised in Taraxacum contain sexually

reproducing taxa, it is a natural idea to confine the phyloge-

netic analysis to the sexual representatives of the genus. First,

the sexuals in most sections are regarded as basal or more

primitive representatives, and secondly, it might be hypoth-

esised that in most sexual species the level of hybridity is

lower than in the polyploid agamosperms, or even that there is

no hybridization involved in the evolutionary history of some

taxa. As a consequence, we expect that the analysis of sexuals

will show more than the level of organisation of haplotypes

(primitive, precursor and derived, as recognized, following

Richards 1973, in Wittzell 1999 and Kirschner et al. 2003, see

also Table 1) but also, at least in some cases of clades

involving no or limited hybridity, real phylogenetic rela-

tionships, perhaps supporting the evolutionary and taxonomic

considerations based on morphological and other data.

There are, therefore, two main objectives of the present

study: (i) elucidation of major features of dandelion nrDNA

differentiation, and (ii), in the case of an unexpected but

possible congruence of cpDNA and nrDNA data, establish-

ment of ‘‘islands’’ of non-hybridity in the genus Taraxacum.

Materials

Material of sexual Taraxacum species for ITS

phylogeny

Taxon sampling

There are 30 sections in the genus Taraxacum where sexuality

is known or is very probable. In the present paper, we analysed

Towards a better understanding of the Taraxacum evolution 1137

123

https://www.researchgate.net/publication/225137976_Principal_features_of_the_cpDNA_evolution_in_Taraxacum_Asteraceae_Lactuceae_A_conflict_with_taxonomy?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

https://www.researchgate.net/publication/230047104_The_origin_of_Taraxacum_agamospecies?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

https://www.researchgate.net/publication/12681313_Wittzell_H_Chloroplast_DNA_variation_and_reticulate_evolution_in_sexual_and_apomictic_sections_of_dandelions_Mol_Ecol_8_2023-2035?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==


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123

sexual samples from 26 sections, in many cases multiple

samples covering the taxonomic diversity of sexuality in those

sections were analysed; in six remaining cases, we used

samples of agamospermous taxa for the sake of completeness.

Voucher specimens are deposited in PRA (if not stated

otherwise). Table 2 shows the representatives used for the

analysis. Nomenclature follows Kristiansen et al. (2005).

Mode of reproduction in the material studied

Samples examined in the present study were taken from

cultivated material; almost all the original samples were

collected by JK and JS or their collaborators in the field (as

roots or seeds) and then cultivated and re-sown to study the

breeding behaviour and variation, all within the period from

1984 to 2011. The method of cultivation was described and

depicted in Kirschner and Stepanek (1993); in this way, most

of the ca 100,000 Taraxacum specimens deposited in PRA

were obtained. For the purposes of this study, the majority of

specimens were chosen from among more than 20 siblings

each; the samples, therefore, do not represent casually

selected herbarium specimens with a lack of information

about their behaviour and variation. In Table 2, sexuality is

indicated where appropriate. For many taxa, the mode of

reproduction was published in the literature. The features

evaluated include: (i) pollen size variation––regular pollen

is a reliable indicator of sexuality (the analyses were done

according den Nijs et al. 1990, always on several siblings

from a progeny cultivated; when pollen grains considerably

vary in size in several siblings, agamospermy is plausible),

(ii) emasculated capitula do not give rise to a seed set (in

selected cases, emasculation was done; the full seed set after

emasculation is a reliable indicator of agamospermy), (iii)

diploidy versus polyploidy (in Taraxacum, with the excep-

tion of three well-known cases of the section Piesis, see

Kirschner and Stepanek 1998, polyploidy is closely associ-

ated with agamospermy while diploids are invariably sex-

ual; chromosome counts given in the Table 2 were

published, the flow-cytometry data come mainly from

Zavesky et al. (2005), and last (iv), absence of matrocliny, i.

e., the progeny of maternal plant considerably varies (in

agamospermous Taraxacum plants, the offspring siblings

are strikingly identical morphologically while sexuals

exhibit a conspicuous variation in size, colour and shape of

leaves and other serial organs).

Methods

Documentation and sources of information

Most of the material studied is deposited in the herbarium

PRA, Institute of Botany, Academy of Sciences, Pruhonice,Ta

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https://www.researchgate.net/publication/232663603_DNA_Taxonomy-the_Riddle_of_Oxychloe_Juncaceae?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

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123

the Czech Republic. It represents the largest collection of

extra-European dandelions in the world, a result of expe-

ditions to many regions of the Mediterranean and Middle

Asia (i.e. Kazakhstan, Kyrgyzstan, Tadzhikistan, Uzbeki-

stan) and Central Asia (mainly S Siberia, Mongolia and

NW, C and NE China). Cultivation of plants grown from

seed obtained from other botanists, seed collected during

expeditions and from cultivation of roots also provided

plants for herbarium collections. Details of the cultivation

methods are given in Kirschner and Stepanek (1993). The

cultivation, especially repeated mass cultivation, reveals

the limits of morphological plasticity of individual taxa.

Moreover, it provides material for the study of reproduc-

tion systems (see below). This study was supplemented by

the examination of numerous herbarium collections. Those

most relevant to the present study are BM, E, GAT, GOET,

K, LE, MW, NS, PE, PRC, S, TI, UPS, W, WRSL, WU

(abbreviation according to Index Herbariorum at http://sci

web.nybg.org/science2/IndexHerbariorum.asp). Most of

our revision labels are numbered and refer to the specimen

to which they are attached (as ‘‘no. det.‘‘, not necessarily to

the duplicates).

A general problem of correct identification of plant

material for phylogenetic studies (e.g., Kristiansen et al.

2005) is particularly relevant for the genus Taraxacum. To

make our identification available for revision, the taxo-

nomic concept of sections and species is documented by a

standard exsiccate series edited and distributed by the

present authors (Kirschner and Stepanek 1993, 1997b). In

the series, over one thousand numbers were distributed

(which represents more than 20,000 specimens) and copies

are deposited in major herbaria with important dandelion

collections (e.g. S, H, L, M, PRA, PRC) and in the col-

lections of leading specialists (H. Øllgaard, I. Uhlemann, P.

Oosterveld, A. J. Richards etc.).

Nomenclature

Sectional nomenclature follows the previous nomenclatural

and taxonomic accounts (Kirschner and Stepanek 1997, see

also Kirschner and Stepanek 1987 and 2004, and Ge et al.

2011). Plant names are in accordance with ICBN (the latest

edition).

DNA extraction

Plant material was taken from herbarium specimens or

fresh leaves. Total DNA was extracted from leaves fol-

lowing Doyle and Doyle (1987) with modifications

according to Wittzel Wittzell (1999). DNA was extracted

from at least 0.1 g of dried or 1 g fresh samples. GenBank

ITS sequences of Taraxacum sect. Naevosa were also

included (accession nos. AF336316–AF336336; for more

details see also Mes et al. 2002). The sequences used for

the construction of data matrices are available from

GenBank.

Techniques of ITS and trnL-F amplification,

sequencing and cloning

Double-stranded copies of ITS1-5.8S-ITS2 were amplified

from total DNA using a set of four primers, ITS4i and

ITS5i published by Roalson (2001), ITS2R and ITS5L

described by White et al. (1990). These primers generated

PCR products in length around 700 bp, the optimal length

for reduction of probability of PCR-mediated recombina-

tion (Croon et al. 2002). Amplifications were performed

with the following program: 30–40 cycles of 94 �C for

1 min, 50 �C for 1 min (in a few cases 45 �C), and 72 �C

for 3 min. As a first strategy we used direct sequencing of

PCR products as recommended by Nieto Feliner and al.

(2004). Sequences were obtained on a CEQ2000XL auto-

mated sequencer. The sequences were deposited in Gen-

Bank under Accession nos. KF437403–KF437460,

KF459942–KF459943 (see also Table 2). Aligned data

matrix contained 562 bp in total and 75 taxa, analysed data

matrix included 520 bp, incomplete 5 and 3 ends of

sequences were not used.

Chloroplast trnL-F was amplified from total DNA using

a set of four universal primers described by Gielly and

Taberlet (1994) with the same PCR specifications as above.

To complete our newly obtained sequence data we inclu-

ded sequences from GenBank (AF208365, AJ240807,

AF116492, AF324624, AJ240804, AF116501, AF324631,

KC119526-KF275138, AF116486, AF324589, AB070924,

AF116499, AF324630, AB070902-AB070904, JQ696795-

JQ696798, AJ240834, AF116484, AF116498, AF324547,

AF116487, AF324620, AJ240801, AB070907-AB070916,

AF116488, AF324621, AJ240811, AJ240800, AF116482,

AF324618, AF324657, AF116491, AF116500, AF324623,

AJ240797, AJ240798, AJ240799, AF116502, AJ240806,

AF116485, AF324619 and AJ240803). The data matrix

analysed contained 576 bp and 72 taxa.

Sequence alignment and phylogenetic analyses

DNA sequences were assembled in GeneSkipper (EMBL,

Heidelberg). Alignment of sequences was done manually

using BioEdit (Hall 1999) where insertions or deletions

were detected.

For the phylogenetic analysis we used NONA under the

shell of WinClada version 1.00.08 (Nixon 2002). We per-

formed the Rachet procedure (Nixon 1999) under the

maximum parsimony (MP) optimality criterion, running

1,000 replicates holding 25 trees at each replicate, and

sampling 45 characters. The ambiguity setting was amb =.


123

http://sciweb.nybg.org/science2/IndexHerbariorum.asp

http://sciweb.nybg.org/science2/IndexHerbariorum.asp

https://www.researchgate.net/publication/257253393_Nixon_K_The_Parsimony_Ratchet_a_New_Method_for_Rapid_Parsimony_Analysis_Cladistics?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

The resultant cladograms were then submitted to com-

mands ‘‘hard collapse unsupported nodes in all trees’’ and

‘‘keep best only’’. Indels have been treated as missing data.

Strict consensus trees were constructed. Jackknife assessed

relative support among clades present in MPTs. Prenanthes

purpurea, which also belongs to the Lactuceae and repre-

sents a species sufficiently close, was used as the outgroup

(accession no. AJ633343).

Maximum likelihood (ML) analysis was run in the CI-

PRES 7.0.3. RAxML web-server (Stamatakis et al. 2008)

to examine difference in optimality between alternative

topologies.

Bayesian analysis (BI) was performed in MrBayes v.3.1

(Ronquist and Huelsenbeck 2003). For Bayesian analysis

we carried out two independent runs (each with four

chains) for 1,1 million generations under the TrN ? G

model of sequence evolution. The posterior probabilities

were calculated discarding the initial 25 % (non-stationary)

of the resulting trees as burn-in.

The best-fitted model of sequence evolution was tested

in Modeltest v.3.7 (Posada and Crandall 1998), and the

TrN ? G model was chosen by the Akaike information

criterion. This model was used for distance calculations in

neighbour-joining analyses with PAUP* v.4.0b10 (Swof-

ford 2002).

A neighbour network (NN) was constructed for the

ITS1-5.8S-ITS2 using the neighbour network method of

SplitsTree version 4.10 (Huson and Bryant 2006) based on

uncorrected p-distances.

Results

Analyses based on nrDNA ITS

We used the maximum parsimony (MP, separately on the

complete material and on the data set under exclusion of

agamospermous samples, underlined in Table 2), maxi-

mum likelihood (ML) and Bayesian inference (BI)

approaches to test whether a consistent phylogeny may be

obtained regardless of the approach and software used. The

subsequent searches found trees of similar length, and all

consensus trees revealed main clades as presented (Figs. 1,

2).

The matrix used for phylogenetic analyses of ITS data

included 75 samples, 520 characters from the ITS1-5.8S-

ITS2 nuclear region including 101 parsimony informative

characters (PICs). The Ratchet analysis of the ITS data for

all taxa including apomictic species performed by NONA

revealed 3,912 equally parsimonious trees of length 401

(CI = 0.64, RI = 0.73). The tree with jackknife support

values for individual branches is shown in Fig. 2. Second

MP analysis shown in Fig. 1 contained 60 sexual

dandelions, 520 characters including 86 PICs. The con-

sensus tree was compiled from 3,073 trees of length 286,

CI = 0.72, RI = 0.81. Eight main clades were found.

Jackknife support was calculated as well.

The reticulation of the nrDNA network was performed

in SplitsTree version 4.10 and indicates the complexity of

the evolutionary history with hybridisation and introgres-

sion. Both ITS data sets were used. SplitsTree analysis

containing sexual and apomictic species is shown in Fig. 4,

only sexuals are shown in Fig. 3.

Results of the nrDNA analyses are displayed in Figs. 1,

2, 3, 4. As the topology of the trees is relatively close to

one another, the corresponding main clades are numbered

using Roman numerals. The picture of relationships

obtained by means of the analyses done on the complete

material (MP complete, NN, see Figs. 2, 4; the results

using NJ, ML and BI not having been included because of

an almost identical pattern shown) are rather obscured by

the inclusion of agamospermous taxa, although the main

clades are usually retained (the consensus tree obtained

from the MP analysis of sexuals has substantially higher

values for consistency and retention indices). Thus, we

consider the result of MP analysis of almost exclusively

sexual samples (Fig. 1) as the most instructive one, and the

following brief explanation of the results is demonstrated

on the basis of Fig. 1 mainly (in addition to sexual samples,

an apomictic polyploid species of the sect. Oligantha, T.

minutilobum, was included in the analyses as a represen-

tative of the morphologically most ancestral group in the

genus Taraxacum). It should be added that branches with

samples belonging to the same species generally have a

high jackknife support, usually over 90 %. There are also a

few individual samples that have a rather ‘‘erratic’’

behaviour (appear at variable positions in different analy-

ses); these are mentioned in the ‘‘Discussion’’.

The following relatively stable clades were recognised

(primarily based on the analyses of sexual samples, ordered

according to decreasing jackknife support; only clades

resulting from all types of analyses are listed):

Clade I

It consists of two samples of T. koksaghyz of sect. Cera-

toidea Kirschner and Stepanek which is generally consid-

ered to be close to sect. Macrocornuta (T. multiscaposum)

on morphological grounds but this presumption is not

corroborated by the results of nrDNA analyses.

Clade II

All the samples of T. erythrospermum (sect. Erythrosper-

ma) and T. pindicum (sect. Erythrocarpa) form a very well-

supported clade showing close relationships between these


123

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https://www.researchgate.net/publication/10618138_MRBAYES_3_Bayesian_Phylogenetic_inference_under_mixed_models?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

https://www.researchgate.net/publication/13370131_MODELTEST_testing_the_model_of_nucleotide_substitution?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

https://www.researchgate.net/publication/23315015_A_rapid_bootstrap_algorithm_for_the_RaxML-VI-HPC_web_servers?el=1_x_8&enrichId=rgreq-4bb31181-db6e-48bf-9442-7b85247de591&enrichSource=Y292ZXJQYWdlOzI2NTM0NjYyOTtBUzoyMTA4MDYzMjgzMDM2MTZAMTQyNzI3MTU1MzMxNA==

two species and sections. It should be noted that only two

sexual taxa are known in sect. Erythrosperma (T. ery-

throspermum and an imperfectly known western Mediter-

ranean taxon erroneously referred to as T. rubicundum in

the literature), and T. pindicola is the only sexual in sect.

Erythrocarpa (its sexuality is reported for the first time in

the present paper).

Clade III

A very stable clade comprised of representatives of the

sections Piesis, Orientalia, Primigenia and Sonchidium, and

an ancestral species of unknown sectional position, T.

cylleneum. This clade forms an umbrella for an assemblage

of ancestral taxa from the eastern Mediterranean and the

Near East; morphologically speaking, they have little in

common.

Clade IV

This clade is comprised of all six samples of T. multisca-

posum (sect. Macrocornuta) and almost all samples of T.

minutilobum (sect. Oligantha, morphologically the most

ancestral taxon in Taraxacum); a single sample of the latter

is found isolated at variable positions in the four analyses.

The distant position of this sample is accounted for by the

Prenanthes purpurea

tenuifolium [Palustria]

stenocephalum [Piesis]bessarabicum [Piesis]

cylleneum [Piesis]

serotinum [Dioszegia]

stevenii 1 [Orientalia]stevenii 2 [Orientalia]

primigenium 1 [Primigenia]

koksaghyz 2 [Ceratoidea]koksaghyz 1 [Ceratoidea]

haussknechtii 1 [Dioszegia]haussknechtii 2 [Dioszegia]

minutilobum 1 [Oligantha]

paludosiforme [Alpestria 2]bulgaricum [Alpina]

paludosiforme [Alpestria 1]linearisquamum 1 [Ruderalia]linearisquamum 3 [Ruderalia]

erythrospermum 2 [Erythrosperma]pindicola 1 [Erythrocarpa]

farinosum [Sonchidium]

linearisquamum 2 [Ruderalia]

japonicum aff. 1 [Mongolica]japonicum aff. 2 [Mongolica]japonicum aff. 3 [Mongolica]japonicum aff. 4 [Mongolica]

sp. [Calanthodia 1]

sp. [Calanthodia 2]sp. [Emodensia 1]

sp. [Calanthodia 3]

pindicola 2 [Erythrocarpa]erythrospermum 3 [Erythrosperma]

erythrospermum 4 [Erythrosperma]

nigrocephalum [Arctica]subalternilobum [Arctica]


minutilobum 2 [Oligantha]minutilobum 3 [Oligantha]minutilobum 4 [Oligantha]

minutilobum 5 [Oligantha]glaciale [Glacialia]

sp. [Qaisera 2]

gilliesii [Antarctica]aristum [Australasica]

carpaticum [Alpestria]

aphrogenes [Scariosa]

multiscaposum [Macrocornuta]

multiscaposum2 [Macrocornuta]multiscaposum3 [Macrocornuta]multiscaposum4 [Macrocornuta]

multiscaposum5 [Macrocornuta]multiscaposum6 [Macrocornuta]

pyrenaicum 2 [Obliqua]pyrenaicum 1 [Obliqua]

sp. aff. dealbatum [Leucantha]


zealandicum [Australasica]

nutans [Biennia]

sp. [Emodensia]

100

80

77

85

99

8086

9095

98

75

96

98

98

90

90

99

96

75

89

89

98

87

I.

VII.

II.

VI.

IV.

III.

V.

Fig. 1 Maximum parsimony

analysis of nrDNA of sexual

dandelions. Strict consensus tree

of 3,073 equally parsimonious

trees of length 286 (CI = 0.72,

RI = 0.81). Circles

apomorphies; open circles

homoplasies. Numbers above

branches are jackknife support

values


123

polyploid agamospermous status of this species, which

causes an imperfect homogenisation of the nrDNA region

with persistent parental copies (see ‘‘Discussion’’). It should

be noted that the presumed closest relative of sect. Macro-

cornuta, T. koksaghyz of sect. Ceratoidea, does not exhibit

any closer relationship to T. multiscaposum in our analyses.

Clade V

This clade corresponds to sect. Dioszegia, another ancestral

group.

Clade VI

An assemblage of usually derived groups recognised as

sections Palustria, Alpestria, Arctica and Obliqua; it also

includes a member of sect. Mongolica (T. japonicum).

Clade VII

Two of the three species of section Australasica were

included in the present study (T. aristum from SE Austra-

lia, and T. zealandicum from New Zealand) and they

invariably form a separate clade.

It should be added that in most analyses also a rather

weakly supported clade is recognised consisting of an

eastern Asiatic group of sect. Calanthodia and Emodensia,

and two sexual species, T. nutans (sect. Biennia) and T.

dealbatum agg. (sect. Leucantha).

Analyses based on cpDNA

Chloroplast trnL-F data matrix contained 450 characters

including 247 PICs. The Ratchet analysis showed 10,479

trees with length 535, CI = 0.85 and RI = 0.97. The strict

consensus was constructed with jackknife support (Fig. 5).

The maximum parsimony analysis (Fig. 5, a strict con-

sensus tree) of the trnL–trnF regions reveals one basic fact,

i.e., there is an intraspecific variation in a number of

ancestral diploid sexual species (T. cylleneum, T. seroti-

num, T. farinosum, T. bessarabicum, T. stenocephalum, T.

stevenii), all present in both main branches of the clado-

gram. Reasons for this phenomenon are considered in the

‘‘Discussion’’; here we can repeat the conclusions from the

previous studies of the dandelion cpDNA: the ancient gene

flow, the incidence of pseudogenes, a low substitution rate

and the common occurrence of homoplasious structural

mutations. The strict consensus tree information content

and interpretability in the evolutionary terms is quite low.

We were not even able to confirm the recently published

results showing the cpDNA differentiation into ancestral

and derived haplotype groups as presented by Wittzell

(1999) and Kirschner et al. (2003).

An analysis of the combined cpDNA and nrDNA data

set

Combined data of ITS and trnL-F contained 27 taxa and

strict consensus tree from Ratchet analysis revealed 72

trees of length 703, CI = 87 and RI = 95, jackknife sup-

port is indicated in each branch of the tree above 50 %

(Fig. 6).

Results of the combined analysis are shown on Fig. 6.

The presumption formulated on the basis of the cpDNA

analyses, i.e., the low interpretability of the analysis of the

Prenanthes purpurea

tenuifolium [Palustria]

stenocephalum [Piesis]bessarabicum [Piesis]

cylleneum [Piesis]

serotinum [Dioszegia]

luridum [Leucantha]

stevenii 1 [Orientalia]stevenii 2 [Orientalia]


koksaghyz 2 [Ceratoidea]koksaghyz 1 [Ceratoidea]

haussknechtii 1 [Dioszegia]haussknechtii 2 [Dioszegia]

sp. [Atrata 1]


sp. [Tibetana 1]

paludosiforme [Alpestria 2]bulgaricum [Alpina]

paludosiforme [Alpestria 1]

linearisquamum 1 [Ruderalia]linearisquamum 3 [Ruderalia]

erythrospermum 2 [Erythrosperma]pindicola 1 [Erythrocarpa]

farinosum [Sonchidium]

linearisquamum 2 [Ruderalia]

japonicum aff. 1 [Mongolicajaponicum aff. 2 [Mongolica]japonicum aff. 3 [Mongolica]japonicum aff. 4 [Mongolica]

sp. [Calanthodia 1]

sp. [Calanthodia 2]sp. [Sikkimensia 1]

sp. [Calanthodia 3]

pindicola 2 [Erythrocarpa]



nigrocephalum [Arctica]subalternilobum [Arctica]


minutilobum 2 [Oligantha]minutilobum 3 [Oligantha]minutilobum 4 [Oligantha]


glaciale [Glacialia]

sp. [Qaisera 2]

sp. [Scariosa 1]sp. [Scariosa 2]

sp. [Scariosa 3]

sp. [Scariosa 4]

arcticum [Arctica]

gilliesii [Antarctica]

aristum [Australasica]

obliquum [Obliqua]

carpaticum [Alpestria]

aphrogenes [Scariosa]

multiscaposum [Macrocornuta]

multiscaposum2 [Macrocornuta]multiscaposum3 [Macrocornuta]multiscaposum4 [Macrocornuta]

multiscaposum5 [Macrocornuta]multiscaposum6 [Macrocornuta]

sp. [Naevosa]

sp. [Tibetana]

sp. [Borealia]

sp. [Dissecta]

pyrenaicum 2 [Obliqua]pyrenaicum 1 [Obliqua]

sp. aff. dealbatum [Leucantha]


zealandicum [Australasica]

pyrenaicum agg. [Obliqua]

mitalii [Parvula]

nutans [Biennia]sp. [Emodensia]

VI.

VII.

V.

I.

II.

III.

IV.

85

9394

8699

8291

96

9694

79

79

99

97

83

83

98

91

92

92

7979

79

7979

87

7989

Fig. 2 Maximum parsimony analysis of complete nrDNA data set,

including the selected agamosperms. Strict consensus tree of 3,912

equally parsimonious trees of length 401 (CI = 0.64, RI = 0.73).

Circles apomorphies; open circles homoplasies. Numbers above

branches are jackknife support values


123

combined nuclear and chloroplast data sets, comes true.

Three ancestral sexual diploids appear in both main clades of

the cladogram (T. haussknechtii, T. pyrenaicum and T. ste-

venii), and not even the most distinct and stable clades

resulting from the nrDNA analyses can be recognised in the

combined tree. For details, see ‘‘Discussion’’; here we can

interpret the principal incongruence between the patterns

found by the analyses of the two data sets as a result of the

persistent hybridity in some, or even the majority of the

samples, irrespective of the reproduction system involved.

Discussion

Plastome analysis

Including the present study, there were four attempts to

reconstruct the cpDNA phylogeny in Taraxacum, all based

on a relatively ample material with overlaps between the

sample selection in individual studies because we provided

a part of the material for Wittzell (1999) and Mes et al.

(2000), and gathered most of the material for Kirschner

et al. (2003). Mes et al. (2000) performed an introductory

methodical analysis of several non-coding regions of

Taraxacum cpDNA and carefully sorted and characterized

individual types of variation. The main features encoun-

tered include relatively low substitution rates and a con-

siderable length variation with the frequent presence of

homoplasious indels. Wittzell (1999) used trnL–trnF

intergenic spacer for the phylogenetic reconstruction and

established basic features of the variation in this cpDNA

region. First, he recognised that a group of ancient hap-

lotypes are distinguished from the derived ones by the

31 bp insertion (see also Kirschner et al. 2003) and

characterized in detail a variety of cpDNA haplotypes

within 20 lineages. The variation revealed by him was

difficult to interpret phylogenetically, mainly because of

the presence of a variable number of trnF pseudogenes in

Fig. 3 Neighbour network

performed on sexual dandelions.

Species names are abbreviated,

for details see Table 2


123



that region, and a parallel variation of the pseudogenes in

ancient and derived haplotypes. However, there are a few

conclusions to be emphasised: there are ancient sexual

taxa characterized by a within-species variation, and very

closely related agamospermous taxa that markedly differ

in their cpDNA haplotypes belonging to different (but

sectionally non-specific) lineages, often combining ancient

and derived haplotypes. Kirschner et al. (2003) exploited

the sequence variation in psbA–trnH and trnL–trnF

regions. Although the regions used differ from those of

Wittzell (l. c.), the results are very similar: A group of

ancestral sections is characterized exclusively by

‘‘ancient’’ haplotypes while the precursor and derived

Taraxacum sections harbour a mixture of ancient and

derived haplotypes or only derived haplotypes. All the

above studies show clearly the weaknesses of the exploi-

tation of cpDNA for the phylogeny of dandelions: (a) a

relatively low substitution rate, (b) a relatively high fre-

quency of structural mutations with high homoplasy,

(c) frequent pseudogene incidence, (d) a substantial

cpDNA variation within sexual species, (e) substantially

different cpDNA profiles in closely related agamosperms,

and (f) multiple ancient and often also recent bi-direc-

tional hybridity with unknown parental taxa.

The present study differs from the above investigations

by the inclusion of multiple samples of a number of

ancestral taxa, so that the within-species variation becomes

more evident and important. There are two possible sources

of this variation, a possible ancient gene flow (introgres-

sion) between sexual dandelions, which is an alternative

supported by the evolutionary history of the genus (cf.

Zeisek and al., submitted). The other source may be a

misidentification of some samples not checked by the

present authors.

Fig. 4 Neighbour network performed on complete material. Species names are abbreviated, for details see Table 2


123


As regards the relatively low phylogenetically infor-

mative variation of the non-coding regions of cpDNA, one

of the possible explanations is the low age of most groups

of the genus Taraxacum in comparison with closely related

groups (such as Crepis and Ixeris). In terms of morphology,

the derived status of Taraxacum is documented by the fact

that most of the morphological characters of this genus can

be shown to have originated through reduction of the more

complex structural diversity found in related genera (e.g.,

the indumentum reduced to aranose hairs (other types of

hairs totally missing), the general habit confined to the

combination of leaf rosette and hollow scapes, and life

forms restricted to perennial hemicryptophyte, for further

data see Bremer 1994).

Variation of cpDNA within ancestral sexual diploid

species

One of the crucial issues in the exploitation of cpDNA in

the reconstruction of Taraxacum phylogeny is the intra-

specific variation. It was Wittzell (1999) who first pointed

out the within-species variation in T. serotinum, and the

data used in the present paper also include several cases of

this type of cpDNA polymorphism. In particular, it con-

cerns several species considered to belong to ancestral

sections (e.g., Piesis, Dioszegia, Orientalia). When we

consider the possible sources of this polymorphism, the

most probable one is the ancient or (less probably) recent

introgressive hybridization associated with chloroplast

capture, probable mostly because of the fact that the extent

of cpDNA intraspecific variation encompasses the taxo-

nomic limits. (King and Ferris 2000; Golden and al. 2000;

Widmer and Baltisberger 1999; Soltis et al. 1997; Okaura

and Harada 2002; Mason-Gamer et al. 1995). Less proba-

ble sources include the persistence of ancestral polymor-

phism and the incomplete lineage sorting, and, at least in

the case of T. serotinum (sect. Dioszegia), a mutation

process in a large, stable, non-panmictic geographical

range. Last, we should not forget the possibility of misi-

dentification of the material used in the cpDNA studies and

listed in GenBank.

We can conclude that the very fact of the extensive

intraspecific cpDNA variation makes the parsimony ana-

lysis of the chloroplast DNA dataset (and consequently of

the combined dataset) quite unreliable.

A limited congruence between the results of the cpDNA

and nrDNA analyses

Wittzell (1999), Mes et al. (2000, 2002) and Kirschner

et al. (2003) analysed various features of the cpDNA var-

iation in Taraxacum. The main result revealed the structure

previously outlined by Richards (1973) on the basis of

morphology, i.e., a division into primitive, precursor and

derived groups. The present cpDNA analysis, however,

failed to reveal even this simple pattern in the data avail-

able. None of the basic nrDNA clades identified in the

present study, however, matches any of the groups delim-

ited by means of the cpDNA study. The incongruence

between the cpDNA and nuclear genome analyses gene-

rally indicates hybridity in the material studied, which is a

fact repeatedly published for Taraxacum (e.g., King 1993,

Van der Hulst et al. 2003). The fact, that not even the

restriction of the analyses to sexually reproducing diploids

did increase the congruence of the two data sets shows that

Fig. 5 Maximum parsimony analysis of cpDNA data of sexual

dandelions. Strict consensus tree of 10,479 equally parsimonious trees

of length 535 (CI = 0.85, RI = 0.97). Circles apomorphies; open

circles homoplasies. Numbers above branches are jackknife support

values


123


in a certain, possibly high proportion of diploids, an ancient

persistent hybridity is present.

Results of nrDNA analyses and their limited overall

congruence with the established taxonomic system

of the genus Taraxacum

The limitations of the nrDNA phylogenetic approaches

when applied to the mixture of material with probable

hybrid origin (young derived sexual diploids) with repre-

sentatives of really ancestral lineages clearly appear in the

present study. There is a general congruence between the

taxonomic concepts developed on morphological and other

grounds, but only regarding cases with very closely related

species and within variable species (e.g., T. japonicum, T.

multiscaposum, T. koksaghyz or section Dioszegia). How-

ever, most of the generally accepted taxonomic solutions at

the sectional or suprasectional levels and hypothesised

relationships on morphological grounds are not supported

by the present results.

Among positive exceptions to this rule we can mention

the close relationships between T. sect. Erythrosperma and

T. sect. Erythrocarpa. Two morphologically close and

widespread sections characterized by usually red or red-

brown achenes, T. sect. Erythrosperma and T. sect. Ery-

throcarpa, have few sexual representatives. Because of a

number of agamospermous taxa intermediate between the

two sections, the relationships of the two sections remained

to be analysed. We included T. pindicola, a Greek–Bul-

garian member and the only known sexual species of the

sect. Erythrocarpa, and T. erythrospermum, a widespread

EC. and SE. European member of the sect. Erythrosperma

(one of the two sexual taxa in this section). Both samples of

T. pindicola and all samples of T. erythrospermum form a

stable clade showing very close relationships among the

samples.

Another case to be mentioned is sect. Dioszegia with

two species (T. serotinum subsp. serotinum and T. haus-

sknechtii) included in the nrDNA study (the third taxon, the

W. Mediterranean T. serotinum subsp. pyrrhopappum, see

also Zeisek and al. (submitted), is included in the cpDNA

study). The two species exhibit close relationships and

form a separate clade in all analyses. The section consists

of two species distributed in the W Mediterranean, in the

Pontic-Pannonian region and in steppe regions of S Russia

from where the section reaches Iran and NW Kazakhstan. It

is remarkable that the section does not exhibit any closer

relationship with the Piesis clade. The possible phyloge-

netic relationship between the two sections as suggested

previously (Kirschner and Stepanek 1996) thus could not

be confirmed in the present study similarly as in other

studies using analyses of isozymes (Hughes and Richards

1988), assessment of cpDNA variation (Wittzell 1999) or

nuclear DNA content variation (Zavesky et al. 2005). In the

latter study, differences in monoploid 1Cx genome size

between T. serotinum (1.43 pg) and T. bessarabicum

(1.11 pg) appeared relatively high (29 %) in comparison

with differences detected within and among other sections.

For example, the interspecific/intrasectional difference

between T. bessarabicum (1.11 pg) and T. stenocephalum

(1.03 pg) was only 7.8 % (Zavesky et al. 2005). On the

other hand, the tetraploid T. stenocephalum itself exhibits

an extensive genome size variation amounting to 17 %

(Travnıcek et al. 2013).

The last case of remarkable congruence between the

modern taxonomic concept and our nrDNA results is that

Fig. 6 Maximum parsimony

analysis of combined cpDNA

and nrDNA data sets. Strict

consensus tree of 72 equally

parsimonious trees of length

703 (CI = 0.87, RI = 0.95).

Circles apomorphies; open

circles homoplasies


123


of the section Australasica (Uhlemann et al. 2004). Two of

the three members of the section form a stable clade (VII)

in all types of analyses.

The most remarkable deviation of the present results

from the established system of sections in Taraxacum is the

case of Clade III. It consists of T. stevenii (the only known

sexual in sect. Orientalia and its type species), T. farino-

sum (the only known sexual in sect. Sonchidium, an

endemic of central Anatolia), T. primigenium (an imper-

fectly known member of sect. Primigenia presumed to be

one of the most ancestral taxa in this genus), two species of

sect. Piesis (T. bessarabicum and T. stenocephalum) and a

species with unknown sectional position, T. cylleneum, an

endemic of Oros Kyllini in Peloponnese. Morphologically

speaking, these taxa have little in common, the sections

have different centres of diversity and there is no literature

report of their possible closer relationships. There is,

therefore, a surprising but plausible hypothesis that the

above taxa have a common origin in spite of few (if any)

morphological synapomorphies. This again refers to the

fact of the low structural diversification of morphological

characters in this genus (cf. Stepanek and Kirschner 2013

and the Introduction). The majority of dandelions have a

very uniform general appearance of rosulate hemicrypto-

phytes with scapes, two series of ciliate or glabrous invo-

lucral bracts and numerous yellow florets in the capitulum,

and occasional aberrant characters states, such as a com-

plex branched system of long pliable thin roots, or tap-

rooted habit with stoloniform shoots, stem with 1–3

branches, leaf hairs sometimes on low protuberances or

ridges, outer bracts with aranose surface, flowers of other

colours, form rare exceptions to this rule. There is, there-

fore, a rather limited room for evolutionary inference on

the morphological grounds only.

A note on the within-species nrDNA variation

in an apomictic polyploid

T. minutilobum, is invariably grouped in Clade IV (four

samples, together with six samples of T. multiscaposum),

with the exception of one of its samples that is found

outside the clade in variably unresolved position. T. min-

utilobum is an agamospermous, probably polyploid taxon

and, as documented in (Zaveska Drabkova et al. 2009) in

detail, Taraxacum agamosperms exhibit an extensive

nrDNA ITS variation, reflecting the parental genomes of

the presumably hybridogenous taxa. The sample of five

plants probably covers two of the dissimilar ITS copies.

Acknowledgments Thanks are due to T. Cerny who determined

diploidy in selected samples by means of flow cytometry. The study

was supported a long-term research development project of Institute

of Botany ASCR, no. RVO 67985939 and by the Ministry of Edu-

cation grant no. ME10143 of the KONTAKT scheme; the support was

also provided by the Czech National Grant Agency grant, no.

GA13–13368S and by an FP7 grant for the project DRIVE4EU, no

613697.

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Documents

Towards a better understanding of the Taraxacum evolution (Compositae–Cichorieae) on the basis of nrDNA of sexually reproducing species