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6 March 2020 Delimitation of Iranian species of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum (Asteraceae, Cichorieae) based on morphological and molecular data
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Abstract

Scorzonera L. is represented by 57 species in Iran including three subgenera: S. subg. Scorzonera, S. subg. Podospermum and S. subg. Pseudopodospermum. Species of S. subg. Podospermum and S. subg. Pseudopodospermum in Iran are morphologically similar, which limits species delimitation. In order to clarify intersubgeneric and interspecific delimitation in Iran, we carried out extensive sampling of the two subgenera in Iran. We conducted phylogenetic analyses based on the nuclear Internal Transcribed Spacer (nrITS), detailed morphological studies, and we evaluated the systematic value of achene features. Our results showed that Scorzonera s.l. is polyphyletic, and both S. subg. Podospermum and S. subg. Pseudopodospermum are monophyletic. The monophyly of S. subg. Podospermum morphologically corresponds to a combination of characters containing pinnatifid leaves, phyllaries with black corniculate projections, and the presence of a swollen carpopodium on the achenes. A comparison of the topology observed in the nrITS phylogeny with achene features indicates that a sculptured achene wall surface in members of S. subg. Pseudopodospermum provides a synapomorphy for this lineage. This study supports a broader circumscription of S. subg. Pseudopodospermum with the addition of S. calyculata (S. sect. Incisae), S. ovata, S. papposa and S. paradoxa (S. sect. Papposae). Finally, we provide a taxonomic treatment, including an identification key and species diagnoses and distributions, with nomenclature of Iranian species.

Citation: Hatami E., Mirtadzadini M., Bordbar F. & Jones K. E. 2020: Delimitation of Iranian species of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum (Asteraceae, Cichorieae) based on morphological and molecular data. – Willdenowia 50: 39–63. doi:  https://doi.org/10.3372/wi.50.50105

Version of record first published online on 6 March 2020 ahead of inclusion in April 2020 issue.

Introduction

Scorzonera L. (Asteraceae, Cichorieae, Scorzonerinae) with 160–175 species, depending on the circumscription and species concepts, has a distribution spanning Europe and the Mediterranean region, N Africa and SW and C Asia, with a particularly high concentration of species in SW Asia (Bremer 1994; Rechinger 1977; Mabberley 2008; Norouzi & al. 2016; Kilian & al. 2009b+). In its widest circumscription, Scorzonera is characterized by simple or pinnatifid leaves, multiseriate and unequal phyllaries, glabrous or entirely lanate achenes, and plumose pappus bristles with soft and interwoven fimbriae (Lipschitz 1964; Rechinger 1977; Mavrodiev & al. 2004; Kilian & al. 2009a). The other unanimously recognized genera of subtribe Scorzonerinae are readily distinguished from Scorzonera in its widest sense: Tragopogon L., the only other large genus of the subtribe (c. 150 species), by its uniseriate involucre; Koelpinia Pall. by its scorpioid achenes without a pappus but with hooked projections; Epilasia (Bunge) Benth. & Hook. f. by its leafy outer series of phyllaries usually as long as or longer than the inner series; the monotypic Tourneuxia Coss. by its pappus laterally situated at the achene apex; and the monotypic Pterachaenia Benth. by its winged achenes (Mavrodiev & al. 2004; Kilian & al. 2009a).

Starting with Candolle (1805), who described the genus Podospermum DC., attempts have been made to segregate Scorzonera into separate genera; the most recent was by Nazarova (1990), who distinguished the monotypic Takhtajaniantha Nazarova from all other species in the genus. Podospermum was characterized by Candolle (1805) at generic rank by the combination of pinnatifid leaves and a well-expressed carpopodium, which is the sterile abscission zone at the base of the achene, attached to the receptacle and composed of one or more rows of cells that are distinct from the rest of the achene wall (Mukherjee & Nordenstam 2004). Due to this attractive diagnosis, the recognition of Podospermum at generic rank has been widely accepted (Candolle 1805, 1838; Cassini 1827; Dumortier 1827; Lessing 1832; Endlicher 1841; Grossheim 1949; Kuthatheladze 1978; Pignatti 1982; Tzvelev 1988; Nazarova 1997; Mavrodiev & al. 2004; Winfield & al. 2006; Greuter 2006+; Kilian & al. 2009a, 2009b+; Makbul & al. 2016). Instead of splitting Scorzonera into different genera, some workers (Lipschitz 1964; Rechinger 1977; Safavi 2013; Coşkunçelebı & al. 2015) recognized three subgenera: S. subg. Scorzonera, S. subg. Podospermum (DC.) Lipsch. and S. subg. Pseudopodospermum (Lipsch. & Krasch.) Lipsch., a treatment first established by Lipschitz (19351939) in his monograph of the genus. Lipschitz (1964) described the three subgenera based on the presence of a carpopodium with simple leaves (S. subg. Pseudopodospermum), the presence of a carpopodium with pinnatifid leaves (S. subg. Podospermum) and the absence of a carpopodium with simple leaves (S. subg. Scorzonera). Rechinger (1977) recognized that the carpopodium is sometimes inconspicuous in species of S. subg. Pseudopodospermum. He therefore considered other morphological characters, including a tuberous root, simple leaves, and a sculptured achene surface (lamellate, muricate, tuberculate or verrucose) to separate S. subg. Pseudopodospermum from S. subg. Scorzonera and S. subg. Podospermum. Morphological studies of achene features by Coşkunçelebı & al. (2016) confirmed that achene surface patterns are valuable for distinguishing between S. subg. Pseudopodospermum and S. subg. Podospermum (Coşkunçelebı & al. 2016). Those studies focused on Turkish species and they only sampled one and three species of S. subg. Pseudopodospermum and S. subg. Podospermum from Iran, respectively.

Previous molecular phylogenetic studies have sampled broadly across subtribe Scorzonerinae. The genus Scorzonera was resolved as polyphyletic, based on the nuclear ribosomal Internal Transcribed Spacer (nrITS; Mavrodiev & al. 2004) and a combined nrITS and external transcribed spacer (ETS) analysis and Amplified Fragment Polymorphisms (AFLPs) by Winfield & al. (2006). Intergeneric nodes in those analyses were, however, statistically unsupported. Both studies revealed that the “Lasiospora clade”, named after the Scorzonera segregate Lasiospora Cass. based on S. hirsuta (Gouan) L., represents a lineage that is far from the core of Scorzonera, in the sense of its type S. humilis L. Mavrodiev & al. (2004) showed that the Lasiospora clade can also be distinguished from Scorzonera based on chromosome number (6 and 7, respectively; see also Nazarova 1977; Diaz De La Guardia & Blanca 1987; Martin & al. 2012). The morphological distinction of Lasiospora species from Scorzonera is, however, unclear. Importantly, both studies confirmed that S. subg. Podospermum is monophyletic, but with S. purpurea L. resolved as sister to the Podospermum clade.

Zaika & al. (2020) recently provided a taxonomic reassessment of Scorzonera s.l. based on broad taxonomic sampling, carpological (including anatomical) data, and nrITS and two plastid markers (partial rbcL and matK) molecular phylogenetic analyses (Zaika & al. 2020). That study confirmed the polyphyly of Scorzonera and proposed a revised classification of the subtribe. As a result of their analyses, the following seven genera were confirmed: Gelasia Cass.; Pseudopodospermum (Lipsch. & Krasch.) Kuth.; Pterachaenia (including S. codringtonii Rech. f.); Scorzonera (including four major clades: Podospermum, Scorzonera s. str., S. albicaulis Bunge and S. purpurea); Takhtajaniantha; and the newly described Lipschitzia Zaika & al. (S. divaricata Turcz. clade) and Ramaliella Zaika & al. (S. polyclada Rech. f. & Köie clade). Therefore, the authors proposed a narrow circumscription of Scorzonera (containing the Podospermum clade) and accepted Pseudopodospermum as a separate genus. At present, we are uncertain of the most appropriate taxonomic concept for the clades Podospermum and Pseudopodospermum. Therefore, for the purpose of this study, we follow the wider circumscription of genus Scorzonera that recognizes these lineages at subgeneric rank: S. subg. Podospermum, and S. subg. Pseudopodospermum. This taxonomic concept is in accordance with the following studies: Lipschitz (1964), Rechinger (1977), Safavi (2013), and Coşkunçelebı & al. (2015). In contrast to Zaika & al. (2020), who investigated generic-level relationships within Scorzonera s.l. Our study focuses on the shallower taxonomic levels and aims to clarify the morphological delimitation among Iranian species within S. subg. Podospermum and S. subg. Pseudopodospermum and compare it with the nrITS tree.

Currently, the genus Scorzonera is represented by 57 species in Iran; of which 33% (20 species) are considered endemic to the country (Rechinger 1977; Safavi 2013; Safavi 2016; Safavi 2019). Of the 57 species in Iran, 36 belong to S. subg. Scorzonera (137 worldwide), nine to S. subg. Pseudopodospermum (20 worldwide) and 12 (21 worldwide) to S. subg. Podospermum (Kamelin & Tagaev 1986; Rechinger 1977; Safavi 2013; Safavi 2016; Safavi 2019). In Iran, S. subg. Podospermum and S. subg. Pseudopodospermum contain closely related species that are currently difficult to distinguish based on morphological characters, which limits species identification. With the exception of leaf-anatomical studies of Iranian species of S. subg. Pseudopodospermum and S. subg. Podospermum (Norouzi & al. 2016), and karyological analyses of a limited number of species from Iran (Safavi 1999; Bordbar & al. 2019; Hatami & al. 2019), no comprehensive study has been carried out to date to clarify the nomenclature and intergeneric and interspecific diagnostic characters of these subgenera in Iran. In order to clarify the circumscription of S. subg. Podospermum and S. subg. Pseudopodospermum and give stronger insight into these lineages in Iran, we conducted extensive sampling of the two subgenera in Iran for detailed morphological studies. We also sampled representatives of all major clades across Scorzonerinae for phylogenetic analysis based on nrITS. Therefore, the aims of the present study are to:

  1. Conduct phylogenetic analyses using nrITS sequence data to test the monophyly of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum in Iran and evaluate the phylogenetic relationship between species. We sampled representatives from across subtribe Scorzonerinae and the two subgenera with a focus on Iranian species.

  2. Investigate morphological characters of species of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum to understand the morphological boundaries and diagnostic characters both between the subgenera and among their species in Iran.

  3. Assess the systematic value of achene features for distinguishing between taxa and to compare the patterns of achene features with the inferred topology from phylogenetic analyses of the nrITS region.

  4. Provide a taxonomic treatment, including diagnoses and distributions, with a clarified circumscription and nomenclature of all species of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum in Iran. We also provide an identification key for the two subgenera and their species in Iran.

Material and methods

Sampling — For nrITS analyses, the sampling approach for Scorzonera subg. Podospermum and S. subg. Pseudopodospermum was guided by treatments in Flora iranica (Rechinger 1977). Refer to Appendix 1 for a list of all samples included in the nrITS analyses with voucher information and GenBank numbers for newly generated sequences in this study. See Table 1 for classifications of Scorzonera species based on previous studies. In order to include representatives from the major clades across Scorzonerinae in the molecular analyses, we also incorporated already published nrITS sequence data of members outside of the focus subgenera. Therefore, the ingroup comprised extensive sampling from Iranian S. subg. Podospermum and S. subg. Pseudopodospermum (Rechinger 1977), and sampling outside of those subgenera: species from S. subg. Scorzonera and from the genera Epilasia, Koelpinia, Pterachaenia and Tragopogon guided by the clades in subtribe Scorzonerinae in the nrITS analyses of Mavrodiev & al. (2004; Appendix 1). Sequences of nrITS for 29 accessions were newly generated in this study: 11 from species of S. subg. Podospermum, seven from species of S. subg. Pseudopodospermum and one species of the Lasiospora clade distributed in Iran. In some cases, there were multiple accessions per species. It was not possible to generate nrITS data for S. turkeviczii Krasch. & Lipsch. or S. syriaca Boiss. & Blanche (S. subg. Pseudopodospermum); however, these species were included in the morphological analyses and taxonomic treatment (see below; Table 1). Scorzonera lachnostegia (Woronow) Lipsch. (S. subg. Podospermum) is very rare in Iran (Safavi 2013); therefore, it was not possible to locate specimens for morphological or molecular studies. Sequences of 22 species from NCBI were included, corresponding to the three subgenera of Scorzonera and other related genera in subtribe Scorzonerinae. In total, nrITS sequences for 44 species of Scorzonerinae were included in the phylogenetic analyses. Sequences for Cichorium intybus L., Lactuca sativa L. and Scolymus maculatus L. from NCBI were included as outgroup species to Scorzonerinae (Appendix 1).

Phylogenetic reconstruction — Genomic DNA was extracted from leaf material using the DNeasy Plant Mini Kit (Qiagen, Hilden, Germany) according to the manufacturer's protocol. For amplification of the nrITS region, primers ITS-A and ITS-B were used (Blattner 1999). The PCR reaction mixture consisted of 20 µl deionized water, 7 µl 2×Taq DNA polymerase master mix Red (Amplicon, Cat. No.180301), 0.75 µl of each primer (50 pmol/µl), and 1.5 µl template DNA. PCR amplification consisted of an initial denaturation step of 3 minutes at 94°C, followed by 38 cycles of 30 seconds denaturation at 94°C, 40 seconds annealing at 53°C and 1-minute extension at 68°C, and a final extension step at 70°C for 10 minutes. Sequencing reactions were performed at Macrogen Inc. (Seoul, Korea) using the same PCR primers.

Sequences were initially aligned using MAFFT v. 6.0 (Katoh & Toh 2008) and checked manually using the program PhyDE v. 0.9971 (Müller & al. 2005). Indels were coded as binary characters using the simple indel coding approach, according to Simmons & Ochoterena (2000) in SeqState v. 1.4.1 (Müller 2005). Phylogenetic analyses were conducted using Maximum Parsimony (MP), Maximum Likelihood (ML) and Bayesian Inference (BI). Maximum Parsimony analyses were performed using heuristic searches in PAUP* v. 4.0b10 (Swofford 2003) in combination with parsimony Ratchet (Nixon 1999) in PRAP (Müller 2004). Ratchet settings included 200 iterations with 25% of the positions randomly unweighted (weight = 2), and 100 random additional cycles. Jackknife (JK) support was estimated in PAUP by conducting a single heuristic search within each 10 000 replicates using the Tree Bisection and Re-connection branch-swapping algorithm and a deletion of 36.79% characters in each replicate. A strict-consensus tree was constructed from all saved trees. The symmetrical (SYM) nucleotide substitution model was selected as the best-fit model using JModelTest v.2.1.6 (Darriba & al. 2012), according to the Akaike Information Criterion (AIC). The neighbour-joining algorithm BIONJ was used for the initial tree search (Gascuel 1997; Saitou & Nei 1987). Maximum Likelihood analyses were conducted using the graphical user interface of RAxML v. 1.5b1 (Silvestro & Michalak 2012). Bootstrap support was estimated based on the majority-rule consensus tree from 1000 replicates with 200 searches and the final tree topology was evaluated under the GTR GAMMA algorithm because the SYM model is not available in RAxML. Bayesian Inference was conducted in MrBayes v. 3.2 (Ronquist & Huelsenbeck 2003) on the CIPRES science gateway (Miller & al. 2010). Four runs each with four chains were performed for 30 million generations, sampling every 2000 generations. After removing 10% of the sampled trees as burn-in, a 50% majority-rule consensus tree was constructed. Final tree visualization was carried out using TreeGraph v. 2.13.0-748 beta (Stöver & Müller 2010). Final DNA sequences were submitted to ENA ( https://www.ebi.ac.uk/ena) using the software tool annonex2embl (Gruenstaeudl 2019).

Table 1.

Scorzonera species included in this study and their subgeneric classification based on previous literature (in column 2: Lipschitz 1964; Rechinger 1977; Kamelin & Tagaev 1986; Mavrodiev & al. 2014; Safavi 2013; Zaika & al. 2020) compared to results of phylogenetic analyses (Fig. 1) and the taxonomic treatment of this study (in column 3).

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Morphological and taxonomic studies — Collections of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum were made between 2015 and 2018 across a broad geographic range in Iran in order to sample the maximum diversity of each taxon. Specimens from those field trips were deposited at MIR (see Appendix 2 for a list of specimens examined for the morphological and taxonomic studies). Live plants in the field and herbarium specimens in B, FMUH, HSHU, IRAN, JE, MIR and W were examined (herbarium codes according to Thiers 2019+; Appendix 2). Digitized specimens were examined via virtual herbarium catalogues at E ( https://data.rbge.org.uk/search/herbarium/), G ( http://www.ville-ge.ch/musinfo/bd/cjb/chg/), LINN ( http://linnean-online.org/linnaean_herbarium.html), P ( https://science.mnhn.fr/institution/mnhn/search) and via JSTOR Global Plants ( https://plants.jstor.org/). Where possible, type specimens were examined by E.H. in the herbaria B, JE and W, from images provided by LE for types in that herbarium, and via virtual herbarium catalogues and JSTOR Global Plants for types in G and LINN. Descriptions of morphological characters were based on our observations and measurements (life cycle, plant height, root, stem, leaves, flowering capitula, fruiting capitula, achenes, pappus; Appendix 4) with comparisons to previous relevant studies (Lipschitz 1964; Rechinger 1977; Safavi 2013). Terminology for vegetative and reproductive morphological characters follows Beentje (2010). For each species the general distribution, updated nomenclature, and synonyms are given based on Flora iranica, Flora of Iran, and the Cichorieae portal (Rechinger 1977; Safavi 2013; Kilian & al. 2009+).

Macro photographs of achenes from species belonging to Scorzonera subg. Podospermum and S. subg. Pseudopodospermum were made using a stereomicroscope (Olympus SZX16) equipped with DP72 (a 12.5 megapixel digital colour camera), connected to cellSens Standard programme with an extended focus imaging function, at the Botanic Garden and Botanical Museum Berlin.

Results

Molecular analyses — The aligned nrITS data matrix comprised of 55 sequences and 826 characters including 126 coded indels, 291 parsimony informative sites and 156 parsimony uninformative sites (see alignment in Appendix 3). Maximum Parsimony analyses resulted in 16 most parsimonious trees with a length of 1096, a consistency index of 0.615, and a retention index of 0.863.

Bayesian Inference, ML, and MP analyses of the nrITS dataset produced identical topologies. The MrBayes 50% majority-rule consensus tree is presented in Fig. 1. Here, we report statistical support values that are well-supported (>0.95 posterior probability [PP], and >80% BS and JK) in parentheses (Fig. 1). Subtribe Scorzonerinae received full statistical support (1 PP, 100 JK, 100 BS; Fig. 1). The Lasiospora clade was resolved as monophyletic (1 PP, 100 JK, 100 BS) and as sister to a clade (1 PP, 99 JK, 97 BS) containing a polytomy that consisted of the rest of subtribe Scorzonerinae. This polytomy comprised five clades; one clade (1 PP, 92 BS) included in two subclades that contained the genera Epilasia (1 PP, 100 JK, 100 BS) and Tragopogon (1 PP, 100 JK, 100 BS), respectively. A second lineage in the polytomy corresponded to a single accession representing the monotypic genus Pterachaenia. The third clade in the polytomy (1 PP, 93 JK, 94 BS) contained the genus Koelpinia, sister to a clade consisting of Scorzonera intricata Boiss, and S. tortuosissima Boiss. (S. intricata clade; 1 PP, 100 JK, 100 BS). In a fourth clade (1 PP, 91 JK, 84 BS), S. humilis and S. aristata Ramond ex DC. (S. humilis clade; 1 PP, 99 JK, 99 BS) and a single accession of S. purpurea were resolved as consecutive sisters to a clade uniting the members of S. subg. Podospermum (1 PP, 100 JK, 100 BS). The relationships within the S. subg. Podospermum clade were largely unresolved, with the exception of the S. songorica (Kar. & Kir.) Lipsch. & Vassilcz. clade (1 PP, 100 JK, 100 BS) and the S. cana (C. A. Mey.) O. Hoffm. clade (0.99 PP, 91 JK, 80 BS). The fifth clade included S. subg. Pseudopodospermum (1 PP, 100 JK, 100 BS). Within S. subg. Pseudopodospermum, an accession of S. calyculata Boiss. was resolved as sister to S. papposa DC., which was sister to the S. mollis M. Bieb. clade (13 samples of nine species; 1 PP, 87 JK, 95 BS). The S. mollis clade contained a polytomy consisting of an accession of S. mollis, one clade (0.99 PP, 64 JK, 71 BS) containing three accessions of S. szowitzii DC. and another clade (1 PP) with the three samples of S. raddeana C. Winkl. (1 PP, 93 JK, 94 BS) in one subclade that was sister to a subclade containing S. phaeopappa (Boiss.) Boiss., S. semicana DC., S. mucida Rech. f. & al., and S. tunicata Rech. f. & Köie (0.93 PP).

Morphology — Images of achenes of 22 species are presented in this study (Fig. 2; Fig. 3). A summary of the achene surface pattern, pubescence, carpopodium and pappus bristles of species in Scorzonera subg. Podospermum and S. subg. Pseudopodospermum from Iran is provided in Table 2. Our observations revealed that, in S. subg. Podospermum, outer achenes are smooth, subterete to sulcate, glabrous or lanate, with a conspicuous carpopodium, and the pappi are apically scabrous with plumose bristles for most of the length. In contrast, in S. subg. Pseudopodospermum, the outer achenes are lamellate, muricate, or verrucose, with or without a conspicuous carpopodium, glabrous, and the pappi either consist of bristles that are plumose for the entire length or for most of the length, and are apically scabrous, sometimes with five obvious longer scabrous bristles. More detailed characteristics of achenes for each species are given in Table 2.

Fig. 1.

Bayesian 50% majority-rule consensus tree inferred from the nuclear Internal Transcribed Spacer dataset. Values above nodes indicate posterior probability (bold) and jack-knife support (italic), and values below nodes indicate bootstrap support. Tip names correspond to species names and GenBank numbers or DNA numbers for newly generated sequences; see Appendix 1 for specimen details and Appendix 3 for the alignment). Clade names are indicated to the right of the phylogenetic tree. The star corresponds to the monophyletic Scorzonera subg. Podospermum and the circle corresponds to S. subg. Pseudopodospermum. Squares next to two tip names correspond to accessions of species names that are newly synonymized with S. szowitzii in this study (LAC540 S. leptophylla; LAC529 S. stenocephala; see the taxonomic treatment for details).

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In addition to achene morphology, a range of morphological features was examined for the identification key and taxonomic treatment below. Voucher information for specimens examined are provided for all species in Appendix 3; and the summary of morphological features (life cycle, plant height, root, stem, leaves, flowering capitula, fruiting capitula, achenes, pappus) for selected species in Scorzonera subg. Podospermum and S. subg. Pseudopodospermum are provided in Appendix 4.

Table 2.

Comparisons of achene features (achene surface, pubescence, carpopodium and pappus features) of representative species within Scorzonera subg. Podospermum and S. subg. Pseudopodospermum.

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Discussion

Relationships within subtribe Scorzonerinae — The topology inferred in our phylogenetic analyses (Fig. 1) confirms the results of previous studies that showed Scorzonera s.l. is polyphyletic (Mavrodiev & al. 2004; Winfield & al. 2006; Zaika & al. 2020). Based on our molecular analysis, the Lasiospora clade is well-resolved as a lineage that is remote from the core of Scorzonera, in the sense of its type S. humilis, in accordance with Mavrodiev & al. (2004), Winfield & al. (2006) and Zaika & al. (2020). However, Zaika & al. revealed that S. villosa Scop. is included in this lineage, and they proposed the oldest generic name: Gelasia. Our molecular analysis showed a sister-group relationship between the genus Koelpinia (K. linearis Pall. and K. macrantha C. Winkl.) and the S. intricata clade (S. intricata and S. tortuosissima here) from S. sect. Intricatae (Boiss.) Lipsch. within S. subg. Scorzonera. Our findings are in agreement with Zaika & al (2019), who revealed a sister relationship between the S. polyclada clade (including S. intricata, S. longipapposa Rech. f. and S. polyclada from S. sect. Intricatae of S. subg. Scorzonera) and Koelpinia proposing the generic name Ramaliella for S. polyclada. The sister relationship between Epilasia and Tragopogon in Fig. 1 is also congruent with previous studies (Mavrodiev & al. 2006; Zaika & al. 2020).

The remainder of the ingroup forms two major well-supported clades: one including the Scorzonera humilis clade, S. purpurea and S. subg. Podospermum and the other including S. subg. Pseudopodospermum. Our phylogenetic analyses incorporated some rare species of S. subg. Podospermum (S. kandavanica Rech. f., S. persepolitana Boiss.) and S. subg. Pseudopodospermum (S. szowitzii, S. tunicata) that had never been sampled before. Scorzonera subg. Podospermum and S. subg. Pseudopodospermum are monophyletic according to our nrITS tree (Fig. 1). Based on our nrITS phylogenetic tree, the S. humilis clade containing S. humilis, the type of Scorzonera, was resolved as sister to a clade containing S. purpurea and S. subg. Podospermum. This supports the treatment of S. subg. Podospermum as a subgenus within the genus Scorzonera (Lipschitz 1964; Rechinger 1977; Kamelin & Tagaev 1986) in contrast to previous treatments that considered it as an independent genus (Candolle 1805; 1838; Cassini 1827; Dumortier 1827; Lessing 1832; Endlicher 1841; Grossheim 1949; Kuthatheladze 1978; Pignatti 1982; Tzvelev 1988; Nazarova 1997; Mavrodiev & al. 2004; Winfield & al. 2006; Greuter 2006+; Kilian & al. 2009a, 2009b+; Makbul & al. 2016). Scorzonera humilis, S. purpurea and species of S. subg. Podospermum are morphologically distinct. However, based on morphological observations by E.H., they share the following morphological characters: woody cylindric root (non-tuberous) and the presence of basal leaves with few and small cauline leaves.

Lipschitz and Krascheninnikov (Lipschitz 1935) described Scorzonera subg. Pseudopodospermum as a section within the genus Scorzonera containing 14 species. Later, Lipschitz (1964) changed its taxonomic rank to subgenus, which is widely accepted in the following floras: Flora URSS (Lipschitz 1964), Flora iranica (Rechinger 1977), and Flora of Iran (Safavi 2013). We took the descriptions of species within this subgenus from different regional Floras into account: Flora URSS (Lipschitz 1964), Flora iranica (Rechinger 1977), Flora of Iran (Safavi 2013) and from recent studies (Coşkunçelebı & al. 2015; Coşkunçelebı & al. 2016; Norouzi & al. 2016; Hatami & al. 2019), which included additional species that were not considered members of S. subg. Pseudopodospermum by Lipschitz (1964): S. aksekiensis A. Duran & M. Öztürk, S. elata Boiss., S. inaequiscapa Boiss., S. mucida, S. pachycephala Podlech & Rech. f., S. syriaca and S. tunicata. The topology inferred by our molecular analyses and morphological observations, in particular of the achene surface, supports a broader circumscription of S. subg. Pseudopodospermum, to include S. calyculata and S. papposa. Zaika & al. (2020) also included members of S. sect. Incisae Lipsch. and S. sect. Papposae Lipsch. & Krasch. in S. subg. Pseudopodospermum, which was treated at generic level, based on their analyses of nrITS and plastid data and carpological features.

The monophyly of clades corresponding to Scorzonera subg. Podospermum and S. subg. Pseudopodospermum was confirmed based on broad taxonomic sampling in Zaika & al. (2020) similar to previous studies that had less sampling (Mavrodiev & al. 2004). In the nrITS and plastid phylogenetic trees in Zaika & al. (2020), there is limited phylogenetic resolution within the Podospermum and Pseudopodospermum clades. Therefore, the fact that we did not include all species that were sampled in the phylogenetic analyses in Zaika & al. (2020) does not cause a bias in our phylogenetic analyses. Furthermore, we broadened the taxonomic sampling compared to Zaika & al. (2020): three species in S. subg. Pseudopodospermum (S. semicana, S. szowitzii and S. tunicata) and two species in Podospermum (S. kandavanica and S. persepolitana). Below, we discuss the results of our morphological analyses of Iranian species of S. subg. Podospermum and S. subg. Pseudopodospermum in the context of our nrITS tree (Fig. 1).

Scorzonera subg. Podospermum — The monophyly of Scorzonera subg. Podospermum (Fig. 1) morphologically corresponds to a combination of morphological characters containing pinnatifid leaves, phyllaries with a black corniculate projection (Fig. 4A), and the presence of a swollen carpopodium (Fig. 2A–J; Fig. 4B). Species of S. subg. Podospermum are mostly distributed in the Euro-Siberian region in the north of Iran, and in the Irano-Turanian region, particularly the Kurdo-Zagrosian zone in the west of Iran (Zohary 1973; Rechinger 1977; Safavi 2013). This subgenus is most common in highland regions (>1000 m a.s.l) of more or less wet meadows, ruderal sandy or gravelly soils, stony slopes, or wet corners of agricultural fields (based on observations by E.H. and M.M.; Fig. 4D–F).

Fig. 2.

Macro photographs of achenes of species within Scorzonera subg. Podospermum (A–J), S. purpurea (K, L), and S. subg. Pseudopodospermum (M–T). – Scale bar lengths are given in parentheses after figure letters. – Voucher locality, collection date, collector(s) and number, and herbarium code for each sample are given in parentheses after species names. – Scorzonera subg. Podospermum: A (2 mm) and B (1 mm): S. cana (Greece, Grevena, 2.1 km NE of Paliouria, 31 May 1990, Laubwald & al. 8941, B). – C (2 mm) and D (1 mm): S. kandavanica (Iran, N Iran, 6 km from Lowshan to Jirandeh, 20 May 2016, Mirtadzadini 2212, MIR). – E (2 mm) and F (2 mm): S. laciniata (Iran, Zanjan to Bijar, 22 May 2016, Mirtadzadini 2216, MIR). – G (5 mm) and H (1 mm): S. persepolitana (Iran, Esfahan, near Delijan on clay hill, 20 May 2010, Mirtadzadini 2218, MIR). – I (2 mm) and J (1 mm): S. songorica (Iran, Kerman, Sardu, 24 Jun 2017, Hatami & al. 2247, MIR). – K (2 mm) and L (1 mm): S. purpurea (Germany, Frankenhausen, Jun 1994, W. Becker s.n., B). – S. subg. Pseudopodospermum: M (5 mm) and N (1 mm): S. papposa (Palestine, Shefela, 23 Mar 2010, Ristow 34/10, B). – O (5 mm) and P (2 mm): S. phaeopappa (Iran, Kordestan, Marivan, Mirtadzadini 2162, MIR). – Q (5 mm) and R (2 mm): S. raddeana (Iran, Fars, between Estahban and Niriz, 3 May 2016, Mirtadzadini & al. 2157, MIR). – S (5 mm) and T (2 mm): S. calyculata, Iran, Between Karaj and Qazvin, 22 Jun 2011, Mirtadzadini 2219, MIR). – Macro photographs produced using a stereomicroscope (Olympus SZX16) equipped with DP72 (a 12.5 megapixel cooled digital colour camera) at the Botanic Garden and Botanical Museum Berlin.

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All species of Scorzonera subg. Podospermum that are distributed in Iran (Rechinger 1977; Safavi 2013) are included in our phylogenetic analyses, with the exception of S. lachnostegia, a rare species, which was sampled by Zaika & al. (2020) and resolved in a polytomy within the Podospermum clade in their nrITS tree. In spite of sampling multiple accessions of different species in our phylogenetic studies, the interspecific relationships were poorly resolved based on nrITS sequences, similar to Zaika & al. (2020) (Fig. 1). However, morphological characters, particularly achene features, were informative for clarifying the interspecific circumscription of this subgenus; see taxonomic treatment below (Table 2; Fig. 2A–J).

Within the Scorzonera songorica clade (Fig. 1), S. meshhedensis (Rech. f.) Rech. f. and S. songorica are morphologically similar to each other in possessing basal or cauline simple leaves (see Fig. 4E for S. meshhedensis). The pappus of these two species can be easily detached; a characteristic that is unique to this lineage among all Scorzonera species sampled in this study. The type of S. subg. Podospermum is S. laciniata L. (Lipschitz 1964). It is morphologically distinctive in having the longest carpopodium (6–7 mm) with the highest ratio of carpopodium length to total achene length among all species of S. subg. Podospermum (Table 2; Fig. 2E, F). The S. cana clade received strong statistical support (0.99 PP, 91 JK, 80 BS), but its internal relationships are unresolved due to the low variation of the nrITS region. However, species within the S. cana clade can be distinguished based on diagnostic morphological characters (Fig. 4C, D; Appendix 4); see taxonomic treatment below.

Previous treatments placed Scorzonera purpurea in S. subg. Podospermum (Candolle 1838; Kamelin & Tagaev 1986), whereas others treated it as a member of S. subg. Scorzonera sect. Purpureae Lipsch. (Lipschitz 1964; Zaika & al. 2020). The achenes of S. purpurea possess pale and tube-like swollen bases (Lipschitz 1964; Chater 1976), which is morphologically similar to the carpopodium of species in S. subg. Podospermum (Fig. 2K, L). However, the swollen bases are entirely fertile in S. purpurea compared to infertile carpopodia in species of S. subg. Podospermum. Furthermore, members of S. subg. Podospermum differ from S. purpurea in having pinnatifid leaves and phyllaries with corniculate projections (Fig. 4A); in contrast, S. purpurea has simple leaves and no corniculate projections. Although a sister relationship between S. purpurea and S. subg. Podospermum is well-supported in our nrITS analyses (95 PP; Fig. 1), we propose to maintain the treatment of this species outside of S. subg. Podospermum based on morphological differences observed here and in accordance with previous studies (Lipschitz 1964; Zaika & al. 2020).

Scorzonera subg. Pseudopodospermum — Our nrITS analyses included all species of S. subg. Pseudopodospermum distributed in Iran (Rechinger 1977; Safavi 2013; except S. syriaca and S. turkeviczii); as well as S. mollis, which represents the type of this subgenus (Lipschitz 1964). Members of this subgenus are widely distributed in dry to humid areas of the Irano-Turanian region (Zohary 1973; Rechinger 1977; Safavi 2013) and mostly grow in highland regions (>1000 m a.s.l) on sandy, clay or gravelly steppe hills, stony and rocky slopes, limestone hills in grassy steppes, stony semi-deserts, and open grassland (based on observations by E.H. and M.M.).

Scorzonera subg. Pseudopodospermum is monophyletic based on our nrITS phylogeny (Fig. 1) and the morphological observations in this study suggest that a sculptured (as opposed to smooth) achene-wall surface provides an exclusive synapomorphy for this lineage (Table 2). Within S. subg. Pseudopodospermum, the type of sculpturing on the achene surface is variable among species, and can be muricate, tuberculate, lamellate or verrucose (Table 2; Fig. 2M–T). Moreover, we include sequences of species from Iran that also have sculptured achenes from S. sect. Incisae and S. sect. Papposae to clarify their phylogenetic position and compare their morphological characters with members of S. subg. Pseudopodospermum. The S. mollis clade in our nrITS tree (Fig. 1) represents S. subg. Pseudopodospermum in its traditional circumscription (Lipschitz 1964; Rechinger 1977; Fig. 1). Based on our nrITS tree, S. calyculata (S. subg. Scorzonera sect. Incisae) and S. papposa (S. subg. Scorzonera sect. Papposae) are sister to the S. mollis clade with full statistical support and together they form a monophyletic clade. In Iran, S. sect. Incisae is represented by S. calyculata, and S. sect. Papposae by S. ovata Trautv., S. papposa and S. paradoxa Fisch. & C. A. Mey. ex DC.; we include all species in our morphological studies and the taxonomic treatment (see below). Morphological comparisons revealed that the sculptured achene surface supports a close relationship between the S. mollis clade and S. calyculata and all members of S. sect. Papposae in Iran, in support of the close relationship observed in the nrITS tree (Table 2; Fig. 1). We therefore propose a broader circumscription of S. subg. Pseudopodospermum to include members of S. sect. Incisae and S. sect. Papposae (S. calyculata and S. papposa, S. ovata and S. paradoxa; Table 1). Members of S. sect. Incisae and S. sect. Papposae outside of Iran also have sculptured achene surfaces (Lipschitz 1964; Rechinger 1977); it would therefore be beneficial incorporate all members of these sections and S. subg. Pseudopodospermum into future phylogenetic studies. Based on previous treatments (Lipschitz 1964; Rechinger 1977), members of S. sect. Incisae and S. sect. Papposae were morphologically distinguishable within S. subg. Scorzonera according to the absence of a carpopodium. Furthermore, we found that the carpopodium is only sometimes swollen among members of the S. mollis clade. The newly circumscribed S. subg. Pseudopodospermum in our study contains species either without a carpopodium or with a carpopodium that may be conspicuous or inconspicuous. Our study therefore suggests that the presence or absence of carpopodia is not a diagnostic character for intersubgeneric classification within the genus Scorzonera, in accordance with Haque & Godward (1984) and Zaika & al. (2020).

The Scorzonera mollis clade within S. subg. Pseudopodospermum (Fig. 1) contains a number of well-supported subclades, which we now discuss. In the nrITS analyses, we include sequences of an accession that we identified as S. szowitzii (LAC530) and accessions that corresponded of S. leptophylla (DC.) Krasch. & Lipsch. (LAC540) and S. stenocephala Boiss. (LAC529) according to species descriptions in Flora iranica (Fig. 1; Rechinger 1977). All three accessions were resolved in a strongly supported clade (0.99 PP; Fig. 1). We also studied morphological characters of multiple populations of S. leptophylla, S. stenocephala and S. szowitzii from several geographic regions in the field and herbaria (Appendix 1; Appendix 2). We observed extreme phenotypic plasticity among these species in vegetative characters including plant height, leaf width, possessing an entire or undulate leaf margin, and glabrous or tomentose indumentum (Appendix 4). All species are indistinguishable according to capitula length, number of florets in each capitulum, and achene and pappus features (Table 2; Appendix 4). Based on overlapping morphological characters and nomenclatural priority, we treat them as S. szowitzii (see taxonomic treatment below).

Three accessions of Scorzonera raddeana in the nrITS analyses show intraspecific variation, which is consistent with morphological variation; length and width of fruiting capitula and width of leaves are variable between individuals; LAC540 and LAC534 were distinct from LAC513 (see taxonomic treatment below). However, all individuals of S. raddeana samples in the nrITS tree have the typical S. raddeana achene and pappus type (Table 2). Scorzonera phaeopappa is resolved as sister to S. semicana with high statistical support (Fig. 1). Based on our observations, a combination of the following characters represents the synapomorphy for the S. phaeopappa and S. semicana subclade: achenes with a swollen carpopodium and five conspicuously long scabrous bristles in the pappus (Table 2; Fig. 2O; Fig. 3Q; Appendix 4). Another strongly supported clade (1 PP, 87 JK, 90 BS) contains S. mucida and S. tunicata with similar morphological characters (Table 2; Appendix 4). We consider them as separate species based on differences in achene and phyllary characters (see Notes under S. mucida). Hatami & al. (2019) recently found that chromosome number and ploidy are also different between these species: tetraploid and 2n = 28 in S. mucida in contrast to diploid and 2n = 14 in S. tunicata. The placement of the diploid S. tunicata in a clade with the tetraploid S. mucida in the nrITS tree may suggest that S. tunicata represents a parent of S. mucida. Further studies are required to determine if S. mucida is an auto- or allotetraploid. It was not possible to include other species from S. subg. Scorzonera that have sculptured achenes in our molecular studies because they are rare in Iran, including S. helodes Rech. f. and S. limnophila Boiss. (S. sect. Dimophopapposae Lipsch.) and S. nivalis Boiss. & Hausskn. (S. sect. Foliosae (Boiss.) Lipsch.) (Rechinger 1977; Kamelin & Tagaev 1986). It would be beneficial to include these rare Scorzonera species that also have sculptured achenes in future studies, in order to explore their relationships with members of S. subg. Pseudopodospermum.

Taxonomic treatment of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum in Iran

Habit — Most taxa in Scorzonera subg. Podospermum and S. subg. Pseudopodospermum are perennial, possessing a taproot or tuberous root with developed lateral roots (Appendix 4). Morphology and placement of tubers are not used here as diagnostic features because they are highly variable within species depending on the ecological conditions. Tubers may be cylindric or spherical and can be deep underground or near to the surface. Some species within S. subg. Podospermum possess a caudex, which is the persisting woody axis of the (former) rosette shoot (Beentje 2010) that may be branched or unbranched, characterized by densely set leaf scars or leaf remains; it is often dark brown and transversely rough with numerous dry and membranous scales at the apex. With the exception of two species in S. subg. Podospermum, all species of S. subg. Podospermum and S. subg. Pseudopodospermum are perennial herbs with either a caespitose, subcaespitose or caulescent habit (Fig. 4: Fig. 5). In caespitose perennials, the flowering stems arise from radical rosettes and are often scape-like, thus leafless or bearing few reduced leaves or bracts (Fig. 4C, F; Fig. 5A, D, E). Caulescent perennials usually have developed cauline leaves and a branched flowering stem (Fig. 4D; Fig. 5B). Two species (S. laciniata and S. songorica from S. subg. Podospermum) are biennial with a thin taproot, typically lacking remains of previously withered leaves.

Leaves — Basal and cauline leaves vary from undivided to deeply pinnatisect among species of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum (Fig. 4; Fig. 5). Undivided leaves may be linear, lanceolate or ovate and the leaf margin may be flat or undulate (Fig. 5F, G). Pinnatifid leaves are pinnately divided but not all the way down to the rachis, whereas pinnatisect leaves (Fig. 4C, D) are deeply divided reaching the rachis (Allaby 1992). Leaf segments may be linear, oval-lanceolate or orbicular. The leaves can be sessile or with a long petiole-like portion usually with an enlarged base.

Capitula and phyllaries — The length and width of full-flowering and fruiting capitula were examined from herbarium samples. Length of capitulum was measured from the base of the longest innermost phyllary to the apex (Appendix 4). Phyllaries are always herbaceous, usually with a scarious margin; the width of the margin varies depending on the species. Small black spiny appendages occur on the apex of phyllaries only in members of Scorzonera subg. Podospermum (Fig. 4A).

Achenes — Achenes are sometimes ribbed and the ribbing depth varies ranging from subterete to sulcate. The ribs are either smooth (Scorzonera subg. Podospermum; Fig. 2A–J) or with tuberculate, lamellate or verrucose sculptures (S. subg. Pseudopodospermum; Fig. 2M–T). Species in S. subg. Pseudopodospermum always have glabrous achenes, however in Podospermum they can be glabrous or hairy (Fig. 2). The achene features are often not fully expressed in the innermost achenes of a capitulum; therefore, we only examine the outermost achenes in this study.

Fig. 3.

Macro photographs of achenes of species within Scorzonera subg. Podospermum and S. subg. Pseudopodospermum. – Scale bar lengths are given in parentheses after figure letters. – Voucher locality, collection date, collector(s) and number, and herbarium code for each sample are given in parentheses after species names. – A (2 mm) and B (1 mm): S. armeniaca (Iran, Azerbaijan, 36 km from Ahar to Tabriz, alt. 1554 m, 18 Jun 2015, Mirtadzadini 2239, MIR). – C (2 mm) and D (1 mm): S. grossheimii (Iran, Gorgan, Almeh, alt. 1500–1800 m, 8–10 Jun 1975, Rechinger 53108, B). – E (5 mm) and F (1 mm): S. luristanica (Iran, Kermanshah, between Quriqala and Paweh, 34°57′28.9″N, 46°26′46.5″E, alt. 1246 m, Mirtadzadini & al. 2213, MIR). – G (2 mm) and H (1 mm): S. meshhedensis (Iran, Kerman to Bam road, Golbaf, near Abolfazl mosque, 14 Apr 2016, Samareh 2244, MIR). – I (2 mm) and J (1 mm): S. meyeri (Iran, Khorassan, SW of Bojnurd, Salook mt., 11 Aug 1994, Zangooei & al. 24493, FUMH). – K (2 mm) and L (1 mm): S. ovata (Iran, Baluchistan, NE of Bazman, Siah Band mt. range, 28 Apr 2017, Mirtadzadini 2322, MIR). – M (5 mm) and N (2 mm): S. mucida (Iran, Kerman, Deh Bala, Bordbar 3000, MIR). – O (2 mm) and P (2 mm): S. mollis subsp. mollis (Greece, Kilkis, E of Polykastro 41°00′21″N, 22°38′12″E, 21 Apr 2006, Willing 153 107, B). – Q (5 mm) and R (2 mm): S. semicana (Turkey, Mardin, 5 km E of Mardin, 1100 m, 25 May 1957, Davis & Hedge D.28603, W). – S (2 mm) and T (2 mm): S. szowitzii (Iran, East Azerbaijan, N of Tabriz, Eynali mountain, 10 Jun 2013, Ebrahimi 2989, MIR). – U (5 mm) and V (2 mm): S. tunicata (Iran, Khorassan, 32 km from Birjand to Qa'en, alt. 1991 m, 7 May 2015, Mirtadzadini 2158, MIR). – W (5 mm) and X (2 mm): S. turkeviczii (Iran, 7 km NE of Karaj toward Tschalus, after Sarv-e Dar village, 18 May 2016, Mirtadzadini 2160, MIR). – Macro photographs produced using a stereomicroscope (Olympus SZX16) equipped with DP72 (a 12.5 megapixel cooled digital colour camera) at the Botanic Garden and Botanical Museum Berlin.

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Fig. 4.

Photographs of representatives of Scorzonera subg. Podospermum in the field. For each image the locality and date of the photograph are given, and where applicable voucher data are given (collector and number, herbarium code). – A: black corniculate appendages on phyllaries (see voucher under E); B: swollen carpopodium on achenes (see voucher under D); C: S. armeniaca, NW Iran, Tabriz, Varzeqan, 5 Jun 2017; D: S. persepolitana, Iran, Esfahan, near Delijan on clay hill, 20 May 2010, Mirtadzadini 2218, MIR; E: S. meshhedensis, Iran, Kerman, Golbaf, 14 Apr 2016, Mirtadzadini 2244, MIR; F: S. meyeri, Iran, Zanjan to Abbar, May 2017. – Photographs by M. Mirtadzadini (A, B, D), A. Ebrahimi (C, F; Tehran university, Tehran, Iran), M. Samareh (E; Shahid Bahonar University of Kerman, Kerman, Iran).

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Fig. 5.

Photographs of representatives of Scorzonera subg. Pseudopodospermum in the field. For each image the locality and date of the photograph are given. – A: S. raddeana, Iran, Kerman, Sirch, 22 Apr 2015; B: S. phaeopappa, Iran, Kordestan, Baneh, May 2019 (B1: habit; B2: inflorescence); C: S. calyculata, N Iran, Gilan, Lowshan, May 2016 (C1: habit; C2: inflorescence); D: S. ovata, SE Iran, Baluchistan, between Iranshahr and Sarbaz; E: S. paradoxa, Iran, Fars, Eqlid, Apr 2007; F: S. mucida, Iran, Kerman, Mahan, May 2019 (F1: habit; F2: inflorescence); G: S. mucida, Iran, Kerman, Kuhbanan, Jun 2017. – All photographs by M. Mirtadzadini.

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Carpopodium — The carpopodium refers to the basal prolongation of the achene wall forming a hollow tube-like sterile foot, which may be swollen or not in comparison to the fertile portion (Mukherjee & Nordenstam 2004). Species within Scorzonera subg. Podospermum almost always have a conspicuous carpopodium (Fig. 2A–H). In contrast, within S. subg. Pseudopodospermum, the carpopodium may be absent (e.g. S. calyculata [Fig. 2S, T], S. ovata, S. papposa [Fig. 2M, N] and S. paradoxa), or inconspicuous to conspicuous (Fig. 2O–R; Fig. 3K, L). The size and presence of the carpopodium is important for interspecific delimitation but not informative at intersubgeneric level.

Pappus — Within Scorzonera subg. Podospermum and S. subg. Pseudopodospermum, the setaceous pappus is typically persistent, but in two cases (S. meshhedensis and S. songorica) the bristles can be easily detached (S. songorica in Fig. 2J). Pappus bristles are entirely plumose in S. ovata (Fig. 3K, L) and S. papposa (Fig. 2M), in contrast to pappus bristles that are plumose in the proximal part and naked or scabrous at the distal part for all other species in both subgenera (Table 2; Fig. 2; Fig. 3). The pappus bristles on a single achene can be of equal or unequal lengths. Some species have only five bristles that are conspicuously longer and darker than the others (e.g. S. phaeopappa; Fig. 2O).

Key to species of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum in Iran

1. Leaves entire (but at least some lobed or pinnately divided in S. calyculata); phyllaries without a corniculate projection; achene surface ridged, muricate, tuberculate, verrucose or rugulose, with or without longitudinal ribs S. subg. Pseudopodospermum

– Leaves pinnatifid to pinnatisect; phyllaries always with a corniculate projection; achene surface always smooth with longitudinal ribs S. subg. Podospermum

Scorzonera subg. Pseudopodospermum

1. Leaves pinnatifid to pinnatisect, or rarely entire but with at least one leaf lobed; achene surface verrucose 1. S. calyculata

– Leaves all entire; achene surface not verrucose 2

2. Radical leaves lanceolate or linear; achenes terete, mostly with a hollow swollen carpopodium at base 3

– Radical leaves elliptic or oblong-elliptic; achenes angulate, always without a hollow swollen carpopodium at base 9

3. Plants 20–40(–60) cm tall; stems branched up to apex, with well-developed cauline leaves 4

– Plants (2–)5–15(–20) cm tall, reaching maximum height in fruit; stems mostly branched and leafy only in lower part, sometimes with one or two reduced leaves reaching apex, without well-developed cauline leaves 5

4. Radical leaves 1.5–2.7(–3) cm wide; outer phyllaries in fruit 1–1.2 cm wide; ligules entirely violet 2. S. phaeopappa

– Radical leaves 0.4–1.2(–2) cm wide; outer phyllaries in fruit 0.4–0.7 cm wide; ligules yellow, sometimes with red or purple stripes 3. S. syriaca

5. Capitula with 9–12 florets, fruiting capitula narrowly cylindric, 0.5–0.6 cm in diam. at base 4. S. szowitzii

– Capitula with 14–24 florets, fruiting capitula broadly cylindric, 0.8–2 cm in diam. at base 6

6. Achenes with a conspicuously swollen carpopodium; pappus with five bristles that are longer and darker than rest 5. S. turkeviczii

– Achenes with an inconspicuous carpopodium; pappus bristles of more or less equal lengths 7

7. Flowering stems erect, thickened especially just below fruit; leaves 1–3(–5) mm wide, margin almost flat 6. S. raddeana

– Flowering stems ascending or flexible, not thickened in fruit; leaves 0.4–0.8(–1.2) cm wide, margin undulate 8

8. Outer phyllaries in fruiting capitula 8–10 mm wide, often with purple scarious margin; achenes creamy white, glabrous 7. S. tunicata

– Outer phyllaries in fruiting capitula 5–7 mm wide, with white scarious margin; achenes almost dark brown, with farinose hairs 8. S. mucida

9. Plant (2–)3–5 cm tall, stems ascending or flexible; leaves green-violet 9. S. paradoxa

– Plant 10–15(–20) cm tall, stems erect; leaves green or yellow-green 10

10. Florets yellow, sometimes with violet veins 10. S. ovata

– Florets completely violet 11. S. papposa

Scorzonera subg. Podospermum

1. Alpine plants, caespitose, always with branched woody caudex; stems 1–8(–10) cm long, rarely with cauline leaves 2

– Plants of lower and middle altitudinal zones, predominately caulescent, rarely subcaespitose, with or without a branched woody caudex; stems 10–40(–80) cm long, always with cauline leaves 3

2. Plants cushion-forming; stems 1–3(–4) cm long; phyllaries 8–10 mm long at flowering; achenes 6–7 mm long 12. S. radicosa

– Plants not cushion-forming; stems 5–10(–15) cm long; phyllaries 15–18 mm long at flowering; achenes 9–10 mm long 13. S. meyeri

3. Radical leaves entire to pinnatisect, phyllaries (6–)8–10 cm long at full flowering, pappus easily detachable on touching 4

– Radical leaves always pinnately divided; phyllaries (10–)12–20 mm long at full flowering; pappus persistent on touching 5

4. Halophyte, perennial herbs, 5–12 cm high; leaf margin yellow, cartilaginous dentate 14. S. meshhedensis

– Hygrophyte, biennial herbs, 15–40 cm high; leaf margin not yellow, entire 15. S. songorica

5. Biennial; fully developed florets less than 1.5 times as long as phyllaries; carpopodium 3–5 mm long, one third to one half of achene length 16. S. laciniata

– Perennial; fully developed florets 1.5–2 times as long as phyllaries; carpopodium 2–3 mm long, one fifth to one third of achene length 6

6. Achenes glabrous 7

– Achenes hairy 9

7. Plants 40–80 cm tall; radical leaves 14–22 cm long 17. S. luristanica

– Plants 8–25 cm tall; radical leaves 6–12 cm long 8

8. Carpopodium 3–4 mm long, 3–4 mm wide, about one third of achene length 18. S. cana

– Carpopodium <3 mm long, <3 mm wide, about one fourth of achene length 19. S. grossheimii

9. Radical leaves mostly pinnatifid, rarely pinnatisect with leaf rachis 4–8 mm wide; outer achenes sulcate, angulate 20. S. kandavanica

– Radical leaves always pinnatisect with leaf rachis 1–3 mm wide, outer achenes subterete, not angulate 10

10. Plants subscapigerous, 10–15 cm tall; outer achenes as long as inner ones, pappus about as long as achenes 21. S. armeniaca

– Plants caulescent, 20–45 cm tall; outer achenes shorter and thicker than inner ones, pappus about two times as long as achenes 22. S. persepolitana

Scorzonera subg. Pseudopodospermum (Lipsch. & Krasch.) Lipsch. in Komarov, Fl. URSS 29: 48. 1964 ≡ Scorzonera sect. Pseudopodospermum Lipsch. & Krasch. in Lipschitz, Fragm. Monogr. Scorzonera 1: 70. 1935 ≡ Pseudopodospermum (Lipsch. & Krasch.) Kuth., Kavk. Predst. Scorzonerineae: 85. 1978. – Type: Scorzonera mollis M. Bieb.

Diagnosis — Members of Scorzonera subg. Pseudopodospermum can be identified by the following combination of characters: tuberous root, entire leaves (except S. calyculata with pinnatifid to pinnatisect leaves), phyllaries without corniculate projections at the apex, and glabrous achenes with their sculptured (muricate, tuberculate, verrucose or denticulate) surfaces even with or without carpopodia. See comparison with S. subg. Podospermum under the diagnosis for S. subg. Podospermum below.

1. Scorzonera calyculata Boiss., Diagn. Pl. Orient., ser. 1, 11: 42. 1849. – Syntypes: Iran, Tehran, in collibus occidentalibus Syach Palas ad radices mt. Damavand, 21 Mar 1843, Kotschy 341-a (P00720135 [image!]), Kotschy 324 (P00720136 [image!]).

DiagnosisScorzonera calyculata can be distinguished from other species of S. subg. Pseudopodospermum in Iran based on a combination of the presence of pinnatifid leaves, ligules that are mostly yellow, but the ligule base and entire tube are black-purple (Fig. 5C2), and verrucose achene surfaces without a carpopodium.

Distribution — Armenia, Iran (north, northwest, west, central, south) and Iraq.

Notes — Leaf shape within Scorzonera calyculata varies from undivided to pinnatisect in different populations or even in one individual (Fig. 5C). Achenes are sometimes with a swollen part due to insect galls. This species is morphologically similar to the following species, which do not occur in Iran: S. incisa DC., S. lacera Boiss. & Balansa and S. violacea D. F. Chamb. Based on Lipschitz (1935), the floret colour is a diagnostic character to distinguish S. calyculata. Individuals with entirely violet florets correspond to S. incisa, S. lacera and S. violacea whereas those with florets that are a combination of yellow and black-purple correspond to S. calyculata. The morphological differences between S. calyculata, S. incisa, S. lacera and S. violacea were not sufficiently resolved in Lipschitz (1935) and Chamberlain (1975). Further molecular and morphological studies are required to examine the delimitation of these species.

2. Scorzonera phaeopappa (Boiss.) Boiss., Fl. Orient. 3: 764. 1875 ≡ Podospermum phaeopappum Boiss., Diagn. Pl. Orient., ser. 1, 7: 5. 1846. – Syntypes: Turkey, Kurdistan, inter Diarbekir et Mardin, 10 Jun 1841, Kotschy 237.251 (K000797177 [image!], K000797178 [image!], W0009727!, W0033701!).

DiagnosisScorzonera phaeopappa can be distinguished by its entirely violet florets based on our observations of live plants and herbarium specimens (Fig. 5B), which is in agreement with previous literature (Boissier 1875; Coşkunçelebı & al. 2015).

Distribution — Iran (northwest, west, central), Iraq, Palestine, Saudi Arabia, Syria and Turkey.

Notes — In contrast with our study, Rechinger (1977) described this species with both yellow florets and entirely violet florets. Therefore, it is possible that individuals with yellow florets, which may be Scorzonera syriaca or S. turkeviczii, could be erroneously determined as S. phaeopappa.

3. Scorzonera syriaca Boiss. & Blanche, Diagn. Pl. Orient., ser. 2, 3: 93. 1856 ≡ Scorzonera mollis var. longi-folia Boiss., Fl. Orient. 3: 762. 1875. – Holotype: Syria, in rupestribus Libani inter Scanderouna et Jumalie prope Saida, 19 Mar 1953, C. I. Blanche (G00780148 [image!]; isotype: W0209864!).

DiagnosisScorzonera syriaca can be identified by the following combination of characters: branched stems from base to middle, the presence of cauline leaves on the stem up to the apex, yellow florets and achenes with a conspicuous carpopodium.

Distribution — Iran (northwest, west, central, east, south), Iraq, Lebanon, Oman, Palestine, Saudi Arabia, Sinai, Syria and Turkey.

4. Scorzonera szowitzii DC., Prodr. 7: 117. 1838 ≡ Scorzonera mollis subsp. szowitzii (DC.) D. F. Chamb. in Notes Roy. Bot. Gard. Edinburgh 33: 433. 1975 ≡ Pseudopodospermum szowitzii (DC.) Kuth., Kavk. Predst. Scorzonerinae: 92. 1978. – Holotype: Iran, Azerbaijan, in collibus argillosis salsis circa Deliman et Distr. Khoi, 4 May 1828, Szowitz s.n. (G00498242 [image!]; isotype: LE01051867 [image!]).

= Scorzonera mollis var. leptophylla DC., Prodr. 7: 122. 1838, syn. nov.Scorzonera leptophylla (DC.) Krasch. & Lipsch. in Lipschitz, Fragm. Monogr. Scorzonera 1: 78. 1935 ≡ Pseudopodospermum leptophyllum (DC.) Kuth., Kavk. Predst. Scorzonerinae: 88. 1978. – Holotype: Iran, Azerbaijan, Deliman in collibus argillosis, 4 Apr 1828, Szowitz 48 (LE01053003 [image!]).

= Scorzonera stenocephala Boiss., Diagn. Pl. Orient., ser. 1, 7: 6. 1846, syn. nov.Scorzonera mollis var. stenocephala (Boiss.) Boiss., Fl. Orient. 3: 762. 1875. – Syntypes: Iran, Fars, in alpe Kuh-Delu, 11 Jun 1842, Kotschy 481 (FI006753 [image!], G00301816 [image!], G00301837 [image!], K000797182 [image!], MO-149527 [image!], W0051305 [image!]).

DescriptionHerb perennial, 3–12 cm tall at flowering, 6–12(–15) cm tall at fruiting. Root thickened into tuber, placed in deep part of soil, or near soil surface below root collar; root collar covered with remnants of leaf sheaths. Stems scape-like, one to seven (sometimes <10), more or less tomentose, becoming glabrescent, slightly bent, leafy mainly in lower part, sometimes with one to three reduced cauline leaves. Leaves narrowly linear, 1–3(–6) mm wide, glaucous or green, pubescent or farinose when young, later becoming glabrous, bent, usually folded lengthwise, less often flat, with plane or undulate margins. Capitula narrow cylindric; phyllaries pubescent, becoming glabrescent; outer phyllaries ovate-lanceolate, obtuse, 0.3–0.4 cm wide at flowering, 0.5–0.6 mm wide at fruiting; inner phyllaries linear-lanceolate, usually acuminate, 1.5–1.8 (–2) cm long at flowering, 2.5–3.5(–4) cm long at fruiting, 3–4 times longer than outer phyllaries. Ligulate florets yellow with violet stripes. Achenes glabrous, narrowly terete, without conspicuous carpopodium, 12–14 mm long, with longitudinal ribs, ribs muricate. Pappus 14–20 mm long, white to greyish, bristles of unequal lengths, plumose proximally, scabrous distally.

DiagnosisScorzonera szowitzii can be distinguished from other species of S. subg. Pseudopodospermum in Iran based on the narrower cylindric fruiting capitula (0.5–0.6 cm in diam. in S. szowitzii compared to 0.8–2.5 cm in others) and fewer florets in flowering capitula (9–12 florets in S. szowitzii compared to 14–28 in others).

Distribution — Armenia, Azerbaijan, Iran (north, northeast, northwest, west, southwest, central), Palestine, Syria and Turkey.

Notes — Specimens from different localities across the distribution of Scorzonera leptophylla, S. stenocephala and S. szowitzii, including Armenia, Iran, Palestine, Syria and Turkey, were examined in herbaria and in the field (in Iran). According to Flora iranica (Rechinger 1977) and Flora of Iran (Safavi 2013), individuals of S. leptophylla, S. stenocephala and S. szowitzii can be differentiated from one another by leaf width, undulate or entire leaf margins and density of hairs of the indumentum. Our field and herbarium observations showed, however, that these characters were very variable, even within the same population, and overlap between species. By comparing the original descriptions of S. leptophylla, S. stenocephala and S. szowitzii (Boissier 1846; Lipschitz 1935), we noted that they also overlap considerably. Lipschitz (1935) also commented on the similarities between S. leptophylla and S. szowitzii, and he differentiated them by the more undulate leaf margin and the tuber located near the surface for individuals of S. leptophylla in contrast to the plane leaf margin and deeper position of the tuber in individuals of S. szowitzii. Based on our observations, these characters are in fact very plastic in nature. Therefore, we conclude that S. leptophylla and S. stenocephala are conspecific with S. szowitzii and they are synonymized here. The characters are poorly represented on the holotype of S. szowitzii at G (G00498242), but an isotype at LE (LE01051867) shows all relevant characteristics for its delimitation.

5. Scorzonera turkeviczii Krasch. & Lipsch. in Lipschitz, Fragm. Monogr. Scorzonera 1: 83. 1935 ≡ Pseudopodospermum turkeviczii (Krasch. & Lipsch.) Kuth., Kavk. Predst. Scorzonerinae: 98. 1978. – Holotype: Turkey, Anatolia boreo-orientalis, Kars. Kagisman, in declivibus argillosis, Turkevicz 65 (LE01053004 [image!]).

DiagnosisScorzonera turkeviczii is similar to S. phaeopappa in Iran in the presence of a swollen carpopodium on the achenes and a pappus with five conspicuous scabrous bristles, which are longer than the rest (Table 2; Fig. 3W). However, the two species differ according to the width of the fruiting capitula (1.2–1.5 cm in S. turkeviczii vs. 1.5–2 cm in S. phaeopappa), basal leaf width (0.4–1.2 cm in S. turkeviczii vs. 1.5–2.7 cm in S. phaeopappa; see Appendix 4) and floret colour (yellow with red or purple stripes in S. turkeviczii vs. completely violet in S. phaeopappa).

Distribution — Iran (north, northwest, southwest, west), Iraq, Palestine, Russia (northern Caucasus) and Turkey.

Notes — In Flora of Turkey (Chamberlain 1975), Scorzonera turkeviczii was considered a synonym of S. semicana. Chamberlain (1975) considered S. semicana an Irano-Turanian element that varies markedly in the length of stem, width and shape of leaves; its morphological characteristics overlap with those of S. turkeviczii. However, in Flora iranica (Rechinger 1977) and the Flora of Iran (Safavi 2013), only S. turkeviczii (not S. semicana) was included in the treatment of Scorzonera. Therefore, there are inconsistencies between Floras from different countries. More field and herbarium observations, as well as molecular and morphological studies including samples from both species across the distribution range, are needed in order to compare populations of the species from Iran and Turkey and to clarify species delimitations. We did not include S. semicana in this study because its occurrence in Iran has not been reported, with the exception of Flora of Turkey (Chamberlain 1975).

6. Scorzonera raddeana C. Winkl. in Trudy Imp. S.-Peterburgsk. Bot. Sada 11: 150. 1889. – Syntypes: Turcomania, Inter Chodscha Kala et Bami, May 1886, Radde 402 (LE00050804 [image!], LE00050805 [image!]).

= Scorzonera turcomanica Krasch. & Lipsch. in Lipschitz, Fragm. Monogr. Scorzonera 1: 80. 1935. – Holotype: Turcomania, Kopet Dagh mountains, Vannovskoje-Czuly, 18 Apr 1912, Lipsky s.n. (LE [image!]).

= Scorzonera afghana Rech. f. in Österr. Bot. Z. 97: 264. 1950. – Holotype: Afghanistan, Bandar-e Amir, 30 Jun 1940, Codrington s.n. (BM000996291 [image!]).

DiagnosisScorzonera raddeana is morphologically similar to S. mucida and S. tunicata. See diagnoses of all three species under S. mucida below.

Distribution — Afghanistan, Iran (northeast, east, southeast, central), Pakistan, Tajikistan and Turkmenistan.

NotesScorzonera raddeana (Fig. 5A) is morphologically very variable (Appendix 4) and we observe geographic structuring of the morphological variation. The populations from eastern Iran are similar to the holotype of this species, which was collected in Turkmenistan to the northeast of Iran. Individuals from the eastern range of S. raddeana have linear basal leaves 1–3(–5) mm wide with a bent apex and an entire margin, few or no cauline leaves, and fruiting capitula 2–2.5 cm long and 1.5–2 cm wide. In contrast, individuals in southwestern and central Iran have wider leaves (5–8 mm wide) and wider and longer fruiting capitula (3.5–4[–4.5] cm long and 2.5–3[–4] cm wide) compared to individuals in the eastern populations. However, individuals across the distribution of this species are similar in achene and pappus features, they all have yellow florets with violet or red stripes, muricate achenes without a conspicuous swollen carpopodium, and a pappus with bristles of unequal lengths; see further discussion under S. mucida below (Appendix 4; Table 2; Fig. 2Q, R).

7. Scorzonera tunicata Rech. f. & Köie in Biol. Skr. 8(2): 196. 1955. – Holotype: Afghanistan, Farah-Shin Dand, Jija, 1200 m, 12 Apr 1949, Köie 3710 (W19560000506!; isotype: W19560003033 [image!]).

DiagnosisScorzonera tunicata is morphologically similar to S. mucida and S. raddeana. See diagnoses of all three species under S. mucida below.

Distribution — Afghanistan, Iran (east, northeast, southeast) and Pakistan.

Notes — Based on our morphological observations, the height of the holotype of Scorzonera tunicata (c. 20 cm tall) is not typical compared to that of most individuals of this species, which are typically 5–10 cm tall and rarely reach 20 cm tall, in accordance with Rechinger (1977) (Appendix 4).

8. Scorzonera mucida Rech. f. & al. in Österr. Bot. Z. 97: 264. 1950 ≡ Scorzonera mollis var. mucida (Rech. f. & al.) Parsa, Fl. Iran 10: 187. 1980. – Holotype: Iran, Kerman, Inter Kerman et Saidabad (Sirdjan), Inter Mashiz, 2000 m, et jugum Khan-e Sorck, 2580 m, 27 Apr 1948, Rechinger 3052-a (W0004704!).

DiagnosisScorzonera mucida (Fig. 5F, G) is morphologically very similar to S. tunicata, but individuals of the two species can be distinguished from each other by the width of the outer phyllaries (5–7 mm in S. mucida vs. 8–10 mm in S. tunicata; Appendix 4), colour of the phyllary margins (white or pale in S. mucida vs. purple in S. tunicata) and colour and indumentum of the achenes (grey with farinose hairs in S. mucida vs. light cream and glabrous in S. tunicata; see images of achenes in Fig. 3M, N for S. mucida and Fig. 3U, V for S. tunicata). Scorzonera mucida is also morphologically similar to S. raddeana, but S. mucida possesses achenes with a white ring between the pappus and the fertile part that is not present in S. raddeana (see images in Fig. 2R vs. Fig. 3N for S. raddeana and S. mucida, respectively). In S. raddeana, the stems are erect and thickened in the fruiting stage whereas in S. mucida and S. tunicata they are procumbent to ascending and not thickened.

Distribution — Iran (west, central, northeast, southeast).

NotesScorzonera mucida is endemic to Iran, where its geographical distribution overlaps with Iranian populations of the more widespread species S. raddeana and S. tunicata (see above).

9. Scorzonera paradoxa Fisch. & C. A. Mey. ex DC., Prodr. 7: 119. 1838. – Lectotype (designated by Rechinger 1977: 62): Iran, Azerbaijan, Ad lacum Urmia, Szowitz s.n. (G).

DiagnosisScorzonera paradoxa (Fig. 5E) is morphologically very similar to S. ovata; see under diagnosis for S. ovata below.

Distribution — Afghanistan, Iran (northeast, east, southeast, central, south) and Pakistan.

10. Scorzonera ovata Trautv. in Trudy Imp. S.-Peterburgsk. Bot. Sada 1: 275. 1872. – Syntypes: Turkmenistan, near Krasnowodsk, 20 May 1870, Maloma s.n. (LE00050806 [image!], LE00050807 [image!]).

DiagnosisScorzonera ovata (Fig. 5D) is similar to S. paradoxa in having yellow florets with red stripes, but differs from the latter in having 10–20(–30) cm long branched flowering stems and green or green-yellow leaves compared to (2–)5–8 cm long simple flowering stems and violet-green leaves in S. paradoxa.

Distribution — Afghanistan, Iran (northeast, east), Kyrgyzstan, Tajikistan, Turkmenistan and Uzbekistan.

11. Scorzonera papposa DC., Prodr. 7: 119. 1838. – Holotype: Turkey, Gazi Antep, Antab, 1837, Aucher-Eloy 3316 (G00498266 [image!]).

= Scorzonera kurdica Boiss. & Noë in Boissier, Diagn. Pl. Orient., ser. 2, 3: 93. 1856. – Type: Iraq, in subalpinis Persiae in Kurdistania prope Mendeli, Noë s.n. (not traced).

DiagnosisScorzonera papposa differs from S. ovata in floret colour (florets entirely violet in S. papposa vs. entirely yellow or sometimes yellow with red stripes in S. ovata) and pappus characters (pappus with five conspicuous scabrous bristles longer than the rest in S. papposa vs. without five conspicuously longer bristles in S. ovata; Fig. 2M vs. Fig. 3K, L, respectively). Furthermore, they have different geographic distributions in Iran: S. papposa is distributed in western Iran, whereas S. ovata is known only from eastern Iran.

Distribution — Iran (northwest, west, southwest, central), Iraq, Palestine, Saudi Arabia, Sinai, Syria and Turkey.

Notes — We could not locate a type specimen of Scorzonera kurdica for this study, and we therefore follow Rechinger (1977) in treating it as a heterotypic synonym of S. papposa.

Scorzonera subg. Podospermum (DC.) Lipsch., Fragm. Monogr. Scorzonera 1: 7. 1935 ≡ Podospermum DC. in Lamarck & Candolle, Fl. Franç., ed. 3, 4: 61. 1805 ≡ Scorzonera sect. Podospermum (DC.) Benth. & Hook. f., Gen. Pl. 2: 532. 1873. – Type: Scorzonera laciniata L.

Diagnosis — Members of Scorzonera subg. Podospermum can be distinguished from S. subg. Pseudopodospermum by a combination of characters. Species of S. subg. Podospermum have pinnatifid leaves, phyllaries with corniculate projections at the apex (Fig. 4A) and glabrous or sparsely lanate achenes with smooth surfaces and conspicuous carpopodia. In contrast, species of S. subg. Pseudopodospermum do not possess pinnatifid leaves (with the exception of S. calyculata), the phyllaries do not have corniculate projections at the apex, and thr achenes are always glabrous with sculptured surfaces, which may be with or without conspicuous carpopodia.

12. Scorzonera radicosa Boiss., Diagn. Pl. Orient., ser. 1, 11: 43. 1849 ≡ Scorzonera cana var. radicosa (Boiss.) D. F. Chamb. in Notes Roy. Bot. Gard. Edinburgh 33: 433. 1975. – Syntypes: Iran, Mazandaran, in glareosis alpium Hasartschal in partibus occidentalibus montis Elbours, 3000 m, 12 Aug 1843, Kotschy 492 (FI006751 [image!], G00418597 [image!], G00418598 [image!], G00780179 [image!], K000797190 [image!], MO-149526 [image!], P00720073 [image!], P00720074 [image!], US00119832 [image!], W0009728!).

DiagnosisScorzonera radicosa can be distinguished from other species in Scorzonera subg. Podospermum by being an alpine cushion-forming perennial, growing at high altitudes (>2500 m), with a branched thickened woody caudex. It has scapose flowering stems up to 3 cm long with only basal simple to pinnatisect leaves.

Distribution — Iran (north, northwest, central, northeast), Iraq and Turkey.

13. Scorzonera meyeri (K. Koch) Lipsch. in Karjagin, Fl. Azerbaijan 8: 518. 1961 ≡ Podospermum meyeri K. Koch in Linnaea 23: 659. 1851 ≡ Podospermum canum var. glabratum DC., Prodr. 7: 111. 1838. – Syntypes: ad Guriel Persiae, Szowitz s.n. (G00473936 [image!], LE01053014 [image!]); in regione alpine Caucasi, 1832, Meyer s.n. (G00473935 [image!]).

DiagnosisScorzonera meyeri (Fig. 4F) is a perennial species of mountainous regions (2000–3000 m). It has a branched caudex, which is covered with remnants of old basal leaves, and scapose flowering stems (5–20 cm long) with basal and cauline simple to pinnatisect leaves. It can be distinguished from S. radicosa by not having the cushion form characteristic of that species.

Distribution — Armenia, Azerbaijan, Georgia, Iran (north, northwest, northeast, central), Russia (northern Caucasus) and Turkey.

14. Scorzonera meshhedensis (Rech. f.) Rech. f., Fl. Iran. 122: 25. 1977 ≡ Podospermum meshhedense Rech. f. in Ann. Naturhist. Mus. Wien 55: 289. 1944. – Holotype: Iran, Khorassan, inter Mashhad et Torbat-e Heydariyeh, in salsis l.d. Sahahtari, 10–11 Jul 1937, Rechinger 1504 (W0011955!; isotype: US00119831 [image!]).

DiagnosisScorzonera meshhedensis is morphologically similar to S. songorica; see the diagnosis under S. songorica for a comparison of these two species.

Distribution — Afghanistan and Iran (northwest, northeast, east, west, central).

15. Scorzonera songorica (Kar. & Kir.) Lipsch. & Vassilcz. in Bot. Mater. Gerb. Bot. Inst. Komarova Akad. Nauk S.S.S.R. 22: 301. 1963 ≡ Podospermum laciniatum var. songoricum Kar. & Kir. in Bull. Soc. Imp. Naturalistes Moscou 15: 396. 1842 ≡ Podospermum songoricum (Kar. & Kir.) Tzvelev, Rast. Tsentral. Azii 14b: 104. 2008. – Syntypes: in arenosis Songariae ad fluv. Lepsa circa radicem M. Alatau, 1841, Karelin & Kirilov 1672 (G390183 [image!], G390223 [image!], LE00050800 [image!], LE00050801 [image!], LE00050802 [image!], LE00050803 [image!]).

DiagnosisScorzonera songorica (Fig. 4E) is morphologically close to S. meshhedensis but a number of characters can be used to distinguish them. Scorzonera meshhedensis is perennial with a plant height of 5–10 cm and leaf margins cartilaginous dentate; in contrast, S. songorica is biennial with a plant height of 15–40 cm and leaf margins not cartilaginous dentate. Scorzonera songorica is hygrophytic, often growing in disturbed areas of fields and gardens, whereas S. meshhedensis is halophytic.

Distribution — Afghanistan, Iran (northeast, southeast, east, central), Kazakhstan, Kyrgyzstan, Tajikistan, Turkmenistan and Uzbekistan.

16. Scorzonera laciniata L., Sp. Pl. 2: 791. 1753 ≡ Podospermum laciniatum (L.) DC. in Lamarck & Candolle, Fl. Franç., ed. 3, 4: 62. 1805. – Lectotype (designated by Alavi 1983: 363): Herb. Linn. No. 947.8 (LINN [image!]).

DiagnosisScorzonera laciniata is similar to S. songorica, but it can be distinguished from the latter species by leaf and pappus characters. In individuals of S. laciniata, all leaves are pinnatifid, in contrast to individuals of S. songorica, which can have both pinnatifid and simple leaves. The pappus of S. songorica can be easily detached by touch but is persistent in S. laciniata.

Distribution — Widespread in Africa, Asia and Europe (Kilian & al. 2009+).

17. Scorzonera luristanica Rech. f. in Anz. Österr. Akad. Wiss., Math.-Naturwiss. Kl. 88: 266. 1951 ≡ Scorzonera laciniata var. luristanica (Rech. f.) Parsa, Fl. Iran 10: 184. 1980. – Holotype: Iran, Luristan, Durud, 1670 m, 21 May 1940, Köelz 15621 (W0003543!; isotype: US00119831 [image!]).

DiagnosisScorzonera luristanica is morphologically similar to S. laciniata, but they differ from each other in the following morphological characters: S. luristanica is perennial with a branched caudex, the outer achenes are sulcate and the length of the carpopodium is one fifth to one fourth of the achene length. In contrast, S. laciniata is biennial without a branched caudex, the outer achenes are subterete and the length of carpopodium is one third to half of the achene length (Fig. 3E, F; Appendix 4).

Distribution — Iran (northwest, west, southwest) and Iraq.

18. Scorzonera cana (C. A. Mey.) O. Hoffm. in Engler & Prantl, Nat. Pflanzenfam. IV(5): 365. 1893 ≡ Podospermum canum C. A. Mey., Verz. Pfl. Casp. Meer.: 62. 1831. – Syntypes: Azerbaijan, in collibus prope Baku, Meyer s.n. (LE01042946 [image!], LE01042947 [image!]).

DiagnosisScorzonera cana is morphologically similar to S. grossheimii; see the diagnosis under S. grossheimii for a comparison of these two species.

Distribution — Armenia, Azerbaijan, Cyprus, Georgia, Iran (northwest, west, central), Iraq, Palestine, Russia (northern Caucasus), Syria, Turkey and widespread in Europe (Kilian & al. 2009+).

NotesScorzonera cana is a perennial species with high morphological variation within and between populations, in particular in plant height (8–25 cm) and indumentum (canescent to glabrous). Individuals of this species can be distinguished from S. meyeri based on the capitula length (10–15 mm in S. cana vs. 15–18 mm in S. meyeri; Appendix 4).

19. Scorzonera grossheimii Lipsch. & Vassilcz. in Komarov, Fl. URSS 29: 718. 1964 ≡ Podospermum grossheimii (Lipsch. & Vassilcz.) Kuth., Kavk. Predst. Scorzonerinae: 117. 1978. – Holotype: Azerbaijan, Talish, in declivibus glareosis montis Sibirdu, 9 Jul 1931, N. Schipzinsky 733 (LE01053017 [image!]).

DiagnosisScorzonera grossheimii is a perennial species that is morphologically similar to S. cana. However, these two species can be distinguished based on their carpopodium (<3 mm long, one fifth to one fourth of achene length in S. grossheimii vs. 3–4 mm long, about one third of achene length in S. cana; Fig. 3C, D vs. Fig. 2A, B) and leaves (both simple and pinnatisect in S. grossheimii vs. only pinnatisect in S. cana; Appendix 4).

Distribution — Azerbaijan and Iran (northwest, west, central).

20. Scorzonera kandavanica Rech. f., Fl. Iran. 122: 30. 1977. – Holoype: Iran, Mazandaran, in declivibus borealibus jugi Kandavan, 2400 m, 21 Jun 1974, Rechinger 48310 (W0001082!; isotypes: B-10-0097174!, E00385284 [image!], G00301821 [image!], GZU000272963 [image!], K000797262 [image!], M0030724 [image!], MA496672 [image!], MO-277012 [image!]).

DiagnosisScorzonera kandavanica is morphologically similar to S. armeniaca and S. persepolitana; see the diagnosis under S. persepolitana for the distinguishing characters of these three species.

Distribution — Iran (north, northwest).

Notes — Different populations of this species vary in lamina indumentum from densely tomentose to glabrous.

21. Scorzonera armeniaca (Boiss. & A. Huet) Boiss., Fl. Orient. 3: 760. 1875 ≡ Podospermum armeniacum Boiss. & A. Huet in Boissier, Diagn. Pl. Orient., ser. 2, 3: 92. 1856. – Holotype: Armenia, prope Kochaponar, inter Baibout et Erzeroum, May 1853, Pavillon s.n. (G00418595 [image!]; isotypes: K000797186 [image!], P00720133 [image!]).

DiagnosisScorzonera armeniaca (Fig. 4C) is a subscapigerous perennial species with a branched or undivided caudex. It is similar to S. cana and S. meyeri in vegetative characters, but S. armeniaca has lanate achenes, whereas S. cana and S. meyeri have glabrous achenes (Table 2). Scorzonera armeniaca is also similar to S. kandavanica and S. persepolitana; see under S. persepolitana for a comparison.

Distribution — Iran (north, northwest), Armenia, Azerbaijan and Turkey.

22. Scorzonera persepolitana Boiss., Fl. Orient. 3: 760. 1875 ≡ Podospermum eriospermum Boiss., Diagn. Pl. Orient., ser. 1, 7: 5. 1846 [non Scorzonera erio-sperma Gouan, Ill. Observ. Bot.: 52. 1773]. – Syntypes: Iran, in rupestribus et in arenosis apricis pr. Ruinas u. Persepolis, 21 Apr 1842, Kotschy 275 (G00390186, G00390187, G00780184, JE00012061!, K000797187 [image!], K000797188 [image!], K000797189 [image!], L.3671120 [image!], W29556!, W29557!, WAG0004210 [image!], WAG0004211 [image!]).

= Podospermum canum var. murdabadense Rech. f. in Ann. Naturhist. Mus. Wien 55: 289. 1944. – Holotype: Iran, montes Elburz, in ditione oppidi Keredj, in montibus Helkedar ad Mardabad, 1300 m, 15 Jun 1937, Rechinger 1054 (W0011943!).

DiagnosisScorzonera persepolitana (Fig. 4D), S. armeniaca and S. kandavanica are morphologically similar in possessing lanate achenes (Fig. 2G, H). Scorzonera armeniaca can, however be distinguished from those species because the inner and outer achenes have similar lengths and widths. In contrast, in S. kandavanica and S. persepolitana, the inner achenes are thinner and longer than the outer achenes (see key above and measurements in Appendix 4). Scorzonera kandavanica and S. persepolitana can be distinguished based on the width of the mid-rachis on the leaves, which is wider in S. kandavanica (4–9 mm) compared to S. persepolitana (1–3 mm) (Appendix 4). Furthermore, based on our morphological observations, S. persepolitana leaves have an accumulation of white lanate hairs at the apex of the segments; this character was not present in any individuals of S. kandavanica examined in this study.

Scorzonera persepolitana is also similar to S. luristanica, but differs in the presence of lanate achenes in contrast to glabrous achenes in S. luristanica. Scorzonera luristanica does not have the accumulation of white lanate hairs at the apex of the leaf segments that is characteristic of S. persepolitana. Scorzonera persepolitana varies in the width of the lateral segments of the pinnatisect leaves (1–5 mm) and the glabrous to tomentose indumentum of the plants.

Distribution — Iran (west, southwest, central).

Acknowledgements

This paper is part of the PhD thesis of Elham Hatami; funding for lab work and nrITS sequencing was supported by the Iranian National Science Foundation (INSF). We are grateful to the herbarium curators and staff at B, FMUH, HSHU, IRAN, JE and W. Visits to the herbaria JE and W were supported by the Research Group Asterales (BGBM). We are grateful to Fereshteh Alifarsangi, Dúban Canal, Targol Chatrenoori, Julia Dietrich, Atefeh Ebrahimi and Nana Silakadze for their help during this study. We also thank Evgeny V. Mavrodiev (Florida Museum of Natural History) and an anonymous reviewer for their comments on an earlier version of this paper. Special thanks are due to Norbert Kilian (Research Group Asterales; BGBM) for valuable comments and suggestions to improve the manuscript and his general support during this study.

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Appendices

Appendices

See the Supplemental Content in the online edition at  https://doi.org/10.3372/wi.50.50105

Appendix 1

Taxon sampling and GenBank accession numbers of examined specimens included in nuclear ribosomal Internal Transcribed Spacer phylogeny of the present study. Data are arranged in the following order: taxon name in bold (in alphabetical order); voucher data (country, locality, collecting date, collector[s], collecting number, herbarium code, accession number).

Appendix 2

Selected specimens examined for taxa in the taxonomic treatment of this study. For each specimen, we provide the following voucher information: country, locality, collecting date, collector(s), collecting number, herbarium code.

Appendix 3

Alignment of sequences of the nuclear ribosomal Internal Transcribed Spacer (nrITS) region analysed in this study (phyDE format).

Appendix 4

Summary of morphological features of all taxa in this study. The following characters are included: life cycle, plant height, root, stem, leaves, flowering capitula, fruiting capitula, achenes, pappus. Terminology of vegetative and reproductive traits is according to Allaby (1992) and Beentje (2010).

© 2020 The Authors · This open-access article is distributed under the CC BY 4.0 licence
Elham Hatami, Mansour Mirtadzadini, Firouzeh Bordbar, and Katy E. Jones "Delimitation of Iranian species of Scorzonera subg. Podospermum and S. subg. Pseudopodospermum (Asteraceae, Cichorieae) based on morphological and molecular data," Willdenowia 50(1), 39-63, (6 March 2020). https://doi.org/10.3372/wi.50.50105
Received: 4 July 2019; Accepted: 17 December 2019; Published: 6 March 2020
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