TY - JOUR
AU - Tilney, Patricia, M
AB - Abstract In Apiaceae, embryos of most species have two cotyledons, but some species are consistently monocotylar. Traditionally, the monocotyly has been considered as taxonomically important at the generic level, despite its presumably multiple origins in the family. In this study, a survey of the published literature and our new findings on cotyledon number, embryo and seedling morphology and nrDNA ITS sequence data are presented to provide modern insights into the taxonomic distribution and phylogenetic relationships of monocotylar taxa. A molecular phylogenetic tree representing much of the diversity of monocotylar Apiaceae was produced to re-evaluate the potential implication of monocotyly for systematics and to elucidate its evolutionary significance in the family. Our data document the presence of monocotylar seedlings in 59 species representing 15 genera, in three species and one genus (Postiella) of which monocotylar seedlings are reported for the first time. Analysis of ITS sequence data indicates that monocotyly in Apiaceae has arisen independently in at least seven different lineages encompassing five of 41 major clades of subfamily Apioideae, but not in early-diverging lineages. Parallel evolution has resulted in a remarkable morphological similarity in monocotylar embryo and seedling organization, especially in the proportion of the cotyledon length to the axis of the embryo and the multifunctional cotyledonary tube in the seedling. These features could be considered as adaptations to a geophilic life form, as all monocotylar species are perennial herbs with tuberous underground organs distributed mainly in the Ancient Mediterranean region. The single cotyledon in Apiaceae, as in most other monocotyledonous eudicots, could be interpreted as two united cotyledons (syncotyly), but further developmental studies are needed to test this hypothesis. cotyledon, embryo – evolution, internal transcribed spacer (ITS), molecular phylogeny, morphology, seedling – syncotyly, Umbelliferae INTRODUCTION The large diversity in cotyledon morphology across seed plants is overwhelmingly associated with variation in their development and, more rarely, with their number. The existence of species with monocotylar seedlings typical of almost all monocot groups (the major exception being orchids) has also long been known in some eudicots, in which this unusual type of embryo organization is referred to as pseudomonocotyly. Reviewed by Titova (2000), pseudomonocotyledonous taxa can exhibit various degrees of reduction of one of the cotyledons, and when it is entirely absent the embryo is characteristic of the so-called ‘monocotyledonous dicotyledons’ (Haccius, 1952). This phenomenon has received attention focused on addressing the general question of the origin of monocotyly in angiosperms (e.g. Hofmeister, 1861; Hegelmaier, 1878; Sargant, 1903; Kudryashov, 1964). At present, c. 80 species of ‘monocotyledonous’ dicotyledons are recognized, representing 24 genera and eight families. They all are eudicots and include members of Papaveraceae and Ranunculaceae (Ranunculales; in the basal grade), Celastraceae (Celastrales; rosids) and Portulacaceae (Caryophyllales), Primulaceae (Ericales), Lentibulariaceae (Lamiales), Asteraceae (Asterales), and Apiaceae (Apiales) (superasterids) (Weisse, 1930; Titova, 2000). Increased knowledge of the taxonomic distribution, morphology and phylogeny has raised interest in the systematic and evolutionary significance of monocotyly in eudicots. This paper focuses on Apiaceae, a family of special interest with respect to the cotyledon evolution. According to reviews by Irmisch (1854), Géneau de Lamarlière (1893), Weisse (1930), Haccius (1952), Haines & Lye (1979) and others, Apiaceae include the greatest number (56) of examples of monocotyly among eudicots. With > 460 genera and 3000 species and an almost cosmopolitan distribution (Pimenov & Leonov, 1993; Plunkett et al., 2019), Apiaceae have distinctive inflorescences and fruits, but there is a mosaic distribution of some important character states, making generic delimitation difficult, depending on which characters are given greater importance (Crowden, Harborne & Heywood, 1969). In many cases, only minute morphological differences (usually of the fruit) help to determine the generic placement of species. Attempts have been made to use unique or rare characteristics for taxonomic purposes, and the monocotyledonous embryo is one such character. Monocotyly in Apiaceae was first reported by Treviranus & Treviranus (1821) and Bernhardi (1832) in the widely distributed European species Bunium bulbocastanum L. Since then, monocotyledonous Apiaceae have received attention from other botanists studying their embryology, seedling anatomy and morphology (including life form) for systematic purposes. Monocotyly in Apiaceae has been hypothesized to be a generic character and, as such, to be valuable in complexes of closely related taxa (Drude, 1898; Wolff, 1927; Vasilchenko, 1941; Haccius, 1952; Engstrand, 1973). Nevertheless, considering the tribal affiliation of monocotyledonous genera in the most comprehensive classification of the family proposed by Drude (1898), Haccius (1952) hypothesized that the monocotyledonous embryo could have independently evolved more than once among Apiaceae. Further evidence of homoplasy in cotyledon evolution relates to the seedling modifications in monocotyledonous species that could be environmentally determined by a geophilic life form. During the last three decades, molecular studies have led to major changes, both in the classification of Apiaceae and their relationships to allied families (Plunkett et al., 2004; Downie et al., 2010; Magee et al., 2010). As the tribal placement on the molecular phylogenetic tree of Apiaceae has more or less stabilized, available molecular data provide a framework in which to examine relationships of the taxa with monocotylar embryos. Recent attempts to investigate patterns in cotyledon number variation have been made in Bunium L. and its allies (Degtjareva et al., 2009, 2013; Zakharova et al., 2016). Molecular data corroborate the morphology-based hypothesis of Haccius (1952), suggesting that monocotyly in Apiaceae has arisen several times. Moreover, monocotyledonous Apiaceae are shown to be homoplasious even at lower taxonomic levels. New monocotylar taxa from Apiaceae continue to be described (Petrova, Kljuykov & Zakharova, 2016), and many aspects of their relationships require further investigation. Here, we provide our own new findings relating to cotyledon number, embryo morphology and nrDNA ITS sequences, and attempt to summarize data from previous studies to provide an updated synthesis on the embryo organization, taxonomy and geographical and ecological distribution of monocotyledonous Apiaceae. We illustrate the current phylogenetic hypothesis for each genus in which monocotyledonous species occur, and we re-evaluate the reliability of monocotyly for taxonomic and systematic considerations. Finally, we discuss the origin of the single cotyledon, and evolutionary significance of monocotyly in Apiaceae and angiosperms as a whole. MATERIAL AND METHODS In the study of cotyledon number, 15 species of Apiaceae-Apioideae were examined (Table 1). In ten of these the cotyledon number was previously unknown [Bunium pinnatifolium Kljuykov, Korshinskia olgae Lipsky, Krasnovia longiloba (Kar. & Kir.) Popov ex Schischk., Meeboldia achilleifolia (DC.) P.K.Mukh. & Constance, Postiella capillifolia (Post) Kljuykov, Scaligeria halophila (Rech.f.) Rech.f., Sinocarum cruciatum (Franch.) H.Wolff ex F.T.Pu, Sinocarum wolffianum (Fedde ex H.Wolff) P.K.Mukh. & Constance, Stefanoffia daucoides H.Wolff, Tongoloa elata H.Wolff]. For the five remaining species [Bunium hermonis (Post) Kljuykov, Bunium petraeum Ten., Horstrissea dolinicola Greuter, Gerstb. & Egli, Kozlovia paleacea Lipsky, Stefanoffia aurea (Boiss.) Pimenov & Kljuykov], new counts were made for comparison with previous reports. For the observation of the cotyledons, embryos were extracted from mature fruits of herbarium specimens and examined under a light microscope. Before embryo extraction, the fruits were kept for 3 days in a mixture of equal parts of glycerin, ethyl alcohol and water. Three to five fruit samples were studied per species. Table 1. Overview of the studied species of Apiaceae Species . Voucher information . Morphology (cotyledon number) . GenBank number (nrDNA ITS) . Bunium hermonis (Post) Kljuykov Turkey, Kazanci, Ermenek Region, 14 viii 2008, Pimenov & Kljuykov 74 (MW) 1 MK309860 Bunium petraeum Ten. Italia, Abruzio, 19 viii 2014, Kljuykov et al. 46 (MW) 1 - Italy, Abruzzo, Central Apennines, Monte Focalone, Contis 36447 (APP) - MK309861 Bunium pinnatifolium Kljuykov Turkey, Izmir, Mariamane, 15 viii 1996, Pimenov & Kljuykov (MW) 1 - Conopodium glaberrimum (Desf.) Engstrand (2) [= Balansaea glaberrima (Desf.) Lange], Algeria, 3 vi 1951, 1701 (W) - MK309869 Geocaryum bornmuelleri (H.Wolff) Engstrand Greece, Thasos, Theologos, 31 v 1891, Halácsy s.n. (W) - MK309863 Geocaryum creticum (Boiss. & Heldr.) Engstrand Crete, 11 vii 1987, (W) - MK309865 Geocaryum cynapioides (Guss.) Engstrand [= Biasolettia balcanica Velen.] Serbia, in silvis pr. Brezovica, distr. Vranye, vi 1903, Bierbach s.n. (LE) - MK309868 Geocaryum parnassicum (Boiss. & Heldr.) Engstrand Greece, Pindos Mts, Lakmos, 13 vii 1978, Krendl s.n. (W) - MK309867 Geocaryum peloponesiacum Engstrand Greece, 7536 (W) - MK309864 Geocaryum pumilum (Sm.) Nyman Greece, Peloponnese, prov. Achaia, Panachaikon, 20 v 1880, Krendl s.n. (W) - MK309866 Geocaryum tuberosum (W.D.J.Koch) Engstrand Albania, Baldecci 20 (W) - MK309862 Horstrissea dolinicola Greuter, Gerstb. & Egli Greece, Crete, 7 ix 1995, Risse 1938 (B) 1 MK309870 Korshinskia olgae (Regel & Schmalh.) Lipsky Kyrgyzstan, Turkestan Ridge, Lajljak River, 09 ix 2015. Kljuykov & Ukrainskaja s.n. (MW) 2 - Kozlovia paleaceae (Regel & Schmalh.) Lipsky Uzbekistan, Zeravshan Ridge, Kitab reservat, 20 vii 2010, Pimenov & Kljuykov s.n. (MW) 1 - Krasnovia longiloba (Kar. & Kir.) Popov ex Schischk. Kazakhstan, Tarbagatai Ridge, Urdzhar, 24 ix 1979, Kljuykov s.n. (MW) 2 - Meeboldia achilleifolia (DC.) P.K.Mukh. & Constance Nepal, Lantang National Park, 31 x 1999, Pimenov & Kljuykov 28 (MW) 2 - Postiella capillifolia (Post) Kljuykov Turkey, Amani, Hessan Beyley, 10 ix 1884, Post 105 (G) 1 - Scaligeria halophila (Rech.f.) Rech.f. Greece, Cyclades, Makares, 5 vi 1958, Runemark & Snogerup 10384 (LD) 1 - Sinocarum bellum (C.B.Clarke) Pimenov & Kljuykov West Bengal [India], 14–15 x 1972, Skvortzov & Proskurjakova (MHA) - MK309872 Sinocarum cruciatum (Franch.) H.Wolff China, Sichuan, Somohe River, 16 ix 1998, Pimenov & Kljuykov 188 (MW) 2 - Sinocarum wolffianum (H.Wolff) P.K.Mukh. & Constance India, Sikkim, Yumthang, 16 x 2003, Pimenov & Kljuykov 62 (MW) 1 - Nepal, 17 ix 1981, Farille 81–696 (G) - MK309871 Stefanoffia aurea (Boiss.) Pimenov & Kljuykov Turkey, E Uludağ, 2 viii 2008, Pimenov & Kljuykov 25 (MW) 1 MK309859 Stefanoffia daucoides H.Wolff Bulgaria, Rodopi, Hjing Garvanica, 10 ix 1987, Kyzmanov s.n. (SOM) 1 - Tongoloa elata H.Wolff China, Sichuan, Moiqu River, 15 ix 1998, Pimenov & Kljuykov 171 (MW) 2 - Species . Voucher information . Morphology (cotyledon number) . GenBank number (nrDNA ITS) . Bunium hermonis (Post) Kljuykov Turkey, Kazanci, Ermenek Region, 14 viii 2008, Pimenov & Kljuykov 74 (MW) 1 MK309860 Bunium petraeum Ten. Italia, Abruzio, 19 viii 2014, Kljuykov et al. 46 (MW) 1 - Italy, Abruzzo, Central Apennines, Monte Focalone, Contis 36447 (APP) - MK309861 Bunium pinnatifolium Kljuykov Turkey, Izmir, Mariamane, 15 viii 1996, Pimenov & Kljuykov (MW) 1 - Conopodium glaberrimum (Desf.) Engstrand (2) [= Balansaea glaberrima (Desf.) Lange], Algeria, 3 vi 1951, 1701 (W) - MK309869 Geocaryum bornmuelleri (H.Wolff) Engstrand Greece, Thasos, Theologos, 31 v 1891, Halácsy s.n. (W) - MK309863 Geocaryum creticum (Boiss. & Heldr.) Engstrand Crete, 11 vii 1987, (W) - MK309865 Geocaryum cynapioides (Guss.) Engstrand [= Biasolettia balcanica Velen.] Serbia, in silvis pr. Brezovica, distr. Vranye, vi 1903, Bierbach s.n. (LE) - MK309868 Geocaryum parnassicum (Boiss. & Heldr.) Engstrand Greece, Pindos Mts, Lakmos, 13 vii 1978, Krendl s.n. (W) - MK309867 Geocaryum peloponesiacum Engstrand Greece, 7536 (W) - MK309864 Geocaryum pumilum (Sm.) Nyman Greece, Peloponnese, prov. Achaia, Panachaikon, 20 v 1880, Krendl s.n. (W) - MK309866 Geocaryum tuberosum (W.D.J.Koch) Engstrand Albania, Baldecci 20 (W) - MK309862 Horstrissea dolinicola Greuter, Gerstb. & Egli Greece, Crete, 7 ix 1995, Risse 1938 (B) 1 MK309870 Korshinskia olgae (Regel & Schmalh.) Lipsky Kyrgyzstan, Turkestan Ridge, Lajljak River, 09 ix 2015. Kljuykov & Ukrainskaja s.n. (MW) 2 - Kozlovia paleaceae (Regel & Schmalh.) Lipsky Uzbekistan, Zeravshan Ridge, Kitab reservat, 20 vii 2010, Pimenov & Kljuykov s.n. (MW) 1 - Krasnovia longiloba (Kar. & Kir.) Popov ex Schischk. Kazakhstan, Tarbagatai Ridge, Urdzhar, 24 ix 1979, Kljuykov s.n. (MW) 2 - Meeboldia achilleifolia (DC.) P.K.Mukh. & Constance Nepal, Lantang National Park, 31 x 1999, Pimenov & Kljuykov 28 (MW) 2 - Postiella capillifolia (Post) Kljuykov Turkey, Amani, Hessan Beyley, 10 ix 1884, Post 105 (G) 1 - Scaligeria halophila (Rech.f.) Rech.f. Greece, Cyclades, Makares, 5 vi 1958, Runemark & Snogerup 10384 (LD) 1 - Sinocarum bellum (C.B.Clarke) Pimenov & Kljuykov West Bengal [India], 14–15 x 1972, Skvortzov & Proskurjakova (MHA) - MK309872 Sinocarum cruciatum (Franch.) H.Wolff China, Sichuan, Somohe River, 16 ix 1998, Pimenov & Kljuykov 188 (MW) 2 - Sinocarum wolffianum (H.Wolff) P.K.Mukh. & Constance India, Sikkim, Yumthang, 16 x 2003, Pimenov & Kljuykov 62 (MW) 1 - Nepal, 17 ix 1981, Farille 81–696 (G) - MK309871 Stefanoffia aurea (Boiss.) Pimenov & Kljuykov Turkey, E Uludağ, 2 viii 2008, Pimenov & Kljuykov 25 (MW) 1 MK309859 Stefanoffia daucoides H.Wolff Bulgaria, Rodopi, Hjing Garvanica, 10 ix 1987, Kyzmanov s.n. (SOM) 1 - Tongoloa elata H.Wolff China, Sichuan, Moiqu River, 15 ix 1998, Pimenov & Kljuykov 171 (MW) 2 - Open in new tab Table 1. Overview of the studied species of Apiaceae Species . Voucher information . Morphology (cotyledon number) . GenBank number (nrDNA ITS) . Bunium hermonis (Post) Kljuykov Turkey, Kazanci, Ermenek Region, 14 viii 2008, Pimenov & Kljuykov 74 (MW) 1 MK309860 Bunium petraeum Ten. Italia, Abruzio, 19 viii 2014, Kljuykov et al. 46 (MW) 1 - Italy, Abruzzo, Central Apennines, Monte Focalone, Contis 36447 (APP) - MK309861 Bunium pinnatifolium Kljuykov Turkey, Izmir, Mariamane, 15 viii 1996, Pimenov & Kljuykov (MW) 1 - Conopodium glaberrimum (Desf.) Engstrand (2) [= Balansaea glaberrima (Desf.) Lange], Algeria, 3 vi 1951, 1701 (W) - MK309869 Geocaryum bornmuelleri (H.Wolff) Engstrand Greece, Thasos, Theologos, 31 v 1891, Halácsy s.n. (W) - MK309863 Geocaryum creticum (Boiss. & Heldr.) Engstrand Crete, 11 vii 1987, (W) - MK309865 Geocaryum cynapioides (Guss.) Engstrand [= Biasolettia balcanica Velen.] Serbia, in silvis pr. Brezovica, distr. Vranye, vi 1903, Bierbach s.n. (LE) - MK309868 Geocaryum parnassicum (Boiss. & Heldr.) Engstrand Greece, Pindos Mts, Lakmos, 13 vii 1978, Krendl s.n. (W) - MK309867 Geocaryum peloponesiacum Engstrand Greece, 7536 (W) - MK309864 Geocaryum pumilum (Sm.) Nyman Greece, Peloponnese, prov. Achaia, Panachaikon, 20 v 1880, Krendl s.n. (W) - MK309866 Geocaryum tuberosum (W.D.J.Koch) Engstrand Albania, Baldecci 20 (W) - MK309862 Horstrissea dolinicola Greuter, Gerstb. & Egli Greece, Crete, 7 ix 1995, Risse 1938 (B) 1 MK309870 Korshinskia olgae (Regel & Schmalh.) Lipsky Kyrgyzstan, Turkestan Ridge, Lajljak River, 09 ix 2015. Kljuykov & Ukrainskaja s.n. (MW) 2 - Kozlovia paleaceae (Regel & Schmalh.) Lipsky Uzbekistan, Zeravshan Ridge, Kitab reservat, 20 vii 2010, Pimenov & Kljuykov s.n. (MW) 1 - Krasnovia longiloba (Kar. & Kir.) Popov ex Schischk. Kazakhstan, Tarbagatai Ridge, Urdzhar, 24 ix 1979, Kljuykov s.n. (MW) 2 - Meeboldia achilleifolia (DC.) P.K.Mukh. & Constance Nepal, Lantang National Park, 31 x 1999, Pimenov & Kljuykov 28 (MW) 2 - Postiella capillifolia (Post) Kljuykov Turkey, Amani, Hessan Beyley, 10 ix 1884, Post 105 (G) 1 - Scaligeria halophila (Rech.f.) Rech.f. Greece, Cyclades, Makares, 5 vi 1958, Runemark & Snogerup 10384 (LD) 1 - Sinocarum bellum (C.B.Clarke) Pimenov & Kljuykov West Bengal [India], 14–15 x 1972, Skvortzov & Proskurjakova (MHA) - MK309872 Sinocarum cruciatum (Franch.) H.Wolff China, Sichuan, Somohe River, 16 ix 1998, Pimenov & Kljuykov 188 (MW) 2 - Sinocarum wolffianum (H.Wolff) P.K.Mukh. & Constance India, Sikkim, Yumthang, 16 x 2003, Pimenov & Kljuykov 62 (MW) 1 - Nepal, 17 ix 1981, Farille 81–696 (G) - MK309871 Stefanoffia aurea (Boiss.) Pimenov & Kljuykov Turkey, E Uludağ, 2 viii 2008, Pimenov & Kljuykov 25 (MW) 1 MK309859 Stefanoffia daucoides H.Wolff Bulgaria, Rodopi, Hjing Garvanica, 10 ix 1987, Kyzmanov s.n. (SOM) 1 - Tongoloa elata H.Wolff China, Sichuan, Moiqu River, 15 ix 1998, Pimenov & Kljuykov 171 (MW) 2 - Species . Voucher information . Morphology (cotyledon number) . GenBank number (nrDNA ITS) . Bunium hermonis (Post) Kljuykov Turkey, Kazanci, Ermenek Region, 14 viii 2008, Pimenov & Kljuykov 74 (MW) 1 MK309860 Bunium petraeum Ten. Italia, Abruzio, 19 viii 2014, Kljuykov et al. 46 (MW) 1 - Italy, Abruzzo, Central Apennines, Monte Focalone, Contis 36447 (APP) - MK309861 Bunium pinnatifolium Kljuykov Turkey, Izmir, Mariamane, 15 viii 1996, Pimenov & Kljuykov (MW) 1 - Conopodium glaberrimum (Desf.) Engstrand (2) [= Balansaea glaberrima (Desf.) Lange], Algeria, 3 vi 1951, 1701 (W) - MK309869 Geocaryum bornmuelleri (H.Wolff) Engstrand Greece, Thasos, Theologos, 31 v 1891, Halácsy s.n. (W) - MK309863 Geocaryum creticum (Boiss. & Heldr.) Engstrand Crete, 11 vii 1987, (W) - MK309865 Geocaryum cynapioides (Guss.) Engstrand [= Biasolettia balcanica Velen.] Serbia, in silvis pr. Brezovica, distr. Vranye, vi 1903, Bierbach s.n. (LE) - MK309868 Geocaryum parnassicum (Boiss. & Heldr.) Engstrand Greece, Pindos Mts, Lakmos, 13 vii 1978, Krendl s.n. (W) - MK309867 Geocaryum peloponesiacum Engstrand Greece, 7536 (W) - MK309864 Geocaryum pumilum (Sm.) Nyman Greece, Peloponnese, prov. Achaia, Panachaikon, 20 v 1880, Krendl s.n. (W) - MK309866 Geocaryum tuberosum (W.D.J.Koch) Engstrand Albania, Baldecci 20 (W) - MK309862 Horstrissea dolinicola Greuter, Gerstb. & Egli Greece, Crete, 7 ix 1995, Risse 1938 (B) 1 MK309870 Korshinskia olgae (Regel & Schmalh.) Lipsky Kyrgyzstan, Turkestan Ridge, Lajljak River, 09 ix 2015. Kljuykov & Ukrainskaja s.n. (MW) 2 - Kozlovia paleaceae (Regel & Schmalh.) Lipsky Uzbekistan, Zeravshan Ridge, Kitab reservat, 20 vii 2010, Pimenov & Kljuykov s.n. (MW) 1 - Krasnovia longiloba (Kar. & Kir.) Popov ex Schischk. Kazakhstan, Tarbagatai Ridge, Urdzhar, 24 ix 1979, Kljuykov s.n. (MW) 2 - Meeboldia achilleifolia (DC.) P.K.Mukh. & Constance Nepal, Lantang National Park, 31 x 1999, Pimenov & Kljuykov 28 (MW) 2 - Postiella capillifolia (Post) Kljuykov Turkey, Amani, Hessan Beyley, 10 ix 1884, Post 105 (G) 1 - Scaligeria halophila (Rech.f.) Rech.f. Greece, Cyclades, Makares, 5 vi 1958, Runemark & Snogerup 10384 (LD) 1 - Sinocarum bellum (C.B.Clarke) Pimenov & Kljuykov West Bengal [India], 14–15 x 1972, Skvortzov & Proskurjakova (MHA) - MK309872 Sinocarum cruciatum (Franch.) H.Wolff China, Sichuan, Somohe River, 16 ix 1998, Pimenov & Kljuykov 188 (MW) 2 - Sinocarum wolffianum (H.Wolff) P.K.Mukh. & Constance India, Sikkim, Yumthang, 16 x 2003, Pimenov & Kljuykov 62 (MW) 1 - Nepal, 17 ix 1981, Farille 81–696 (G) - MK309871 Stefanoffia aurea (Boiss.) Pimenov & Kljuykov Turkey, E Uludağ, 2 viii 2008, Pimenov & Kljuykov 25 (MW) 1 MK309859 Stefanoffia daucoides H.Wolff Bulgaria, Rodopi, Hjing Garvanica, 10 ix 1987, Kyzmanov s.n. (SOM) 1 - Tongoloa elata H.Wolff China, Sichuan, Moiqu River, 15 ix 1998, Pimenov & Kljuykov 171 (MW) 2 - Open in new tab To illustrate the different types of cotyledon in monocotylar seedlings, the following species were used: Acronema commutatum H.Wolff [China, Yunnan, 16.10.2010, Sytin et al. (LE)], Bunium microcarpum (Boiss.) Freyn & Sint. (Turkey, Isparta, 05 vii 2007, Pimenov & Kljuykov), Hellenocarum multiflorum (Sm.) H.Wolff (Central Greece, Parnassios, 29 vi 2012, Zakharova & Ukrainskaja no.10) and Scaligeria napiformis (Willd. ex Spreng.) Grande (Greece, Peloponnisos, 05 vii 2012, Zakharova & Ukrainskaja no.48). Seedlings were grown and fixed in 70% ethanol. For molecular phylogenetic analysis, the nuclear ribosomal DNA internal transcribed spacer (nrDNA ITS) region was used. This marker provides the most comprehensive sampling for molecular phylogenetic analyses, and more than one-third of the species of Apiaceae have thus been studied (Banasiak et al., 2013). Representatives from all major clades were included in accordance with available data on the taxonomy and phylogeny of Apiales. Special attention was given to the lineages with monocotylar embryos. In addition to sequences obtained from GenBank, sequences of nuclear ribosomal DNA ITS region were generated for 15 accessions belonging to monocotylar Bunium, Conopodium W.D.J.Koch, Geocaryum Coss., Horstrissea Greuter, Gerstberger & Egli, Sinocarum H.Wolff ex Shan RenHwa & Pu FaTing and Stefanoffia H.Wolff. In total, 198 accessions from 117 genera were examined (Table 1, Appendix 1). Specifically, all monocotylar genera and 40 species were sampled. A species of Sambucus L. (Caprifoliaceae) was used as outgroup based on previous higher-level phylogenetic studies (Tank & Donoghue, 2010). Total DNA was extracted from leaf or fruit material with the NucleoSpin plant isolation kit (Macherey-Nagel, Düren, Germany) following the protocol of the manufacturer. The PCR procedure followed Valiejo-Roman et al. (2002). Amplification products were purified using the DNA Cleanup Mini kit (Evrogen, Moscow, Russia). Direct sequencing was performed using an ABI PRISM 3100 Genetic Analyzer (Applied Biosystems, Foster City, CA, USA) and a BigDye Terminator Cycle Sequencing Ready Reaction kit. GenBank accession numbers and voucher information for investigated taxa are presented in Table 1. The ITS sequences were aligned using MAFFT 7.215 (Katoh & Standley, 2013) and edited using BioEdit 7.2.5 (Hall, 1999). The ITS sequences of Apiales could be more or less unambiguously aligned in the majority of positions. Ambiguous and gap rich positions were excluded from the analysis. To infer phylogenetic relationships, the Bayesian analysis was performed using MrBayes v.3.2.6 (Ronquist et al., 2012) with the GTR+G model of nucleotide substitutions, which was selected by AIC in MrModeltest v.2.3 (Nylander, 2004). Twenty-five million generations were run in two independent analyses, each with four Markov chains. One tree was saved every 1000 generations. The first 50 trees were discarded as burn-in and the remaining trees were used to build a majority-rule consensus tree to obtain the Bayesian posterior probabilities (PP). To evaluate the evolution of cotyledon number, an ancestral state reconstruction was performed in Mesquite v.3.51 (Maddison & Maddison, 2010) using parsimony. The Bayesian 50% majority-rule consensus tree was used. Information about the cotyledon number in taxa of Apiales was obtained from specimen observations and the literature (Irmisch, 1854; Haccius, 1952; Cerceau-Larrival, 1962; Engstrand, 1973; Burtt, 1991; Pimenov & Kljuykov, 2002; Tilney et al., 2009; Kljuykov et al., 2014; Petrova, 2016; Petrova et al., 2016; Zakharova et al., 2016; Zakharova, 2017) and from online resources (Agro Slide Bank; Australian Tropical Rainforest Plants; PlantInvasive-Kruger). Data about cotyledon number for Eleutherospermum cicutarium (M.Bieb.) Boiss., Komarovia anisosperma Korovin, Lomatium nudicaule (Nutt.) J.M.Coult. & Rose, Opopanax hispidus Griseb., Physospermum cornubiense DC., Pleurospermum uralense Hoffm., Smyrniopsis aucheri Boiss. and Sphallerocarpus gracilis (Besser ex Trev.) Koso-Pol., cultivated in the Botanical Garden of the Lomonosov Moscow State University (Russia), were obtained from E.A. Zakharova and T.A. Ostroumova (pers. comm.). RESULTS Morphology The embryos are 0.11–0.96 mm long, differentiated into an axis (radicle and hypocotyl) and have one or two cotyledons (Table 1, Fig. 1). A monocotylar embryo was observed in Bunium pinnatifolium, Postiella capillifolia, Scaligeria halophila and Stefanoffia daucoides and was confirmed for Bunium hermonis, B. petraeum, Horstrissea dolinicola, Kozlovia paleacea and Stefanoffia aurea. The number of cotyledons in the embryos of the additional specimens studied was consistent with previous reports for all five species. Figure 1. Open in new tabDownload slide Embryo morphology of studied species of Apiaceae. A–J, Front views of monocotylar embryos and K–O, side views of dicotylar embryos. A, Bunium hermonis. B, Bunium petraeum. C, Bunium pinnatifolium. D, Horstrissea dolinicola. E, Kozlovia paleaceae. F, Postiella capillifolia. G, Scaligeria halophila. H, Sinocarum wolffianum. I, Stefanoffia aurea. J, Stefanoffia daucoides. K, Korshinskia olgae. L, Krasnovia longiloba. M, Meeboldia achilleifolia. N, Sinocarum cruciatum. O, Tongoloa elata. cot, cotyledon; hol, hollow; hyp, hypocotyl; rad, radicula apex. Scale bars: 0.5 mm (E, K–L) and 0.1 mm (A–D, F–J, M–O). Figure 1. Open in new tabDownload slide Embryo morphology of studied species of Apiaceae. A–J, Front views of monocotylar embryos and K–O, side views of dicotylar embryos. A, Bunium hermonis. B, Bunium petraeum. C, Bunium pinnatifolium. D, Horstrissea dolinicola. E, Kozlovia paleaceae. F, Postiella capillifolia. G, Scaligeria halophila. H, Sinocarum wolffianum. I, Stefanoffia aurea. J, Stefanoffia daucoides. K, Korshinskia olgae. L, Krasnovia longiloba. M, Meeboldia achilleifolia. N, Sinocarum cruciatum. O, Tongoloa elata. cot, cotyledon; hol, hollow; hyp, hypocotyl; rad, radicula apex. Scale bars: 0.5 mm (E, K–L) and 0.1 mm (A–D, F–J, M–O). The cotyledon in monocotylar embryos is spade-like with an entire or bilobed (Scaligeria halophila) apex and concave side. In dicotylar embryos, the cotyledons are ovate and sometimes have slightly acuminate apices (Korshinskia olgae). At the base of single cotyledons, there is a hollow in which the plumule will later develop. In embryos, the plumule is not yet differentiated. In the case of dicotyly, the plumule develops between the two cotyledons. The relative lengths of the cotyledon(s) to the axis in monocotylar and dicotylar embryos differ (Fig. 1). In the former, the cotyledon is three (to five) times longer than the axis whereas in the latter, the cotyledons are of the same length or even shorter than the axis. Illustrations of the morphological structure of seedlings and the shape of cotyledons are provided in Figure 2. Figure 2. Open in new tabDownload slide Сotyledon and seedling types of monocotylar Apiaceae. A, Lanceolate cotyledon of Hellenocarum multiflorum. B, Oblong cotyledon of Bunium microcarpum. C, Leaf-like ternately dissected cotyledon of Acronema commutatum. D, Oval cotyledon bilobed distally of Scaligeria napiformis. E, Seedling of Hellenocarum multiflorum. F, Seedling of Bunium microcarpum. cot, cotyledon. c.tb, cotyledonary tube. f.lf, first leaf. a.r, adventive root. p.r, primary root. tr, tuber. Scale bars: 10 mm. Figure 2. Open in new tabDownload slide Сotyledon and seedling types of monocotylar Apiaceae. A, Lanceolate cotyledon of Hellenocarum multiflorum. B, Oblong cotyledon of Bunium microcarpum. C, Leaf-like ternately dissected cotyledon of Acronema commutatum. D, Oval cotyledon bilobed distally of Scaligeria napiformis. E, Seedling of Hellenocarum multiflorum. F, Seedling of Bunium microcarpum. cot, cotyledon. c.tb, cotyledonary tube. f.lf, first leaf. a.r, adventive root. p.r, primary root. tr, tuber. Scale bars: 10 mm. Phylogenetic analyses Phylogenetic analysis of the concatenated ITS1 and ITS2 data matrix resulted in a tree comprising recognizable clades (Fig. 3). The relationships among several clades differed from those of previous analyses, especially in the poor resolution of higher-level relationships in Apiales and Apiaceae (relationships among subfamilies). These differences related to nodes that were strongly supported in previous studies involving analysis of plastid markers (Plunkett et al., 2004; Magee et al., 2010), and reflected the limitation of ITS data in resolving relationships at higher taxonomic levels (Katz-Downie et al., 1999). Nevertheless, differences concerning nodes in subfamily Apioideae, the main focus of our study, are consistent with the trees presented by Downie et al. (2010) and Banasiak et al. (2013). The phylogenetic placements of newly sequenced accessions were ascertained. The Opopanax clade is expanded to include the monotypic genus Horstrissea, and Stefanoffia aurea is a member of the Pyramidoptereae clade. The additional species of Bunium, Conopodium, Geocaryum and Sinocarum included support the previous circumscriptions of these genera. Figure 3. Open in new tabDownload slide Summary of relationships among monocotylar representatives in the order Apiales as revealed by the Bayesian analysis of nrDNA ITS sequence data. Figure 3. Open in new tabDownload slide Summary of relationships among monocotylar representatives in the order Apiales as revealed by the Bayesian analysis of nrDNA ITS sequence data. Ancestral state reconstructions The maximum parsimony reconstruction of character evolution based on the ITS phylogenetic analysis is presented in Figures 4 and 5. A dicotyledonous embryo represents the ancestral state for Apiaceae. A monocotyledonous embryo seems to have evolved independently at least seven times, arising in Pyramidoptereae, the Opopanax clade, Scandiceae, the Acronema clade and Erigenieae. Six out of the 15 known monocotylar genera are situated in the Pyramidoptereae clade. This clade also includes the greatest number of monocotylar species (22 out of 59). The second largest clade in which monocotylar taxa occur is Scandiceae, with three genera and five species. The remaining monocotylar taxa are placed in two small clades or occupy isolated positions in the tree (e.g. Erigenia Nutt.). Among the monocotylar taxa, 11 genera possess monocotylar seedlings only and the other four contain species with both monocotylar and dicotylar seedlings (see also Tables 2, 3). Table 2. Summary of information about monocotylar Apiaceae. Tribal names are given according to the traditional classification proposed by Pimenov & Leonov (1993). Clade names are given according to the molecular classification proposed by Downie et al. (2010) Clade . Genus . Tribe . Number of species . Number of studied species . Number of monocotylar species . Number of dicotylar species . Acronema clade Acronema Apieae 26 11 11 - Sinocarum Apieae 21 4 3 1 Erigenieae Erigenia Apieae 1 1 1 - Opopanax clade Horstrissea Apieae 1 1 1 - Stefanoffia Apieae 3 2 2 - Pyramidoptereae Astomaea Apieae 1 1 1 - Bunium Apieae 29 22 22 - Elaeosticta Apieae 25 19 1 18 Hellenocarum Apieae 3 2 2 - Neomuretia Apieae 2 2 1 1 Postiella Smyrnieae 1 1 1 - Scaligeria Apieae 4 3 2 1 Scandiceae Conopodium Scandicineae 9 5 5 - Geocaryum Scandicineae 13–15 5 5 - Kozlovia Scandicineae 1 1 1 - Clade . Genus . Tribe . Number of species . Number of studied species . Number of monocotylar species . Number of dicotylar species . Acronema clade Acronema Apieae 26 11 11 - Sinocarum Apieae 21 4 3 1 Erigenieae Erigenia Apieae 1 1 1 - Opopanax clade Horstrissea Apieae 1 1 1 - Stefanoffia Apieae 3 2 2 - Pyramidoptereae Astomaea Apieae 1 1 1 - Bunium Apieae 29 22 22 - Elaeosticta Apieae 25 19 1 18 Hellenocarum Apieae 3 2 2 - Neomuretia Apieae 2 2 1 1 Postiella Smyrnieae 1 1 1 - Scaligeria Apieae 4 3 2 1 Scandiceae Conopodium Scandicineae 9 5 5 - Geocaryum Scandicineae 13–15 5 5 - Kozlovia Scandicineae 1 1 1 - Open in new tab Table 2. Summary of information about monocotylar Apiaceae. Tribal names are given according to the traditional classification proposed by Pimenov & Leonov (1993). Clade names are given according to the molecular classification proposed by Downie et al. (2010) Clade . Genus . Tribe . Number of species . Number of studied species . Number of monocotylar species . Number of dicotylar species . Acronema clade Acronema Apieae 26 11 11 - Sinocarum Apieae 21 4 3 1 Erigenieae Erigenia Apieae 1 1 1 - Opopanax clade Horstrissea Apieae 1 1 1 - Stefanoffia Apieae 3 2 2 - Pyramidoptereae Astomaea Apieae 1 1 1 - Bunium Apieae 29 22 22 - Elaeosticta Apieae 25 19 1 18 Hellenocarum Apieae 3 2 2 - Neomuretia Apieae 2 2 1 1 Postiella Smyrnieae 1 1 1 - Scaligeria Apieae 4 3 2 1 Scandiceae Conopodium Scandicineae 9 5 5 - Geocaryum Scandicineae 13–15 5 5 - Kozlovia Scandicineae 1 1 1 - Clade . Genus . Tribe . Number of species . Number of studied species . Number of monocotylar species . Number of dicotylar species . Acronema clade Acronema Apieae 26 11 11 - Sinocarum Apieae 21 4 3 1 Erigenieae Erigenia Apieae 1 1 1 - Opopanax clade Horstrissea Apieae 1 1 1 - Stefanoffia Apieae 3 2 2 - Pyramidoptereae Astomaea Apieae 1 1 1 - Bunium Apieae 29 22 22 - Elaeosticta Apieae 25 19 1 18 Hellenocarum Apieae 3 2 2 - Neomuretia Apieae 2 2 1 1 Postiella Smyrnieae 1 1 1 - Scaligeria Apieae 4 3 2 1 Scandiceae Conopodium Scandicineae 9 5 5 - Geocaryum Scandicineae 13–15 5 5 - Kozlovia Scandicineae 1 1 1 - Open in new tab Table 3. Information about cotyledon number in the genera of Apiaceae in which monocotylar species occur Species . Cotyledon number . Reference . Acronema astrantiifolium H.Wolff 1 Kljuykov et al. (2014) Acronema chinense H.Wolff 1 Kljuykov et al. (2014) Acronema commutatum H.Wolff 1 Kljuykov et al. (2014) Acronema edosmioides (H.Boissieu) Pimenov & Kljuykov 1 Kljuykov et al. (2014) Acronema forrestii H.Wolff 1 Kljuykov et al. (2014) Acronema hookeri (C.B.Clarke) H.Wolff 1 Kljuykov et al. (2014) Acronema johrianum Babu 1 Kljuykov et al. (2014) Acronema muscicola (Hand.-Mazz.) Hand.-Mazz. 1 Kljuykov et al. (2014) Acronema paniculatum (Franch.) H.Wolff 1 Kljuykov et al. (2014) Acronema tenerum (DC.) Edgew. 1 Kljuykov et al. (2014) Acronema xizangense S.L.Liou & R.H.Shan 1 Kljuykov et al. (2014) Astomaea seselifolia (DC.) Rauschert 1 Haccius (1952; = Astoma seselifolium DC.) Bunium alpinum Waldst. & Kit. 1 Hegelmaier (1878; = Bunium montanum W.D.J.Koch); Géneau de Lamarlière (1893) Bunium aphyllum Jan. ex DC. 1 Kljuykov (1988) Bunium avromanum (Boiss. & Hausskn.) H.Wolff 1 Kljuykov (1988) Bunium bulbocastanum L. 1 Treviranus & Treviranus (1821); Treviranus (1831); Bernhardi (1832); Irmisch [1854; = Carum bulbocastanum (L.) Koch]; Hegelmaier [1875; = Carum bulbocastanum (L.) Koch]; Hegelmaier [1878; = Carum bulbocastanum (L.) Koch]; Géneau de Lamarlière (1893); Schmid (1902); Haccius (1952) Bunium cornigerum (Boiss. & Hausskn.) Drude 1 Kljuykov (1988) Bunium elegans (Fenzl) Freyn 1 Kljuykov (1988) Bunium fallax Freyn 1 Kljuykov (1988) Bunium ferulaceum Sibth. & Sm. 1 Kljuykov (1988) Bunium hermonis (Post) Kljuykov 1 Petrova et al. (2016); Present study Bunium macuca Boiss. 1 Silvestre [1972; = Bunium alpinum Waldst. & Kit. subsp. macuca (Boiss.) P.W. Ball] Bunium mauritanicum (Boiss. & Reut.) Batt. 1 Kljuykov et al. (1988) Bunium microcarpum (Boiss.) Freyn & Sint. 1 Kljuykov (1988) Bunium nothum (C.B.Clarke) P.K.Mukh. 1 Zakharova et al. (2014) Bunium pachypodum P.W.Ball 1 Hegelmaier (1878; = Carum incrassatum Boiss.); Silvestre (1972); Kljuykov (1988) Bunium paucifolium DC. 1 Kljuykov (1988) Bunium pestalozzae Boiss. 1 Kljuykov (1988) Bunium petraeum Ten. 1 Bernhardi (1832); Hegelmaier (1878); Present study Bunium pinnatifolium Kljuykov 1 Present study Bunium rectangulum (Boiss. & Hausskn.) H.Wolff 1 Kljuykov (1988) Bunium scabrellum Korovin 1 Kljuykov (1988) Bunium simplex (C.Koch) Kljuykov 1 Kljuykov (1988) Bunium verruculosum C.C.Townsend. 1 Kljuykov (1988) Conopodium bunioides (Boiss.) Calest. 1 Hegelmaier (1878; = Butinia bunioides Boiss.); Silvestre (1972) Conopodium glaberrimum (Desf.) Engstrand 1 Haccius (1952; = Balansaea fontanesii Boiss. & Reut.) Conopodium majus (Gouan) Loret 1 Géneau de Lamarlière (1893; = Conopodium denudatum W.D.J.Koch); Haccius (1952); Thompson (1988); Silvestre [1972; = Conopodium majus subsp. ramosum sensu Silvestre in Lagascalia 2: 151]; Blandino et al. (2019) Conopodium pyrenaeum (Loisel.) Miégev. 1 Hegelmaier (1878; = Conopodium bourgaei Coss.); Silvestre (1972; = Conopodium bourgaei Coss.) Conopodium subcarneum (Boiss. & Reut.) Boiss. & Reut. 1 Hegelmaier (1878; = Conopodium subcarneum Boiss.) Elaeosticta allioides (Regel & Schmalh.) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta bucharica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta conica Korovin 2 Kljuykov (1980) Elaeosticta ferganensis (Lipsky) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta glaucescens (DC.) Boiss. 2 Haccius [1952, = Scaligeria glaucescens (DC.) Boiss.] Elaeosticta hirtula (Regel & Schmalh.) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta knorringiana (Korovin) Korovin 2 Kljuykov (1980) Elaeosticta korovinii (Bobr. ex Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta lutea (M.Bieb. ex Hoffm.) Kljuykov, Pimenov & V.N.Tikhom.. 2 Kljuykov (1980) Elaeosticta meifolia Fenzl 2 Haccius [1952, = Scaligeria meifolia (Fenzl) Boiss.] Elaeosticta paniculata (Korovin) Kljuykov & Pimenov 2 Kljuykov (1980) Elaeosticta platyphylla (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta polycarpa (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta samarkandica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta transcaspica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta transitoria (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta tschimganica (Korovin) Kljuykov, Pimenov & V.Tikhom. 1 Korovin (1928; = Scaligeria tschimganica Korovin) Elaeosticta ugamica (Korovin) Korovin 2 Kljuykov (1980) Elaeosticta vvedenskyi (Kamelin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Erigenia bulbosa (Michx.) Nutt. 1 Hegelmaier (1878); Holm (1901); Haccius (1952) Geocaryum capillifolium (Guss.) Coss. 1 Hegelmaier (1878; = Conopodium capillifolium Boiss.); Silvestre [1972; = Conopodium capillifolium (Guss.) Boiss.] Geocaryum cynapioides (Guss.) Engstrand 1 Haccius [1952; = Biasolettia congesta (Boiss. & Heldr.) Nyman]; = Biasolettia cynapioides (Guss.) Drude; = Biasolettia balcanica Velen.) Geocaryum macrocarpum (Boiss. & Spruner) Engstrand 1 Haccius [1952; = Biasolettia macrocarpa (Boiss. & Spruner) Nyman] Geocaryum parnassicum (Boiss. & Heldr.) Engstrand 1 Haccius [1952; = Biasolettia parnassica (Boiss. & Heldr.) Nyman] Geocaryum tuberosum (W.D.J.Koch) Engstrand 1 Domin (1909; = Biasolettia tuberosa W.D.J.Koch); Haccius (1952; = Biasolettia tuberosa W.D.J.Koch) Hellenocarum multiflorum (Sm.) H.Wolff 1 Engstrand (1973) Hellenocarum strictum (Griseb.) Kljuykov 1 Zakharova et al. (2016) Horstrissea dolinicola Greuter, Gerstb. & Egli 1 Petrova et al. (2016); Present study Kozlovia paleacea (Regel & Schmalh.) Lipsky 1 Pimenov & Kljuykov (2002) Neomuretia amplifolia (Boiss. & Hausskn. ex Boiss.) Kljuykov, Degtjareva & Zakharova 1 Zakharova et al. (2016) Neomuretia pisidica (Kit Tan) Kljuykov, Degtjareva & Zakharova 2 Zakharova et al. (2016) Postiella capillifolia (Post ex Boiss.) Kljuykov 1 Present study Scaligeria halophila (Rech.f.) Rech.f. 1 Present study Scaligeria moreana Engstrand 2 Petrova et al. (2016) Scaligeria napiformis (Willd. ex Spreng.) Grande 1 Irmisch (1858; = Bunium creticum Urv.); Hegelmaier (1878; = Bunium creticum Urv.); Haccius (1952) Sinocarum bellum (C.B.Clarke) Pimenov & Kljuykov 1 Mukherjee & Constance (1993, = Acronema bella C.B.Clarke) Sinocarum cruciatum (Franch.) H.Wolff 2 Present study Sinocarum sikkimense (P.K.Mukh.) P.K.Mukh. & Constance 1 Mukherjee & Constance (1993) Sinocarum wolffianum (H.Wolff) P.K.Mukh. & Constance 1 Mukherjee & Constance (1993) Stefanoffia aurea (Boiss.) Pimenov & Kljuykov 1 Petrova et al. (2016); Present study Stefanoffia daucoides (Boiss.) H.Wolff 1 Present study Species . Cotyledon number . Reference . Acronema astrantiifolium H.Wolff 1 Kljuykov et al. (2014) Acronema chinense H.Wolff 1 Kljuykov et al. (2014) Acronema commutatum H.Wolff 1 Kljuykov et al. (2014) Acronema edosmioides (H.Boissieu) Pimenov & Kljuykov 1 Kljuykov et al. (2014) Acronema forrestii H.Wolff 1 Kljuykov et al. (2014) Acronema hookeri (C.B.Clarke) H.Wolff 1 Kljuykov et al. (2014) Acronema johrianum Babu 1 Kljuykov et al. (2014) Acronema muscicola (Hand.-Mazz.) Hand.-Mazz. 1 Kljuykov et al. (2014) Acronema paniculatum (Franch.) H.Wolff 1 Kljuykov et al. (2014) Acronema tenerum (DC.) Edgew. 1 Kljuykov et al. (2014) Acronema xizangense S.L.Liou & R.H.Shan 1 Kljuykov et al. (2014) Astomaea seselifolia (DC.) Rauschert 1 Haccius (1952; = Astoma seselifolium DC.) Bunium alpinum Waldst. & Kit. 1 Hegelmaier (1878; = Bunium montanum W.D.J.Koch); Géneau de Lamarlière (1893) Bunium aphyllum Jan. ex DC. 1 Kljuykov (1988) Bunium avromanum (Boiss. & Hausskn.) H.Wolff 1 Kljuykov (1988) Bunium bulbocastanum L. 1 Treviranus & Treviranus (1821); Treviranus (1831); Bernhardi (1832); Irmisch [1854; = Carum bulbocastanum (L.) Koch]; Hegelmaier [1875; = Carum bulbocastanum (L.) Koch]; Hegelmaier [1878; = Carum bulbocastanum (L.) Koch]; Géneau de Lamarlière (1893); Schmid (1902); Haccius (1952) Bunium cornigerum (Boiss. & Hausskn.) Drude 1 Kljuykov (1988) Bunium elegans (Fenzl) Freyn 1 Kljuykov (1988) Bunium fallax Freyn 1 Kljuykov (1988) Bunium ferulaceum Sibth. & Sm. 1 Kljuykov (1988) Bunium hermonis (Post) Kljuykov 1 Petrova et al. (2016); Present study Bunium macuca Boiss. 1 Silvestre [1972; = Bunium alpinum Waldst. & Kit. subsp. macuca (Boiss.) P.W. Ball] Bunium mauritanicum (Boiss. & Reut.) Batt. 1 Kljuykov et al. (1988) Bunium microcarpum (Boiss.) Freyn & Sint. 1 Kljuykov (1988) Bunium nothum (C.B.Clarke) P.K.Mukh. 1 Zakharova et al. (2014) Bunium pachypodum P.W.Ball 1 Hegelmaier (1878; = Carum incrassatum Boiss.); Silvestre (1972); Kljuykov (1988) Bunium paucifolium DC. 1 Kljuykov (1988) Bunium pestalozzae Boiss. 1 Kljuykov (1988) Bunium petraeum Ten. 1 Bernhardi (1832); Hegelmaier (1878); Present study Bunium pinnatifolium Kljuykov 1 Present study Bunium rectangulum (Boiss. & Hausskn.) H.Wolff 1 Kljuykov (1988) Bunium scabrellum Korovin 1 Kljuykov (1988) Bunium simplex (C.Koch) Kljuykov 1 Kljuykov (1988) Bunium verruculosum C.C.Townsend. 1 Kljuykov (1988) Conopodium bunioides (Boiss.) Calest. 1 Hegelmaier (1878; = Butinia bunioides Boiss.); Silvestre (1972) Conopodium glaberrimum (Desf.) Engstrand 1 Haccius (1952; = Balansaea fontanesii Boiss. & Reut.) Conopodium majus (Gouan) Loret 1 Géneau de Lamarlière (1893; = Conopodium denudatum W.D.J.Koch); Haccius (1952); Thompson (1988); Silvestre [1972; = Conopodium majus subsp. ramosum sensu Silvestre in Lagascalia 2: 151]; Blandino et al. (2019) Conopodium pyrenaeum (Loisel.) Miégev. 1 Hegelmaier (1878; = Conopodium bourgaei Coss.); Silvestre (1972; = Conopodium bourgaei Coss.) Conopodium subcarneum (Boiss. & Reut.) Boiss. & Reut. 1 Hegelmaier (1878; = Conopodium subcarneum Boiss.) Elaeosticta allioides (Regel & Schmalh.) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta bucharica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta conica Korovin 2 Kljuykov (1980) Elaeosticta ferganensis (Lipsky) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta glaucescens (DC.) Boiss. 2 Haccius [1952, = Scaligeria glaucescens (DC.) Boiss.] Elaeosticta hirtula (Regel & Schmalh.) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta knorringiana (Korovin) Korovin 2 Kljuykov (1980) Elaeosticta korovinii (Bobr. ex Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta lutea (M.Bieb. ex Hoffm.) Kljuykov, Pimenov & V.N.Tikhom.. 2 Kljuykov (1980) Elaeosticta meifolia Fenzl 2 Haccius [1952, = Scaligeria meifolia (Fenzl) Boiss.] Elaeosticta paniculata (Korovin) Kljuykov & Pimenov 2 Kljuykov (1980) Elaeosticta platyphylla (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta polycarpa (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta samarkandica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta transcaspica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta transitoria (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta tschimganica (Korovin) Kljuykov, Pimenov & V.Tikhom. 1 Korovin (1928; = Scaligeria tschimganica Korovin) Elaeosticta ugamica (Korovin) Korovin 2 Kljuykov (1980) Elaeosticta vvedenskyi (Kamelin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Erigenia bulbosa (Michx.) Nutt. 1 Hegelmaier (1878); Holm (1901); Haccius (1952) Geocaryum capillifolium (Guss.) Coss. 1 Hegelmaier (1878; = Conopodium capillifolium Boiss.); Silvestre [1972; = Conopodium capillifolium (Guss.) Boiss.] Geocaryum cynapioides (Guss.) Engstrand 1 Haccius [1952; = Biasolettia congesta (Boiss. & Heldr.) Nyman]; = Biasolettia cynapioides (Guss.) Drude; = Biasolettia balcanica Velen.) Geocaryum macrocarpum (Boiss. & Spruner) Engstrand 1 Haccius [1952; = Biasolettia macrocarpa (Boiss. & Spruner) Nyman] Geocaryum parnassicum (Boiss. & Heldr.) Engstrand 1 Haccius [1952; = Biasolettia parnassica (Boiss. & Heldr.) Nyman] Geocaryum tuberosum (W.D.J.Koch) Engstrand 1 Domin (1909; = Biasolettia tuberosa W.D.J.Koch); Haccius (1952; = Biasolettia tuberosa W.D.J.Koch) Hellenocarum multiflorum (Sm.) H.Wolff 1 Engstrand (1973) Hellenocarum strictum (Griseb.) Kljuykov 1 Zakharova et al. (2016) Horstrissea dolinicola Greuter, Gerstb. & Egli 1 Petrova et al. (2016); Present study Kozlovia paleacea (Regel & Schmalh.) Lipsky 1 Pimenov & Kljuykov (2002) Neomuretia amplifolia (Boiss. & Hausskn. ex Boiss.) Kljuykov, Degtjareva & Zakharova 1 Zakharova et al. (2016) Neomuretia pisidica (Kit Tan) Kljuykov, Degtjareva & Zakharova 2 Zakharova et al. (2016) Postiella capillifolia (Post ex Boiss.) Kljuykov 1 Present study Scaligeria halophila (Rech.f.) Rech.f. 1 Present study Scaligeria moreana Engstrand 2 Petrova et al. (2016) Scaligeria napiformis (Willd. ex Spreng.) Grande 1 Irmisch (1858; = Bunium creticum Urv.); Hegelmaier (1878; = Bunium creticum Urv.); Haccius (1952) Sinocarum bellum (C.B.Clarke) Pimenov & Kljuykov 1 Mukherjee & Constance (1993, = Acronema bella C.B.Clarke) Sinocarum cruciatum (Franch.) H.Wolff 2 Present study Sinocarum sikkimense (P.K.Mukh.) P.K.Mukh. & Constance 1 Mukherjee & Constance (1993) Sinocarum wolffianum (H.Wolff) P.K.Mukh. & Constance 1 Mukherjee & Constance (1993) Stefanoffia aurea (Boiss.) Pimenov & Kljuykov 1 Petrova et al. (2016); Present study Stefanoffia daucoides (Boiss.) H.Wolff 1 Present study Open in new tab Table 3. Information about cotyledon number in the genera of Apiaceae in which monocotylar species occur Species . Cotyledon number . Reference . Acronema astrantiifolium H.Wolff 1 Kljuykov et al. (2014) Acronema chinense H.Wolff 1 Kljuykov et al. (2014) Acronema commutatum H.Wolff 1 Kljuykov et al. (2014) Acronema edosmioides (H.Boissieu) Pimenov & Kljuykov 1 Kljuykov et al. (2014) Acronema forrestii H.Wolff 1 Kljuykov et al. (2014) Acronema hookeri (C.B.Clarke) H.Wolff 1 Kljuykov et al. (2014) Acronema johrianum Babu 1 Kljuykov et al. (2014) Acronema muscicola (Hand.-Mazz.) Hand.-Mazz. 1 Kljuykov et al. (2014) Acronema paniculatum (Franch.) H.Wolff 1 Kljuykov et al. (2014) Acronema tenerum (DC.) Edgew. 1 Kljuykov et al. (2014) Acronema xizangense S.L.Liou & R.H.Shan 1 Kljuykov et al. (2014) Astomaea seselifolia (DC.) Rauschert 1 Haccius (1952; = Astoma seselifolium DC.) Bunium alpinum Waldst. & Kit. 1 Hegelmaier (1878; = Bunium montanum W.D.J.Koch); Géneau de Lamarlière (1893) Bunium aphyllum Jan. ex DC. 1 Kljuykov (1988) Bunium avromanum (Boiss. & Hausskn.) H.Wolff 1 Kljuykov (1988) Bunium bulbocastanum L. 1 Treviranus & Treviranus (1821); Treviranus (1831); Bernhardi (1832); Irmisch [1854; = Carum bulbocastanum (L.) Koch]; Hegelmaier [1875; = Carum bulbocastanum (L.) Koch]; Hegelmaier [1878; = Carum bulbocastanum (L.) Koch]; Géneau de Lamarlière (1893); Schmid (1902); Haccius (1952) Bunium cornigerum (Boiss. & Hausskn.) Drude 1 Kljuykov (1988) Bunium elegans (Fenzl) Freyn 1 Kljuykov (1988) Bunium fallax Freyn 1 Kljuykov (1988) Bunium ferulaceum Sibth. & Sm. 1 Kljuykov (1988) Bunium hermonis (Post) Kljuykov 1 Petrova et al. (2016); Present study Bunium macuca Boiss. 1 Silvestre [1972; = Bunium alpinum Waldst. & Kit. subsp. macuca (Boiss.) P.W. Ball] Bunium mauritanicum (Boiss. & Reut.) Batt. 1 Kljuykov et al. (1988) Bunium microcarpum (Boiss.) Freyn & Sint. 1 Kljuykov (1988) Bunium nothum (C.B.Clarke) P.K.Mukh. 1 Zakharova et al. (2014) Bunium pachypodum P.W.Ball 1 Hegelmaier (1878; = Carum incrassatum Boiss.); Silvestre (1972); Kljuykov (1988) Bunium paucifolium DC. 1 Kljuykov (1988) Bunium pestalozzae Boiss. 1 Kljuykov (1988) Bunium petraeum Ten. 1 Bernhardi (1832); Hegelmaier (1878); Present study Bunium pinnatifolium Kljuykov 1 Present study Bunium rectangulum (Boiss. & Hausskn.) H.Wolff 1 Kljuykov (1988) Bunium scabrellum Korovin 1 Kljuykov (1988) Bunium simplex (C.Koch) Kljuykov 1 Kljuykov (1988) Bunium verruculosum C.C.Townsend. 1 Kljuykov (1988) Conopodium bunioides (Boiss.) Calest. 1 Hegelmaier (1878; = Butinia bunioides Boiss.); Silvestre (1972) Conopodium glaberrimum (Desf.) Engstrand 1 Haccius (1952; = Balansaea fontanesii Boiss. & Reut.) Conopodium majus (Gouan) Loret 1 Géneau de Lamarlière (1893; = Conopodium denudatum W.D.J.Koch); Haccius (1952); Thompson (1988); Silvestre [1972; = Conopodium majus subsp. ramosum sensu Silvestre in Lagascalia 2: 151]; Blandino et al. (2019) Conopodium pyrenaeum (Loisel.) Miégev. 1 Hegelmaier (1878; = Conopodium bourgaei Coss.); Silvestre (1972; = Conopodium bourgaei Coss.) Conopodium subcarneum (Boiss. & Reut.) Boiss. & Reut. 1 Hegelmaier (1878; = Conopodium subcarneum Boiss.) Elaeosticta allioides (Regel & Schmalh.) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta bucharica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta conica Korovin 2 Kljuykov (1980) Elaeosticta ferganensis (Lipsky) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta glaucescens (DC.) Boiss. 2 Haccius [1952, = Scaligeria glaucescens (DC.) Boiss.] Elaeosticta hirtula (Regel & Schmalh.) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta knorringiana (Korovin) Korovin 2 Kljuykov (1980) Elaeosticta korovinii (Bobr. ex Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta lutea (M.Bieb. ex Hoffm.) Kljuykov, Pimenov & V.N.Tikhom.. 2 Kljuykov (1980) Elaeosticta meifolia Fenzl 2 Haccius [1952, = Scaligeria meifolia (Fenzl) Boiss.] Elaeosticta paniculata (Korovin) Kljuykov & Pimenov 2 Kljuykov (1980) Elaeosticta platyphylla (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta polycarpa (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta samarkandica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta transcaspica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta transitoria (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta tschimganica (Korovin) Kljuykov, Pimenov & V.Tikhom. 1 Korovin (1928; = Scaligeria tschimganica Korovin) Elaeosticta ugamica (Korovin) Korovin 2 Kljuykov (1980) Elaeosticta vvedenskyi (Kamelin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Erigenia bulbosa (Michx.) Nutt. 1 Hegelmaier (1878); Holm (1901); Haccius (1952) Geocaryum capillifolium (Guss.) Coss. 1 Hegelmaier (1878; = Conopodium capillifolium Boiss.); Silvestre [1972; = Conopodium capillifolium (Guss.) Boiss.] Geocaryum cynapioides (Guss.) Engstrand 1 Haccius [1952; = Biasolettia congesta (Boiss. & Heldr.) Nyman]; = Biasolettia cynapioides (Guss.) Drude; = Biasolettia balcanica Velen.) Geocaryum macrocarpum (Boiss. & Spruner) Engstrand 1 Haccius [1952; = Biasolettia macrocarpa (Boiss. & Spruner) Nyman] Geocaryum parnassicum (Boiss. & Heldr.) Engstrand 1 Haccius [1952; = Biasolettia parnassica (Boiss. & Heldr.) Nyman] Geocaryum tuberosum (W.D.J.Koch) Engstrand 1 Domin (1909; = Biasolettia tuberosa W.D.J.Koch); Haccius (1952; = Biasolettia tuberosa W.D.J.Koch) Hellenocarum multiflorum (Sm.) H.Wolff 1 Engstrand (1973) Hellenocarum strictum (Griseb.) Kljuykov 1 Zakharova et al. (2016) Horstrissea dolinicola Greuter, Gerstb. & Egli 1 Petrova et al. (2016); Present study Kozlovia paleacea (Regel & Schmalh.) Lipsky 1 Pimenov & Kljuykov (2002) Neomuretia amplifolia (Boiss. & Hausskn. ex Boiss.) Kljuykov, Degtjareva & Zakharova 1 Zakharova et al. (2016) Neomuretia pisidica (Kit Tan) Kljuykov, Degtjareva & Zakharova 2 Zakharova et al. (2016) Postiella capillifolia (Post ex Boiss.) Kljuykov 1 Present study Scaligeria halophila (Rech.f.) Rech.f. 1 Present study Scaligeria moreana Engstrand 2 Petrova et al. (2016) Scaligeria napiformis (Willd. ex Spreng.) Grande 1 Irmisch (1858; = Bunium creticum Urv.); Hegelmaier (1878; = Bunium creticum Urv.); Haccius (1952) Sinocarum bellum (C.B.Clarke) Pimenov & Kljuykov 1 Mukherjee & Constance (1993, = Acronema bella C.B.Clarke) Sinocarum cruciatum (Franch.) H.Wolff 2 Present study Sinocarum sikkimense (P.K.Mukh.) P.K.Mukh. & Constance 1 Mukherjee & Constance (1993) Sinocarum wolffianum (H.Wolff) P.K.Mukh. & Constance 1 Mukherjee & Constance (1993) Stefanoffia aurea (Boiss.) Pimenov & Kljuykov 1 Petrova et al. (2016); Present study Stefanoffia daucoides (Boiss.) H.Wolff 1 Present study Species . Cotyledon number . Reference . Acronema astrantiifolium H.Wolff 1 Kljuykov et al. (2014) Acronema chinense H.Wolff 1 Kljuykov et al. (2014) Acronema commutatum H.Wolff 1 Kljuykov et al. (2014) Acronema edosmioides (H.Boissieu) Pimenov & Kljuykov 1 Kljuykov et al. (2014) Acronema forrestii H.Wolff 1 Kljuykov et al. (2014) Acronema hookeri (C.B.Clarke) H.Wolff 1 Kljuykov et al. (2014) Acronema johrianum Babu 1 Kljuykov et al. (2014) Acronema muscicola (Hand.-Mazz.) Hand.-Mazz. 1 Kljuykov et al. (2014) Acronema paniculatum (Franch.) H.Wolff 1 Kljuykov et al. (2014) Acronema tenerum (DC.) Edgew. 1 Kljuykov et al. (2014) Acronema xizangense S.L.Liou & R.H.Shan 1 Kljuykov et al. (2014) Astomaea seselifolia (DC.) Rauschert 1 Haccius (1952; = Astoma seselifolium DC.) Bunium alpinum Waldst. & Kit. 1 Hegelmaier (1878; = Bunium montanum W.D.J.Koch); Géneau de Lamarlière (1893) Bunium aphyllum Jan. ex DC. 1 Kljuykov (1988) Bunium avromanum (Boiss. & Hausskn.) H.Wolff 1 Kljuykov (1988) Bunium bulbocastanum L. 1 Treviranus & Treviranus (1821); Treviranus (1831); Bernhardi (1832); Irmisch [1854; = Carum bulbocastanum (L.) Koch]; Hegelmaier [1875; = Carum bulbocastanum (L.) Koch]; Hegelmaier [1878; = Carum bulbocastanum (L.) Koch]; Géneau de Lamarlière (1893); Schmid (1902); Haccius (1952) Bunium cornigerum (Boiss. & Hausskn.) Drude 1 Kljuykov (1988) Bunium elegans (Fenzl) Freyn 1 Kljuykov (1988) Bunium fallax Freyn 1 Kljuykov (1988) Bunium ferulaceum Sibth. & Sm. 1 Kljuykov (1988) Bunium hermonis (Post) Kljuykov 1 Petrova et al. (2016); Present study Bunium macuca Boiss. 1 Silvestre [1972; = Bunium alpinum Waldst. & Kit. subsp. macuca (Boiss.) P.W. Ball] Bunium mauritanicum (Boiss. & Reut.) Batt. 1 Kljuykov et al. (1988) Bunium microcarpum (Boiss.) Freyn & Sint. 1 Kljuykov (1988) Bunium nothum (C.B.Clarke) P.K.Mukh. 1 Zakharova et al. (2014) Bunium pachypodum P.W.Ball 1 Hegelmaier (1878; = Carum incrassatum Boiss.); Silvestre (1972); Kljuykov (1988) Bunium paucifolium DC. 1 Kljuykov (1988) Bunium pestalozzae Boiss. 1 Kljuykov (1988) Bunium petraeum Ten. 1 Bernhardi (1832); Hegelmaier (1878); Present study Bunium pinnatifolium Kljuykov 1 Present study Bunium rectangulum (Boiss. & Hausskn.) H.Wolff 1 Kljuykov (1988) Bunium scabrellum Korovin 1 Kljuykov (1988) Bunium simplex (C.Koch) Kljuykov 1 Kljuykov (1988) Bunium verruculosum C.C.Townsend. 1 Kljuykov (1988) Conopodium bunioides (Boiss.) Calest. 1 Hegelmaier (1878; = Butinia bunioides Boiss.); Silvestre (1972) Conopodium glaberrimum (Desf.) Engstrand 1 Haccius (1952; = Balansaea fontanesii Boiss. & Reut.) Conopodium majus (Gouan) Loret 1 Géneau de Lamarlière (1893; = Conopodium denudatum W.D.J.Koch); Haccius (1952); Thompson (1988); Silvestre [1972; = Conopodium majus subsp. ramosum sensu Silvestre in Lagascalia 2: 151]; Blandino et al. (2019) Conopodium pyrenaeum (Loisel.) Miégev. 1 Hegelmaier (1878; = Conopodium bourgaei Coss.); Silvestre (1972; = Conopodium bourgaei Coss.) Conopodium subcarneum (Boiss. & Reut.) Boiss. & Reut. 1 Hegelmaier (1878; = Conopodium subcarneum Boiss.) Elaeosticta allioides (Regel & Schmalh.) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta bucharica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta conica Korovin 2 Kljuykov (1980) Elaeosticta ferganensis (Lipsky) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta glaucescens (DC.) Boiss. 2 Haccius [1952, = Scaligeria glaucescens (DC.) Boiss.] Elaeosticta hirtula (Regel & Schmalh.) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta knorringiana (Korovin) Korovin 2 Kljuykov (1980) Elaeosticta korovinii (Bobr. ex Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta lutea (M.Bieb. ex Hoffm.) Kljuykov, Pimenov & V.N.Tikhom.. 2 Kljuykov (1980) Elaeosticta meifolia Fenzl 2 Haccius [1952, = Scaligeria meifolia (Fenzl) Boiss.] Elaeosticta paniculata (Korovin) Kljuykov & Pimenov 2 Kljuykov (1980) Elaeosticta platyphylla (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta polycarpa (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta samarkandica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta transcaspica (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta transitoria (Korovin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Elaeosticta tschimganica (Korovin) Kljuykov, Pimenov & V.Tikhom. 1 Korovin (1928; = Scaligeria tschimganica Korovin) Elaeosticta ugamica (Korovin) Korovin 2 Kljuykov (1980) Elaeosticta vvedenskyi (Kamelin) Kljuykov, Pimenov & V.N.Tikhom. 2 Kljuykov (1980) Erigenia bulbosa (Michx.) Nutt. 1 Hegelmaier (1878); Holm (1901); Haccius (1952) Geocaryum capillifolium (Guss.) Coss. 1 Hegelmaier (1878; = Conopodium capillifolium Boiss.); Silvestre [1972; = Conopodium capillifolium (Guss.) Boiss.] Geocaryum cynapioides (Guss.) Engstrand 1 Haccius [1952; = Biasolettia congesta (Boiss. & Heldr.) Nyman]; = Biasolettia cynapioides (Guss.) Drude; = Biasolettia balcanica Velen.) Geocaryum macrocarpum (Boiss. & Spruner) Engstrand 1 Haccius [1952; = Biasolettia macrocarpa (Boiss. & Spruner) Nyman] Geocaryum parnassicum (Boiss. & Heldr.) Engstrand 1 Haccius [1952; = Biasolettia parnassica (Boiss. & Heldr.) Nyman] Geocaryum tuberosum (W.D.J.Koch) Engstrand 1 Domin (1909; = Biasolettia tuberosa W.D.J.Koch); Haccius (1952; = Biasolettia tuberosa W.D.J.Koch) Hellenocarum multiflorum (Sm.) H.Wolff 1 Engstrand (1973) Hellenocarum strictum (Griseb.) Kljuykov 1 Zakharova et al. (2016) Horstrissea dolinicola Greuter, Gerstb. & Egli 1 Petrova et al. (2016); Present study Kozlovia paleacea (Regel & Schmalh.) Lipsky 1 Pimenov & Kljuykov (2002) Neomuretia amplifolia (Boiss. & Hausskn. ex Boiss.) Kljuykov, Degtjareva & Zakharova 1 Zakharova et al. (2016) Neomuretia pisidica (Kit Tan) Kljuykov, Degtjareva & Zakharova 2 Zakharova et al. (2016) Postiella capillifolia (Post ex Boiss.) Kljuykov 1 Present study Scaligeria halophila (Rech.f.) Rech.f. 1 Present study Scaligeria moreana Engstrand 2 Petrova et al. (2016) Scaligeria napiformis (Willd. ex Spreng.) Grande 1 Irmisch (1858; = Bunium creticum Urv.); Hegelmaier (1878; = Bunium creticum Urv.); Haccius (1952) Sinocarum bellum (C.B.Clarke) Pimenov & Kljuykov 1 Mukherjee & Constance (1993, = Acronema bella C.B.Clarke) Sinocarum cruciatum (Franch.) H.Wolff 2 Present study Sinocarum sikkimense (P.K.Mukh.) P.K.Mukh. & Constance 1 Mukherjee & Constance (1993) Sinocarum wolffianum (H.Wolff) P.K.Mukh. & Constance 1 Mukherjee & Constance (1993) Stefanoffia aurea (Boiss.) Pimenov & Kljuykov 1 Petrova et al. (2016); Present study Stefanoffia daucoides (Boiss.) H.Wolff 1 Present study Open in new tab Figure 4. Open in new tabDownload slide Bayesian tree based on nrDNA ITS sequence data with the reconstruction of ancestral state of cotyledon number using the parsimony approach. Geophilic species are marked with asterisks. Part 1. Figure 4. Open in new tabDownload slide Bayesian tree based on nrDNA ITS sequence data with the reconstruction of ancestral state of cotyledon number using the parsimony approach. Geophilic species are marked with asterisks. Part 1. Figure 5. Open in new tabDownload slide Bayesian tree based on nrDNA ITS sequence data with the reconstruction of ancestral state of cotyledon number using the parsimony approach. Geophilic species are marked with asterisks. Part 2. Figure 5. Open in new tabDownload slide Bayesian tree based on nrDNA ITS sequence data with the reconstruction of ancestral state of cotyledon number using the parsimony approach. Geophilic species are marked with asterisks. Part 2. DISCUSSION Morphology of embryos and seedlings with reference to plant life form and geographical distribution In Apiaceae, the embryo is minute but often well-differentiated into an axis (radicle and hypocotyl) and cotyledons. Some details of embryo structure are similar (the plumule is not differentiated) and most variation in embryos is in cotyledon structure. The cotyledon in monocotylar embryos is spade-like and entire (majority of species: Haccius, 1952; this study), bilobed (Scaligeria DC.: Haccius, 1952; this study) or divided into three segments (Acronema Falc. ex Edgew.: Kljuykov et al., 2014) at the apex. The variation in the shape of the cotyledons in dicotylar embryos is not so great; they are mainly ovate with sometimes a slightly acuminate apex (see, e.g. Korshinskia olgae; Fig. 1). Another important peculiarity regarding the diversity of embryo organization in Apiaceae is the proportion of its components, e.g. the relative length of the cotyledon(s) to the axis (Fig. 1). When the embryos have one cotyledon, then the cotyledon is three (to five) times longer than the axis, but when they have two, the cotyledons are of the same length or even shorter than the hypocotyl and radicle. Similar proportions for mono- and dicotylar embryos have previously been reported (Haccius, 1952; Kljuykov et al., 2014). A different ratio of the length of cotyledons to the axial part is also observed among dicotyledonous species from other genera of Apiaceae that partly depends on the presence or absence of the cotyledonary tube. Thus, Denisova (1961) showed that in a mature embryo of Caropodium platycarpum (Boiss. & Hausskn.) Schischk. (now treated as Grammosciadium platycarpum Boiss. & Hausskn.), the cotyledons (including cotyledonary tube, which is interpreted as a part of cotyledons) are c. 3.5 times longer than the axis, whereas in Angelica decurrens (Ledeb.) B.Fedtsch., the length of the axis is almost equal to the length of the cotyledons. This is due to the peculiarities in the growth of the embryo: in the first case, the dimensions of the axis almost do not change over time and the embryo increases in size mainly due to the intensive growth of the cotyledon laminas and the cotyledonary tube. In Angelica decurrens, the axis and the cotyledons increase almost evenly in size, so that by the end of development they are almost equal to each other. Monocotyly in Apiaceae is associated with a characteristic appearance of the seedlings. The single cotyledon of monocotylar seedlings is usually entire and narrowly linear; such cotyledons are similar in most species (Fig. 2A, B; see also Haccius, 1952; Géneau de Lamarlière, 1893). In Scaligeria napiformis and S. halophila, the cotyledon lamina is ovate and bilobed distally (Fig. 2D). In Acronema, of which 11 out of 25 species were studied, some species were found to have narrowly linear cotyledons (Kljuykov et al., 2014). However, the embryos of the five species reported in this study for the first time exhibit an unusual cotyledon type, one with a deeply dissected lamina (Fig. 2C). It was also discovered that, in the monocotylar A. commutatum (which has a deeply dissected cotyledon), the cotyledon lamina of the seedling is similar to that of the first true leaf of the plant. In dicotylar seedlings of Apiaceae, the variation in shape of the cotyledons is restricted to two main types, recognized by Cerceau-Larrival (1962) as L (long) and R (round). Burtt (1991) pointed out that the rounded cotyledons of Lichtensteinia Cham. & Schltdl. are unusual in that they are toothed. Based on the type of cotyledonary sheath in the seedlings of monocotylar Apiaceae, at least two groups of species can be distinguished: those with a long cotyledonary tube surrounding the plumule, e.g. Bunium hermonis, B. microcarpum (Fig. 2F); and those with cotyledons on a poorly developed open base growing out of the cotyledon node and having a free plumule, e.g. Scaligeria napiformis and species of Hellenocarum H.Wolff (Fig. 2E; see also Petrova et al., 2016). The length of the cotyledonary tube depends on the depth of immersion into the substrate; the lowermost, positively geotropic portion can function as a root, developing root hairs and lateral roots as does the radicle. Monocotyledons with a long cotyledonary tube and related dicotyledons are characterized by the rapid formation of a tuber due to the thickening of the hypocotyl and poor differentiation of the terminal bud. In contrast, in species with an open sheath, the terminal bud is clearly differentiated, the first leaves appear early and the tuber is late in forming. The most noteworthy anatomical feature of monocotylar seedlings is the structure of the cotyledonary tube. It varies from being root-like in the underground part of the tube near the hypocotyl to being petiole-like at the base of the cotyledon lamina (Haccius, 1952; Petrova et al., 2016). Thus, the cotyledonary tube can serve as a root, shoot and leaf. The formation of a long multifunctional cotyledonary tube with a similar anatomical structure has been observed in some other geophilic taxa, notably Podophyllum L. and Anemone L. (both Ranunculales; Haccius, 1953; Barykina, 1971, 1999). The vascular system in the cotyledonary tube of monocotylar Apiaceae goes from the root apex to the cotyledon lamina, without any branches to the shoot apex that differentiates rather late. Thus, the shoot apex is located far from the main line of conductive elements and is not connected to them during the early stages of development. Almost the same anatomical structure is observed in the monocotylar seedlings of Anemone apennina L. (Haccius & Fischer, 1959). However, when studying the position of the conductive elements, one should bear in mind that, with the development of the first leaves and the formation of their conductive elements, their original location in the cotyledonary node usually changes. In monocotylar seedlings with an open sheath at the cotyledonary node, one can usually see a large central double vascular bundle, e.g. in Scaligeria napiformis, and often also two lateral bundles, e.g. in Acronema commutatum, extending to the cotyledon. Above the cotyledonary node is the meristematically active zone of the shoot apex. In the studied plants, the morphology and anatomy of the seedlings often appears to reflect the degree of geophily. The most specialized species have the following combination of characters: a long cotyledonary tube, early formation of the hypocotylous tuber, a deep position in the soil and late differentiation of the main shoot apex (Haccius, 1952; Petrova et al., 2016; Blandino et al., 2019). All Apiaceae with monocotylar embryos are perennial monocarpic or polycarpic herbs with tuberous underground organs. Typically, umbellifers are herbaceous annuals, biennials or perennials, but some species may become woody at the base, and a few species are truly woody trees, shrubs or subshrubs (Plunkett et al., 2019). A woody habit points to early-diverging members of Apiaceae (van Wyk & Tilney, 2004), with more derived members of Apioideae representing secondary woodiness (Spalik et al., 2017). Dicotylar species of genera which have monocotylar species (Elaeosticta Fenzl, Neomuretia Kljuykov, Degtjareva & Zakharova, Scaligeria) or dicotylar species from other genera that are closely related to monocotylar taxa (e.g. Elwendia Boiss., Hyalolaena Bunge, Mogoltavia Korovin and Galagania Lipsky to Elaeosticta; Krasnovia Popov ex Schischk. to Kozlovia Lipsky) are also mainly geophytes with tubers, but there are some exceptions. Sinocarum cruciatum (the type species of Sinocarum) has a taproot and an embryo with two cotyledons, whereas the tuberous species form an embryo with a single cotyledon. It should be noted that a possible correlation between the number of cotyledons and the life form exists. Further investigation of geophilic Apioideae may reveal new records of monocotylar embryos. A possible candidate is the tuberous genus Korshinskia Lipsky, placed among early-divergent lineages of subfamily Apioideae, but the present study of the embryo of K. olgae revealed two cotyledons. Tuberous underground organs serve as adaptations to very peculiar ecological conditions. Within Apiaceae, geophilic taxa are widely distributed in the Ancient Mediterranean area [following the concept of Popov (1927), Meusel, Jäger & Weinert, 1965; Ovchinnikov, 1971], being xerophytes or ephemerals (Pimenov et al., 1981). So far, monocotylar embryos in Apiaceae have been found in taxa from Western Europe and North-West Africa in the west to the western Himalayas in the east (Fig. 6). Two genera with monocotylar embryos, Acronema and Sinocarum, are distributed in East Asia (in the Sino-Himalayan region) and one, Erigenia, is native to North America. It seems that most dispersal events of monocotylar taxa occurred among the areas that comprise the major diversification centres of apioid umbellifers: western Eurasia and the Mediterranean and the Irano-Turanian and eastern Asiatic regions. In general, Apiaceae subfamily Apioideae, in which the monocotylar species occur, are widely distributed in temperate regions of the Northern Hemisphere, with fewer representatives occurring in the south (Pimenov & Leonov, 1993). The Southern Hemisphere members of the subfamily either represent early-branching lineages (Downie & Katz-Downie, 1999; Calviño et al., 2006; Magee et al., 2010) or crown taxa of recent Northern Hemisphere origin (Spalik et al., 2010). The branches forming a basal grade in Apioideae (the protoapioids sensuMagee et al., 2010) occur almost exclusively in sub-Saharan Africa, a region that was also reconstructed as the ancestral area for the subfamily (Calviño et al., 2006). The remaining Apioideae (i.e. euapioids) probably originated in the Northern Hemisphere, and the adaptation of a euapioid ancestor to the temperate climatic zone in the early to mid Tertiary provided the subsequent evolutionary success of umbellifers (Banasiak et al., 2013). Figure 6. Open in new tabDownload slide The geographical distribution of monocotylar genera of Apiaceae. Figure 6. Open in new tabDownload slide The geographical distribution of monocotylar genera of Apiaceae. Taxonomy and systematic position of monocotyledonous Apiaceae Before the present study, seedlings with a single cotyledon were known in 14 of the > 460 recognized genera of Apiaceae: Acronema, Astomaea Rchb., Bunium, Conopodium, Elaeosticta, Erigenia, Geocaryum, Hellenocarum, Horstrissea, Kozlovia, Neomuretia, Scaligeria, Sinocarum and Stefanoffia (Haccius, 1952; Engstrand, 1973; Pimenov & Kljuykov, 2002; Kljuykov et al., 2014; Zakharova et al., 2016; Petrova et al., 2016). Haccius (1952) would have added Orogenia S.Watson to this list, but its embryo was too young to ascertain the cotyledon number. Later, Juguet (2002) found that O. linearifolia S.Watson possesses two cotyledons. Our present study has provided four additional records of monocotyledonous seedlings, with a new finding in Postiella Kljuykov. Thus, there are now records of 59 species of Apiaceae with monocotylar embryos, belonging to 15 genera (Table 2). A list of these species is presented in Table 3, together with the reference in which each report of monocotyly was published. All genera containing species with monocotylar embryos are members of Apiaceae subfamily Apioideae; no species with a monocotylar embryo have been found in subfamilies Saniculoideae, Azorelloideae or Mackinlayoideae or in other families of Apiales. Traditionally, genera of Apiaceae with monocotyledonous embryos were not assumed to be closely related and were placed in different tribes. Following the systems proposed by Drude (1898) and Pimenov & Leonov (1993), based largely on fruit characters, these genera were attributed to three different tribes (Scandiceae, Smyrnieae and Apieae). In a more recent review by Downie et al. (2010), in which a provisional molecular (ITS-based) classification of the subfamily Apioideae was presented, monocotylar taxa were detected in five of 41 major clades (Pyramidoptereae, Scandiceae, the Opopanax clade, Erigeniaeae and the Acronema clade; Fig. 3; Table 2). These clades are radically different from the groups originally recognized in both generic composition and affinities (Downie et al., 2001). Next, we discuss the phylogenetic affinities of each clade with monocotylar taxa in more detail. Pyramidoptereae This clade comprises more than a third of all known monocotylar species (22 of 59) from eight genera. Herein, Bunium and Elaeosticta are the largest and the others are oligotypic (Hellenocarum, Neomuretia, Scaligeria, Stefanoffia) or monotypic (Astomaea, Postiella) with narrow distribution ranges (Pimenov & Leonov, 1993; Hand, 2011). In Pyramidoptereae, monocotyledonous taxa are found in all three main lineages (Fig. 5). One lineage includes taxa distributed mainly in the Mediterranean region and consists almost exlusively of monocotylar species belonging to the genera Astomaea, Bunium, Hellenocarum, Neomuretia, Postiella, Scaligeria and Stefanoffia. Another lineage includes Central Asian genera such as Elaeosicta, Mogoltavia, Oedibasis Koso-Pol., Hyalolaena, Gongylotaxis Pimenov & Kljuykov and Elwendia, but only Elaeosticta contains monocotylar species. The third lineage is formed by members of Scaligeria, in which all species except S. moreana Engstrand are monocotylar, and the dicotyledonous Carum appuanum (Viv.) Grande. All these taxa are distributed in the Mediterranean region (Engstrand, 1970; Hand, 2011). Bunium was one of the first members of the family in which an embryo with a single cotyledon was discovered (Treviranus & Treviranus, 1821; Treviranus, 1831; Bernhardi, 1832), and, to date, it includes the greatest number of monocotylar species (Tables 1, 2). Cotyledon number has previously been used to separate Bunium from the taxonomically close Carum L. (Drude, 1898; Calestani, 1905; Wolff, 1927). Molecular investigation supported Bunium and C. carvi L. (the type species of Carum) as separate taxa (Zakharova, Degtjareva & Pimenov, 2012). Traditionally, Bunium comprised 51 species, both mono- and dicotylar, distributed in Asia, Europe and North Africa. Cotyledon number and some other fruit characters (width of commissure) were used to divide the genus into two groups. The distribution of monocotylar vs. dicotylar species varies with chromosome number and plant geography (Kljuykov, 1988). Molecular data supported the segregation of the dicotylar and more easterly distributed species in a separate genus Elwendia (Degtjareva et al., 2013). Thus, the genus Bunium now numbers 29 species, 20 of which are monocotylar; nine species have an as yet unknown cotyledon number. In its current circumscription, however, Bunium is still not monophyletic. Molecular data suggest that some additional genera [Astomaea, Carum (but not Carum s.s., see Zakharova et al., 2012), Hellenocarum, Neomuretia, Postiella, Stefanoffia, Tamamschjanella Pimenov & Kljuykov] fall within Bunium. Morphologically, they differ from Bunium in many taxonomically important characters (life form, fruit structure, shape of bracts), but are similar to Bunium in their distribution in the Mediterranean and Aegean Turkey and in cotyledon number as many of these genera, exept Carum and Tamamschjanella, possess a monocotylar embryo. Thus, a mixture of dissimilar species in one clade makes further subdivision of Bunium difficult, as morphological data do not provide any diagnostic characters for the clades. The monotypic Postiella was initially described as a Turkish species of Scaligeria (Post, 1888). Later, based on fruit characters (absence of calyx teeth, low conical stylopodia with constrictions), it was recognized as a separate genus with only one species (Kljuykov, 1985a). In the ITS tree, this genus is sister to Bunium pinnatifolium and distant from Scaligeria. Another species closely related to Postiella is Stefanoffia aurea, a representative of a small eastern Mediterranean genus, previously treated as a species of Muretia Boiss. (Pimenov & Kljuykov, 1980). Present and earlier molecular studies revealed that the second species of Stefanoffia, S. daucoides, is misplaced in Pyramidoptereae (Degtjareva et al., 2013), and Stefanoffia is therefore not monophyletic. It includes three species, distributed in south-western Asia (Turkey) and southern Europe (Bulgaria, Greece). Although all species show considerable similarity in fruit anatomy and cotyledon number (monocotyly), they differ in many others traits (shape of terminal lobe of leaf and bracts, petal colour, mericarp vittae number), traditionally assumed to be unimportant at the generic level (Pimenov & Kljuykov, 1980). Molecular data suggest distinguishing them as distinct genera. Additional morphological studies are required to assess the status of these taxa. Nevertheless, petal shape (entire, not deeply inflexed) could be considered as a potential synapomorphy of the clade including Postiella, Stefanoffia aurea and Bunium pinnatifolium. The monotypic monocotylar Astomaea is mainly known under the name of Astoma DC. Earlier, it was placed near to Scaligeria (Drude, 1898) or included in Conopodium (Koso-Poljansky, 1916). Astomaea seselifolia (DC.) Rauschert is endemic to south-western and Mediterranean Asia. In a previous molecular study (Ajani et al., 2008), A. seselifolia appears to be most closely related to Bunium, although only one species, B. elegans (Fenzl) Freyn, was included in the analysis. In our ITS tree, Astomaea continues to be closely related to Bunium. Moreover, the species is deeply submerged in one of the clades, constituted only of Bunium species. Its placement in the molecular tree raises the question about the independent status of Astomaea in relation to Bunium. Morphologically, Astomaea possesses both similarities (monocotylar embryo, number of bracts and bracteoles, width of mericarp commissure) and differences (shape of fruits, shape of dorsal mericarp ribs, shape of endosperm on commissural side), which support its consideration as a separate taxon. Hellenocarum now comprises three species, Hellenocarum depressum (Hartvig & Kit Tan) Kljuykov & Zakharova, H. multiflorum (the type species) and H. strictum (Griseb.) Kljuykov, distributed in south-western Asia and southern and south-eastern Europe (Zakharova et al., 2016). Two species are monocotylar but the cotyledon number of H. depressum is unknown. As for Bunium, cotyledon number was used to separate Hellenocarum from closely related Carum (Engstrand, 1973; Kljuykov, 1985b). A distant position of Hellenocarum from Carum was futher supported by molecular phylogenetic studies (Papini, Banci & Nardi, 2007; Degtjareva et al., 2009; Zakharova et al., 2012, 2016). Neomuretia is a small genus with two species, native to Iran, Iraq and Turkey. Earlier, this genus was not proposed based on morphology and was recently segregated from Hellenocarum following a molecular phylogenetic study (Zakharova et al., 2016). Monocotylar seedlings were found in N. amplifolia (Boiss. & Hausskn.) Kljuykov, Degtjareva & Zakharova but not in N. pisidica (Kit Tan) Kljuykov, Degtjareva & Zakharova, in which the embryo is dicotylar. The relationships of Neomuretia to Hellenocarum, Bunium and Carum (but not to the generitype C. carvi) are still ambiguous due to the incongruent relationships recovered for these genera in trees based on nuclear and plastid DNA (Zakharova et al., 2016). Scaligeria includes four species, one of which, S. alziarii Hand, Hadjik. & Zetzsche, was recently described on Crete (Hand, Hadjikyriakou & Zetzsche, 2012). The genus is distributed in the eastern Mediterranean (Engstrand, 1970). Many species previously treated in Scaligeria were transferred to the Central Asian genus Elaeosticta (Kljuykov, Pimenov & Tikhomirov, 1976). This was further supported by a molecular phylogenetic study (Degtjareva et al., 2013). All species of Scaligeria group together, but, Carum appuanum is nested in this clade. Scaligeria, in which one out of the four species was studied (Haccius, 1952), has long been considered as a monocotylar genus. Recently, however, seedlings with two cotyledons in S. moreana were found (Petrova et al., 2016). The present study revealed one more species of Scaligeria, S. halophila, to possess an embryo with one cotyledon. Scaligera moreana, with a dicotylar embryo, occupies a relatively distant position from other Scaligeria spp., forming a early-diverging lineage in the clade. Elaeosticta (25 species) is one of the largest genera of geophilic Central Asian umbellifers; only one of its 24 studied species [E. tschimganica (Korovin) Kljuykov et al.] has a single cotyledon (Korovin, 1928; Haccius, 1952; Kljuykov, 1980). Elaeosticta is rendered paraphyletic by the inclusion of the enigmatic Hyalolaena melanorrhiza Pimenov & Kljuykov. Separation of dicotylar Elaeosticta (24 species) from monocotylar Scaligeria (three species) was confirmed by molecular data (Degtjareva et al., 2013). The only monocotylar Elaeosticta, E. tschimganica, is closely related to other Elaeosticta spp. with two cotyledons, and is not close to monocotylar S. napiformis and S. halophila. Scandiceae This clade includes three monocotylar genera: Conopodium (eight species); Geocaryum (13–15 species) and Kozlovia (one species). Although all mentioned genera are nested in a strongly supported clade, there are several dicotyledonous taxa that are closer to Geocaryum or Conopodium than these genera are to each other (Fig. 3). The rather large genera Geocaryum and Conopodium are still insufficiently studied in respect of cotyledon number (Table 2). Delimitation of Conopodium and Geocaryum from Bunium has been a major taxonomic challenge (Engstrand, 1973, 1977). These taxa grow together in mountainous regions of the western Mediterranean and are morphologically similar (monocotyledonous embryo, globose tuber, similar vegetative parts). The present study and previous molecular phylogenetic analyses (Downie, Katz-Downie & Spalik, 2000a; Downie et al., 2000b; Spalik, Wojewódzka & Downie, 2001) revealed that both Conopodium and Geocaryum are far removed from all Bunium spp. Moreover, they are distant from Bunium also in fruit structure (Engstrand, 1973, 1977). Their life-form similarity to Bunium seems to be convergent. The extended sampling of species of Geocaryum and Conopodium presented here demonstates that Geocaryum is monophyletic; all of its studied species form a strongly supported clade, whereas the monophyly of Conopodium continues to be questionable. All Conopodium spp. group together, but the variability of the ITS sequence is not sufficient to delimit Conopodium from the morphologically different Todaroa aurea (Aiton) Parl., Athamanta cervariifolia (DC.) DC. and A. cretensis L. It is unlikely that Conopodium is paraphyletic with regard to Athamanta L. and Todaroa Parl., as its characteristic morphology strongly suggests monophyly of the genus (Downie et al., 2000a). The monotypic genus Kozlovia is distributed in Central Asia and Afghanistan. Molecular data (Downie et al., 2000b) showed a close affinity between Kozlovia and the monotypic Krasnovia and oligotypic Neoconopodium (Koso-Pol.) Pimenov & Kljuykov (two species, one included in this analysis). Based mainly on molecular data, it has been suggested that all the mentioned species could possibly be included in Kozlovia (Spalik & Downie, 2001). However, morphologically, they differ in exocarp structure and indumentum of the fruit (see Pimenov & Kljuykov, 1987), and so could be interpreted as independent genera. Additionally, Kozlovia and Krasnovia differ in cotyledon number; Kozlovia is monocotyledonous, whereas Krasnovia is dicotyledonous. The number of cotyledons in Neoconopodium is still uncertain as the available embryo was too young to study. Opopanax clade The occurrence of monocotyly in the Opopanax clade was revealed in the present study and attributed to Horstrissea, which had not previously been studied using molecular data. This monotypic genus was described by Egli et al. (1990) from Crete (Greece). Morphological peculiarities of the genus (unusual chromosome number, shape of bracts, shape of endosperm) suggest several genera (Bunium, Scaligeria, Stefanoffia) as potential relatives (Egli et al., 1990). The observation of a monocotyledonous seedling in the genus (Petrova et al., 2016) is therefore of special interest. The molecular study presented here shows Horstrissea to be placed distantly from both Bunium and Scaligeria, being sister to the southern Balkan and western Anatolian Stefanoffia daucoides. A potential synapomorphy for the grouping of Horstrissea and Stefanoffia daucoides could be divided involucral bracts, a rare feature in Apioideae. In addition, as revealed in the present study, Stefanoffia daucoides, like Horstrissea, possesses a monocotylar embryo. Erigenieae This lineage consists of the genus Erigenia alone (Downie et al., 2010). It is a monotypic genus with E. bulbosa Nutt., the only species, being narrowly distributed in North America. It is a small spring ephemeroid (common name ‘harbinger of spring’). The discovery of monocotyly in the genus is attributed to Hegelmaier (1878) and Holm (1901). All molecular phylogenetic studies to date in which Erigenia is included (e.g. Downie & Katz-Downie, 1999; Katz-Downie et al., 1999; Downie et al., 2002; Calviño et al., 2006) have placed the genus in an isolated position as one of the early-diverging lineages of Apioideae. Acronema and Physospermopsis clades Monocotyly in Acronema and Sinocarum was observed by Mukherjee & Constance (1993) and Kljuykov et al. (2014). Acronema comprises c. 25 species, distributed from Nepal to south-western China and Thailand. Sinocarum includes 20 species native to Sino-Himalaya, from Nepal to south-western China. They represent a taxonomically complex group with unclear generic boundaries between them and Tongoloa H.Wolff. Among Apiaceae, Acronema and Sinocarum are delimited by the shape of the petals, which are deeply dissected in Sinocarum and have a long attenuate apex in Acronema. In terms of phylogenetic relationships, Sinocarum and Acronema are not sister taxa, being placed in different clades (see also Zhou et al., 2008, 2009). All studied Acronema spp. form a clade with Sinocarum bellum (C.B.Clarke) Pimenov & Kljuykov nested in it, and they are together situated in the Acronema clade. The other four Sinocarum species analysed do not form a clade. Two species, S. cruciatum (the generitype) and S. dolichopodum (Diels) H.Wolff, fall in the Physospermopsis clade with Tongoloa elata H.Wolff. Sinocarum wolffianum is placed in the Acronema clade but not close to Acronema. Sequence data from a wider range of species are required to delimit the genera in this group. Moreover, Acronema includes only monocotylar species to date; in Sinocarum s.l., both dicotylar and monocotylar embryos are found. All monocotylar species of Acronema and Sinocarum are placed in the Acronema clade, but do not group together. The origin of the single cotyledon in Apiaceae There are two main theories about the origin of a single cotyledon: (1) syncotyly, in which the single cotyledon appears to have been derived, phylogenetically, from a fused ancestral pair (Sargant, 1902, 1903); and (2) anisocotyly with the reduction or suppression of one cotyledon in the ancestral pair (Hegelmaier, 1875, 1878). However, there is no direct evidence to suggest two different origins for the cotyledon lamina in monocotylar Apiaceae. There is no trace of a second cotyledon that could have been lost, nor are there any intermediates between bilaminar and unilaminar seedlings [as noted even by Irmisch (1854), Schmid (1902) and others]. However, in other families, e.g. Lentibulariaceae (Pinguicula L.), such intermediates may be found (Haccius & Hartle-Baude, 1957; Titova, 2012). When studying embryos of Bunium bulbocastanum with an oblong cotyledon, Hegelmaier (1875) found in some a rudiment of a second cotyledon in addition to a single well-developed cotyledon, and he also observed seedlings of B. bulbocastanum with two unequal cotyledons. Therefore, he explained monocotyly in Apiaceae in terms of the reduction of one cotyledon of the pair. This point of view was supported by Domin (1909). Géneau de Lamarlière (1893) and Haccius (1952) after studying several Apiaceae species, supported the first hypothesis. At the top of the cotyledon lamina of Scaligeria napiformis, Haccius (1952) found a recess that was regarded as two incompletely fused cotyledons. Additionally, in dicotylar taxa of Apiaceae closely related to monocotylar taxa, two cotyledons are basally united with each other to form a complete tube. In contrast, with regard to monocotylar taxa of some other families, e.g. Lentibulariaceae (Pinguicula), Haccius & Hartle-Baude (1957) considered a single cotyledon to result from anisocotyly and reduction. Among other indirect morphological data, an argument in favour of syncotyly may be the partial unilateral fusion of two cotyledons and the presence of cotyledonary tubes in dicotylar species of Apiaceae (Sargant, 1903; Vasilchenko, 1941; Haccius, 1952; Petrova et al., 2016). Further evidence for syncotyly, according to Haines & Lye (1979), may be the position of the cotyledons and foliage leaves. In normal dicotyledons, in which the cotyledon laminas are not united, the first foliage leaf appears in the plane between the cotyledons, with the second leaf forming opposite to it. In the case of monocotyly resulting from the loss of one cotyledon, the foliage leaves would remain in their original plane unless they had changed their position with regard to the remaining cotyledon. However, this is not the case with most seedlings (Haines & Lye, 1979). In many plants with one cotyledon lamina, the first foliage leaf lies opposite to it, as would be expected if it were formed by syncotyly. According to our data, there are exceptions such as Acronema commutatum, in which the second foliage organ (which we regard as the first true leaf), is initially located at an acute angle to the first foliage organ (which we regard as the original single cotyledon) but not opposite to it (Kljuykov et al., 2014). A comparison of the structure of the single cotyledons of the monocotylar Apiaceae with that observed in Ranunculaceae would probably be most informative as, in many cases, the pattern of development is similar. Physiological experiments have suggested that the deviated cotyledon phenotype can result from the influence of developmental-stage-specific hormones (Haccius, 1960; Haccius & Trompeter, 1960). If non-differentiated embryos of normally dicotylar Eranthis hyemalis Salisb. (Ranunculaceae) are treated with different growth-regulating substances, monocotyly can be induced, and syncotyly or anisocotyly in various degrees can be obtained. In a comparative study of E. hyemalis, monocotylar specimens, obtained by induced anisocotyly or syncotyly, were found to differ considerably in macro- and microstructure from ‘syncotylar’ specimens (Haccius & Trompeter, 1960), being more similar to ‘anisocotylar’ specimens (Haccius, 1960). This suggests that the single cotyledon in monocotylar Ranunculaceae is homologous to only one of the two cotyledons in the dicotylar species. To date, there are reports on various dicotyledonous plants that claim that fusion during the developmental processes leads to abnormal seedlings with a single cotyledon (Mogensen, 1970; van Cotthem, 1981). Although they could display a type of total cotyledonary fusion, they should be recognized as isolated cases and should not strictly be used for the verification of hypotheses of syncotyly vs. anisocotyly. Titova (2000) suggested a theory to reconcile the two main hypotheses regarding the origin of a single cotyledon in dicotylar angiosperms (anisocotyly vs. syncotyly). She stated that anisocotyly always seems to occur against the backdrop of a partial congenital fusion of the cotyledons during embryogenesis. All the theories mentioned above suppose the reduction in cotyledon number to the monocotyledonous condition as a gradual process. Alternatively, a case with no intermediate states such as that observed in Apiaceae allows suggesting abrupt changes in cotyledon number. As examples, deviations from dicotyly to pleiocotyly observed in Degeneria I.W.Bailey & A.C.Sm. (Degeneriaceae; Swamy, 1949), Pittosporum Banks ex Gaertn. (Pittosporaceae; Kumazawa, 1970) and, as an abnormality, in Cosmos Cav. (Asteraceae; Banerji, 1961) should probably not be interpreted as a result of a longitudinal splitting of the two original cotyledons. The variation in the cotyledon number in the direction of reduction gives a monocotyledonous embryo, and it could be proposed as one of the extremes in the variation of the cotyledon number. It is necessary to note that in Apiales, deviations from the typical number of cotyledons can be both in the direction of decreasing to one (in Apiaceae) and increasing to three to five in some Pittosporum spp. (Godley, 1985; Cayzer, Crisp & Telford, 2000). Based on some mutant plants from model families [Brassicaceae: Arabidopsis (DC.) Heynh.; Scrophulariaceae: Antirrhinum L.; Solanaceae: Petunia Juss., Solanum L.; Fabaceae: Pisum L.], some candidate genes have been identified that may trigger the single-cotyledon program and the key involvement of auxin has also been demonstrated (reviewed by Chandler, 2008). For example, in Pisum, these genes influence the positioning and shaping of the cotyledon (Liu et al., 1999). Regarding these mutants, however, it would be incorrect to describe their cotyledons as ‘fused’, because they appear to arise as single structures at an early stage in embryo development. Such a developmental process is normally termed congenital, rather than ontogenetic fusion because it results from zonal growth (Liu et al., 1999; reviewed in Sokoloff et al., 2018). As the origin of monocotyly in Apiaceae is still unclear, further genetic research is needed to shed more light on the issue. Evolutionary significance of monocotyly A parsimonious optimization indicates considerable homoplasy in the evolution of cotyledon number in Apiaceae (Figs 4, 5) that cannot be aligned with our phylogenetic tree based on nrITS sequences. At least seven shifts to monocotyly occur in the family. Monocotyly is also not congruent with plastid phylogenetic trees for Apiaceae (Zhou et al., 2009; Degtjareva et al., 2009) or with the morphological classification of the family, based largely on fruit characters (Drude, 1898; Pimenov & Leonov, 1993). In addition, monocotyly has independently arisen within major clades in the classification based on ITS (Downie et al., 2010) as several dicotyledonous taxa are closer to monocotyledonous genera than they are to each other. Such a pattern of distribution of monocotyly in Apiaceae is of special interest, because it seems that members of all related families, such as Araliaceae, Pittosporaceae, Myodocarpaceae, Torricelliaceae, Griseliniaceae and Pennantiaceae, possess embryos with two cotyledons. Our optimization shows that a dicotyledonous embryo seems to be primitive in Apiaceae because it is characteristic for the earliest-diverging lineages in Apiaceae (subfamilies Saniculoideae, Azorelloideae and Mackinlayoideae) and in other families of Apiales, and deviations to monocotyly occur in the derived subfamily Apioideae only. In the related orders Asterales, Aquifoliales and Dipsacales, an embryo with one cotyledon is known only in Sineilesis aconitifolia (Bunge) Maxim. (Asteraceae), as reviewed by Weisse (1930). Considering ITS sequence data, parallel origins of monocotyly in Apiaceae rather than reversals could be accepted. Although more data concerning cotyledon number and more resolution in the molecular tree are needed, it can be hypothezised that reversal to dicotyledony occurred only once, in Neomuretia in Pyramidoptereae (Fig. 5). In general, the presence of species having embryos with one developed cotyledon has been noted for a relatively small number of eudicot families, namely Papaveraceae, Ranunculaceae, Celastraceae, Portulacaceae, Lentibulariaceae and Asteraceae (Weisse, 1930; Titova, 2000), which are scattered across nearly all major clades of angiosperms, but not reported for the early-diverging angiosperms from which monocots are believed to be derived (APG IV, 2016). One possible candidate could be provided by Hydatellaceae which were initially placed in the monocot order Poales and appeared recently to be an early-diverging lineage of angiosperms sister to all other Nymphaeales (Saarela, Rai & Doyle, 2007). Seedling morphology of Hydatellaceae has been widely discussed and controversially described either as monocotylar or dicotylar (Cooke, 1987; Tillich, Tuckett & Facher, 2007; Sokoloff et al., 2008). Detailed developmental investigations have clearly demonstrated the occurrence of two cotyledons in Hydatellaceae (Friedman, Bachelier & Hormaza, 2012), although the cotyledon morphology is highly unusual in some species (Sokoloff et al., 2014). Results of recent studies on angiosperm phylogeny (APG IV, 2016), provide evidence that monocotyledonous dicots are homoplasious in both the angiosperms as a whole and at a lower taxonomic level in Apiaceae. In some other eudicot groups showing monocotyly, the evolution of this character is also homoplastic. It is evident, for example, for the carnivorous genus Pinguicula (Lentibulariaceae) (Degtjareva et al., 2006). Despite independent origins of monocotyly in Apiaceae, there is a remarkable morphological similarity in monocotylar embryo and seedling organization, especially in the proportion of cotyledon to axis in the embryo and the multifunctional cotyledonary tube in the seedling. The taxonomic value of cotyledon morphology and seedling structure may sometimes be uncertain as these features frequently appear to be related to plant ecological factors (e.g. Haccius, 1952). All monocotyledonous species are geophilic plants, xerophytes or ephemerals, possessing adaptations to peculiar ecological conditions and are abundantly distributed in the Ancient Mediterranean area. Although the presence of monocotyledonous embryos is homoplasious, this feature is useful for defining most generic limits (e.g. Bunium vs. Carum, Bunium vs. Elwendia, Hellenocarum vs. Carum, Kozlovia vs. Krasnovia) in Apiaceae (Drude, 1898; Wolff, 1927; Engstrand, 1973; Kljuykov, 1985a; Degtjareva et al., 2013; Zakharova et al., 2016). A comprehensive study of the cotyledon number is necessary to assist in the revision of the poorly known genera Sinocarum and Acronema. The addition of more taxa and other molecular markers for Apiaceae may produce new hypotheses on embryo evolution in the family. CONCLUSIONS Possessing the greatest number of monocotyledonous species among eudicots, Apiaceae represent a particularly notable example of cotyledon number diversity. We have summarized all data currently available on monocotylar Apiaceae. The occurrence of a single cotyledon plays a significant role in our understanding of the morphology, systematics and ecology of Apiaceae. Despite the fact that many of the characters appear to be related to the environment, cotyledon number is important for the taxonomy of some genera. Therefore, further identification of monocotylar species is essential. In addition, studies of monocotylar Apiaceae appear to extend the boundaries of our understanding of the diversity of plant organs. This primarily refers to the structure of the cotyledonary tube that can function as a root and a shoot and to the unusual morphology of the single cotyledon in Acronema. Further study of the nature of monocotyly in Apiaceae may help in understanding the mechanisms that have led to the appearance of monocotylar plants in some other taxa. Monocotyly in Apiaceae is not congruent with the morphological classification of the family, based largely on fruit characters (Drude, 1898; Pimenov & Leonov, 1993) or molecular data, and has arisen independently more than once in the course of evolution. As more monocotyledonous species are identified, they can be used to test evolutionary hypotheses, especially as molecular tree resolution increases with greater taxonomic sampling and additional molecular markers. SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article at the publisher’s web-site: Appendix 1. Previously published nrDNA ITS accessions taken from GenBank. ACKNOWLEDGEMENTS We are indebted to the curators of all herbaria where material was studied. We are grateful to D. D. Sokoloff for helpful discussions and to Prof. Michael F. Fay, Prof. Julien B. Bachelier and two anonymous reviewers for their critical reading of the manuscript. This work was supported by Russian Foundation for Basic Research (grant 15-29-02748), the Goverment Order for the Lomonosov Moscow State University (project numbers АААА-А16-116021660045-2, AAAA-A16-116021660046-9) and Moscow State University Grant for Leading Scientific Schools “Depository of the Living Systems” in frame of the MSU Development Program. CONFLICT OF INTEREST The authors declare that they have no conflict of interest. REFERENCES Agro Slide Bank [online] . Available at: http://asb.com.ar/. Accessed 20 October 2018 . Ajani Y , Ajani A , Cordes JM , Watson MF , Downie SR . 2008 . Phylogenetic analysis of nrDNA ITS sequences reveals relationships within five groups of Iranian Apiaceae subfamily Apioideae . Taxon 57 : 383 – 401 . OpenURL Placeholder Text WorldCat APG IV . 2016 . An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV . Botanical Journal of the Linnean Society 181 : 1 – 20 . Crossref Search ADS WorldCat Australian Tropical Rainforest Plants Edition 6 [online] . Available at: https://www.anbg.gov.au/cpbr/cd-keys/rfk/. Accessed 20 September 2018 . Banasiak Ł , Piwczyński M , Uliński T , Downie SR , Watson MF , Shakya B , Spalik K . 2013 . Dispersal patterns in space and time: a case study of Apiaceae subfamily Apioideae . Journal of Biogeography 40 : 1324 – 1335 . Google Scholar Crossref Search ADS WorldCat Banerji ML . 1961 . On the anatomy of teratological seedlings—I. Cosmos bipinnatus Cav . Proceedings of the Indiana Academy of Science 53 : 10 – 19 . OpenURL Placeholder Text WorldCat Barykina RP . 1971 . Characteristic features of the first ontogenetic stages in Podophyllum emodi Wall . and P. peltatum L . Botanicheskii Zhurnal 56 : 921 – 931 [in Russian]. OpenURL Placeholder Text WorldCat Barykina RP . 1999 . On some transformation modes of ontogenesis, organogenesis and histogenesis in somatic evolution of the family Ranunculaceae . Bulletin of Moscow Society of Naturalists. Biological Series 104 : 49 – 53 [in Russian]. OpenURL Placeholder Text WorldCat Bernhardi JJ . 1832 . Über die merkwürdigsten Verschiedenheiten des entwickelten Pflanzenembryo und ihren Werth für Systematik . Linnaea 7 : 561 – 613 . OpenURL Placeholder Text WorldCat Blandino C , Fernández-Pascual E , Marin M , Vernet A , Pritchard HW . 2019 . Seed ecology of the geophyte Conopodium majus (Apiaceae), indicator species of ancient woodland understories and oligotrophic meadows . Plant Biology (Stuttgart, Germany) 21 : 487 – 497 . Google Scholar Crossref Search ADS PubMed WorldCat Burtt BL . 1991 . Umbelliferae of southern Africa: an introduction and annotated check-list . Edinburgh Journal of Botany 48 : 133 – 282 . Google Scholar Crossref Search ADS WorldCat Calestani V . 1905 . Contributo alla sistematica delle ombellifere d’Europa . Webbia 1 : 89 – 250 . Google Scholar Crossref Search ADS WorldCat Calviño CI , Tilney PM , Wyk BE , Downie SR . 2006 . A molecular phylogenetic study of southern African Apiaceae . American Journal of Botany 93 : 1828 – 1847 . Google Scholar Crossref Search ADS PubMed WorldCat Cayzer LW , Crisp MD , Telford IRH . 2000 . Revision of Pittosporum (Pittosporaceae) in Australia . Australian Systematic Botany 13 : 845 – 902 . Google Scholar Crossref Search ADS WorldCat Cerceau-Larrival M-Th . 1962 . Plantules et pollen d’Ombellifères . Mémoires du Muséum National d’Histoire Naturelle, Sér. B 14 : 1 – 166 . OpenURL Placeholder Text WorldCat Chandler JW . 2008 . Cotyledon organogenesis . Journal of Experimental Botany 59 : 2917 – 2931 . Google Scholar Crossref Search ADS PubMed WorldCat Cooke DA . 1987 . Hydatellaceae. In: George AS , ed. Flora of Australia , Vol. 45 . Canberra : Australian Government Publishing Service , 1 – 5 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Crowden RK , Harborne JB , Heywood VH . 1969 . Chemosystematics of the Umbelliferae—a general survey . Photochemistry 8 : 1963 – 1984 . Google Scholar Crossref Search ADS WorldCat Degtjareva GV , Casper SJ , Hellwig FH , Schmidt AR , Sokoloff DD . 2006 . Morphology and nrITS phylogeny of the genus Pinguicula L. (Lentibulariaceae), with focus on embryo evolution . Plant Biology 8 : 1 – 13 . Google Scholar Crossref Search ADS PubMed WorldCat Degtjareva GV , Kljuykov EV , Samigullin TH , Valiejo-Roman CM , Pimenov MG . 2009 . Molecular appraisal of Bunium and some related arid and subarid geophilic Apiaceae–Apioideae taxa of the Ancient Mediterranean . Botanical Journal of the Linnean Society 160 : 149 – 170 . Google Scholar Crossref Search ADS WorldCat Degtjareva GV , Kljuykov EV , Samigullin TH , Valiejo-Roman CM , Pimenov MG . 2013 . ITS phylogeny of Middle Asian geophilic Umbelliferae-Apioideae genera, with comments on their morphology and utility of psbA-trnH sequences . Plant Systematics and Evolution 299 : 985 – 1010 . Google Scholar Crossref Search ADS WorldCat Denisova GA . 1961 . The peculiarities of embryo development in the seeds of some Apiaceae . Doklady Akademii Nauk SSSR 139 : 999 – 1000 [in Russian]. OpenURL Placeholder Text WorldCat Domin K . 1909 . Morphologische und phylogenetische Studien über die Familie der Umbelliferen. II . Bulletin International de l’Academie des Sciences. Classe des Sciences Mathématiques, Naturelles, etc. Prague 13 : 108 – 153 . OpenURL Placeholder Text WorldCat Downie SR , Hartman RL , Sun F-J , Katz-Downie DS . 2002 . Polyphyly of the spring-parsleys (Cymopterus): molecular and morphological evidence suggests complex relationships among the perennial endemic taxa of western North American Apiaceae . Canadian Journal of Botany 80 : 1295 – 1324 . Google Scholar Crossref Search ADS WorldCat Downie SR , Katz-Downie DS . 1999 . Phylogenetic analysis of chloroplast rps16 intron sequences reveals relationships within the woody southern African Apiaceae subfamily Apioideae . Canadian Journal of Botany 77 : 1120 – 1135 . Google Scholar Crossref Search ADS WorldCat Downie SR , Katz-Downie DS , Spalik K . 2000a . A phylogeny of Apiaceae tribe Scandiceae: evidence from nuclear ribosomal DNA internal transcribed spacer sequences . American Journal of Botany 87 : 76 – 95 . Google Scholar Crossref Search ADS WorldCat Downie SR , Plunkett GM , Watson MF , Spalik K , Katz-Downie DS , Valiejo-Roman CM , Terentieva EI , Troitsky AV , Lee B-Y , Lahham J , El-Oqlah A . 2001 . Tribes and clades within Apiaceae subfamily Apioideae: the contribution of molecular data . Edinburgh Journal of Botany 58 : 301 – 330 . Google Scholar Crossref Search ADS WorldCat Downie SR , Spalik K , Katz-Downie DS , Reduron J-P . 2010 . Major clades within Apiaceae subfamily Apioideae as inferred by phylogenetic analysis of nrDNA ITS sequences . Plant Diversity and Evolution 128 : 111 – 136 . Google Scholar Crossref Search ADS WorldCat Downie SR , Watson MF , Spalik K , Katz-Downie DS . 2000b . Molecular systematics of Old World Apioideae (Apiaceae): relationships among some members of tribe Peucedaneae sensu lato, the placement of several island-endemic species, and resolution within the apioid superclade . Canadian Journal of Botany 78 : 506 – 528 . Google Scholar Crossref Search ADS WorldCat Drude CGO . 1898 . Umbelliferae. In: Engler A , Prantl K , eds. Die natürlichen Pflanzenfamilien , Vol. 3(8). Leipzig : Wilhelm Engelmann , 63 – 250 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Egli B , Gerstberger P , Greuter W , Risse H . 1990 . Horstrissea dolinicola, a new genus and species of umbels (Umbelliferae, Apiaceae) from Kriti (Greece) . Willdenowia 19 : 389 – 399 . OpenURL Placeholder Text WorldCat Engstrand L . 1970 . The European species of Scaligeria (Umbelliferae) . Botaniska Notiser 123 : 505 – 511 . OpenURL Placeholder Text WorldCat Engstrand L . 1973 . Generic delimination of Bunium, Conopodium and Geocaryum (Umbelliferae) . Botaniska Notiser 126 : 146 – 154 . OpenURL Placeholder Text WorldCat Engstrand L . 1977 . Biosystematics and taxonomy in Geocaryum Cosson (Umbelliferae) . Lund : University of Lund . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Friedman WE , Bachelier JB , Hormaza JI . 2012 . Embryology in Trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early-diverging flowering plants . American Journal of Botany 99 : 1083 – 1095 . Google Scholar Crossref Search ADS PubMed WorldCat Géneau de Lamarlière ML . 1893 . Recherches sur le développement de quelques Ombellifères . Revue Générale de Botanique 5 : 159 – 171 , 224 – 229 , 258 – 264 . OpenURL Placeholder Text WorldCat Godley EJ . 1985 . Paths to maturity . New Zealand Journal of Botany 23 : 687 – 706 . Google Scholar Crossref Search ADS WorldCat Haccius B . 1952 . Verbreitung und Ausbildung der Einkeimblättrigkeit bei den Umbelliferen . Österreichische Botanische Zeitung 99 : 483 – 505 . Google Scholar Crossref Search ADS WorldCat Haccius B . 1953 . Histogenetische Untersuchungen an Wurzelhaube und Kotyledonarscheide geophiler Keimpflanzen (Podophyllum und Eranthis) . Planta 41 : 439 – 458 . Google Scholar Crossref Search ADS WorldCat Haccius B . 1960 . Experimentell induzierte Einkeimblättrigkeit bei Eranthis hiemalis. II. Monocotylie durch Phenilborsäure . Planta 54 : 482 – 497 . Google Scholar Crossref Search ADS WorldCat Haccius B , Fischer E . 1959 . Embryologische und histogenetische Studien an ‘monokotylen Dikotylen’. III. Anemona apennina L . Österreichische Botanische Zeitung 106 : 373 – 389 . Google Scholar Crossref Search ADS WorldCat Haccius B , Hartle-Baude E . 1957 . Embryologische und histogenetische Studien an ‘monokotylen Dikotylen’ II. Pinguicula vulgaris L . und Pinguicula alpina L . Österreichische Botanische Zeitung 103 : 567 – 587 . Google Scholar Crossref Search ADS WorldCat Haccius B , Trompeter G . 1960 . Experimentell induzierte Einkeimblättrigkeit bei Eranthis hiemalis. I. Synkotylie durch 2,4-Dichlorphenoxyessigsäure . Planta 54 : 466 – 481 . Google Scholar Crossref Search ADS WorldCat Haines RW , Lye KA . 1979 . Monocotylar seedlings: a review of evidence supporting an origin by fusion . Botanical Journal of the Linnean Society 78 : 123 – 140 . Google Scholar Crossref Search ADS WorldCat Hall TA . 1999 . BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT . Nucleic Acids Symposium Series 41 : 95 – 98 . OpenURL Placeholder Text WorldCat Hand R . 2011 . Apiaceae. In: Euro+Med Plantbase – the information resource for Euro-Mediterranean plant diversity . Available at: http://ww2.bgbm.org/EuroPlusMed/. Accessed 31 August 2018 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Hand R , Hadjikyriakou G , Zetzsche H . 2012 . Scaligeria alziarii, a new sibling species of S. napiformis from Cyprus . Willdenowia 42 : 199 – 207 . Google Scholar Crossref Search ADS WorldCat Hegelmaier F . 1875 . Embryologie von Carum bulbocastanum . Botanische Zeitung 33 : 75 . OpenURL Placeholder Text WorldCat Hegelmaier F . 1878 . Vergleichende Untersuchungen über Entwicklung dikotyledoner Keime mit Berücksichtigung der Pseudo-monokotyledonen . Stuttgart : Schweizerbart . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Hofmeister W . 1861 . Neue Beiträge zur Kenntniss der Embryobildung der Phanerogamen. II. Monokotyledonen . Abhandlungen der matematisch-physischen Classe der Königlich Sächsischen Gesellschaft der Wissenschaften 5 : 631 – 760 . OpenURL Placeholder Text WorldCat Holm T . 1901 . Erigenia bulbosa Nutt . American Journal of Science. Series 4 . 11 : 63 – 72 . Google Scholar Crossref Search ADS WorldCat Irmisch T . 1854 . Beitrage zur vergleichenden Morphologie der Pflanzen I-IV . Abhandlungen der Naturforschenden Gesellschaft Halle 2 : 31 – 80 . OpenURL Placeholder Text WorldCat Irmisch T . 1858 . Keimung von Bunium creticum Mill . Flora 3 : 38 – 39 . OpenURL Placeholder Text WorldCat Juguet M . 2002 . Origine et étapes de la monocotylie chez les monocotylédones. IV—La zone cotylédogène annulaire des spermaphytes et l’origine de la monocotylie . Acta Botanica Gallica 149 : 3 – 33 . Google Scholar Crossref Search ADS WorldCat Katoh K , Standley DM . 2013 . MAFFT multiple sequence alignment software version 7: improvements in performance and usability . Molecular Biology and Evolution 30 : 772 – 780 . Google Scholar Crossref Search ADS PubMed WorldCat Katz-Downie DS , Valiejo-Roman CM , Terentieva EI , Troitsky AV , Pimenov MG , Lee B-Y , Downie SR . 1999 . Towards a molecular phylogeny of Apiaceae subfamily Apioideae: additional information from nuclear ribosomal DNA ITS sequences . Plant Systematics and Evolution 216 : 167 – 195 . Google Scholar Crossref Search ADS WorldCat Kljuykov EV . 1980 . Monographic review of the genus Elaeosticta Fenzl (Umbelliferae - Apioideae) . D.Sc. thesis, Moscow State University , Moscow [in Russian]. Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Kljuykov EV . 1985a . Taxonomic position of the near eastern species of the genus Scaligeria Umbelliferae Apioideae described by G . Post . Bulletin of Moscow Society of Naturalists. Biological Series 90 : 100 – 104 . OpenURL Placeholder Text WorldCat Kljuykov EV . 1985b . Note on Muretia amplifolia Boiss. et Hausskn. and the genus Hellenocarum Wolff (Umbelliferae-Apioideae) . Biologicheskie Nauki (Scientific Essays of Higher Education, Moscow) 8 : 60 – 63 . OpenURL Placeholder Text WorldCat Kljuykov EV . 1988 . A survey of the genus Bunium L. Revision of the generic system . Bulletin of Moscow Society of Naturalists . Biological Series 93 : 76 – 88 [in Russian]. OpenURL Placeholder Text WorldCat Kljuykov EV , Pimenov MG , Tikhomirov VN . 1976 . Elaeosticta Fenzl, a self-contained genus of the family Umbelliferae, distinct from Scaligeria DC . Bulletin of Moscow Society of Naturalists. Biological Series 81 : 83 – 94 [in Russian]. OpenURL Placeholder Text WorldCat Kljuykov EV , Zakharova EA , Petrova SE , Tilney PM . 2014 . On the unusual structure of the monocotylar embryo and seedling of Acronema commutatum H. Wolff (Apiaceae) and related species . Plant Diversity and Evolution 131 : 53 – 62 . Google Scholar Crossref Search ADS WorldCat Korovin EP . 1928 . Le genre Scaligeria D.C. (Umbelliferae) et sa philogénie. Essai d’application de l’écologie à la philogénie des petites unites sistématiques . Trudy Sredneasiatskogo Universiteta, ser. VIII-b Bot . 2 : 1 – 92 . OpenURL Placeholder Text WorldCat Koso-Poljansky BM . 1916 . Sciadophytorum systematis lineamenta . Bulletin de la Société Impériale des Naturalistes (Moscou) 29 : 93 – 222 . OpenURL Placeholder Text WorldCat Kudryashov LV . 1964 . The origin of monocotyly (Helobiae as an example) . Botanicheskii Zhurnal 49 : 473 – 486 . OpenURL Placeholder Text WorldCat Kumazawa M . 1970 . On the pleiocotyly in the genus Pittosporum. A preliminary note . The Botanical Magazine [Shokubutsu-gaku zasshi]. Tokyo 83 : 119 – 124 . Google Scholar Crossref Search ADS WorldCat Liu C-M , Johnson S , Gregorio SD , Wang TL . 1999 . Single cotyledon (sic) mutants of pea and their significance in understanding plant embryo development . Developmental Genetics 25 : 11 – 22 . Google Scholar Crossref Search ADS WorldCat Maddison WP , Maddison DR . 2010 . Mesquite: a modular system for evolutionary analysis, version 2.74 . Vancouver : University of British Columbia & Oregon State University . Available at: http://mesquiteproject.org. Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Magee AR , Calviño CI , Liu M , Downie SR , Tilney PM , van Wyk B-E . 2010 . New tribal delimitations for the early diverging lineages of Apiaceae subfamily Apioideae . Taxon 59 : 567 – 580 . Google Scholar Crossref Search ADS WorldCat Meusel H , Jäger E , Weinert E . 1965 . Vergleichende Chorologie der zentraleuropäischen Flora , Vol. 2 . Jena : Gustav Fischer Verlag . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Mogensen HL . 1970 . Syncotyly in Quercus arizonica . American Journal of Botany 57 : 1207 – 1210 . Google Scholar Crossref Search ADS WorldCat Mukherjee PK , Constance L . 1993 . Umbelliferae (Apiaceae) of India . New Delhi : Oxford & IBH Publishing Co. PVT. LTD . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Nylander JAA . 2004 . MrModeltest 2.3. Program distributed by the author . Evolutionary Biology Centre, Uppsala University . Available at: https://github.com/nylander/MrModeltest2. Accessed 26 January 2018 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Ovchinnikov PN . 1971 . Flora i rastitel‘nost ushchel’ya reki Varzob . Leningrad : Nauka , 396 – 449 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Papini A , Banci F , Nardi E . 2007 . Molecular evidence of polyphyletism in the plant genus Carum L . (Apiaceae) . Genetics and Molecular Biology 30 : 475 – 482 . Google Scholar Crossref Search ADS WorldCat Petrova SE . 2016 . Umbelliferae of Central Russia: biomorphological analysis . Moscow : MAKS Press . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Petrova SE , Kljuykov EV , Zakharova EA . 2016 . On the peculiarities of seedling structure in some tuberous pseudomonocotyledonous and dicotyledonous Umbelliferae . Botanicheskii Zhurnal 101 : 396 – 415 [in Russian]. OpenURL Placeholder Text WorldCat Pimenov MG , Kljuykov EV . 1980 . Notes on Muretia and Stefanoffia . Notes from the Royal Botanic Garden, Edinburgh 38 : 267 – 272 . OpenURL Placeholder Text WorldCat Pimenov MG , Kljuykov EV . 1987 . Neoconopodium—a new genus of the Umbelliferae from the Himalaya . Feddes Repertorium 98 : 373 – 378 . Google Scholar Crossref Search ADS WorldCat Pimenov MG , Kljuykov EV . 2002 . Umbelliferae of Kirghizia . Moscow : KMK . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Pimenov MG , Kljuykov EV , Teriokhin AT , Deviatkova GN . 1981 . The delimitation of the genera of the geophilic Umbelliferae of the Middle Asia by the methods of multivariate statistics . Botanicheskii Zhurnal 66 : 328 – 340 . OpenURL Placeholder Text WorldCat Pimenov MG , Leonov MV . 1993 . The genera of Umbelliferae. A nomenclator . Kew : Royal Botanic Gardens . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC PlantInvasive-Kruger [online] . Available at: http://publish.plantnet-project.org/project/plantinvasivekruger. Accessed 20 October 2018 . Plunkett GM , Chandler GT , Lowry II PP , Pinney SM , Sprenkle TS , van Wyk B-E , Tilney PM . 2004 . Recent advances in understanding Apiales and a revised classification . South African Journal of Botany 70 : 371 – 381 . Google Scholar Crossref Search ADS WorldCat Plunkett GM , Pimenov MG , Reduron JP , Kljuykov EV , Lee BY , van Wyk B-E , Tilney PM , Watson MF , Ostroumova TA , Spalik K , Hart JM , Henwood MJ , Webb CJ , Pu FT , Mitchell AD , Muckensturm B . 2019 . Apiaceae. In: Kubitzski K , ed. The families and genera of vascular plants , Vol. XV . Berlin : Springer , 9 – 206 . Google Scholar Crossref Search ADS Google Scholar Google Preview WorldCat COPAC Popov MG . 1927 . Osnovnye cherty istorii i razvitija flory Srednej Azii [The main features of history and development of the Central Asian flora] . Bulleten’ Sredneasiatskogo Universiteta 5 : 1 – 53 . OpenURL Placeholder Text WorldCat Post GE . 1888 . Diagnoses plantarum novarum orientalium . Journal of the Linnean Society 24 : 419 – 440 . OpenURL Placeholder Text WorldCat Ronquist F , Teslenko M , van der Mark P , Ayres DL , Darling A , Höhna S , Larget B , Liu L , Suchard MA , Huelsenbeck JP . 2012 . MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space . Systematic Biology 61 : 539 – 542 . Google Scholar Crossref Search ADS PubMed WorldCat Saarela JM , Rai HS , Doyle JA , Endress PK , Mathews S , Marchant AD , Briggs BG , Graham SW . 2007 . Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree . Nature 446 : 312 – 315 . Google Scholar Crossref Search ADS PubMed WorldCat Sargant E . 1902 . The origin of the seed-leaf in monocotyledons . New Phytologist 1 : 107 – 113 . Google Scholar Crossref Search ADS WorldCat Sargant E . 1903 . A theory of the origin of monocotyledons . Annals of Botany 17 : 1 – 92 . Google Scholar Crossref Search ADS WorldCat Schmid B . 1902 . Beitrage zur Embryo-entwickelung einiger Dicotylen . Botanische Zeitung 60 : 207 – 230 . OpenURL Placeholder Text WorldCat Silvestre S . 1972 . Estudio taxonomico de los generos Conopodium Koch y Bunium L. en la Peninsula Iberica. I. Parte experimental . Lagascalia 2 : 143 – 173 . OpenURL Placeholder Text WorldCat Sokoloff DD , Remizowa MV , Conran JG , Macfarlane TD , Ramsay MM , Rudall PJ . 2014 . Embryo and seedling morphology in Trithuria lanterna (Hydatellaceae, Nymphaeales): new data for infrafamilial systematics and a novel type of syncotyly . Botanical Journal of the Linnean Society 174 : 551 – 573 . Google Scholar Crossref Search ADS WorldCat Sokoloff DD , Remizowa MV , Macfarlane TD , Tuckett RE , Ramsay MM , Beer AS , Yadav SR , Rudall PJ . 2008 . Seedling diversity in Hydatellaceae: implications for the evolution of angiosperm cotyledons . Annals of Botany 101 : 153 – 164 . Google Scholar Crossref Search ADS PubMed WorldCat Sokoloff DD , Remizowa MV , Timonin AC , Oskolski AA , Nuraliev MS . 2018 . Types of organ fusion in angiosperm flowers (with examples from Chloranthaceae, Araliaceae and monocots) . Biologia Serbica 40 : 16 – 46 . OpenURL Placeholder Text WorldCat Spalik K , Downie SR . 2001 . The utility of morphological characters for inferring phylogeny in Scandiceae subtribe Scandicinae (Apiaceae) . Annals of the Missouri Botanical Garden 88 : 270 – 301 . Google Scholar Crossref Search ADS WorldCat Spalik K , Frankiewicz K , Oskolski AA , Banasiak Ł . 2017 . Secondary woodiness in umbellifer subfamily Apioideae: a preliminary survey. In: Oskolski A , Nuraliev M , Tilney P , eds. IX Apiales Symposium Abstract Book . 31 July—2 August 2017 , Guangzhou, China , 39 . Spalik K , Piwczyński M , Danderson CA , Kurzyna-Młynik R , Bone TS , Downie SR . 2010 . Amphitropic amphiantarctic disjunctions in Apiaceae subfamily Apioideae . Journal of Biogeography 37 : 1977 – 1994 . OpenURL Placeholder Text WorldCat Spalik K , Wojewódzka A , Downie SR . 2001 . The evolution of fruit in Scandiceae subtribe Scandicinae (Apiaceae) . Canadian Journal of Botany 79 : 1358 – 1374 . Google Scholar Crossref Search ADS WorldCat Swamy BGL . 1949 . Further contributions to the morphology of the Degeneriaceae . Journal of the Arnold Arboretum 30 : 10 – 38 . OpenURL Placeholder Text WorldCat Tank DC , Donoghue MJ . 2010 . Phylogeny and phylogenetic nomenclature of the Campanulidae based on an expanded sample of genes and taxa . Systematic Botany 35 : 425 – 441 . Google Scholar Crossref Search ADS WorldCat Thompson K . 1988 . Cotyledon number in Conopodium majus (Gouan) Loret . Watsonia 17 : 95 – 96 . OpenURL Placeholder Text WorldCat Tillich H-J , Tuckett R , Facher E . 2007 . Do Hydatellaceae belong to the monocotyledons or basal angiosperms? Evidence from seedling morphology . Willdenowia 37 : 399 – 406 . OpenURL Placeholder Text WorldCat Tilney PM , van Wyk B-E , Downie SR , Calviño CI . 2009 . Phylogenetic relationships in the genus Lichtensteinia (Apiaceae) based on morphological, anatomical and DNA sequence data . South African Journal of Botany 75 : 64 – 82 . Google Scholar Crossref Search ADS WorldCat Titova GE . 2000 . On the nature of pseudomonocotyly in flowering plants . Botanicheskii Zhurnal 85 : 76 – 91 [in Russian]. OpenURL Placeholder Text WorldCat Titova GE . 2012 . Germination biology of Pinguicula vulgaris (Lentibulariaceae) . Botanicheskii Zhurnal 97 : 1137 – 1162 . OpenURL Placeholder Text WorldCat Treviranus GR , Treviranus LC . 1821 . Vermischte Schriften anatomischen und physiolologischen Inhalts 4 . Bremen : J.G. Heyse . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Treviranus LC . 1831 . Symbolarum phytologicarum, quibus res herbaria illustratus, fasciculus I . Göttingen : Dieterich . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC van Cotthem W. 1981. Syncotyly, pseudomonocotyly, schizocotyly and pleiocotyly within some dicotyledons. Biologisch Jaarboek. Dodonaea 49: 166–183. Valiejo-Roman CM , Terentieva EI , Samigullin TH , Pimenov MG . 2002 . Relationships among genera in Saniculoideae and selected Apioideae (Umbelliferae) inferred from nrITS sequences . Taxon 51 : 91 – 101 . Google Scholar Crossref Search ADS WorldCat Vasilchenko IT . 1941 . On the phylogenetic meaning of germination morphology in Apiaceae (Umbelliferae) . Sovetskaya Botanika 3 : 30 – 41 [in Russian]. OpenURL Placeholder Text WorldCat Weisse A . 1930 . Blattstellungsstudien an Sämlingen abnorm keimender Dikotylen . Beträge zur Biologie der Pflanzen 18 : 17 – 80 . OpenURL Placeholder Text WorldCat Wolff H . 1927 . Umbelliferae–Apioideae–Ammineae–Carinae, Ammineae novemjugatae et genuinae. In: Engler A , ed. Das Pflanzenreich , Vol. 4 (90). Leipzig, Berlin : Engelmann , 1 – 398 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC van Wyk B-E , Tilney PM . 2004 . Diversity of Apiaceae in Africa . South African Journal of Botany 70 : 433 – 445 . Google Scholar Crossref Search ADS WorldCat Zakharova EA . 2017 . Critical analysis of the genus Carum L. (Umbelliferae) in the light of morphological and molecular data . D.Sc. thesis, Moscow State University , Moscow [in Russian]. Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Zakharova EA , Degtjareva GV , Kljuykov EV , Tilney PM . 2014 . The taxonomic affinity of Carum piovanii Chiov. and some Bunium species (Apiaceae) . South African Journal of Botany 94 : 122 – 128 . Google Scholar Crossref Search ADS WorldCat Zakharova EA , Degtjareva GV , Pimenov MG . 2012 . Redefined generic limits of Carum (Umbelliferae, Apioideae) and new systematic placement of some of its taxa . Willdenowia 42 : 149 – 168 . Google Scholar Crossref Search ADS WorldCat Zakharova EA , Kljuykov EV , Degtjareva GV , Samigullin T , Ukrainskaya UA , Downie SR . 2016 . A taxonomic study of the genus Hellenocarum H.Wolff (Umbelliferae-Apioideae) based on morphology, fruit anatomy, and molecular data . Turkish Journal of Botany 40 : 176 – 193 . Google Scholar Crossref Search ADS WorldCat Zhou J , Gong X , Downie SR , Peng H . 2009 . Towards a more robust molecular phylogeny of Chinese Apiaceae subfamily Apioideae: additional evidence from nrDNA ITS and cpDNA intron (rpl16 and rps16) sequences . Molecular Phylogenetics and Evolution 53 : 56 – 68 . Google Scholar Crossref Search ADS PubMed WorldCat Zhou J , Peng H , Downie SR , Liu Z-W , Gong X . 2008 . A molecular phylogeny of Chinese Apiaceae subfamily Apioideae inferred from nuclear ribosomal DNA internal transcribed spacer sequences . Taxon 57 : 402 – 416 . OpenURL Placeholder Text WorldCat © 2019 The Linnean Society of London, Botanical Journal of the Linnean Society This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - A taxonomic survey of monocotylar Apiaceae and the implications of their morphological diversity for their systematics and evolution
JF - Botanical Journal of the Linnean Society
DO - 10.1093/botlinnean/boz095
DA - 2020-02-27
UR - https://www.deepdyve.com/lp/oxford-university-press/a-taxonomic-survey-of-monocotylar-apiaceae-and-the-implications-of-GH0eIbje0c
SP - 449
VL - 192
IS - 3
DP - DeepDyve
ER -