Abstract
Cynoglossinae with ca. 200 spp. is one of the taxonomically most challenging subtribes of tribe Cynoglosseae with regard to generic delimitations. Here, we present a phylogenetic analysis based on nuclear ITS and cpDNA trnL-F and rps16 sequences of 270 accessions including 102 newly sequenced ones, representing all currently recognized genera of Cynoglossinae to clarify relationships among Cynoglossum and allied genera. We conducted maximum likelihood, maximum parsimony, and Bayesian inference analyses on separate and combined datasets. Cynoglossinae is recovered as a monophylum of closely related genera. Subtribe Cynoglossinae falls into three major groups: (1) Clade I including Microparacaryum spp., (2) Clade II comprising two species of Lindelofia, several Cynoglossum and Paracynoglossum spp., and (3) a larger clade (Clades III + IV) consisting of Solenanthus, Rindera, Trachelanthus, Paracaryum, Pardoglossum, Mattiastrum, and the remainder of Cynoglossum. None of the genera were monophyletic in the combined nuclear-plastid and nuclear datasets, except for Microparacaryum. A close relationship between Solenanthus apenninus and Cynoglossum officinale is shown, which suggests transferring S. apenninus to Cynoglossum. Moreover, Pardoglossum atlanticum, the type of the genus, is placed within Mediterranean Cynoglossum corroborating its synonymy under Cynoglossum. Lindelofia olgae is distantly related to the type of the genus (L. longiflora), but more closely connected with Solenanthus core-group. The majority of species currently recognized as members of Rindera do not form a clade with the type of the genus (R. tetraspis). The genus Paracaryum as currently circumscribed is paraphyletic and includes some species of Mattiastrum and Rindera.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Barbier E, Mathez J (1973) Contribution à l’étude des Cynoglossées (Boraginacées): Pardoglossum, genre nouveau du Bassin méditerranéen occidental. Candollea 28:281–323
Bigazzi M, Nardi E, Selvi F (2006) Palynological contribution to the systematics of Rindera and the allied genera Paracaryum and Solenanthus (Boraginaceae–Cynoglosseae). Willdenowia 36:37–46. https://doi.org/10.3372/wi.36.36103
Boissier E (1879) Flora orientalis, vol. 4. H Georg, Bibliopolam, Genevae et Basileae
Brand A (1915) Neue Borraginaceen-Studien. Feddes Repert Spec Nov Regni Veg 14:146–156. https://doi.org/10.1002/fedr.19150141004
Brand A (1921) Borraginaceae–Borraginoideae–Cynoglosseae. In: Engler A (ed) Das Pflanzenreich IV.252. W Engelmann, Leipzig, pp 54–66
Buys MH, Hilger HH (2003) Boraginaceae cymes are exclusively scorpioid and not helicoid. Taxon 52:719–724. https://doi.org/10.2307/3647346
Chacón J, Luebert F, Hilger HH, Ovchinnikova S, Selvi F, Cecchi L, Guilliams CM, Hasenstab-Lehman KE, Sutorý K, Simpson MG, Weigend M (2016) The borage family (Boraginaceae s.str.): a revised infrafamilial classification based on new phylogenetic evidence, with emphasis on the placement of some enigmatic genera. Taxon 65:523–546. https://doi.org/10.12705/653.6
Chacón J, Luebert F, Weigend M (2017) Biogeographic events are not correlated with diaspore dispersal modes in Boraginaceae. Front Ecol Evol 5:26. https://doi.org/10.3389/fevo.2017.00026
Clarke GCS, Chanda S, Sahay S (1979) Pollen morphology in the genus Pardoglossum (Boraginaceae) with some observations on heterocolpate pollen. Rev Palaeobot Palynol 28:301–309. https://doi.org/10.1016/0034-6667(79)90030-7
Cohen JI (2015) Adelinia and Andersonglossum (Boraginaceae), two new genera from New World species of Cynoglossum. Syst Bot 40:611–619. https://doi.org/10.1600/036364415X68838
Costea M, Stefanović S (2010) Evolutionary history and taxonomy of the Cuscuta umbellata complex (Convolvulaceae): evidence of extensive hybridization from discordant nuclear and plastid phylogenies. Taxon 59:1783–1800. https://doi.org/10.2307/41059873
Cunningham CW (1997) Can three incongruence tests predict when data should be combined? Molec Biol Evol 14:733–740. https://doi.org/10.1093/oxfordjournals.molbev.a025813
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Meth 9:772. https://doi.org/10.1038/nmeth.2109
Davis PH (ed) (1979) Flora of Turkey and the East Aegean Islands, vol. 6. Edinburgh University Press, Edinburgh, pp 237–437
Dimon RJ, Renner MAM (2017) A new Cynoglossum species, and transfers to Hackelia in eastern Australian Boraginaceae. Austral Syst Bot 30:113–123. https://doi.org/10.1071/SB17004
Farris J, Kallersjo M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319. https://doi.org/10.1111/j.1096-0031.1994.tb00181.x
Ferguson LF (1972) Solenanthus. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea: Diapensiaceae to Myoporaceae, vol. 3. Cambridge University Press, Cambridge, p 121
Greuter W (ed) (1981) Med-checklist Notulae, 3. Willdenowia 11:23–43
Hilger HH, Balzer M, Frey W, Podlech D (1985) Heteromericarpy and fruit polymorphism in Microparacaryum, gen. nov. (Boraginaceae). Pl Syst Evol 148:291–312
Hilger HH, Greuter W, Stier V (2015) Taxa and names in Cynoglossum sensu lato (Boraginaceae, Cynoglosseae): an annotated, synonymic inventory, with links to the protologues and mention of original material. Biodivers Data J 3:e4831. https://doi.org/10.3897/BDJ.3.e4831
Holstein N, Chacón J, Hilger HH, Weigend M (2016) No longer shipwrecked-Selkirkia (Boraginaceae) back on the mainland with generic rearrangements in South American “Omphalodes” based on molecular data. Phytotaxa 270:231–251. https://doi.org/10.11646/phytotaxa.270.4.1
Iv APG (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20. https://doi.org/10.1111/boj.12385
Johnston IM (1924) Studies in the Boraginaceae III. 1. The New World genera of the Boraginoideae. Contr Gray Herb 73:42–78
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molec Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Kazmi SMA (1971) A revision of the Boraginaceae of West Pakistan and Kashmir. J Arnold Arbor 52:110–136
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kellogg EA, Appels R, Mason-Gamer RJ (1996) When genes tell different stories: the diploid genera of Triticeae (Gramineae). Syst Bot 21:321–347. https://doi.org/10.2307/2419662
Khatamsaz M (2002) Boraginaceae. In: Assadi M, Maassoumi AA, Khatamsaz M, Mozaffarian VA (eds) Flora of Iran, vol. 39. Research Institute of Forests and Rangelands, Tehran, pp 1–504 (In Persian)
Khoshsokhan M, Mozaffar M, Kazempour Osaloo S, Oskoueiyan R, Naderi Saffar K, Amirahmadi A (2013) Tribe Eritrichieae (Boraginaceae s.str.) in West Asia: a molecular phylogenetic perspective. Pl Syst Evol 299:197–208. https://doi.org/10.1007/s00606-012-0715-4
Luebert F, Cecchi L, Frohlich MW, Gottschling M, Guilliams CM, Hasenstab-Lehman KE, Hilger HH, Miller JS, Mittelbach M, Nazaire M, Nepi M, Nocentini D, Ober D, Olmstead RG, Selvi F, Simpson MG, Sutorý K, Valdés B, Walden GK, Weigend M (2016) Familial classification of the Boraginales. Taxon 65:502–522. https://doi.org/10.12705/653.5
Maddison WP (1997) Gene trees in species trees. Syst Biol 46:523–536. https://doi.org/10.1093/sysbio/46.3.523
Mill RR, Miller AG (1984) Studies in the flora of Arabia, IX: a synopsis of Paracynoglossum (Boraginaceae). Notes Roy Bot Gard Edinburgh 41:473–482
Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Amer J Bot 83:383–404. https://doi.org/10.2307/2446172
Oxelman B, Lidén M, Berglund D (1997) Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Pl Syst Evol 206:393–410
Podlech D, Anders O (1977) Florula des Wakhan (Nordost-Afghanistan). Mitt Bot Staatssamml München 13:361–502
Podlech D, Bader O (1974) Chromosomenstadien an afghanischen Pflanzen II. Mitt Bot Staatssamml München 11:457–488
Popov MG (1953) Boraginaceae. In: Shishkin BK (ed) Flora of the U.S.S.R: Tubiflorae, vol. 19. Izdatel’stvo Akademii Nauk SSSR, Moscow, pp 97–691, 703–718
Riedl H (1963) Borraginaceae. In: Køie M, Rechinger KH (eds) Symbolae Afghanicae V, enumeration and descriptions of the plants collected by L. Edelberg and M. Køie on “The third Danish expedition to Central Asia” and by W Koelz and others in Afghanistan, vol. 13. Enjar Munksgaard, København, pp 205–216
Riedl H (1967) Boraginaceae. In: Rechinger KH (ed) Flora Iranica, vol. 48. Akademische Druck- und Verlagsanstalt, Graz, pp 1–281
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. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rothfels CJ, Pryer KM, Li FW (2017) Next-generation polyploid phylogenetics: rapid resolution of hybrid polyploid complexes using PacBio single-molecule sequencing. New Phytol 213:413–429. https://doi.org/10.1111/nph.14111
Salmaki Y, Zarre S, Ryding O, Lindqvist C, Scheunert A, Bräuchler C, Heubl G (2012) Phylogeny of the tribe Phlomideae (Lamioideae: Lamiaceae) with special focus on Eremostachys and Phlomoides: new insights from nuclear and chloroplast sequences. Taxon 61:161–179. https://doi.org/10.1002/tax.611012
Salmaki Y, Zarre S, Ryding O, Lindqvist C, Bräuchler C, Heubl G, Barber J, Bendiksby M (2013) Molecular phylogeny of tribe Stachydeae (Lamiaceae subfamily Lamioideae). Molec Phylogen Evol 69:535–551. https://doi.org/10.1016/j.ympev.2013.07.024
Salmaki Y, Kattari S, Heubl G, Bräuchler C (2016) Phylogeny of non-monophyletic Teucrium (Lamiaceae: Ajugoideae): implications for character evolution and taxonomy. Taxon 65:805–822. https://doi.org/10.12705/654.8
Sang T, Zhong Y (2000) Testing hybridization hypotheses based on incongruent gene trees. Syst Biol 49:422–434. https://doi.org/10.1080/10635159950127321
Seelanan T, Schnabel A, Wendel JF (1997) Congruence and consensus in the cotton tribe (Malvaceae). Syst Bot 22:259–290. https://doi.org/10.2307/2419457
Selvi F, Sutorý K (2012) A synopsis of the genus Cynoglossum (Boraginaceae–Cynoglosseae) in Italy. Pl Biosystems 146:461–479. https://doi.org/10.1080/11263504.2012.667842
Selvi F, Coppi A, Cecchi L (2011) High epizoochorous specialization and low DNA sequence divergence in Mediterranean Cynoglossum (Boraginaceae): evidence from fruit traits and ITS region. Taxon 60:969–985. https://doi.org/10.1002/tax.604003
Soltis DE, Kuzoff RK (1995) Discordance between nuclear and chloroplast phylogenies in Heuchera group (Saxifragaceae). Evolution 49:727–742. https://doi.org/10.2307/2410326
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Sutorý K (2010) Oncaglossum, a new genus of the Boraginaceae, tribe Cynoglosseae, from Mexico. Novon 20:463–469. https://doi.org/10.3417/2008059
Sutorý K (2019) Microparacaryum longipedicellatum (Boraginaceae)—a new combination. Phytotaxa 391:233–239. https://doi.org/10.11646/phytotaxa.391.3.7
Swofford DL (2019) PAUP*: Phylogenetic analysis using parsimony and other methods, Version 4.0a165. Sinauer Associates, Sunderland
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109. https://doi.org/10.1007/bf00037152
Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) (1972) Flora Europaea: Diapensiaceae to Myoporaceae, vol. 3. Cambridge University Press, Cambridge, pp 83–122
Verdcourt B (1991) Boraginaceae. In: Polhill RM (ed) Flora of tropical East Africa. Royal Botanic Gardens, Kew, pp 1–124
Weigend M, Luebert F, Selvi F, Brokamp G, Hilger HH (2013) Multiple origins for Hounds tongues (Cynoglossum L.) and Navel seeds (Omphalodes Mill.)—the phylogeny of the borage family (Boraginaceae s.str.). Molec Phylogen Evol 68:604–618. https://doi.org/10.1016/j.ympev.2013.04.009
Weigend M, Selvi F, Thomas DC, Hilger HH (2016) Boraginaceae. In: Kadereit JW, Bittrich V (eds) Flowering plants: Eudicots; Aquifoliales, Boraginales, Bruniales, Dipsacales, Escalloniales, Garryales, Paracryphiales, Solanales (except Convolvulaceae), Icacinaceae, Metteniusaceae, Vahliaceae, vol. 14. The families and genera of vascular plants. Springer, Cham, pp 41–102. https://doi.org/10.1007/978-3-319-28534-4_5
White TJ, Bruns T, Lee S, Taylor J (1990) Amplifications and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Acknowledgements
The corresponding author is grateful to “Alexander von Humboldt Stiftung” for partial financial support as well as the Research Council, University of Tehran. We confirm that the manuscript has been read and approved by all named authors. We also confirm that the order of authors listed in the manuscript has been checked by all co-authors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights statement
This work did not involve animal and human participants as subjects.
Ethical statement
As the corresponding author, I am prepared to present further documents of compliance with ethical standards.
Additional information
Handling Editor: Marcus Koch.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Information on Electronic Supplementary Material
Information on Electronic Supplementary Material
Online Resource 1. Species included in the phylogenetic analyses of subtribe Cynoglossinae with their corresponding geographic origins, herbarium vouchers, DNA, and GenBank accession numbers.
Online Resource 2. Sequence alignment of combined datasets (ITS + trnL-F + rps16).
Rights and permissions
About this article
Cite this article
Pourghorban, Z., Salmaki, Y. & Weigend, M. Phylogenetic relationships within the subtribe Cynoglossinae (Cynoglossoideae: Boraginaceae): new insights from nuclear and plastid DNA sequence data. Plant Syst Evol 306, 45 (2020). https://doi.org/10.1007/s00606-020-01671-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-020-01671-x