ArticlePDF Available

Phylogeny of non-monophyletic Teucrium (Lamiaceae: Ajugoideae): Implications for character evolution and taxonomy

Authors:

Abstract

Teucrium, with an almost cosmopolitan distribution, comprises about 250 species and is the second-largest genus of subfamily Ajugoideae (Lamiaceae). Phylogenetic studies were conducted using nuclear ribosomal DNA (ITS) and chloroplast (ndhF gene, trnL-F region) DNA sequence data from 101 taxa to estimate phylogenetic relationships among Teucrium and its closest allies. We conclude that: (1) Teucridium, Spartothamnella and Oncinocalyx are nested within Teucrium, thus rendering the latter paraphyletic; (2) previously proposed taxonomic classification systems for Teucrium mostly are not supported by our phylogenetic results; (3) Rubiteucris and Schnabelia appear to be sister to Teucrium. Our results indicate that, among various morphological characters, the calyx shape is diagnostic for different clades within Teucrium. Based on the cladograms derived in this study, the pattern of karyotype evolution suggests that switches in ploidy level are common in at least two groups. Adaptations to drought stress and the regional establishment of Mediterranean climates obviously facilitated speciation and the spread of the genus. Molecular dating analyses indicate diversification of Teucrium at the middle/late Miocene boundary, correlated with Tertiary climatic and tectonic changes.
... ex Griff., Ombrocharis Hand.-Mazz., Peronema Jack, Petraeovitex Oliv., and Tectona L. that were treated as incertae sedis, the remaining 226 genera were assigned to seven subfamilies: Ajugoideae, Lamioideae, Nepetoideae, Prostantheroideae, Scutellarioideae, Symphorematoideae, and Viticoideae [1]. Since the publication of this classification [1], numerous molecular phylogenetic studies have been carried out to explore the relationships at the subfamilial [19], tribal [23][24][25][26][27][28][29][30][31][32][33], or generic [34][35][36][37][38][39][40][41][42][43][44][45][46][47][48][49][50] level. However, relationships among four subfamilies (Nepetoideae, Tectonoideae, Premnoideae, and Ajugoideae) remain unresolved and those among some tribes were also unclear in those studies. ...
... Ajugoideae are the third-largest subfamily within Lamiaceae and contain about 770 species in 23 genera [19,48,54,118,119] distributed worldwide but most common in tropical regions [1]. A possible synapomorphy of Ajugoideae may be pollen with branched to granular columellae [9]. ...
... Teucrium is the largest genus in this tribe. A previous phylogenetic study [48] suggested the inclusion of Oncinocalyx F. Muell., Spartothamnella Briq., and Teucridium Hook.f. in Teucrium, and this treatment was confirmed by Xiang et al. [54]. Although both Rubiteucris and Schnabelia are small genera, the taxonomy and systematic relationships of Rubiteucris and Schnabelia were not sufficiently resolved until recent molecular phylogenetic studies based on a broad sampling [48,54]. ...
Article
Full-text available
Background: A robust molecular phylogeny is fundamental for developing a stable classification and providing a solid framework to understand patterns of diversification, historical biogeography, and character evolution. As the sixth largest angiosperm family, Lamiaceae, or the mint family, consitutes a major source of aromatic oil, wood, ornamentals, and culinary and medicinal herbs, making it an exceptionally important group ecologically, ethnobotanically, and floristically. The lack of a reliable phylogenetic framework for this family has thus far hindered broad-scale biogeographic studies and our comprehension of diversification. Although significant progress has been made towards clarifying Lamiaceae relationships during the past three decades, the resolution of a phylogenetic backbone at the tribal level has remained one of the greatest challenges due to limited availability of genetic data. Results: We performed phylogenetic analyses of Lamiaceae to infer relationships at the tribal level using 79 protein-coding plastid genes from 175 accessions representing 170 taxa, 79 genera, and all 12 subfamilies. Both maximum likelihood and Bayesian analyses yielded a more robust phylogenetic hypothesis relative to previous studies and supported the monophyly of all 12 subfamilies, and a classification for 22 tribes, three of which are newly recognized in this study. As a consequence, we propose an updated phylogenetically informed tribal classification for Lamiaceae that is supplemented with a detailed summary of taxonomic history, generic and species diversity, morphology, synapomorphies, and distribution for each subfamily and tribe. Conclusions: Increased taxon sampling conjoined with phylogenetic analyses based on plastome sequences has provided robust support at both deep and shallow nodes and offers new insights into the phylogenetic relationships among tribes and subfamilies of Lamiaceae. This robust phylogenetic backbone of Lamiaceae will serve as a framework for future studies on mint classification, biogeography, character evolution, and diversification.
... For four clades in which phylogenetic data exist but were either without or with only a parsimonybased ancestral range reconstruction (Teucrium L. s.l.: Salmaki et al., 2016;Leucadeae: Scheen & Albert, 2009;Mentha: Bunsawat et al., 2004;and Stachydeae: Roy et al., 2013), we reanalysed the available aligned DNA matrices from these studies, assigning priority to nuclear DNA matrices, when available, and ignoring plastid data if both were available. Matrices were analysed using RAxML (Stamatakis, 2014) under GTR + Γ with 20 search replicates for the best tree. ...
... The latter young age is almost certainly due to constraining the age of Lamiaceae based on the young stem age for the family given in Martínez-Millán (2010). In Ajugoideae, Salmaki et al. (2016) estimated the crown age of Clades II-IV of Xiang et al. (2018) to be c. 16 Myr, considerably younger than our estimate of 45 Myr for this node. ...
... 16 Myr, considerably younger than our estimate of 45 Myr for this node. Although the methods of Salmaki et al. (2016) are somewhat unclear, they may have estimated these divergence times based on secondary calibrations from Roy & Lindqvist (2015). Given the apparent disparity in ages recovered across previous studies, we hope that our list of vetted and conservatively assigned primary calibrations will aid in choosing a common set of fossils with which to calibrate phylogenetic trees. ...
Article
Lamiaceae are one of the largest and most economically important families of flowering plants. Despite focused study on relationships within subclades, higher-level relationships have been under-studied. Moreover, the herbaceous habit of much of the family has resulted in a poor fossil record and has hampered estimates of divergence times. Using a new dataset of five plastid loci from 178 members of Lamiaceae representing all subfamilies and nearly all tribes, we clarify major infrafamilial relationships and present a robust set of divergence times. We use this phylogenetic hypothesis as a platform to test previous hypotheses regarding the historical biogeography and evolution of major traits in the family. We confirm the placement of subfamily Nepetoideae, show continued uncertainty in the placement of subfamilies Ajugoideae and Premnoideae and highlight extreme discordance with recent results from nuclear data. Lamiaceae originated during the Late Cretaceous as woody plants with nutlet fruits and four stamens, probably in South-East Asia. Most subfamilies diverged during the Eocene, perhaps facilitated by climatic cooling. Our results provide a valuable set of secondary dates for Lamiaceae and highlight the need for focused study of subfamilies Callicarpoideae and Viticoideae. Our results also provide several hypotheses regarding trait or range-dependent diversification.
... DNA barcoding based on chloroplast DNA molecular markers is a promising method or technique for species and/or varieties' identification, generating a taxon-specific fingerprint that allows traceability. Furthermore, to estimate the phylogenetic relationships among members of Teucrium, a phylogenetic study has been performed using nuclear ribosomal (ITS region) and chloroplast DNA (ndhF gene, trnL-F region) for Teucrium flavum L., T. scorodonia L., and T. polium [39,40] and DNA sequence data from 101 Teucrium taxa [41]. Moreover, sequencing of the whole chloroplast DNA genome has been completed only for six Teucrium species, i.e., T. stocksianum Boiss. ...
Article
Full-text available
In the context of plant conservation and sustainable use of unique neglected and underutilized phytogenetic resources, this study focused on the Tunisian local endemic Teucrium luteum subsp. gabesianum (Lamiaceae). Using Geographical Information Systems and online databases, detailed taxon-specific ecological profiling was produced for the first time, which illustrated the temperature and climate conditions in its wild habitats and facilitated the investigation of how temperature affects its seed germination, thus making its cultivation in anthropogenic environments possible. Following the seed propagation first reported herein (77.5–81.25% at temperatures between 15 and 25 °C), species-specific in situ and ex situ conservation efforts or sustainable exploitation strategies can be enabled. This study also reported for the first time how chemical and integrated nutrient management (INM) fertilizers affect the growth and pilot cultivation of its seedlings (INM more advantageous). The firstly-reported herein DNA barcoding may enable its traceability, allowing future product design. The multidisciplinary approach followed has paved the way to bridge important research gaps hindering conservation efforts and/or the sustainable exploitation of this local Tunisian endemic plant to date. Based on the aforementioned results, the feasibility and readiness timescale for its sustainable exploitation was overviewed and re-evaluated herein, upgrading (>two-fold) its potential value for the medicinal-cosmetic, agro-alimentary, and ornamental-horticultural sectors.
... Obtained data based nrITS and trnL-F sequences supports the separation of sect. Teucrium presented by the previously above-mentioned studies (presented by Melnikov, 2014;Salmaki et al., 2016;Aksoy et al., 2020). Teucrium turcicum is a characteristic member of Fruticantia subgroup of sect. ...
... A main aim in systematic studies is to assess whether taxonomic classifications based on morphology are congruent with molecular phylogenetic findings (e.g., Cohen 2014;Weigend et al. 2014;Salmaki et al. 2016;Moharrek et al. 2017). ...
Article
The Irano-Turanian (I-T) bioregion harbours one of the Old world’s greatest repositories of botanical diversity; however, the diversification patterns and the phenotypic evolution of its flora are sorely understudied. The subtribe Cynoglossinae is characteristic of the western I-T bioregion, species–rich both in the desertic lowlands and the more mesic highlands of the Iranian plateau. About 70 species of Cynoglossinae are present in the Iranian plateau, 47 of which are endemic to the plateau.Herein, nuclear ITS and cpDNA rpl32-trnL and trnH–psbA sequences were used to investigate the molecular phylogeny, historical biogeography and ancestral character states of Cynoglossinae. Molecular dating and ancestral range reconstruction analyses indicated that the subtribe Cynoglossinae has initiated its diversification from the eastern part of the western I-T during the mid-Miocene, concomitantly with the uplift of the Pamir and Hindu Kush mountains. Moreover, from the Pliocene onwards the Afghan-India collision and extensive deformation of the Arabia-Eurasia convergence probably promoted allopatric speciation in Cynoglossinae via mostly vicariance events. Evolution of annuals with small nutlets from perennials with large nutlets was accompanied by mesic to desert habitats shifts. Herein, to explain distribution of Cynoglossinae in the western I-T, the congruence between cladogenetic, geological and palaeoclimatic events was investigated.
... Another difference was observed for the evolution grade concerning the two Teucrium species. In fact, as reported in literature (Salmaki et al., 2016), Teucrium polium should be more evolved than Teucrium chamaedrys but not according to the phytochemical evolution. ...
Article
In this work, the continuation of the study of the plant evolution based on phytochemistry was presented. Flavonoids were used to draw a Sporne evolution diagram of selected Lamiaceae taxa. From a phytochemical evolution standpoint, results showed similarities and differences with regard to the previous work on iridoids. In addition, analogies and diversities from the phylogenetic tree based on molecular and genetic data were evidenced. Findings suggest again the potentiality to further use phytochemical data for the evaluation of Lamiaceae evolution.
Article
Full-text available
Teucrium fruticans L. is a shrub in Lamiaceae that is native to Mediterranean countries where it is used in medicine ornamental gardens. Here, we report the complete chloroplast genome of T. fruticans which is 150,808 bp in length, with a pair of inverted repeat regions (IRs) (25,597 bp) separated by a large single-copy area (LSC) (82,634 bp) and a small single-copy area (SSC) (16,912 bp). The completed chloroplast genome of T. fruticans comprises 130 unique genes, including 86 protein-coding genes, 36 tRNA genes, and eight rRNA genes. The results of the phylogenetic analysis significantly supported the grouping of T. fruticans with nine Teucrium species. The complete chloroplast genome of T. fruticans can provide a powerful tool to accelerate breeding, biotechnological and phylogenetic study.
Article
Full-text available
Some plant traits may be legacies of coevolution with extinct megafauna. One example is the convergent evolution of "divaricate" cage architectures in many New Zealand lineages, interpreted as a response to recently-extinct flightless avian browsers whose ancestors arrived during the Paleogene. Although experiments have confirmed the divaricate habit deters extant browsers, its abundance on frosty, droughty sites appears consistent with an earlier interpretation as a response to cold, dry Plio-Pleistocene climates. We used 45 protein-coding sequences from plastid genomes to reconstruct the evolutionary history of the divaricate habit in extant New Zealand lineages. Our dated phylogeny of 215 species included 91% of New Zealand eudicot divaricate species. We show that 86% of extant divaricate plants diverged from non-divaricate sisters within the last 5 Ma, implicating Plio-Pleistocene climates in the proliferation of cage architectures in New Zealand. Our results, combined with other recent findings, are consistent with the synthetic hypothesis that the browser-deterrent effect of cage architectures was strongly selected only when Plio-Pleistocene climatic constraints prevented woody plants from quickly growing out of reach of browsers. This is consistent with the abundance of cage architectures in other regions where plant growth is restricted by aridity or short frost-free periods.
Article
A molecular phylogeny of Chloantheae (Lamiaceae) based on a three-marker chloroplast and nuclear DNA dataset was used to test the monophyly of Lachnostachys Hook., Newcastelia F.Muell. and Physopsis Turcz. A clade consisting of at least one species from each of these genera was recovered separately from the ‘core’ Lachnostachys, Newcastelia and Physopsis clades. The members of this composite clade are here transferred to the new genus, Apatelantha T.C.Wilson & M.J.Henwood, which can be recognised by a combination of the base of the style being glabrous or with only non-glandular trichomes (glandular trichomes lacking), apex of corolla lobes (when present) acute to obtuse (not extending into an apical protrusion) and thin-textured (not distinctively thickened), pherophylls subtending three flowers, and anther connectives glabrous (sessile glands absent). A description of the new genus, together with new combinations for five species of Apatelantha, and amended descriptions of Lachnostachys, Newcastelia and Physopsis, are provided. A new species, Newcastelia clavipetala T.C.Wilson & Radunz, is described and illustrated. A taxonomic key to genera of Chloantheae, and keys to species of Lachnostachys, Newcastelia, Physopsis and Apatelantha are provided.
Chapter
The generative morphology related with corolla and calyx construction, pollen, inflorescence type and nutlets are of great importance in Teucrium L. These characters are the basis for the classic systematic and recent classifications. Teucrium has a corolla usually 1-lipped or 2-lipped (bilabiate). Spartothamnella Briq., Oncinocalyx F. Muell., and Teucridium F. Hook, closely related to Teucrium, present a corolla 5-lobed in the upper half, lobes slighty spreading, 4 posterior ± similar, anterior lobe larger than the others and not concave. The calyx in these genera is actinomorphic. This is an exceptional corolla conformation in Teucrium and only found in these species. The main difference between Spartothamnella and Teucrium is that the former has drupaceous fruit and between Teucrium and Teucridium is the ovary form. Oncinocalyx differs from Teucrium in the conspicuously hooked calyx lobes. Teucrium Sections Pycnobotrys Benth., Stachyobotrys Benth., Scorodonia (Hill) Schreb., and Teucriopsis Benth., have weakly 2-lipped corolla and zygomorphic calyx. Species of section Teucrium have 1-lipped spurred corolla and actinomorphic calyx except for the Australian species with non-spurred corollas. Teucrium show a great diversity in floral phenotypic diversity and adaptive significance to pollination and dispersal. Functional redundancy is found in the gullet-shaped corollas with nectar guides and nototribic pollination of the sections Chamaedrys (Mill.) Kästner, lsotriodon Boiss., subsection Scordium (Mill.) Kästner, Montana Lazaro Ibiza and subsection Pumila (Lazaro Ibiza) Rivas Mart. Teucrium is the only genus within the sub family Ajugoideae with two derived pollen characteristics, granulate or verrucate sculpturing and operculate colpi and with a considerable variation in pollen sculpturing. Nototribic pollination of the gullet-shaped corollas with closed gullet mechanism (by a palate of hairs associated to a slight pouch in the corolla tube) are exclusive of the section Teucrium. The sternotribic pollination of the brush-shaped corollas closed by a tuft of hair in the entrance of the corolla tube (base of the anterior lobe), are specific of the ginodioecious species of section Polium (Mill.) Schreb. Resupinate flag-shaped corollas with sternotribic pollination is present in subsection Spinularia (Boiss.) Kästner and Stachyobotrys. The main dispersal modes in section Chamaedrys, lsotriodon and Polium is the semachory. Sections Teucrium and Teucriopsis are wind-dispersal by pogonospores, subsection Spinularia, section Scorodonia and Teucrium betonicum and Teucrium abutiloides L’Hér from section Teucriopsis are ballospores.
Article
Full-text available
ABSTRACT. Synopsis of the genus Teucrium L. (Lamiaceae) in Morocco. The present paper recognizes 60 taxa grouped in 52 species, placed in 8 sections for the Teucrium genus in Morocco. The correct nomenclature is established on the basis of full synonymies and type designations. T. rifanum (Maire & Sennen) T. Navarro & El Oualidi, T. joannis (S auvage & Vindt) El Oualidi, T. Navarro & A. Martin and T. embergeri (Sauvage & Vindt) El Oualidi, T. Navarro & A. Martin, are proposed as the new combinations for the Teucrium genus in Morocco. Key word: Teucrium, Lamiaceae, typification, Morocco. RESUMEN. Sinopsis del género Teucrium (Lamiaceae) en Marruecos. Para el género Teucrium en Marruecos, se reconocen 60 taxa distribuidos en 52 especies ordenadas en 8 secciones. La nomenclatura correcta ha sido establecida en base a las sinonimias principales y designación de tipos en la mayoría de los casos. Se proponen tres nuevas combinaciones para el género Tettcrium en Marruecos: T. rifanum (Maire & Sennen) T. Navarro & El Oualidi, T. joannis (Sauvage & Vindt) El Oualidi, T. Navarro & A. Martin y T. embergeri (Sauvage & Vindt) El Oualidi, T. Navarro & A. Martin. Palabras clave: Teucrium, Lamiaceae, tipificación, Marruecos. RESUME. Synopsis du genre Teucrium (Lamiaceae) au Maroc. Dans le present travail 60 taxa, reagroupés en 52 especes et arrangées en 8 sections, sont reconnues pour le genre Teucrium au Maroc. La correcte nomenclature est etablie sur la base des principals synonymies et la désignation des types. T. rifanum (Maire & Sennen) T. Navarro & El Oualidi, T. joannis (Sauvage & Vindt) El Oualidi, T. Navarro & A. Martin et T. embergeri (Sauvage & Vindt) El Oualidi, T. Navarro & A. Martin. sont proposées comme nouvelles combinations pour le genre Teucrium au Maroc. Mots cié: Teucrium, Lamiaceae, typification, Maroc.
Article
The inflorescences of Teucrium have been investigated. There is a. wide variation in morphological characters, wich depend on different factors: on the partialinflorescences and on the flowers. The comparative study of inflorescences and flowers demonstrates morphological differentiations between related groups. The mediterranean species show a remarkable variety. Special distribution patterns and morphological features of species are discussed. As a. result of his studies the author proposes a new classification of the genus in the section Teucropsis, Teucrium, Ghamaedrys, Isotriodon, Seorodonia and Scordium.
Article
The Teucriumflavum-T. polium group is rich in species. Hence, the analysis of growth forms are only carried out on the basis of some characteristical representatives. The semi-shrub growth form is especially richly developed within this species group. The semi shrub growth is characterized by a sympodial branching system with primary and secondary axes which are differently lignified. The mainly erect growth of the stems in T. flavum is the best representation of the semishrub growth. Most of the other species form orthotropic or ortho-plagiotropic (T. polium), plagiotropic (T. montanum, T. pyrenaicum) or descending-prostrate (T. cuneifolium) stem systems. Therefore, a clear designation of the growth forms is not always possible.