The generic position of Stachys tibetica
Vatke and amalgamation of the genera
Eriophyton and Stachyopsis (Lamiaceae
subfam. Lamioideae)
Mika Bendiksby, Yasaman Salmaki,
Christian Bräuchler & Olof Ryding
Plant Systematics and Evolution
ISSN 0378-2697
Plant Syst Evol
DOI 10.1007/s00606-013-0935-2
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Author's personal copy
Plant Syst Evol
DOI 10.1007/s00606-013-0935-2
ORIGINAL ARTICLE
The generic position of Stachys tibetica Vatke and amalgamation
of the genera Eriophyton and Stachyopsis (Lamiaceae subfam.
Lamioideae)
Mika Bendiksby • Yasaman Salmaki
Christian Bräuchler • Olof Ryding
•
Received: 2 March 2013 / Accepted: 12 October 2013
Ó Springer-Verlag Wien 2013
Abstract We have investigated the phylogenetic position
of Stachys tibetica by use of both plastid (rps16 intron,
trnL-F region and matK) and nuclear ribosomal (ITS) DNA
sequence data and both parsimony and Bayesian phylogenetic methods. All data corroborate that S. tibetica is
extraneous in Stachys (tribe Stachydeae) and suggest a
phylogenetic affiliation in a different lamioid tribe, Lamieae. The molecular data suggest that the species is most
closely related to the genus Stachyopsis, while most of the
morphological data suggest an intermediate position
between Stachyopsis and Eriophyton. Due to difficulties in
distinguishing Stachyopsis and Eriophyton, and the possible embedding of the former in the latter genus, we prefer
to amalgamate the two closely related genera and refer S.
M. Bendiksby (&)
NTNU University Museum, Norwegian University of Science
and Technology, 7491 Trondheim, Norway
e-mail: mika.bendiksby@ntnu.no
Y. Salmaki
Center of Excellence in Phylogeny of Living Organisms,
Department of Plant Science, School of Biology, College of
Science, University of Tehran, PO Box 14155-6455,
Tehran, Iran
C. Bräuchler
Department of Biology I, Biodiversity Research-Systematic
Botany, Ludwig-Maximilians Universität München,
Menzinger Str. 67, 80638 Munich, Germany
C. Bräuchler
Botanische Staatssammlung München, Menzinger Str. 67,
80638 Munich, Germany
O. Ryding
Botanical Garden, Natural History Museum of Denmark,
University of Copenhagen, Sølvgade 83, opg. S,
1353 Copenhagen, Denmark
tibetica to the expanded Eriophyton. As a consequence,
five new combinations are made: Eriophyton lamiflorum
(Rupr.) Bräuchler, Eriophyton maleolens (Rech.f.) Salmaki, Eriophyton marrubioides (Regel) Ryding, Eriophyton oblongatum (Schrenk) Bendiksby and Eriophyton
tibeticum (Vatke) Ryding.
Keywords W Himalaya Molecular phylogenetics
Stachyopsis Eriophyton Stachys tibetica
Taxonomy
Introduction
Scheen et al. (2010) and Bendiksby et al. (2011a) studied
the phylogeny of the whole subfamily Lamioideae (Lamiaceae) and discerned altogether ten tribes, among them
Stachydeae and Lamieae. The largest genus of the subfamily, the subcosmopolitan Stachys L. alone comprises
about 300 species (Harley et al. 2004), of which one, S.
tibetica Vatke (from the highlands of northern Pakistan and
northern India; Dickoré 2013), is the main focus of the
present study. Kumar et al. (2012) mentions the species as
an important medicinal plant in traditional medicine.
Originally (Vatke 1875), Stachys tibetica was placed in
the predominantly American section Calostachys Benth.,
with similarities to the large section Lamiotypus Benth.
Hooker (1885) considered the Iranian to Caucasian S.
macrocheilos Boiss. (now treated as synonym under S.
fruticulosa M. Bieb.) as closely related, while a more
recent treatment (Hedge 1990) regarded it as very distinct
with respect to some unusual characteristics such as spiny
bracteoles and triquetrous, apically truncate nutlets. Consequently, Krestovskaya (2003) placed the species in the
new monotypic subgenus Menitskia, raising it to generic
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M. Bendiksby et al.
rank only 3 years later (Krestovskaya 2006). Diagnostic
features provided for Menitskia are: bracteoles subulate
instead of herbaceous or absent; flowers sessile; corolla lips
equally long, instead of the lower longer; mid-lobe of
lower lip of corolla bent down at a right angle at the base,
equal to lateral lobes and boat-shaped; all stamens long,
curved and projecting forward instead of having the anterior pair bending outward after pollination; anthers slightly
hairy; nutlets triquetrous and apically truncate instead of
rounded; leaves indistinctly three to five lobed. Govaerts
et al. (2013), nonetheless, reduce Menitskia to synonymy
and retain the species in Stachys.
Embedded in ongoing research on the phylogeny and
classification of Stachys (Salmaki et al. 2008, 2009, 2011,
2012a, b, 2013), this paper aims at establishing the phylogenetic position of S. tibetica using molecular and morphological analyses, and to help review this part of the
World Checklist of Seed Plants (Govaerts et al. 2013) by
improving the classification.
Materials and methods
The names used for taxa in the present study follow
Govaerts et al. (2013), with Betonica L. recognized as the
distinct genus (see e.g., Scheen et al. 2010).
Taxon sampling
We have generated altogether 19 DNA sequences for the
present study, of which 16 are the nuclear ribosomal
internal transcribed spacer (nrITS) and three are plastid
DNA (pDNA) regions of S. tibetica (trnL intron, trnL-F
spacer and rps16 intron). We aligned the plastid sequences
of S. tibetica into a trimmed version (82 accessions) of the
dataset used by Bendiksby et al. (2011a) that includes all
currently recognized lamioid genera except three (i.e.,
Metastachydium Airy Shaw ex C.Y. Wu & H.W. Li,
Paralamium Dunn. and Pseudomarrubium Popov), from
which no DNA sequences are available. We established the
nrITS dataset (59 accessions) by sequencing a subset of the
accessions included in the plastid data and also included a
few lamioid nrITS sequences from GenBank. All tribes
except for Gomphostemmatae, Synandreae and Leucadeae
are represented in the nrITS dataset. We have deposited all
sequences new to the present study in GenBank. Voucher
information and GenBank accession numbers to all included specimens are provided (see Table 2 in Appendix).
The molecular work
We performed the molecular work (PCR-amplification,
PCR purification, cycle sequencing, sequence editing and
123
aligning) in different laboratories (Munich and Oslo) as
described in previous studies (Scheen et al. 2010; Bendiksby et al. 2011a; Salmaki et al. 2012a, b).
To test for potential errors in the process from tissue to
phylogenetic position in a gene tree, we compared separate
gene tree results prior to final analyses on concatenated
congruent datasets. It is well known that the risk of PCR
contamination increases with decreasing DNA quality as
well as with the use of universal primers. We included
some poor-quality DNA templates and used several universal primer combinations. Despite this, we detected only
a single contaminated sequence: the nrITS of Eriophyton
rhomboideum (Benth.) Ryding, which we excluded from
further analysis.
We analyzed both datasets using maximum parsimony
and Bayesian phylogenetic methods. We performed the
parsimony analyses using NONA (Goloboff 1999) in
combination with WinClada v. 1.0 (Nixon 1999) applying
the heuristic search option with 2,000 replicates and
maxtrees set to 10,000 and otherwise default settings. We
performed parsimony jackknifing with 2,000 replicates and
otherwise default setting. For the Bayesian phylogenetic
analyses, we used Mr Bayes 3.1.2 (Huelsenbeck and
Ronquist 2001; Ronquist and Huelsenbeck 2003) with prior
models of nucleotide substitution set according to the
output of TreeFinder (Jobb et al. 2004). We determined
posterior probabilities by running one cold and three heated
chains for five million generations in parallel mode, saving
trees every 1,000th generation. We performed the analyses
twice to check their convergence for the same topology. To
test whether the Markov chain converged, we monitored
the average standard deviation of split frequencies
(ASDSF), which should fall below 0.01 when comparing
two independent runs.
Morphology
We re-examined morphology in light of the molecular
phylogenetic results presented herein based on herbarium
material in C, GB, M, MSB and UPS, images in the JSTOR
plant science (2013) database and the illustrations in Hedge
(1990).
Results
Alignments and analyses
The lengths in aligned characters of the various DNA
regions were: 1,031 for the trnL-F region (intron and
spacer), 1,058 for the rps16 intron, 1,155 for the matK gene
and 702 for the nrITS. The estimated best-fit model of
nucleotide substitution for the trnL-F region, rps16 intron,
Author's personal copy
The generic position of Stachys tibetica Vatke
1
97
1
100
1
91
1
89
1
100
Cymaria dicotoma
Achyrospermum fruticosum
Eurysolen gracilis
1 Leucosceptrum canum
Comanthosphace japonica
94 1
Rostrinucula dependens
99
Colebrookea oppositifolia
Craniotome furcata
Microtoena patchoulii
1
Anisomeles indica
100
Gomphostemma parviflorum
1
1
Bostrychanthera deflexa
87
Chelonopsis longipes
100
Colquhounia elegans
1
1
1
1
100
1
99
1
90
POGOSTEMONEAE
Pogostemon heyneanus
GOMPHOSTEMMATEAE
1
Synandra hispidula
Macbridea alba
Physostegia virginiana
Brazoria truncata
Warnockia scutellarioides
SYNANDREAE
Betonica alupecuros
Betonica officinalis
Galeopsis angustifolia
Galeopsis pubescense
1
Melittis melissophyllum 1
Melittis melissophyllum 2
100
Stachys alpigena
1
1
Stachys sylvatica
1
1
100
Suzukia shikikunensis
98
100
Stachys debilis
1
87
1
Haplostachys haplostachya
99
1
1 Phyllostostegia velutina
94
100
65 Stenogyne sessilis
1
Stachys spinosa
Sideritis hyssopifolia
86
1
Stachys byzantina
Prasium majus
100
.99
Stachys hyssopoides
1
Phlomidoschema parviflorum
77 1
1
Hypogomphia turkestana
86
1
Chamaesphacos illicifolius
100
Thuspeinanta persica
100
1
Ajugoides humilis
Matsumurella tuberifera
PARAPHLOMIDEAE
97
Paraphlomis javanica 1
Phlomis fruticosa 1
1
Phlomoides rotata 3
.99
100
PHLOMIDEAE
1
Eremostachys laevigata 1
71
Phlomoides tuberosa
82
Lagochilus cabulicus 1
1
Chaiturus marrubiastrum
1
Loxocalyx ambiguus
99
1
80
Leonurus glaucescens
65
Leonurus turkestanicus 1
LEONUREAE
1
Lagopsis marrubiastrum
1
Panzerina lanata
99
.99
1
Leonurus chaituroides
99
Leonurus sibiricus 2
98
60
Roylea cinerea 1
Acanthoprasium integrifolium
1
Moluccella laevis
83
1
MARRUBIEAE
Ballota nigra subsp. ruderalis
.99
Marrubium supinum
1
95
Marrubium
vulgare
63
86
Rydingia integrifolia
1
Leucas lavandulifolia
1
97
Isoleucas arabica
1
98
Otostegia modesta
1
LEUCADEAE
92
Leucas spiculifolia
79
1
Leucas inflata
59
1
Acrotome
hispida
100
Leonotis leonurus
99
Lamium album
1
Lamium amplexicaule 1
1
99
Lamium galeobdolon subsp. galeobdolon 1
99
Lamium multifidum
Lamium purpureum 1
Stachys tibetica
1
Stachyopsis oblongata 2
Stachyopsis oblongata 3
84
Eriophyton wallichii 1
Eriophyton rhomboideum 1
Eriophyton rhomboideum 2
STACHYDEAE
1
62
0.0080
1
98
LAMIEAE
Fig. 1 The 50 % majority rule consensus phylogram from a Bayesian
analysis of a concatenated matrix with 83 accessions and 3,244
aligned base pairs from four pDNA regions (trnL intron, trnL-F
spacer, rps16 intron and matK). The Bayesian posterior probability
values of at least 0.95 are reported above branches and parsimony
jackknifing of at least 50 % in italics below branches. Multiple
accessions of the same species are numbered according to Table 2 in
Appendix. Lamioid tribes are indicated. Inset picture of Stachys
tibetica (with permission from the photographer: Dr. Ori FragmanSapir, Jerusalem Botanical Gardens, www.en.botanic.co.il)
and nrITS was GTR ? G ? I, whereas GTR ? G was
selected for matK. Preliminary parsimony analyses of each
plastid region resulted in congruent topologies that were
resolved to different extents. Therefore, we concatenated
all plastid regions prior to the final analyses. This concatenated pDNA matrix of 3,244 aligned characters contained
604 parsimony informative characters. The nrITS contained 278 parsimony informative characters.
The parsimony analysis of the pDNA and nrITS datasets
produced 2,688 and 162 most parsimonious trees of lengths
1,749 and 1,304 steps, and the rescaled consistency and
homoplasy indices were 0.6/0.30 and 0.33/0.52,
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M. Bendiksby et al.
Craniotome furcata
Colebookea oppositifolia
1
99
Anisomeles indica
1
100
Colquhounia elegans
Paraphlomis hispida
1
Paraphlomis javanica 2
99
Paraphlomis javanica 3
79
1
97
Lagochilus cabulicus 2
Leonurus glaucescens
LEONUREAE
Leonurus turkestanicus 2
1
Leonurus chaituroides
100
Leonurus sibiricus 1
1
Roylea cinerea 1
100
Roylea cinerea 2
1
Ballota hirsuta
99
1
Ballota hispanica
MARRUBIEAE
1
91
Marrubium supinum
79
Marrubium vulgare
1
Phlomis fruticosa 2
100
Phlomis fruticosa 1
1
Phlomoides tuberosa
50
1
1
Eremostachys laevigata 1
PHLOMIDEAE
84
100
Eremostachys laevigata 2
1
Phlomoides rotata 2
99
Phlomoides rotata 1
1
Eriophyton wallichii 1
99
Eriophyton wallichii 2
89 .98
Stachys tibetica
79 .98 Stachyopsis oblongata 1
64 Stachyopsis oblongata 2
Lamium galeobdolon subsp. galeobdolon
1
.99 Lamium multifidum
95
1
Lamium purpureum 2
1
98
Lamium amplexicaule 2
79
Lamium album
.97
Betonica alopecuros
99
Betonica officinalis 2
1
100
1
Melittis melissophyllum 1
100
Melittis melissophyllum 2
Stachys byzantina
57
Prasium majus
1
.96
Stachys spinosa
98
81
Sideritis hyssopifolia
Stachys hyssopoides
1
Phlomidoschema parviflorum
60
95 .98
Thuspeinantha persica
1
81
Chamaesphacos illicifolius
100
93
Hypogomphia turkestana
Stachys alpigena
Stachys sylvatica
.95
Stachys debilis
76
Suzukia shikikuensis
Haplostachys haplostachya
1
59
Stenogyne bifida
90
Phyllostegia velutina
1
100
1
81
.99
0.07
POGOSTEMONEAE
Pogostemon cablin
Pogostemon heyneanus
LAMIEAE
Galeopsis angustifolia
Galeopsis pubescens
STACHYDEAE
Fig. 2 The 50 % majority rule consensus phylogram from a Bayesian
analysis of 59 accessions and 702 aligned base pairs from the nuclear
ribosomal ITS region. The Bayesian posterior probability values of at
least 0.95 are reported above branches and parsimony jackknifing of
at least 50 % italics below branches. Multiple accessions of the same
species are numbered according to Table 2 in Appendix. Lamioid
tribes are indicated. Inset picture of Stachys tibetica (with permission
from the photographer: Dr. Ori Fragman-Sapir, Jerusalem Botanical
Gardens, www.en.botanic.co.il)
respectively. In the Bayesian analyses of the pDNA and the
nrITS datasets, the ASDSF had fallen to 0.003165 and
0.005567, respectively, at termination (5th million generation). We discarded 1,250 generations (25 %) as burn-in
and summarized the remaining trees as Bayesian 50 %
majority rule consensus trees (Figs. 1, 2) with Bayesian
posterior probabilities above branches and parsimony
jackknife support in italics below branches.
with Stachyopsis oblongata (Schrenk) Popov & Vved.
(accession 2) in both the pDNA and nrITS trees (Figs. 1,
2). Note that the second accession of S. oblongata in the
two gene trees are represented by different specimens (1 vs.
3; see Table 2 in Appendix), which attain somewhat different positions in the plastid versus nuclear trees.
Stachyopsis oblongata is paraphyletic in the plastid topology (Fig. 1) and monophyletic in the nuclear topology
(Fig. 2), although neither are strongly supported.
The topology of the Lamioideae pDNA phylogeny
published by Bendiksby et al. (2011a) is retained herein
(Fig. 1) despite a strongly reduced number of accessions
(280 vs 83), the only difference being lower branch support
for some clades (e.g., Pogostemoneae and Eriophyton
Benth.) and higher for others (e.g., Leonureae and a few of
Phylogenies
Both gene trees (pDNA and nrITS) are generally well
resolved with well-supported clades that are largely congruent at the tribal level (Figs. 1, 2). Stachys tibetica
attains a phylogenetic position in tribe Lamieae and groups
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The generic position of Stachys tibetica Vatke
Table 1 Comparison of morphological charactersistics between
Stachys tibetica and the genera Eriophyton and Stachyopsis
Eriophyton
s.lat.
Stachyopsis
Stachys tibetica
Number of
species
6
4
1
Number of
flowers per
cyme
1–4
3–10
1–3
Flower length
20–40
15–23
15–24
Quotient: corolla
length/calyx
length
1.8–4
1.4–2.1
2–3.5
Annulus in
corolla tube
Absent or
sometimes
present
Mostly
[0.5mm or
sometimes all
\0.5 mm
Present
Present
Mostly
[0.5 mm
All \0.5 mm
Serrate,
crenate or
subentire
Pinnately lobed,
crenate,
serrate or
subentire
Length of the
hairs of the
upper lip of the
corolla
Leaf shape
Serrate, crenate
or subentire
the backbone branches). Most major, supported clades in
the pDNA tree (Fig. 1) are corroborated by the nrITS tree
(Fig. 2), except for a few nuclear–plastid incongruent
patterns within some genera [e.g., Lamium L. and Stachys;
investigated in more detail by Bendiksby et al. (2011b) and
Salmaki et al. (2013), respectively]. Monophyly of tribe
Lamieae, to which S. tibetica belongs, is inferred by both
plastid and nuclear data, but receives less than 50 % support by parsimony jackknifing.
Re-examination of morphology supports a closer relationship to genera of tribe Lamieae than the genus Stachys.
Morphologically, S. tibetica attains an intermediate position between the genera Eriophyton and Stachyopsis
(Table 1).
Discussion
Our molecular phylogenetic results, based on both plastid
(Fig. 1) and nuclear (Fig. 2) genetic data, suggest a phylogenetic position of S. tibetica in the lamioid tribe Lamieae, sister to the genus Stachyopsis, supporting
Krestovskaya’s (2006) view that this morphologically
distinct species is extraneous in Stachys. As argued in the
following paragraph, the suggestion that S. tibetica belong
to Lamieae close to Stachyopsis is also supported by
morphological data.
Lamieae sensu Bendiksby et al. (2011a) contains the
three genera Lamium, Eriophyton s.lat. (sensu Bendiksby
et al. 2011a) and Stachyopsis. The tribe is best characterized by having the anthers usually hairy and also differs
from Stachydeae in having the nutlets apically truncate or
subtruncate. Lamium clearly differs from the latter two
genera in having the lateral lobes of the lower lip of the
corolla acute, reduced or replaced by narrow teeth. There
seems to be no consistent differences between Eriophyton
and Stachyopsis, but the two genera can be distinguished
by a combination of differences in the following four
characters: number of flowers per cyme, flower length,
relation between corolla length and calyx length, and the
presence or absence of an annulus in the corolla tube
(Table 1). The only species of Eriophyton that resembles
Stachyopsis in having an annulate corolla tube, E. nepalense (Hedge) Ryding, strongly differs from the latter
genus in having the corolla c. 30 mm long and c. three
times longer than the calyx.
Judging from our herbarium studies, we agree with
Krestovskaya (2006) that the following characteristics of S.
tibetica are rare or unique within Stachys: subsessile
flowers, near equally long corolla lips, anterior stamens
that do not curve sideward after pollination, hairy anthers
and triquetrous and apically truncate nutlets. While most of
these features are common in many other lamioid genera,
only Stachyopsis and Eriophyton (emend. Bendiksby et al.
2011a) combine all of them. Hairy anthers are comparatively uncommon in Lamioideae and are only known in
Galeopsis L. and the three genera of the tribe Lamieae.
Stachys tibetica clearly differs from Galeopsis in having
triquetrous, apically truncate nutlets and clearly differs
from Lamium in having the lateral lobes of the lower lip of
the corolla prominent and rounded. Stachys tibetica is
almost equally similar to the remaining two genera of
Lamieae, Stachyopsis and Eriophyton. In the five characters mentioned in Table 1, the species agrees better with
Stachyopsis in having the corollas short and annulate in the
tube. On the other hand, the species agrees better with
Eriophyton in having the corolla much longer than the
calyx, the hairs on the upper corolla lip short and only few
flowers in the cymes (Table 1).
Stachys tibetica should obviously be excluded from
Stachys as proposed by Krestovskaya (2006). We see three
alternatives of classifying the species. The first alternative
is to resurrect Krestovskaya (2006) genus Menitskia that
accommodates S. tibetica as the single species. Adopting
her classification will not require new nomenclatorial
combinations. The genus can be distinguished from both
Eriophyton and Stachyopsis in having a narrower posterior
corolla lip, stiffer bracteoles and often deeply crenate to
lobed leaves (Table 1). However, we do not find it informative to place the species in a monotypic genus. Monotypic taxa are redundant in classification as they do not
communicate information on the relationship.
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M. Bendiksby et al.
The second alternative is to include S. tibetica in
Stachyopsis, the most closely related genus according to
our molecular phylogenetic results (Figs. 1, 2). Stachyopsis
has a western to central Asian distribution, adjacent to, but
not overlapping with the more eastern distribution of S.
tibetica. Eriophyton has a wider distribution that overlaps
entirely with the distributions of S. tibetica and most of the
distribution of Stachyopsis (Govaerts et al. 2013). Introgression seems to be common among co-occurring outcrossing species of the same or closely related genera in the
Lamiaceae and is often detected by incompatible plastid
versus nuclear DNA-based tree topologies (see Bräuchler
et al. 2010 for an overview). In such cases, nuclear data
often correlate better with morphology, while plastid data
contain a strong geographical signal (Albaladejo et al.
2005). Our nuclear data support a phylogenetic sister
relationship between S. tibetica and Stachyopsis. The
morphological data suggest that S. tibetica is about as
closely related to Eriophyton as to Stachyopsis. The four
species of Stachyopsis (S. lamiiflora [Rupr.] Popov &
Vved., S. maleolens [Rech.f.] Hedge, S. marrubioides
[Regel] Ikonn.-Gal. and S. oblongata) are more similar to
each other than to S. tibetica. Hence, inclusion of S. tibetica would render the genus more variable and increase the
distribution area to a moderate extent. It is more problematic as the distinction between Stachyopsis and Eriophyton is rather weak and would be further diminished by
inclusion of S. tibetica which is intermediate in several
differential characters (Table 1). This problem with distinguishing and defining the two genera provides reasons to
question their status as separate genera.
The third alternative, to include both Stachyopsis and S.
tibetica in Eriophyton, is the least problematic. The group
is supported as monophyletic in both the plastid tree
(Fig. 1) and the nuclear tree (Fig. 2). An expanded genus
Eriophyton will contain 11 species and can be defined by
having the following combination of characters: usually
hairy anthers, prominent and apically rounded to slightly
emarginate lateral lobes of the lower lip of the corolla and
apically truncate or subtruncate nutlets. For the above
given reasons, favoring the latter option, we propose the
corresponding five nomenclatural changes.
Taxonomic conclusions
Eriophyton Benth. in N. Wallich, Pl. Asiat. Rar. 1:63.
1830. –Type: E. wallichii Benth.
= Erianthera Benth., Hooker’s J. Bot. Kew Gard. Misc.
3:880. 1833, nom illeg., non Nees 1832 : Alajja Ikonn.,
Novosti Sist. Vyssh. Rast. 8:274. 1971 : Susilkumara
Bennet, Indian Forester 107:432. 1981. –Type: E. rhomboidea Benth.
123
= Stachyopsis Popov & Vved., Trudy Turkestansk.
Nauchn. Obshch. 1:120 (1923), syn. nov. –Type: S.
oblongata (Schrenk) Popov & Vved., designated here.
= Menitskia (Krestovsk.) Krestovsk., Bot. Zhurn.
(Moscow & Leningrad) 91:1893 (2006), syn. nov. –Type:
M. tibetica (Vatke) Krestovsk.
Bendiksby et al. (2011a) presented a revised version of
the genus description in Harley et al. (2004). After the
inclusion of S. tibetica and the genus Stachyopsis, this
description has to be modified again:
Perennial herbs with a woody root and unbranched hairs.
Leaves crenate or sometimes shallowly pinnately lobed.
Calyx actinomorphic or slightly zymomorphic, subequally
5-lobed. Corolla 15–40 mm long, tube longer or shorter than
the calyx, exannulate or annulate, upper lip hairy above, not
bearded along the margin, lower lip 3-lobed, mid-lobe
slightly to much larger than the lateral lobes, emarginate to
almost entire and lateral lobes prominent, rounded or
sometimes emarginate. Anthers usually hairy. Nutlets apically truncate or subtruncate. Eleven species growing in
alpine area at 2,000–5,000 m in Kazakhstan, Uzbekistan,
Kyrgyzstan, Tadzhikistan, Afghanistan, N Pakistan, N
India, China (Xinjiang, Tibet, Yunnan) and Nepal.
Eriophyton lamiflorum (Rupr.) Bräuchler, comb. nov.
: Stachys lamiiflora Rupr. in F.von der Osten-Saken &
F.J.Ruprecht, Sert. Tianschan.: 67 (1869) : Stachyopsis
lamiiflora (Rupr.) Popov & Vved., Trudy Turkestansk.
Nauchn. Obshch. 1:122 (1923). –Type: Kyrgyzstan, Tien
Shan, ‘‘Kastek-schlucht’’, ‘‘Sary-dschasyk’’ 6 July 1867
(18 July 1867), Osten-Saken s.n. (holotype in LE?).
Eriophyton maleolens (Rech.f.) Salmaki, comb. nov.
: Stachys maleolens Rech.f., Biol. Skr. 8(1): 60 (1955);
Stachyopsis maleolens (Rech.f.) Hedge, Notes Roy. Bot.
Gard. Edinburgh 28:142 (1968). –Type: Afghanistan, Badakhshan Province, Khash District, 9 Aug. 1937, Koelz
13014 (holotype in W; isotype in US).
Eriophyton marrubioides (Regel) Ryding, comb. nov.
: Phlomis marrubioides Regel, Trudy Imp. S.-Peterburgsk. Bot. Sada 6:375 (1879) : Stachyopsis marrubioides (Regel) Ikonn.-Gal., Izv. Glavn. Bot. Sada S.S.S.R.
26:72 (1927). –Type: China, Xinjiang Uyghur A.R. (Sinkiang), ‘‘in Turkestaniae orientalis trajectu Tschubaty
9-100000 alt.’’, Regel s.n. (syntype in LE?, isotype in P?);
‘‘ad lacum Sairam’’, Fetissof s.n. (syntype in LE?).
= Phlomis oblongata var. canescens Regel, Trudy Imp. S.Peterburgsk. Bot. Sada 9:593 (1886) : Stachyopsis
oblongata var. canescens (Regel) Popov & Vved., Trudy
Turkestansk. Nauchn. Obshch. 1:122 (1923) : Stachyopsis canescens (Regel) Adylov & Tulyag., Opred. Rast.
Sred. Azii 9:114 (1987). –Type: China, Xinjiang Uyghur
A.R. (Sinkiang), ‘‘in alpium Dschungariae iliensis
Author's personal copy
The generic position of Stachys tibetica Vatke
orientalis trajectu montium Tschubaty a lacu Sairam ad fl.
Borotalam ducente ad alt. 9-100000 ’’, Aug 1878, Regel s.n.
(holotype in LE?).
Eriophyton oblongatum (Schrenk) Bendiksby, comb. nov.
: Phlomis oblongata Schrenk in F.E.L.von Fischer &
C.A.von Meyer, Enum. Pl. Nov. 1:29 (1841) : Stachyopsis oblongata (Schrenk) Popov & Vved., Trudy Turkestansk. Nauchn. Obshch. 1:121 (1923). –Type: Tajikistan,
‘‘in vallibus graminosis montim Dschillkaragai (Dzhilkaragai)’’, Schenk s.n. (holotype in LE).
= Leonurus dschungaricus Regel, Trudy Imp. S.-Peterburgsk. Bot. Sada 6:367 (1879). –Types: China, Xinjiang
Uyghur A.R (Sinkiang), ‘‘in alpium lacum Sairam cingentium valle fluvii Chorgos, 5-60000 alt.’’, Regel s.n.
(syntype in LE?); China, Xinjiang Uyghur A.R. (Sinkiang),
‘‘in angustis fluvii Talki’’, Regel s.n. (syntype in LE?);
China, Xinjiang Uyghur A.R. (Sinkiang), ‘‘in alpibus dschungaricus lacum Sairam adjacentibus’’, Regel s.n. (syntype in LE?); Kazakhstan, ‘‘ad fluvium Almatinka majore
prope Wernoje’’, Regel s.n. (syntype in LE?).
= Stachyopsis ovata Diugaeva, Novosti Sist. Vyssh. Rast.
1968:180 (1968). –Type: Asia Media, Pamiro-Alaj, jugum
Hissaricum, declive austro-orientale, in loco Darja-Sary,
pratum subalpinum, 2,500 m s. m., 25 VII 1965, fl., n° 44,
A. Aschirmuchamedov et R. Saprunova (LE).
Eriophyton tibeticum (Vatke) Ryding, comb. nov.
: S. tibetica Vatke, Bot. Zeitung (Berlin) 33:447
(1875) : Menitskia tibetica (Vatke) Krestovsk., Bot.
Zhurn. (Moscow & Leningrad) 91:1894 (2006). –Type:
India?, Kashmir?, ‘‘in Tibetiae occidentalis alt.
10-140000 ’’, T. Thomson s.n. (types in E, K, C, PH?).
Acknowledgments We thank the NRC (Norwegian Research
Council: grant no 154145) and the Natural History Museum (University of Oslo, Norway) for financial support to M.B., the DAAD
(Deutscher Akademischer Austausch Dienst) for a grant to Y.S. and
the EU for a SYNTHESYS-II grant to C.B. (DK-TAF-2392). We also
appreciate the help and support of Prof. Dr. Günther Heubl and kind
assistance from Tanja Ernst (Munich) in Heubl’s laboratory of plant
molecular systematics, Prof. Shahin Zarre (Tehran, Iran) and Charlotte Lindqvist (Buffalo, USA).
Appendix
See Table 2.
Table 2 Alphabetical list of specimens used in the present study including voucher information, country of origin and GenBank accession
numbers
Taxon
Voucher information
Origin
nrITS
GenBank accession no.
trnL intron
trnL-F
spacer
rps16
intron
matK
Acanthoprasium integrifolium
(Benth.) Ryding
H. Lindberg s.n.
11.06.1939 (sS)
Cyprus
N/A
FJ854263
FJ854150
FJ854016
HQ911486
Achyrospermum fruticosum
Benth.
P. Phillipson 2082 (S)
Madagascar
N/A
FJ854250
FJ854137
FJ854003
HQ911420
Acrotome hispida Benth.
P. Herman 1990 (C)
South
Africa
N/A
EU138376
EU138299
EU138224
HQ911530
Ajugoides humilis (Miq.)
Makino
J. Ohwi & K. Okamoto
1401 (UPS)
Japan
N/A
HQ911678
HQ911746
HQ911609
HQ911452
Anisomeles indica (L.) Kuntze
E. Emanuelsson 2027
(S)
Pakistan
KF769017*
FJ854259
FJ854146
FJ854012
HQ911395
Ballota hirsuta Benth.
Podlech 53328 (M)
Morokko
JN680359
N/A
N/A
N/A
N/A
B. hispanica (L.) Benth.
ASG s.n. (ORT)
N/A
AF335641
N/A
N/A
N/A
N/A
B. nigra L. subsp. ruderalis
(Sw.) Briq.
M. Bendiksby & A.-C.
Scheen 0431 (O)
Greece
N/A
FJ854264
FJ854151
FJ854017
HQ911497
Betonica alopecuros L.
S. Vautier 2661390
(US)
Italy
KF769018*
FJ854308
FJ854203
FJ854088
HQ911446
B. officinalis L.
1. C. Lindqvist & V.A.
Albert 357 (UNA)
Cultivated
N/A
AF502056
FJ854224
FJ854109
N/A
2. Schuhwerk 09-150
N/A
JN680360
N/A
N/A
N/A
N/A
Bostrychanthera deflexa Benth.
Sino-American Guizhou
Bot. Exped. 1923 (A)
China
N/A
FJ854267
FJ854154
FJ854020
HQ911423
Brazoria truncata (Benth.)
Engelm. & A.Gray
D. S. Corell 16051 (DH,
TEX)
Texas
N/A
EF546969
EF546892
HQ911601
HQ911433
Chaiturus marrubiastrum (L.)
Ehrh. ex Rchb.
A. Pedersen 14 (C)
Germany
N/A
FJ854268
FJ854155
FJ854022
HQ911464
123
Author's personal copy
M. Bendiksby et al.
Table 2 continued
Taxon
Voucher information
Origin
nrITS
GenBank accession no.
trnL intron
trnL-F
spacer
rps16
intron
matK
Chamaesphacos ilicifolius
Schrenk
K. H. Rechinger 50961 (C)
Iran
KF529540*
FJ854269
FJ854156
FJ854023
HQ911549
Chelonopsis longipes
Makino
S. Okuyama & N. Maruyama
s.n. Nov. 1951 (UPS)
Japan
N/A
EF546938
EF546861
FJ854024
HQ911424
Colebrookea oppositifolia
Sm.
B. Hansen & T. Smitinand
12747 (C)
Thailand
KF769019*
HQ911655
HQ911723
HQ911585
HQ911389
Colquhounia elegans Wall.
C. F. van Beusekom & C.
Phengklai 3008 (C)
Thailand
KF769020*
EF546937
EF546859
FJ854027
HQ911422
Comanthosphace japonica
(Miq.) S.Moore
M. Ono & S. Kobayashi 45908
(S)
Japan
N/A
FJ854272
FJ854159
FJ854029
HQ911407
Craniotome furcata (Link)
Kuntze
O. Polunin & al. 5638 (UPS)
Nepal
KF769021*
FJ854275
FJ854162
FJ854032
HQ911392
Cymaria dichotoma Benth.
C. Wang 33150 (US)
China
N/A
FJ854245
FJ854132
FJ853998
HQ911388
Eremostachys laevigata
Bunge
1. J. Frödin 202 (UPS)
Kurdistan
KF769022*
GU993260
GU993069
GU993165
HQ911484
2. Salmaki & Siadati 39152
(TUH)
Iran
JN680397
N/A
N/A
N/A
N/A
1. Dr. J.E.T. Aitchison 831 (C)
Afghanistan
N/A
HQ911683
HQ911753
HQ911614
HQ911460
Eriophyton rhomboideum
(Benth.) Ikonn.
2. T. Thomson (C) Typus
Tibet
N/A
HQ911684
HQ911754
HQ911615
HQ911461
E. wallichii Benth.
1. Stainton & al. 7748 (UPS)
2. D990
Nepal
China
KF769023*
JF976304
FJ854277
N/A
FJ854164
N/A
FJ854034
N/A
HQ911462
N/A
Eurysolen gracilis Prain.
E. Hennipman 3215 (C)
Thailand
N/A
HQ911664
HQ911732
HQ911593
HQ911402
Galeopsis angustifolia
Hoffm.
E. Dahl s.n. 26.08.1979 (O)
France
KF529535*
EF546939
EF546862
FJ854035
HQ911441
Galeopsis pubescens Besser
T. Tacik & M. Sychowa 366
(O)
Poland
KF529536*
EF546940
EF546863
FJ854036
HQ911444
Gomphostemma javanicum
(Blume) Benth.
G.E. Juan s.n. 17.08.1945 (US)
Myanmar
N/A
HQ911667
HQ911735
HQ911595
N/A
Haplostachys haplostachya
(A.Gray) H.St.John
S. Perlman 14328 (NY)
Hawaii
KF529541*
AF502029
FJ854166
FJ854039
HQ911565
Hypogomphia turkestana
Bunge
O. Paulsen 275 (C)
C Asia
KF529543*
HQ911703
HQ911774
HQ911634
HQ911551
Isoleucas arabica O.
Schwartz
M. Thulin & al. 8402 (UPS)
Yemen
N/A
EU138380
EU138303
EU138227
HQ911508
Lagochilus cabulicus
Benth.
1. E. Emanuelsson 2456 (S)
Pakistan
N/A
FJ854279
FJ854167
FJ854040
HQ911468
2. Rechinger 56201 (M)
Iran
JN680362
N/A
N/A
N/A
N/A
Lagopsis marrubiastrum
(Stephan) Ikonn.-Gal.
T. Thomson s.n. no date (C)
Tibet
N/A
HQ911690
HQ911761
HQ911619
HQ911472
Lamium album L.
M. Bendiksby 05-014 (O)
Norway
KF529537*
JF779961
JF779961
JF780035
JF779864
L. amplexicaule L.
1. J. I. Båtvik 102 (O)
2. Jap 06/79 (BO)
Norway
Japan
N/A
AB266245
JF779969
N/A
JF779969
N/A
JF780043
N/A
N/A
N/A
L. galeobdolon (L.) L.
subsp. galeobdolon
M. Bendiksby 05-016 (O)
Norway
KF529538*
JF779994
JF779994
JF780068
JF779869
L. multifidum L.
J. & F. Bornmüller 14536 (S)
Turkey
KF769024*
FJ854335
FJ854241
FJ854128
HQ911457
L. purpureum L.
1. N. Orderud s.n. 18.7.1999
(O)
Russia
N/A
JF780027
JF780027
JF780100
N/A
2. Jap 06/78 (BO)
Japan
AB266244
N/A
N/A
N/A
N/A
123
Author's personal copy
The generic position of Stachys tibetica Vatke
Table 2 continued
Taxon
Voucher information
Origin
nrITS
GenBank accession no.
trnL intron
trnL-F
spacer
rps16
intron
matK
Leonotis leonurus (L.) R. Br.
F. Venter & P. Vorster 171
(US)
S Africa
N/A
EU138382
EU138305
EU138229
HQ911521
Leonurus chaituroides C.Y. Wu &
H.W. Li
Z. Chao 030730001 (SHMU)
N/A
DQ903316
N/A
N/A
N/A
EF395813
L. glaucescens Bunge
Z. Chao 060728002 (SHMU)
N/A
EF395808
N/A
N/A
N/A
EF395811
L. sibiricus L.
1. H. Xie 050619003
(SHMU)
N/A
EF395806
N/A
N/A
N/A
N/A
2. T. M. Pedersen 16317
(UPS)
Argentina
N/A
EF546930
EF546852
FJ854045
HQ911471
1. I. Roldugin & V. Fissjun
5393 (S)
Kazakhstan
N/A
EF546931
EF546853
FJ854046
HQ911466
2. Z. Chao 060728003
(SHMU)
N/A
EF395809
N/A
N/A
N/A
N/A
Leucas inflata Benth.
M. Thulin & al. 3869 (UPS)
Ethiopia
N/A
EU138410
EU138333
EU138257
HQ911518
L. lavandulifolia Sm.
C.A. Salsedo 164 (US)
Palau,
N/A
EU138414
EU138337
EU138261
HQ911505
L. spiculifolia (Balf.f.) Gürke
M. Thulin & A.N. Gifri 8688
(UPS)
Yemen,
Socotra
N/A
EU138425
EU138348
EU138272
HQ911517
Leucosceptrum canum Sm.
C.T. Mason Jr. & P.B. Mason
3963 (US)
Nepal
N/A
FJ854283
FJ854171
FJ854047
HQ911404
Loxocalyx ambiguus (Makino)
Makino
G. Murata & T. Shimizu
1233 (S)
Japan
N/A
HQ911680
HQ911750
HQ911611
N/A
Macbridea alba Chapm.
E. S. Ford & E. West s.n.
14.06.1955 (GH)
USA
N/A
EF546962
EF546885
HQ911598
HQ911428
L. turkestanicus V.I. Krecz. &
Kuprian.
Marrubium supinum L.
J. Barber 203 (TEX)
Spain
AF335642
AF335681
N/A
N/A
N/A
M. vulgare L.
I. & O. Hedberg 92075
(UPS)
Saudi
Arabia
d*
EU138443
EU138366
EU138294
HQ911499
Matsumurella tuberifera (Makino)
Makino
C-C. Liao 1125 (GH)
Taiwan
N/A
HQ911679
HQ911747
HQ911610
HQ911453
Melittis melissophyllum L.
1. M. Bendiksby 09-010 (O)
Cultivated
KF529544*
HQ911702
HQ911773
HQ911633
HQ911534
2. M. E. Steiner & al. 1127
(UPS)
Hungary
KF529545*
EF546929
EF54849
FJ854051
HQ911535
H. Y. Liang 66028 (US)
China
N/A
FJ854287
FJ854174
FJ854052
HQ911393
Microtoena patchoulii (Hook.f.) C.Y.
Wu & S.J. Hsuan
Moluccella laevis L.
W. C. Brumbach 7249 (S)
USA
N/A
EU138444
EU138367
FJ854055
N/A
Otostegia modesta S. Moore
M. G. Gilbert & D. Sebsebe
8631 (UPS)
Ethiopia
N/A
EU138437
EU138360
EU138283
XXXX
Panzerina lanata (L.) Soják
T. Norlindh & T. Ahti 10044
(S)
Mongolia
N/A
FJ854290
FJ854177
FJ854059
XXXX
Paraphlomis javanica (Blume) Prain
1. J. F. Rock 1097 (US)
Thailand
N/A
FJ854292
FJ854178
FJ854061
XXXX
2. Fang 091066 (KUN)
N/A
EU827095
N/A
N/A
N/A
N/A
3. Liu & Chen 67 (E)
Taiwan
JN680357
N/A
N/A
N/A
N/A
P. hispida C. Y. Wu
Fang 091058 (KUN)
N/A
EU827112
N/A
N/A
N/A
N/A
Phlomidoschema parviflorum
(Benth.) Vved.
J. S. Andersen & I.C.
Petersen 394 (C)
Afghanistan
KF529546*
FJ854293
FJ854179
FJ854062
HQ911546
Phlomis fruticosa L.
1. E. Julin s.n. 19.04.1985
(UPS)
Greece
KF529539*
FJ854294
FJ854180
FJ854063
HQ911475
2. Roessler 6880 (MSB)
Montenegro
JN680364
N/A
N/A
N/A
N/A
Phlomoides rotata (Benth. ex
Hook.f.) Mathiesen
1. Dikore 3537 (MSB)
China
JN680371
N/A
N/A
N/A
N/A
2. Fang 091022 (KUN)
N/A
EU827099
N/A
N/A
N/A
N/A
3. Ludlow & al. 15600 (US)
Tibet
N/A
GU993241
GU993050
HQ911620
HQ911479
123
Author's personal copy
M. Bendiksby et al.
Table 2 continued
Taxon
P. tuberosa (L.) Moench
Phyllostegia velutina (Sherff)
H.St.John
Physostegia virginiana (L.)
Benth.
Pogostemon cablin (Blanco)
Benth.
P. heyneanus Benth.
Prasium majus L.
Rostrinucula dependens (Rehder)
Kudô
Roylea cinerea (D.Don) Baill.
Rydingia integrifolia (Benth.)
Scheen & V.A. Albert
Sideritis hyssopifolia L.
Stachyopsis oblongata (Schrenk)
Popov & Vved.
Stachys alpigena T.C.E.Fr.
S. byzantina K.Koch
S. debilis Kunth
S. hyssopoides Burch. ex Benth.
S. spinosa L.
S. sylvatica L.
S. tibetica Vatke.
Stenogyne sessilis Benth.
S. bifida Hillebr.
Suzukia shikikunensis Kudô
Synandra hispidula (Michx.)
Baill.
Thuspeinanta persica (Boiss.)
Briq.
Warnockia scutellarioides
(Engelm. & A. Gray) M.W.
Turner
Voucher information
Origin
nrITS
GenBank accession no.
trnL intron
trnL-F
spacer
rps16
intron
matK
M. Bendiksby 09-001 (O)
V. A. Albert & al. HI03-061
(O)
M. Bendiksby 09-011 (O)
Cult.
Hawaii
KF769025*
KF529547*
HQ911691
HQ911704
HQ911762
HQ911775
HQ911621
HQ911635
HQ911481
HQ911566
Cult.
N/A
HQ911671
HQ911738
HQ911602
HQ911437
PS0119MT02
N/A
FJ980282
N/A
N/A
N/A
N/A
J. Klackenberg 100 (S)
M. Thulin 5752 (UPS)
D.E. Boufford & al. 24415
(A)
1. O. Polunin & al. 837
(UPS)
2. W. Koeltz 4651 (US)
M. Thulin & al. 8161 (UPS)
Sri Lanka
Spain
China
KF769026*
KF529550*
N/A
FJ854297
FJ854300
FJ854302
FJ854184
FJ854187
FJ854189
FJ854069
FJ854072
FJ854074
HQ911401
HQ911541
HQ911405
Nepal
KF769027*
EU138450
EU138373
EU138290
HQ911454
India
Yemen
KF769028*
N/A
HQ911682
EU138435
HQ911752
EU138358
HQ911613
EU138282
HQ911455
HQ911502
J. Barber 202 (TEX)
1. I. Roldugin & V. Fissjun
3006795 (US)
2. I. Roldugin & V. Fissjun
5394 (C)
3. M. Popov & A. Vvedensky
s.n. (H)
O. Ryding 2133 (UPS)
C. Lindqvist and V.A. Albert
356 (UNA)
C. Jativa and C. Epling 242
(US)
E. Retief 1080 (US)
M. Bendiksby & A.-C.
Scheen 04-022 (O)
M. Bendiksby & A. Tribsch
06-011 (O)
Dikore 13712 (MSB)
V. A. Albert & al. HI03-067
(O)
V. A. Albert & al. HI03–032
(O)
C–C. Liao & al. 564 (A)
V. E. McNeilus 97-143 (GH)
Spain
Kazachstan
AF335633
KF769029*
AF502037
N/A
FJ854193
N/A
FJ854078
N/A
N/A
N/A
Kazachstan
KF769030*
HQ911686
HQ911757
HQ911616
HQ911463
Uzbekistan
N/A
HQ911687
HQ911758
N/A
N/A
Ethiopia
Cult.
KF529561*
KF529577*
FJ854309
AF502046
FJ854204
FJ854211
FJ854089
FJ854096
HQ911555
N/A
Ecuador
KF529584*
FJ854317
FJ854216
FJ854101
HQ911563
South Africa
Greece
KF529600*
KF529639*
FJ854319
FJ854329
FJ854218
FJ854232
FJ854103
FJ854117
HQ911544
HQ911537
Italy
KF529643*
AF502063
FJ854235
FJ854120
N/A
Pakistan
Hawaii
KF769031*
N/A
KF769032*
HQ911705
KF769033*
HQ911776
KF769034*
HQ911636
N/A
HQ911567
Hawaii
KF529652*
N/A
N/A
N/A
N/A
Taiwan
USA
KF529655*
N/A
FJ854332
EF546970
FJ854238
EF546893
FJ854123
FJ854124
HQ911562
HQ911427
K. H. Rechinger 9604 (S)
Iraq
KF529657*
FJ854334
FJ854240
FJ854126
HQ911550
M. H. Mayfield & G. Nesom
1970 (US)
USA
N/A
EF546971
EF546894
FJ854127
HQ911430
Multiple accessions from the same species are numbered. Missing data are indicated with N/A
* Sequence data generated for this study are indicated with an asterisk behind the accession number
d Sequence shorter than 200 bp: L. multifidum L, Turkey,. J. & F. Bornmüller 14536 (S), ITS2, partial CACCTCCGCGCGCGGCCGGCCCAAATGCCAATCCGCCGTCGACTCACGTCGCGACCAGTGGTGGTTGAACTATCAACTCGCGTGCTGTCGCGCTCCACGGCGTCGTCGGTCCGGAAACAK
CAACGCAACCCAACGGCGCGAGCACGCATCGTGCCCACGACCGCGACCCC
123
Author's personal copy
The generic position of Stachys tibetica Vatke
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