TAXONOMIC SIGNIFICANCE OF NUTLET AND LEAF CHARACTERS IN
HYMENOCRATER, NEPETA SECT. PSILONEPETA AND LOPHANTHUS
(NEPETINAE, NEPETOIDEAE: LAMIACEAE)
F. Serpooshan, Z. Jamzad, T. Nejadsattari & I. Mehregan
Received 2013. 06. 30. Accepted for publication 2013. 12. 08
Serpooshan, F., Jamzad, Z., Nejadsattari, T. & Mehregan, I. 2014. 06. 31: Taxonomic significance of nutlet and
leaf characters in Hymenocrater, Nepeta sect. Psilonepeta and Lophanthus (Nepetinae, Nepetoideae: Lamiaceae).Iran. J. Bot. 20 (1): 80-95. Tehran.
Hymenocrater (Lamiaceae) in Iran was studied using morphological characters of nutlets and leaves. The species of
the genus Nepeta sect. Psilonepeta and a few species of the genus Lophanthus were also examined for comparison.
Scanning electron micrographs showed the surface of the nutlets and trichome types on leaves in detail. Two types
of nutlets including smooth and sculptured were recognized. Among the species with smooth nutlets H. incanus is
very characteristic having an absolutely smooth nutlet surface. Sculptures may be prominently tuberculate e.g. in H.
bituminosus and H. calycinus or verrucose e.g. in H. sessilifolius and N. sessilifolia. Most species have constant
features in nutlet surface, but minor differences could be identified within a few species, i.e. H. elegans and H.
yazdianus. Leaf surfaces in studied group are covered with dense or laxe trichomes. Different trichome types are
observed including glandular and non-glandular trichomes. Two different glandular trichomes were identified:
peltate or sub-sessile glands and capitate or stalked glands. Non-glandular trichomes consist of short or long
trichomes with (1)2-8(11) cells. Relationship among the species of the three genera was investigated based on data
provided from morphological features, using cluster and PCA analysis. Three species groups are provided by the
cluster analysis. Sculptured nutlets and peltate glands with two- or multi-celled head are characteristic features of
most species grouped in the first cluster. Most species of the second and third clusters have smooth nutlets. Micropapillate trichomes and capitate glands with a long, one- or multi-celled stalk are significant respectively in species
of second and third clusters. Characters with the most variation were identified using FA based on PCA. Closely
placement of Hymenocrater species together with Nepeta and Lophanthus species in obtained phenogram and
ordination supports the affinity of these genera. It also reveals that the morphological features are not significant for
defining the boundaries of the studied genera but raised the proposal of very close relationships among the studied
species and the possibility of re-circumscribing the genera within Nepetinae.
Fariba Serpooshan (correspondence< fa_serpooshan@yahoo.com>), Taher Nejadsattari and Iraj Mehregan,
Department of Biology, Science and Research Branch, Islamic Azad University, Tehran, Iran. –Ziba Jamzad,
Research Institute of Forests and Rangelands, P. O. Box 13185-116, Tehran, Iran.
Key words: Hymenocrater; Nepeta; Lophanthus; micromorphology; trichome, nutlet
Lophanthus
وPsilonepeta ﺑﺨﺶNepeta ،Hymenocrater ارزش ﺗﺎﮐﺴﻮﻧﻮﻣﯿﮏ ﺻﻔﺎت ﻣﻮرﻓﻮﻟﻮژﯾﮑﯽ ﻓﻨﺪﻗﻪ و ﺑﺮگ در ﺟﻨﺲﻫﺎي
داﻧﺸﺠﻮي دﮐﺘﺮي داﻧﺸﮕﺎه آزاد اﺳﻼﻣﯽ ﺗﻬﺮان واﺣﺪ ﻋﻠﻮم و ﺗﺤﻘﯿﻘﺎت ﺗﻬﺮان:ﻓﺮﯾﺒﺎ ﺳﺮﭘﻮﺷﺎن
اﺳﺘﺎد ﭘﮋوﻫﺶ ﻣﻮﺳﺴﻪ ﺗﺤﻘﯿﻘﺎت ﺟﻨﮕﻠﻬﺎ و ﻣﺮاﺗﻊ ﮐﺸﻮر: زﯾﺒﺎ ﺟﻢزاد
داﻧﺸﯿﺎر داﻧﺸﮕﺎه آزاد اﺳﻼﻣﯽ ﺗﻬﺮان واﺣﺪ ﻋﻠﻮم و ﺗﺤﻘﯿﻘﺎت ﺗﻬﺮان:ﻃﺎﻫﺮ ﻧﮋاد ﺳﺘﺎري
داﻧﺸﯿﺎر داﻧﺸﮕﺎه آزاد اﺳﻼﻣﯽ ﺗﻬﺮان واﺣﺪ ﻋﻠﻮم و ﺗﺤﻘﯿﻘﺎت ﺗﻬﺮان:اﯾﺮج ﻣﻬﺮﮔﺎن
از ﻧﻈﺮLophanthus و ﺳﻪ ﮔﻮﻧﻪ از ﺟﻨﺲPsilonepeta ﺑﺨﺶNepeta در اﯾﺮان ﻫﻤﺮاه ﺑﺎ ﮔﻮﻧﻪﻫﺎي ﺟﻨﺲHymenocrater ﮔﻮﻧﻪﻫﺎي ﺟﻨﺲ
ﺗﺼﺎوﯾﺮ ﻣﯿﮑﺮوﺳﮑﻮپ اﻟﮑﺘﺮوﻧﯽ از آراﺳﺘﺎر ﺳﻄﺢ ﻓﻨﺪﻗﻪ. و ﻣﯿﮑﺮوﻣﻮرﻓﻮﻟﻮژﯾﮑﯽ ﻓﻨﺪﻗﻪ و ﺑﺮگ ﻣﻮرد ﻣﻄﺎﻟﻌﻪ ﻗﺮار ﮔﺮﻓﺘﻨﺪ-ﺻﻔﺎت ﻣﺎﮐﺮو
ﺻﺎفﺗﺮﯾﻦ ﺳﻄﺢ ﻓﻨﺪﻗﻪ ﺑﺎ ﺑﺎﻓﺖ ﺳﻠﻮﻟﯽ ﻣﺸﺒﮏ در ﮔﻮﻧﻪ.ﺣﺎﻟﺖﻫﺎي ﮔﻮﻧﺎﮔﻮﻧﯽ از دو ﺗﯿﭗ ﺻﺎف و داراي ﺗﺰﺋﯿﻨﺎت را ﻧﺸﺎن داده اﺳﺖ
IRAN. J. BOT. 20 (1), 2014
F. Serpooshan & al.
81
وH. calycinus وH. bituminosus دﯾﺪه ﻣﯽﺷﻮد و در ﺑﯿﻦ ﻓﻨﺪﻗﻪﻫﺎي داراي ﺗﺰﺋﯿﻨﺎت اﻧﻮاع ﻣﺨﺘﻠﻔﯽ ﻣﺎﻧﻨﺪ ﺗﺰﺋﯿﻨﺎت ﺑﺮﺟﺴﺘﻪ درH. incanus
اﮔﺮ ﭼﻪ در اﮐﺜﺮ ﻣﻮارد آراﺳﺘﺎر ﻓﻨﺪﻗﻪ ﺻﻔﺖ ﺛﺎﺑﺘﯽ در ﺳﻄﺢ ﮔﻮﻧﻪ. وﺟﻮد داردN. sessilifolia وH. sessilifolius ﺗﺰﺋﯿﻨﺎت ﺑﺎ ﻣﺮﮐﺰ ﻓﺮو رﻓﺘﻪ در
ﺑﺮ اﺳﺎس ﺗﺼﺎوﯾﺮ ﻣﯿﮑﺮوﺳﮑﻮپ اﻟﮑﺘﺮوﻧﯽ. اﯾﻦ ﺻﻔﺖ ﺗﻨﻮع ﮐﻮﭼﮑﯽ ﻧﺸﺎن ﻣﯽدﻫﺪH. elegans وH. yazdianus اﺳﺖ اﻣﺎ در ﮔﻮﻧﻪﻫﺎي
ﻏﺪهﻫﺎﯾﯽ ﺑﺎ ﭘﺎﯾﻪ ﯾﮏ ﯾﺎ ﭼﻨﺪ ﺳﻠﻮﻟﯽ ﺑﻠﻨﺪ،وﻣﯿﮑﺮوﺳﮑﻮپ ﻧﻮري در ﺳﻄﺢ ﺑﺮگ اﯾﻦ ﮔﻮﻧﻪﻫﺎ ﻏﺪهﻫﺎي ﯾﮏ ﯾﺎ ﭼﻨﺪ ﺳﻠﻮﻟﯽ ﺑﺪون ﭘﺎﯾﻪ ﯾﺎ ﭘﺎﯾﻪ ﮐﻮﺗﺎه
دادهﻫﺎي ﺑﻪدﺳﺖ آﻣﺪه ﺑﺎ روش، ﺑﻪﻣﻨﻈﻮر ﺗﻌﯿﯿﻦ ﺧﻮﯾﺸﺎوﻧﺪي ﮔﻮﻧﻪﻫﺎي اﯾﻦ ﺳﻪ ﺟﻨﺲ.( ﺳﻠﻮﻟﯽ وﺟﻮد دارد1)2 -8(11) و ﮐﺮكﻫﺎي ﻏﯿﺮ ﻏﺪهاي
ﺑﺮ اﺳﺎس ﻓﻨﻮﮔﺮام ﺑﻪدﺳﺖ آﻣﺪه ﮔﻮﻧﻪﻫﺎ در ﺳﻪ ﺧﻮﺷﻪ اﺻﻠﯽ ﺟﺎي ﻣﯽﮔﯿﺮﻧﺪ ﮐﻪ دراﮐﺜﺮ ﮔﻮﻧﻪﻫﺎي.ﺧﻮﺷﻪاي و رﺳﺘﻪﺑﻨﺪي ﻣﻮرد آﻧﺎﻟﯿﺰ ﻗﺮار ﮔﺮﻓﺘﻨﺪ
وﺟﻮد اﺷﮑﺎل.ﺧﻮﺷﻪ اول ﻓﻨﺪﻗﻪ داراي ﺗﺰﺋﯿﻨﺎت اﺳﺖ و ﺑﯿﺸﺘﺮ ﮔﻮﻧﻪﻫﺎﯾﯽ ﮐﻪ در دو ﺧﻮﺷﻪ دﯾﮕﺮ ﻗﺮارﮔﺮﻓﺘﻪاﻧﺪ ﻓﻨﺪﻗﻪﻫﺎﯾﯽ ﺑﺎ ﺳﻄﺢ ﺻﺎف دارﻧﺪ
ﺑﺎ ﮔﻮﻧﻪﻫﺎي دوHymenocrater ﺣﻀﻮر ﻧﺰدﯾﮏ ﮔﻮﻧﻪﻫﺎي ﺟﻨﺲ.ﺧﺎﺻﯽ از ﮐﺮكﻫﺎ ﻧﯿﺰ درﮔﻮﻧﻪﻫﺎي ﻫﺮ ﯾﮏ از ﺧﻮﺷﻪﻫﺎ ﻗﺎﺑﻞ ﺗﻮﺟﻪ ﻣﯽﺑﺎﺷﺪ
ﻃﺒﻖ اﯾﻦ ﻧﺘﺎﯾﺞ ﺗﺮﮐﯿﺐ ﺻﻔﺎت ﻓﻨﺪﻗﻪ و ﺑﺮگ در ﺗﻔﮑﯿﮏ ﺟﻨﺲﻫﺎي ﻓﻮق از.ﺟﻨﺲ دﯾﮕﺮ در اﯾﻦ ﻓﻨﻮﮔﺮام ﻗﺮاﺑﺖ اﯾﻦ ﺳﻪ ﺟﻨﺲ را ﺗﺎﯾﯿﺪ ﻣﯽﮐﻨﺪ
ﻣﯽﺑﺎﯾﺴﺘﯽ ﺗﻌﺮﯾﻒNepetinae ﯾﮑﺪﯾﮕﺮ ﻗﺎﺑﻞ اﺳﺘﻔﺎده ﻧﻤﯽﺑﺎﺷﺪ وﻟﯽ اﯾﻦ ﻓﺮﺿﯿﻪ را ﺗﻘﻮﯾﺖ ﻣﯽﮐﻨﺪ ﮐﻪ ﻣﺮزﻫﺎي ﺗﺎﮐﺰوﻧﻮﻣﯿﮑﯽ ﺟﻨﺲﻫﺎي زﯾﺮﻃﺎﯾﻔﻪ
.ﻣﺠﺪد ﺑﺸﻮﻧﺪ
INTRODUCTION
The genera considered in Nepetinae Coss. & Germ.
(Mentheae, Nepetoideae, Lamiaceae) are characterized
with 15-nerved calyx, strongly 2-lipped corolla, having
the posterior pair of stamens longer than the anterior
pair and pericarp structure (Wagstaff 1992). Twelve
genera are classified within this subtribe (Harley & al.
2004), among which Nepeta L., Lophanthus Adans.,
Hymenocrater Fisch. & C. A. Mey. and Marmoritis
Benth. are phylogenetically closely related (Budantsev
& Lobova 1997 and Drew & Systma 2012).
Hymenocrater with 12 species is mainly distributed in
Iran and Afghanistan (Rechinger 1982 and Pojarkova
1954). The western limit of its geographical
distribution is Turkey where it is represented with one
species in east Turkey. In Iran the genus is present with
nine species from which four are endemics (Rechinger
1982; Budantsev 1992; Harley & al. 2004 and Jamzad
2012). The genus is characterized by large, broad,
membranous and mostly colored calyx teeth and
resupinate corolla in most species. The genus
Lophanthus has c. 22 species in the alpine regions of
central Asia, Afghanistan, Mongolia, China and
Turkey ( Dirmenci & al. 2010). In Lophanthus calyx is
15-nerved with a hairy annulus in throat, similar to
Hymenocrater and Nepeta sect. Psilonepeta Benth. and
corolla is resupinate, similarly in Hymenocrater
(Pojarkova 1954; Rechinger 1982 and Dirmenci & al
2010). The similarities between Nepeta species sect.
Psilonepeta and species belonging to the genus
Lophanthus has been discussed by different authors.
Levin (1941) included the species belonging to Nepeta
sect. Psilonepeta in the genus Lophanthus and
classified them as sect. Psilonepeta. Budantsev (1992)
divided the species of Lophanthus into two sections
(Lophanthus and Psilonepeta).
The usefulness of nutlet and trichome
morphological characters for different taxonomic
levels in family Lamiaceae has been proved by
different authors i.e. Hedge 1992; Marin & al. 1996;
Budantsev & Lobova 1997; Jamzad & al. 2000;
Navarro & Oualidi 2000; Padure 2003; Abbas-Azimi
& al. 2006; Moon & Hong 2006; Kaya & Dirmenci
2008; Dinc & al. 2009; Moon & al. 2009; Salmaki & al
2009; Ryding 2010 and Eshratifar & al. 2011.
Budantsev & Lobova (1997) admitted that the surface
ornamentation of nutlets in Hymenocrater is quite
similar to species of Lophanthus and Nepeta but is
distinguished from these by its lack of myxocarpy.
In a phylogenetic study of Nepeta (Jamzad & al.
2003), species of the section Psilonepeta were grouped
in a clade within the genus Nepeta, furthermore a few
species of Hymenocrater were examined and added to
the analysis matrix, they were nested in Nepeta sect.
Psilonepeta clade (Jamzad unpublished). Yet a few of
Hymenocrater species have been included in
morphological,
anatomical,
palynological
and
phytochemical studies (Satil & al. 2007; Jafari &
Jafarzadeh 2008; Moon & al. 2008a; Moon & al.
2008b; Moon & al. 2009; Gohari & al. 2010 and
Ryding 2010).
In this study morphological examination of nutlets
and leaves of 9 species of Hymenocrater, 7 species of
Nepeta sect. Psilonepeta and 3 species of Lophanthus
is represented and taxonomic significance of these
characters in defining the generic boundaries is
discussed. It is part of a Ph.D. thesis undertaken by F.
Serpooshan.
82 Nutlet and leaf characters in Hymenocrater
MATERIALS AND METHODS
Most specimens examined in this study were from
TARI herbarium that include some new collections
from northern and north-eastern parts of Iran.
Lophanthus species are dedicated duplicates to TARI
and materials of two species were taken from IRAN
herbarium (Tab. 1). Macro-morphological charaters
were studied using an OLYMPUS stereomicroscope
and for micro-morphological studies nutlets and
dissected middle part of the leaves were fixed on stubs
using a double adhesive tape. Coating were done by
platinum or gold and scanning electron micrographs
were supplied respectively using Cambridge LEO 440i
or VEGA\\ TESCAN SEM. Leaf trichomes were
studied also using LEICA DM500 Light Microscope
(LM). Terminology and description of nutlet micromorphology is based on Budantsev & Lobova (1997)
and general classification and typology of trichomes is
based on Roe (1971) and Cantino (1990). Twenty two
macro- and micro-morphological characters of nutlets
and leaves were chosen, quantitative characters were
measured and the state of qualitative ones were
determined (Tabs. 2-3). Variables were standardized
(range 0 to 1), and then taxa were clustered using
WARD method with Squared Euclidean distance.
Ordination of taxa based on Principal Component
Analysis (PCA) was performed with Varimax rotation.
Factor analysis based on PCA was performed to
determine the most influential variable characters of
nutlet and leaf among the taxa (Tab. 4). SPSS version
21 software was used for analysis.
RESULTS
The nutlet and trichome characters of the studied
species are described below. Micrographs of nutlets
and leaf surfaces are illustrated in details (Figs. 1-4).
The comparison of characters among the studied taxa
is given (Tabs. 2-3). Cluster analysis and ordination of
the species were achieved (Fig. 5).
Nutlet
Hymenocrater. Nutlets of nine species were examined
(Tab. 1). They are elliptic, ovate or oblong, mostly
trigonous in shape with the size of 2-3.65 × 1.1-1.9
mm. The nutlet apex is rounded and the base is
truncate to attenuate. Hymenocrater incanus and H.
longiflorus have the smallest and largest nutlets
respectively (Figs. 1A & C). Usually on the dorsal side
of nutlets 3-5 nerves are observed. Areole is whitish,
lateral and bilobed. Attachment scar has a granular
texture. Two types of ornamentation, smooth and
sculptured are recognized on the surface of nutlets.
Smooth nutlets: H. incanus and H. longiflorus are
IRAN. J. BOT. 20 (1), 2014
characterized by smooth nutlets (Fig. 1A, C). In H.
incanus absolutely smooth surface is consisting of
reticulate-cellular texture with oblong or polygonal
cells. The anticlinal walls (AW) are straight; the
external periclinal walls (EPW) are flat or convex and
smooth (Fig. 1B) or wrinkled. In H. longiflorus surface
texture is reticulate-cellular, consisting of rounded to
polygonal cells, with prominent AW and depressed
EPW (Fig. 1D).
Sculptured nutlets: H. bituminosus, H. calycinus, H.
oxyodontus, H. platystegius and H. sessilifolius are
characterized with sculptured nutlets (Figs. 1G, I, K).
The following structures can be recognized within this
group: Hymenocrater bituminosus, H. calycinus, H.
oxyodontus and H. platystegius have tuberculate
nutlets; tubercles have a truncate apex in H.
oxyodontus and H. bituminosus (Fig. 1H). In H.
calycinus tubercles are truncate (Fig. 1J) similar to H.
bituminosus, or have convex apex. Tubercles are less
prominent in H. platystegius (Fig. 1L). Hymenocrater
sessilifolius has verrucose nutlets. These sculptures
consist of a ring of radial cells with a depression on
their center.
In H. elegans nutlet surface is sculptured with an
undulate reticulate-cellular texture (Fig. 1E, F) or
sculptured with pressed and flattened ornamentations.
Within H. yazdianus two different nutlet types were
found, smooth nutlet with reticulate-cellular in which
anticlinal wall (AW) is prominent and external
periclinal wal (EPW) is depressed, similar to H.
longiflorus, or sculptured nutlets with verrucose
consisting of radial cells and a depression on their
center, similar to H. sessilifolius.
Nepeta. The nutlets of six species of Nepeta sect.
Psilonepeta were studied (Tab. 1). They are oblong or
obovate, trigonous and rounded at the apex. Their sizes
varies between 1.75-2.55 × 0.85-1.2(1.65) mm. Areole
is whitish, lateral, bilobed and has a granular texture
the same as Hymenocrater. Nutlet surface is smooth or
sculptured.
Smooth nutlets: Nutlet surface is smooth in N.
dschuparensis, N. depauperata and N. makuensis (Fig.
2A). It is characterized by ridged cellular texture
consisting of irregular cells with prominent AW in N.
dschuparensis. Nutlet surface of N. depauperata
consist of rounded or polygonal cells with convex
EPW. Rounded or polygonal cells with straight AW
and depressed EPW were observed in N. makuensis
(Fig. 2B).
Sculptured nutlets: N. laxiflora, N. oxyodonta and N.
sessilifolia are characterized by verrucose nutlets (Fig.
2C). Similar to some Hymenocrater species, these are
forming by a ring of convex radial cells and have a
depression on their center (Fig. 2D).
IRAN. J. BOT. 20 (1), 2014
F. Serpooshan & al.
83
Fig. 1. SEM micrographs of nutlet in Hymenocrater: A, B, H. incanus; C, D, H. longiflorus; E, F, H. elegans. Scale
bar: A=200 µ; C, E=300 µ; B, F=20 µ; D=30 µ.
84 Nutlet and leaf characters in Hymenocrater
IRAN. J. BOT. 20 (1), 2014
Fig. 1. Continued: G, H, H. bituminosus; I, J, H. calycinus; K, L, H. platystegius Scale bar: G, K=300 µ; I=500 µ; H,
L=20 µ; J=100 µ.
IRAN. J. BOT. 20 (1), 2014
F. Serpooshan & al.
85
Fig. 2. SEM micrographs of nutlet in Nepeta sect. Psilonepeta and Lophanthus: A, B, N. makuensis; C, D, N.
sessilifolia; E, F, L. tschimganicus. Scale bar: A=500 µ; C=200 µ; E=300 µ; B, F=20 µ; D=30 µ.
86 Nutlet and leaf characters in Hymenocrater
IRAN. J. BOT. 20 (1), 2014
Fig. 3. SEM micrographs of non-glandular and glandular trichomes in studied species: A, N. oxyodonta; B, N.
depauperata; C, H. platystegius; D, N. allotria; E, F, N. makuensis. Scale bar: A, C, E=100 µ; B, D=50 µ; F=20 µ.
IRAN. J. BOT. 20 (1), 2014
F. Serpooshan & al.
87
Fig. 4. LM micrographs of trichomes in studied species: A, H. bituminosus; B, H. incanus; C, N. dschupSarensis; D,
E, H. yazdianus; F, N. makuensis; G, N. sessilifolia; H, I, H. calycinus.
88 Nutlet and leaf characters in Hymenocrater
IRAN. J. BOT. 20 (1), 2014
Table 1. Voucher specimen of examined materials. (*:species endemic to Iran)
Taxa
Nutlet
Collecting data
Hymenocrater
Iran, Mazandaran, Kandavan, Pol-e Zangule, after Mazid village, between
Valashed & Takor, 1700 m, Jamzad & Serpooshan, 98737 (TARI).
•
Iran, Azarbayejan, Kuh-e Sahand, between Lighvan and Isperekhan, 22002600 m, Assadi & Mozaffarian, 30629 (TARI).
•
H. bituminosus
Fisch. & C. A. Mey. Iran, Esfahan, Natanz, Mazdeh, Kuh-e Karkas, 1800-2320 m, Shams &
Feyzi, 10716 (TARI).
Iran, Tehran, Sorkhehesar, 1700 m, Dini & Arazm , 12850 (TARI).
•
Iran, Tehran, Road of Qom, 1170 m, Babakhanlou & Amin, 12854 (TARI).
•
Iran, Isfahan, Golpayegan, Hende, 2400-2500 m, Feyzi & Shams, 12551
(TARI).
•
H. calycinus (Boiss.) Iran, Isfahan, Ghamsar, Kuh-e Kargaz, above Barazuk village, 2081 m,
Benth.
Asadi, 82731 (TARI).
•
Semnan, Turan protected region, W. of Oshtoran Kuh, 1300-1500 m,
Freitag & Mozaffarian, 28465 (TARI).
•
Iran, Mazandaran, Kandavan, Pol-e Zangule, road to Baladeh, after Mazid
village, 1900 m, Jamzad & Serpooshan, 98729 (TARI).
•
H. elegans Bunge
Iran, Tehran, Firuzkuh, Chehel Cheshme, Abbarik, 2350 m, Dini & Arazm,
13303 (TARI).
•
Hamadan, 100 km N. Aq Bolaq, Aq Daque mts., 2050-2350 m, Safikhani,
•
H. incanus* Bunge Kalvandi & Faramarzi, 2809 (TARI).
Iran, Isfahan, 10 km Dehaghan to Borujen, Noruzi, 3980 (TARI).
•
H. longiflorus
Iran, Kermanshah, N.W. of Kermanshah, Shamshir village, Shahu
Benth.
mountains, 1760-1980 m , Assadi, 60748 & Hamzeh, 1277 (TARI).
•
Iran, Semnan, Shahrud, Turan protected region, Kuh-e Peyghambar, S.
Zamanabad, 1300-1600 m, Iranshahr, 35661 (IRAN).
H. oxyodontus*
Rrech. f.
Iran, Khorasan, Shahrud, Biarjmand, Kuh-e Mollahado, Gharb Khane
Khody, 1450 m, Maddah & Moradi, 3931 (TARI).
•
Iran, Khorasan, Mashad, Torghabe, Noghondar village, 1500 m,
Serpooshan, 97852 (TARI).
•
H. platystegius*
Iran, Khorasan, Dargaz, Laein-e No, Hezarmasjed, Khakestar village,
Rech. f.
1600 m, Serpooshan, 97854 (TARI). .
•
Iran, Khorasan, 42 km to Birjand, on the road from Ghayen, 2000 m,
Assadi & Amirabadi, 84719 (TARI).
•
H. sessilifolius
Iran, Khorasan, 14 km from Kashmar to Neyshabur, 1400-1500 m, Assadi
Benth.
& Mozaffarian, 35593 (TARI).
•
Iran, Yazd, Nudushan, Geyluk, 2400 m, Mozaffarian, 77766 (TARI).
•
H. yazdianus*
Yazd, Taft, Deh Bala village, Shir Kuh, 3400 m, Mahmoodi & Noruzi,
Rech. f.
98646 (TARI).
•
Nepeta
N. allotria* Rech.
Iran, Mazandaran, Ileka, between Makloz and Dahla, 3800 m, Terme,
f.
15184 (IRAN).
N. depauperata*
Iran, Bandar-Abbas, N. slope of rocky mts. of Bokhon, N. of Fareghan,
Benth.
1500-2000 m, Mozaffarian, 44723 (TARI).
•
N. dschuparensis* Iran, Kerman, Kuh-e Lalezar, Zarda valley, 3000 m, Foroughi & Assadi,
Bornm.
16289 (TARI).
•
N. laxiflora*
Iran, Chaharmahal-e Bakhtiari, Darr-e Bazoft, Mavarz, Kuh-e Sefid,from
Benth.
Talkhedan valleys, 1450-2200 m, Mozaffarian, 74565 (TARI).
•
Leaf
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
IRAN. J. BOT. 20 (1), 2014
Table. 1. Continued
Taxa
N. makuensis* Jamzad
& Mozaffarian
N. oxyodonta* Boiss.
N. sessilifolia* Bunge
Lophanthus
L. lipskyanus Ikonn.Gal. & Nevski
L. tschimganicus
Lipsky
L. turcicus Dirmenci,
Yildiz & Hedge
Collecting data
Iran, Azarbayejan, Maku, rocky mountain between Shut and
Umeridash and Nieyaz to Dashfishel, 1700 m, Mozaffarian, 71140
(TARI).
Iran, Chaharmahal-e Bakhtiari, Shahr-e Kord to Naghan, N. of Sulegan,
Kuh-e Shahpurnaz, 2200-2700 m, Mozaffarian, 57425 (TARI).
Iran, Arak, Shazand, Hafteh-o Emarat, Anbarteh and Tajereh, Kuh-e
Sero, 2150-2950 m, Mozaffarian, 63945 (TARI).
Nutlet
Leaf
•
•
•
•
•
•
Turkmenistan, Kugitang, without herbarium number (TARI).
Uzbekistan, W. of Tian-Shan, Tschimgan, Baranov & Raikova, 6426
(TARI).
Turkey,Van , Dirmenci, Yildiz & Yildiz, 16959 (TARI).
Lophanthus. Two species of Lophanthus were
examined (Tab. 1). They are obovate and trigonous
with the size of 2.25-2.7 × 1.2-1.3 mm. The nutlet apex
is acute and areole is lateral and bilobed with two short
lobes (Fig. 2E). Attachment scar has a granular texture
similar to Hymenocrater and Nepeta. Nutlet surface is
smooth and has rounded or polygonal cells with
convex EPW (Fig. 2F) the same kind as in N.
depauperata.
Trichome
Trichome of different plant parts in studied group of
genera follows most Lamiaceae. Two basic types of
trichomes, glandular and non-glandular, were observed
on the leaf surfaces by SEM and LM.
Type 1. Non-glandular trichomes include uni-cellular
and multi-cellular (uni-seriate) which are explained in
more detailes below:
Uni-cellular trichomes: Uni-cellular trichomes were
found very rarely in the studied species e.g. conical
shape uni-cellular trichomes in H. longiflorus and L.
lipskyanus.
Multi-cellular trichomes: Multi-cellular trichomes
show a considerable variation based on number of
consisting cells (2-11), trichome length (50-300 µm),
shape of basal cell (inflated or not), shape of terminal
cell (triangular, narrow or elongated) and presence or
absence of micro-papillae.
Short multi-cellular trichomes (<200 µm), which
contained 2-3(5) cells, with a rather wider basal cell
and a narrower or triangular terminal cell were found
for example in H. calycinus, H. elegans, H.
oxyodontus, H. bituminosus and N. depauperata (Fig.
4A; 3B).
Long multi-cellular trichomes were observed in
most species studied in which following features can
be distinguished: long (>200 µm), 3-5(7) celled multi-
89
F. Serpooshan & al.
•
•
•
•
•
cellular trichomes were observed in N. oxyodonta and
H. incanus on both abaxial and adaxial leaf surfaces
(Fig. 3A, 4B). Very long (>500 µm), 4-8 celled multicellular trichomes with thin-walled and long basal cell
were observed in H. longiflorus, H. yazdianus and L.
lipskyanus (Fig. 4D), basal cell may be rather short and
inflated as in N. dschuparensis (Fig. 4C). Based on the
shape of consisting cells, multi-cellular trichomes are
bead-like for example in H. longiflorus, H. yazdianus
and N. depauperata ( Fig. 3B), or have enlarged basal
cell and subsequent more or less uniform cells
terminating to a narrow terminal cell for example in L.
lipskyanus.
Non-glandular trichomes were observed mostly on
veins of abaxial leaf surface. Uni- and multi-cellular
trichomes densely covered with micro-papillae were
the common features in N. depauperata (Fig. 3B).
Micro-papillate trichomes were also found in N.
dschuparensis, H. incanus, H. oxyodontus and H.
platystegius.
Type 2. Glandular trichomes include peltate (sessile or
sub-sessile glands) and capitate or stipitate glands with
short or long stalk.
Peltate trichomes: Peltate trichomes were observed
in all studied species (see for example in H.
platystegius Fig. 3C). Most of the glands have a onecelled head (Fig. 4H), but glands composed of two- or
multi-celled head were also found (Fig. 4I).
Capitate trichomes: The length and cell number of
stalk varied among the studied species. Capitate
trichomes with a short/long thin-walled (ribbon-like)
stalk cell are the common features in L. turcicus, N.
allotria and N. sessilifolia (Fig. 3D; 4G). The capitate
trichomes were found in some species including H.
longiflorus and N. dschuparensis. The capitate
glandular trichomes with 2-4(6) stalk cells occurred
with two different forms, with smooth stalk cells e.g. in
90 Nutlet and leaf characters in Hymenocrater
IRAN. J. BOT. 20 (1), 2014
Table 2. Quantitative characters of nutlet and leaf in studied taxa.
No.
1
Taxa
Code
H. bituminosus
12854
H. calycinus
12551
3
H. elegans
13303
4
H. incanus
3980
5
H. longiflorus
1277
6
H. oxyodontus
3931
7
H. platystegius
84719
8
H. sessilifolius
35593
9
H. yazdianus
98646
10
N. depauperata
44723
11
N. dschuparensis
16289
N. laxiflora
74565
13
N. makuensis
71140
14
N. oxyodonta
57425
15
N. sessilifolia
63945
16
L. tschimganicus
6426
17
L. turcicus
16959
2
12
Limit
Nutlet
length
(mm)
Nutlet
width
(mm)
Areole
length
(µm)
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
Mean
Min
Max
2.60
2.45
2.70
2.35
2.33
2.36
3.42
3.20
3.65
2.95
2.92
2.97
3.47
3.31
3.65
2.65
2.60
2.70
3.10
3.00
3.30
2.50
2.35
2.60
2.35
2.32
2.37
1.77
1.75
1.80
1.77
1.73
1.80
2.47
2.40
2.56
1.95
1.85
2.10
2.50
2.45
2.55
2.35
2.30
2.38
2.47
2.25
2.70
2.35
2.31
2.39
1.45
1.35
1.55
1.50
1.48
1.52
1.45
1.30
1.55
1.37
1.35
1.40
1.75
1.72
1.77
1.90
1.75
2.00
1.85
1.75
1.90
1.58
1.50
1.70
1.25
1.22
1.27
1.00
0.80
1.20
.87
0.85
0.90
1.10
1.00
1.20
1.12
1.10
1.16
1.15
1.10
1.20
1.65
1.64
1.66
1.27
1.25
1.30
1.20
1.18
1.21
500.00
460.00
530.00
653.00
651.00
655.00
729.60
655.80
793.00
480.00
475.00
485.00
966.00
964.00
968.00
760.00
740.00
780.00
724.00
694.00
753.00
690.80
685.00
700.00
780.00
760.00
800.00
475.00
470.00
480.00
435.90
432.50
438.00
666.70
665.00
669.00
476.20
465.00
483.00
616.70
612.00
622.00
766.70
762.00
770.00
415.40
411.00
420.00
402.00
401.00
403.00
Angle of
areole
lobes
(degree)
133.00
127.00
137.00
121.00
120.00
122.00
104.00
97.00
110.00
125.00
120.00
130.00
71.00
69.00
72.00
133.00
130.00
139.00
120.00
118.50
121.00
117.00
116.00
118.00
70.00
68.00
71.00
91.00
88.00
93.00
105.00
103.00
108.00
85.00
80.00
89.00
85.00
81.00
90.00
102.00
101. 00
103.00
105.00
102.00
107.00
98.00
95.00
100.00
113.00
111.00
116.00
Leaf
length
(mm)
Leaf
width
(mm)
10.60
10.10
11.00
16.00
15.50
16.50
27.00
26.00
28.00
15.00
14.00
17.00
45.00
40.00
52.00
18.66
18.00
20.00
22.00
21.00
23.00
26.00
20.00
29.00
12.00
11.00
12.50
8.25
7.75
9.00
8.75
7.75
10.00
14.30
11.00
16.00
26.00
24.00
27.00
15.00
14.50
15.30
25.60
24.00
27.00
16.25
15.75
17.00
27.00
26.00
28.00
7.75
7.00
8.50
10.25
9.50
10.75
16.50
16.00
17.25
7.00
6.00
8.00
26.00
22.00
29.00
11.50
10.50
12.00
12.75
12.50
13.25
22.00
18.00
25.00
8.25
8.00
8.50
4.50
4.25
4.75
6.25
5.50
7.00
8.10
6.50
9.75
22.00
21.00
23.00
11.50
10.00
13.00
19.00
18.00
20.00
13.50
13.00
14.25
15.60
15.30
16.00
Basal
petiole
length
(mm)
4.50
4.00
5.00
4.00
3.80
4.20
15.00
14.25
15.50
7.00
6.75
7.50
2.00
1.75
2.25
11.00
10.50
11.50
5.00
4.75
5.25
4.50
4.25
5.00
7.00
6.50
7.50
6.25
6.00
6.50
2.00
1.75
2.25
6.80
5.30
8.50
8.00
7.50
8.50
8.50
7.00
10.00
1.25
1.00
1.50
8.00
7.75
8.25
15.00
14.75
15.25
Stem
petiole
length
(mm)
3.00
2.50
3.30
3.25
3.00
3.75
9.00
7.00
11.00
4.50
3.75
5.00
0.00
0.00
0.00
6.83
6.00
7.50
3.25
3.00
3.75
3.10
2.25
4.50
7.25
6.25
8.50
5.75
5.25
6.75
1.00
0.75
1.25
5.60
5.00
6.00
2.00
1.70
2.20
3.75
3.50
3.90
0.00
0.00
0.00
4.75
4.50
5.00
9.00
8.75
9.50
IRAN. J. BOT. 20 (1), 2014
Table 3. Qualitative characters state of nutlet and leaf in studied taxa. (Sc, Sculptured; Sm, Smooth)
Nutlet
No.
Taxa
Herbarium
code
Shape Surface Structure
H.
bituminosus
12854
Elliptic
Sc
2 H. calycinus
12551
Elliptic
Sc
3 H. elegans
13303
Oblong
Sc
4 H. incanus
3980
Elliptic
Sm
5 H. longiflorus
1277
Oblong
Sm
1
Leaf
Truncate
tubercle
Convex
tubercle
Undulate
Flattened
EPW
Prominent
AW
Truncate
tubercle
Minute
tubercle
H.
oxyodontus
H.
7
Platystegius
H.
8
sessilifolius
3931
Elliptic
Sc
84719
Oblong
Sc
35593
Elliptic
Sc
Verrucose
9 H. yazdianus
98646
Elliptic
Sc
Verrucose
44723
Oblong
Sm
16289
Oblong
Sm
12 N. laxiflora
74565
Oblong
Sc
13 N. makuensis
71140
Obovate
Sm
14 N. oxyodonta
57425
Oblong
Sc
15 N. sessilifolia
63945
Late
obovate
Sc
L.
tschimganicus
6426
Obovate
Sm
16959
Obovate
Sm
6
N.
depauperate
N.
11
dschuparensis
10
16
17 L. turcicus
Shap
Base
Apex
F. Serpooshan & al.
Leaf trichomes
Short
MultiLong
Microcell
Indumentum multiLong
multi-cell papillate
cell
head capitate
density
trich.
trich.
trich.
gland
OvateSubLaxe
Present Absent
Acute
cordate cordate
OvateSubObtuse
Laxe
Present Absent
cordate cordate
Ribbon
OvateSubSub-dense Present
Obtuse
cordate cordate
like
OblongVery
dense
Present
Frequent
Truncate Obtuse
ovate
Ribbon
OblongDense
Absent
Truncate Acute
ovate
like
OblongSubLaxe
Present Absent
Acuminate
ovate
cordate
OblongSubSub-dense Present
Rare
Acute
ovate
cordate
OvateLaxe
Present
Rare
Cordate
Acute
cordate
Ribbon
OvateSubDense
Absent
Obtuse
cordate cordate
like
SubDense
Present Absent
Triangular
Acute
cordate
Convex
EPW
Irregular
Dense
Absent Frequent
Triangular Cordate Acuminate
texture
SubLaxe
Present Absent
Verrucose Oblong
Acute
cordate
Depressed OvateSub-dense Absent Absent
Cordate Obtuse
EPW
cordate
OvateSubVerrucose
Obtuse Very dense Present Frequent
cordate cordate
OvateSubSub-dense Absent Absent
Verrucose
Acute
cordate cordate
Ribbon
Convex
OvateSubSub-dense Present
Obtuse
EPW
cordate cordate
like
Convex
OvateSubVery dense Absent Absent
Acute
EPW
cordate cordate
Multicell
stalk
gland
91
Wax
Absent Present Absent
Absent Absent
Absent Present Absent
Absent Absent
Absent Present
Absent Absent
Rare
Present Present Absent
Absent Absent
Absent Absent Frequent Smooth Absent
Absent Present Absent
Absent Absent
Present Present Absent
Absent Absent
Absent Present Absent
Absent Absent
Absent Absent Frequent Smooth Absent
Present Absent Absent
Absent Absent
Present Absent Frequent Absent Absent
Absent Absent Absent
Absent Absent
Absent Absent Frequent Striate Present
Absent Present
Rare
Absent Absent
Absent Present Frequent Smooth Present
Absent Absent
Rare
Striate Absent
Absent Absent Frequent Smooth Absent
92 Nutlet and leaf characters in Hymenocrater
IRAN. J. BOT. 20 (1), 2014
Squared Euclidean distances
H. bituminosus -1
H. calycinus -2
H. sessilifolius -8
H. oxyodontus -6
H. Platystegius -7
H. elegans -3
N. oxyodonta -14
N. depauperata -10
N. laxiflora -12
H. incanus -4
N. dschuparensis -11
L. tschimganicus -16
L. turcicus -17
N. makuensis -13
H. yazdianus -9
N. sessilifolia -15
H. longiflorus -5
Factor 2
+
Multi-celled head glands
Short trichomes
Multi-celled stalk glands
+
+
s
Factor 1
Leaf length
Leaf width
Nutlet length
Areole length
Nutlet width
+
+
+
+
+
Fig. 5. Cluster analysis (WARD) and ordination of studied taxa. Species number as in tables. 2-3.
IRAN. J. BOT. 20 (1), 2014
L. turcicus and H. yazdianus (Fig. 4E) and with striate
stalk cells e.g. in L. tschimganicus and N. makuensis
(Fig. 3E; 4F).
Epicuticular waxes
Epicuticular waxes are structural elements of leaf
surface and of fundamental functional and ecological
importance (Barthlott & al. 1998). Different types of
waxes have been described in plants. Crystalloids are
the local wax projections and are of crystalline nature.
Crystalloids may arrange in locally restricted patterns
in contrast to their usual orientation patterns that cover
the whole epidermal surface. Locally restricted patterns
are connected to a certain epidermal structure i.e.
around stomata and at the base of trichome (Barthlott &
al. 1998). In a few species of Nepeta studies in this
work, locally restricted orientation pattern of
crystalloid type of waxes were observed. Crystalloids
of plate type with irregular shapes (amoeba shape) and
dentate margins were observed around trichomes and
stomata on abaxial and adaxial leaf surfaces in N.
sessilifolia and N. makuensis (Fig. 3F). These
structures were not observed in any studied
Hymenocrater species.
DISCUSSION
Cluster analysis and ordination among species of
Hymenocrater, Nepeta sect. Psilonepeta and
Lophanthus support the affinities among these genera.
Three main clusters are produced and every cluster is
enclosed by species of two or three genera. The first
cluster with two sub-clusters consists of six species of
Hymenocrater and one species of Nepeta. In the first
sub-cluster H. bituminosus, H. calycinus, H.
sessilifolius, H. oxyodontus and H. platystegius are
placed very closely to each other. Hymenocrater
elegans and N. oxyodonta form the second sub-cluster.
As illustrated in the results, the studied species show
two types based on nutlet surface, smooth and
sculptured. All species placed in first cluster have
sculptured nutlets. There are clear differences among
H. bituminosus, H. calycinus, H. elegans, H.
oxyodontus and H. platystegius with sculptured nutlets
and other species which have smooth nutlets. This
characteristic is congruent with their life form, the
sculptured nutlet type occurs in species that are
strongly lignose at the base. Nepeta depauperata, N.
laxiflora, H. incanus and N. dschuparensis form the
second cluster from which H. incanus has absolutely
smooth surface. In the third cluster L. tschimganicus, L.
turcicus and N. makuensis are placed closely in one
sub-cluster and H. yazdianus, N. sessilifolia and H.
longiflorus form another sub-cluster. All species of
third cluster have smooth nutlets except H. yazdianus
F. Serpooshan & al.
93
(98646, TARI) and N. sessilifolia. Budantsev &
Lobova (1997) in their studies on tribe Nepeteae,
demonstrated taxonomic importance of fruit
morphology. They have considered the species of
Nepeta sect. Psilonepeta in the genus Lophanthus
based on their morphological similarites. In this study
nutlet surfaces show a constant feature within most
species of Hymenocrater but intraspecific variation
were also found in nutlets of H. elegans and H.
yazdianus. The examination of trichomes on leaf
surfaces of studied taxa shows different features among
species groups that are congruent with nutlet surface
patterns. The presence of multi-celled head glands and
the absence or rarely presence of long stalked capitate
glands is the characteristic features in species of the
first cluster. Non-glandular trichomes covered with
micro-papillae are common in most species placed in
second cluster. In the third cluster species with capitate
glandular trichomes with a long ribbon-like stalk cell or
multi-cellular stalk are grouped. We did not have any
nutlet of N. allotria and L. lipskyanus available, so they
have not been included in our data set and analysis. As
illustrated in results, N. allotria has significant long
stalked capitate glands, similar to N. sessilifolia and L.
turcicus, while L. lipskyanus has multi-cellular nonglandular trichomes with long and thin-walled basal
cell, similar to H. longiflorus and H. yazdianus.
According to our results different patterns of trichome
types have taxonomic value and the group of species in
each cluster have similar trichome types, so it seems
that N. allotria and L. lipskyanus may be close to
species formed the third cluster.
Factor analysis revealed the most influential variable
characters among studied species (Tab. 4). The first 3
factors comprise about 46% and the first 7 factors
comprise about 88% of total variation. The leaf length,
leaf width, nutlet length, areole length, nutlet width,
multi-celled head glands, short trichomes, multi-celled
stalk glands, nutlet shape and the nutlet surface, with
the highest correlation are the most variable characters
in grouping the taxa in ordination (Fig. 5). The nutlet
length, nutlet width, leaf length, leaf width and the
length of areole are the most important and diagnostic
characters in defining the group comprising H.
longiflorus and N. sessilifolia and the group comprising
N. dschuparensis, N. depauperata and H. incanus,
besides the other characters which may be common
within other species group. The group comprising of
H. bituminosus, H. calycinus, H. sessilifolius, H.
oxyodontus, H. platystegius, H. elegans, N. oxyodonta
and N. laxiflora share the diagnostic characters
including multi-celled head glands, short trichomes and
sculptured nutlet surface. The group comprising of L.
tschimganicus, L. turcicus, N. makuensis and H.
94 Nutlet and leaf characters in Hymenocrater
IRAN. J. BOT. 20 (1), 2014
Table 4. Factor analysis of nutlet and leaf characters in studied taxa.
Characters
Leaf length
Leaf width
Nutlet length
Areole length
Nutlet width
Areole lobes angle
Multi-celled head glands
Short trichomes
Multi-celled stalk glands
Nutlet shape
Leaf shape
Wax
Nutlet surface
Nulet structure
Micro -papillae
Stem leaf petiole
Basal leaf petiole
Long trichomes
Long capitate
Leaf apex
Leaf base
Indumentum density
1
2
3
Component
4
5
6
7
0.922
0.846
0.755
0.678
0.667
-0.146
-0.176
0.088
-0.259
-0.041
-0.248
-0.112
0.022
0.079
0.404
-0.174
0.045
-0.006
-0.186
-0.225
-0.251
-0.206
-0.189
-0.177
0.271
-0.102
0.490
0.924
-0.863
-0.674
0.636
0.021
-0.238
0.171
0.066
-0.297
-0.173
0.020
0.065
0.051
0.357
0.171
-0.060
-0.330
0.202
0.378
-0.220
-0.163
0.101
0.099
-0.092
0.467
-0.611
0.928
-0.745
-0.665
-0.058
-0.041
0.442
-0.119
0.065
0.263
-0.283
-0.058
0.140
0.076
-0.140
-0.070
0.082
0.582
0.287
-0.047
-0.340
-0.133
-0.010
-0.081
-0.140
0.079
0.954
-0.900
0.449
-0.012
-0.216
0.107
0.062
-0.094
0.059
-0.388
-0.048
-0.108
0.164
-0.158
-0.104
0.046
0.067
-0.285
0.015
-0.007
-0.211
0.367
-0.083
0.100
0.407
0.930
0.923
0.137
-0.269
0.070
-0.082
0.018
0.059
-0.003
-0.115
0.031
0.216
0.111
0.090
-0.098
-0.053
0.184
0.295
-0.123
0.026
-0.216
0.027
0.031
-0.122
0.861
0.724
-0.641
-0.081
-0.443
-0.083
0.191
-0.443
-0.189
-0.220
0.011
0.092
-0.032
0.324
0.066
0.016
-0.314
0.102
-0.042
0.244
-0.122
0.018
0.304
-0.039
0.283
0.863
-0.586
yazdianus share the multi-celled stalk glands as a
significant character. The results of cluster analysis and
ordination show almost the same species gropus (Fig.
5).
The morphological features of some genera in
Nepetinae
including
Lophanthus,
Nepeta,
Hymenocrater and Marmoritis are very similar. We did
not have access to specimens of the genus Marmoritis
for our morphological studies but in our results the
distribution of Hymenocrater species within all clusters
together with species of Nepeta sect. Psilonepeta and
Lophanthus, may be inferred as their close relationships
and the possibility of inclusion of them in one genus.
These results support previous idea about affinities
between Lophanthus and Nepeta section Psilonepeta
(Levin 1941 and Budantsev 1992) bringing the idea of
the possible inclusion of some of these genera
considering the nomenclatural rules. The phylogenetic
relationships of the above mentioned genera have been
elucidated by Drew & Systma (2012), but they
examined one species from each genus, so in their
result, the real relationship among the species of these
four genera could not be inferred properly.
Although our results enhance the taxonomic
significance
of
morphological
characters,
a
comprehensive phylogenetic study is needed for
defining systematic relationships in this group. We
hope that it could be achieved by means of molecular
study which will be done in continue of this project.
ACKNOWLEDGEMENTS
We wish to thank the authorites of Research Institute of
Forests and Rangelands for the permision of using the
herbarium specimens of TARI. We are also thankful to
the authorities of the IRAN herbarium for the
permision of examining some type specimens. We
acknowledge the Islamic Azad University, science and
research Branch (Tehran) and Razi Metallurgical
Research Center (Tehran) for their cooperatin in this
project.
REFERENCES
Abbas Azimi, R., Jamzad, Z., Sefidkon, F. and
Bakhshi-Khaniki, Gh. 2006: The potential value of
phytochemical and micromorphological characters
in taxonomic treatment of genus Vitex L.
(Lamiaceae). Iran. Journ. Bot. 12(1): 15-35.
Barthlott, W., Neinhuis, C., Cutler, D., Ditsch, F.,
Meusel, I., Theisen, I., Wilhelm, H., 1998:
Classification and terminology of plant epicuticular
waxes. Bot. Journ. Linn. Soc. 126: 237-260.
Budantsev, A.L. 1992: The system and synopsis of the
genus Lophanthus (Lamiaceae). Bot. Zhurn. 77(9):
69-77 (in Russian).
Budantsev, A.L. & Lobova T.A. 1997: Fruit
morphology, anatomy and taxonomy of tribe
Nepeteae (Labiatae) Edinb. J. Bot. 54(2): 183-216.
Cantino, P.D. 1990: The phylogenetic significance of
IRAN. J. BOT. 20 (1), 2014
stomata and trichomes in the Labiatae and
Verbenaceae. J. Arnold Arbor. 71: 323-370.
Dinc, M., Pinar, N.M., Dogu, S. & Yildirimli S. 2009:
Micromorphological studies of Lallemantia L.
(Lamiaceae) species growing in Turkey. Acta
Biologica Cracoviensia Series Botanica. 51(1):4554.
Dirmenci, T., Yildiz, B., Hedge, I.C. & Firat, M. 2010:
Lophanthus (Lamiaceae) in Turkey: a new generic
record and a new species. Turk. J. Bot. 34: 123-129.
Drew, B.T. & Systma, K.J. 2012: Phylogenetics,
biogeography and staminal evolution in the tribe
Mentheae (Lamiaceae). Am. J. Bot. 99(5): 933-953.
Eshratifar, M., Attar, F. & Mahdigholi, K. 2011:
Micromorphological studies on nutlet and leaf
indumentum of genus Teucrium L. (Lamiaceae) in
Iran. Turk. J. Bot. 35: 25-35.
Gohari, A.R., Saeidnia, S., Mollazadeh, K., Yassa, N.,
Malmir, M. & Shahverdi A.R. 2010: Isolation of a
new quinic acid derivative and its antibacterial
modulating activity. Daru J. Pharm. Sci. 18(1): 6973.
Harley, R.M., Atkins, S., Budantsev, A.L., Cantino,
P.D., Conn, B.J., Grayer, R., Harley, M.M., de Kok,
R., Krestovskaja, T., Morales, R., Paton, A.J.,
Ryding, O. and Upson, T. 2004: Labiatae. In:
Kubitzki, K. and Kadereit, J.W. (eds.) The families
and genera of vascular plants. vol. 7. Spriger,
Berlin. 167-275.
Hedge, I.C. 1992: A global survey of the biogeography
of the Labiatae. In: Harley, R.M. & Reynolds, T.
(eds) Advances in Labiatae science. 7-17. Royal
Botanic Gardens, Kew.
Jafari, A. & Jafarzadeh, F. 2008: Anatomical and
pollen Ornamentation study on Hymenocrater
species in North East of Iran. Pakistan Journal of
Botanical Sciences 11(17): 2149-2153.
Jamzad, Z., Harley, M.M., Ingrouille, M., Simmonds,
M.S.J. & Jalili, A. 2000: Pollen exine and nutlet
surface morphology of the annual species of Nepeta
L. (Lamiaceae) in Iran. In: Harley M.M., Morton,
C.M. & Blackmore, S., (eds.). Pollen and Spores:
Morphology and Biology. 385-397. Royal Botanic
Gardens, Kew.
Jamzad, Z., Chase, M.W., Ingrouille, M., Simmonds,
M.S.J., & Jalili, A. 2003: Phylogenetic relationships
in Nepeta L. (Lamiaceae) and related genera based
on ITS sequence data. Taxon. 52: 21-32.
Jamzad, Z. 2012: Fl. of Iran no. 76: Lamiaceae.
Research Institute of Forests and Rangelands,
Tehran.
Kaya, A. & Dirmenci, T. 2008: Nutlet Surface
Micromorphology of the Genus Nepeta L.
(Lamiaceae) in Turkey. Turk. J. Bot. 32: 103-112.
Levin, E.G. 1941: The genus Lophanthus and its
F. Serpooshan & al.
95
analogon Pseudolophanthus. Trudy Bot. Inst. Akad.
Nauk SSSR. Ser. 1, 5: 256-318 (in russian).
Marin, P.D., Duletic, S. and Petkovic, B. 1996: Nutlet
ornamentation in selected Salvia L. species
(Lamiaceae). Fl. Medit. 6: 203-211.
Moon, H.K. and Hong, S.P. 2006; Nutlet morphology
and anatomy of the genus Lycopus (Lamiaceae:
Mentheae). J. Plant. Res. 119: 633-644.
Moon, H.K., Vinckier, S., Smets, E. & Huysmans S.
2008a: Comparative pollen morphology and
ultrastructure of Mentheae subtribe Nepetinae (
Lamiaceae). Review of Paleobotany and
Palynology. 149: 174-186.
Moon, H.K., Vinckier, S., Smets, E. & Huysmans S.
2008b: Palynological evolutionary trends within the
tribe Mentheae with special emphasis on subtribe
Menthinae (Nepetoideae: Lamiaceae). Plant Syst.
Evol. 275: 93-108.
Moon, H.K., Hong, S.P., Smets, E. and Huysmans, S.
2009:
Phylogenetic
significance
of
leaf
micromorphology and anatomy in the tribe
Mentheae (Nepetoideae: Lamiaceae). Bot. Journ.
Linn. Soc. 160: 211-231.
Navarro, T. and Oualidi, J.El. 2000: Trichome
morphology in Teucrium L. (Labiatae). A
taxonomic review. Anales Jard. Bot. Madrid. 57(2):
277-297.
Padure, I.M. 2003: Fruit morphology, anatomy and
mixocarpy in Nepeta cataria L. 'Citriodora' and
Nepeta grandiflora Bieb. (Lamiaceae).
Pojarkova, A.L. 1954: Flora U.S.S.R. in Shishkin, B.K.
& Yuzepchuk, S.V. (eds.). Ed. Akad. Nauk CCCP,
Moscova-Leningrad. XX: 286-437.
Rechinger, K.H. 1982: Flora Iranica. Vol. 150.
Akademische Druck. U. Verlagsanstalt, Graz.
Austria.
Roe, K.E. 1971: Terminology of Hairs in The Genus
Solanum. Taxon 20(4): 501-508.
Ryding, O. 2010: Pericarp structure and phylogeny of
tribe Mentheae (Lamiaceae). Plant Syst Evol. 285:
165-175.
Salmaki, Y., Zarre, SH., Jamzad, Z. and Brauchler, CH.
2009: Trichome micromorphology of Iranian
Stachys (Lamiaceae) with emphasis on its
systematic implication. Flora. 204: 371-381.
Satil, F., Unal, M. & Hopa, E. 2007: Comparative
morphological and anatomical studies of
Hymenocrater bituminosus Fisch. & C.A. Mey.
(Lamiaceae) in Turkey. Turk. J. Bot. 31: 269-275.
Wagstaff, S.J. 1992: A phylogenetic interpretation of
pollen morphology in tribe Mentheae (Labiatae). In:
Harley, R.M. & Reynolds, T. (Eds.), Advances in
Labiatae Science. Royal Botanic Gardens, Kew, pp.
113-124.