Morphometric study of some Salvia L. (Lamiaceae

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Morphometric study of some Salvia L. (Lamiaceae) species in
Iran
Navaz Kharazian1* Department of Botany, Faculty of Sciences, University of Shahrekord, 115,
Shahrekord, Iran, Telfax:+98-3814424419, E-mail: [email protected]
Abstract
1 This study concerns the morphological studies in some Salvia L. (Lamiaceae) species
in Iran. In order to elucidate the taxonomic status and morphological studies, 53
accessions of 12 Salvia species were collected from their natural habitats in Iran. A
total of 17 quantitative and 13 qualitative morphological characters were selected as
diagnostic characters in Salvia species through the use of numerical methods. The
statistical analysis consisted of cluster analysis with Euclidean distance coefficient,
factor analysis, descriptive analysis and variance analysis using SPSS V.20.0 software.
The clustering results of quantitative and qualitative morphological characters showed
five groups. Despite the high morphological similarity between S. nemorosa L. and S.
10 virgata Jaq., these species were separated using qualitative and quantitative
characters and factor analysis. Regarding cluster and factor analyses, S. spinosa L. and
S. atropatana Bunge accessions displayed high morphological diversity. Based on these
findings, morphological characteristics such as the features of the leaf, calyx, corolla,
bract, stamen and style were considered to be the appropriate diagnostic characters in
the taxonomy of the Salvia species studied.
Keywords: Iran, Lamiaceae, morphology, Salvia, variability.
Introduction
Salvia L., with nearly 1000 species worldwide and 55 species in Iran, is
one of the largest genus of Lamiaceae. It represents an enormous and
cosmopolitan distribution and displays a remarkable range of variation (Walker
20 et al., 2004). The main speciation centers of this taxon are considered to be
the eastern Mediterranean regions, south- west, western, eastern and central
regions of Asia, South Africa, and Central and South America (Hedge, 1990;
Kahraman and Dogan, 2010; Walker et al., 2004). It is distributed in
subtropical, temperate, sub- arctic and arctic areas as well as the tropical regions
of Iran (Hedge, 1982a; Walker et al., 2004). Some species are perennial,
herbaceous, suffruticose, fruticose and sub-shrubby (Hedge, 1982a; Khan et al.,
2002).
Having such morphological variability throughout the world, the genus
has a significant taxonomic position among the plant taxonomists (Baikova,
1996). In addition, owing to greater similarity in morphological characters and
1
30 the prevailing hybridization among Salvia species, high diversity in
polyploid levels, the presence of heterozygous individuals and the taxonomical,
ecological and genomic complexity, the species boundaries have become
blurred (Haque, 1983; Hedge, 1982a). So far, a comprehensive numerical
taxonomic study has not been sufficiently performed on Salvia species and it
needs to be revised in terms of the systematic positions.
The stamen type and the leaf, calyx and corolla characters were useful
features in taxonomic studies of the genus Salvia (Kahraman et al., 2010a;
Ozdemir and Senel, 1999; Ozkan and Soy, 2007). The taxonomy of S. officinalis
L. and S. fruticosa Mill. belonging to the section Salvia (Benth.) Hedge has been
40 studied using leaf form, inflorescence axis indumentums, petiole and calyx
indumentums (Reals et al., 2004). These characters have been mentioned for the
taxonomic insights. In addition, using the stamen properties Walker and Sytsma
(2006) determined the evolutionary interpretations which are related to the
polyphyletic origin of Salvia. Through the morphological characters such as leaf
and stem indumentums, bract form, bract color, bract margin, bract
indumentums, calyx indumentums, filament appendage, calyx length, corolla
length, bract length/bract width and corolla length/stamen length, Torke (2000)
studied the phenetic analysis among the species belonging to the section
Ekmania Epling. Corsi and Bottega (2002) and Kandemir (2003) also mentioned
50 that the bract characteristics and the type of glandular hairs served to identify
the Salvia species.
Based on the diversity properties, phenotypic variability in foliar
characters among Salvia species has been provided and most of the characters
showed highly significant inter- and intra- specific variations (Haque, 1983).
Also, the morphological diversity and genetic variability among some of the
Salvia species and accessions were reported using RAPD, AFLP and ISSR
markers (Darmono and Okada, 2008; Saeidnia et al., 2009; Song et al., 2010;
Zhand et al., 2009). Moreover, in our research Sajadi et al. (2010) reported the
genetic diversity among 12 Salvia species using AFLP molecular markers.
60 Consequently, this study aims to identify the taxonomic position of 12
Salvia species in Iran via numerical analyses, evaluate the extent of the
variations in the morphological characteristics, define the variability of Salvia
accessions and introduce the diagnostic characters useful in separation of the
species.
Materials and Methods
Morphological studies
70 In this section, 53 accessions of 12 Salvia species were collected from
their natural habitats in Iran (Tab. 1) and selected as OTUs. The voucher
specimens were deposited in the Herbarium of Shahrekord University. A total of
17 quantitative and 13 qualitative characters were assessed as diagnostic
characters in Salvia species and were used to study the taxonomic status and
morphometric analysis using a stereo-microscope (Reals et al., 2004). The
measured characters are presented in Tables 2, 3 and 4. These characters were
2
selected according to two criteria: 1) the common use for taxonomic
identification based on floras and our own observations and 2) the variability
among different taxa. The taxa studied were as follows: S. macrosiphon Boiss.,
80 S. spinosa L., S. sharifii Rech. f. & Esfand., S. nemorosa L., S. virgata Jaq.,
S. syriaca L., S. sclarea L., S. ceratophylla L., S. limbata C.A. Mey., S.
atropatana Bunge, S. multicaulis Vahl. and S. hydrangea DC. ex Hedge.
Statistical analysis
Statistical methods such as cluster analysis with Euclidean distance
coefficient and Ward method, factor analysis (PCA), variance analysis test
(ANOVA) and descriptive analysis as Coefficient of Variation (C.V.) using
SPSS V. 20.0 software were applied and the variability of Salvia accessions, the
taxonomic positions of Salvia species and the variability of morphological
characters were determined. The Pearson Correlation Coefficient also was
determined in each character.
3
Table 1: The locality of Salvia species studied in Iran
Species
Locality
Height
1- S. atropatana 41
Guilan- Kelardasht
2400
2- S. atropatana 91
Chahrmahal va Bakhtiari - Tangeh sayad,
dashteh chah
2850
3- S. atropatana 4
Mazandaran- pol-e Zangoule
2280
4- S. ceratophylla 15
Kermanshah- Sanandaj
1360
5- S. ceratophylla 13
Chahrmahal va Bakhtiari- Tangeh sayad, Sefid dasht, 2120
Bostan Shir
6- S. ceratophylla 4
Fars- Abadeh
1500
7- S. ceratophylla 16
Tehran- Karaj
1489
8- S. limbata 106
Chahrmahal va Bakhtiari– Saman, Horeh, Savadjan
2070
9- S. limbata 107
Chahrmahal va Bakhtiari– Saman, Horeh
2200
10- S. spinosa 1
Hamadan- ganjnameh
1800
11- S. spinosa 8
Chahrmahal va Bakhtiari- Rousta-e kaj
1600
12- S. spinosa 9
Chahrmahal va Bakhtiari- North west of
Ghaleh Darvish
1720
13- S. spinosa 10
Lurestan- Khoramabad
1850
14- S. spinosa 11
Chahrmahal va Bakhtiari- Saman- poleh zaman khan, 2040
shate Aliabad
15- S. spinosa 12
Chahrmahal va Bakhtiari- Saman, Horeh, Savadjan
2070
16- S. spinosa 17
Qazvin-manjil
450
17- S. spinosa 18
Isfahan- sadeh Zayandeh rood
2500
18- S. spinosa 42
Tehran-Delijan
2950
19- S. sharifii 5
Isfahan-Kolahghazi
1670
20- S. sharifii 8
Isfahan-Kolahghazi
1690
21- S. sharifii 4
Isfahan-Kolahghazi
1700
22- S. sclarea 22
Chaharmahal va Bakhtiari- Chartagh, Sabzeh kooh
2150
23- S. sclarea 23
West of Azerbayjan-Moghan
700
24- S. sclarea 24
Chahrmahal va Bakhtiari- 10 Km Baba Heydar, 2320
Chelgerd
25- S. sclarea 25
Kohkilouy-e va Boyerahmad- Sisakht
2110
26- S. macrosiphon 6
Isfahan-koh-e Sopheh
2300
4
Table 1: continue
27- S. macrosiphon 7
Fars- abadeh, Tashak,
1850
28- S. macrosiphon 63
Isfahan-Kolahghazi
1700
29- S. macrosiphon 64
Isfahan-Kolahghazi
1710
30- S. macrosiphon 5
Kermanshah- Karand
1730
31- S. macrosiphon 66
Chahrmahal va Bakhtiari- Saman,Ilbagi
2070
32- S. macrosiphon 68
Lurestan-Khoramabad
1200
33- S. syriaca 28
Chahrmahal va Bakhtiari- Boldaji,
Hamzeh Ali
2180
34- S. syriaca 29
West of Azerbayjan-Ardabil
1250
35- S. syriaca 80
Chahrmahal va Bakhtiari- Rousta-e Hosein 1720
abad, Ghaleh Darvish
36- S. syriaca 82
Hamedan- Ganjnameh
1900
37- S. syriaca 83
Guilan- Masouleh
2070
38- S. syriaca 84
Isfahan- Dalan kouh
1970
39- S. syriaca 8
Kokkilouye va boyer Ahmad-sisakht
2050
40- S. syriaca 2
Kokkilouye va boyer Ahmad- Yasouj
1980
41- S. multicaulis 43
Chahrmahal va Bakhtiari- Tangeh sayad, Sefid 2120
dasht, Bostan Shir
42- S. multicaulis 44
Mazandaran-Siyah bisheh
2000
43- S. multicaulis 45
Kermanshah- Harsin
2335
44- S. multicaulis 47
Chahrmahal va Bakhtiari- Tangeh sayad, koh-e 2550
Kondeh Rahim
45- S. multicaulis 48
Kordestan- Bijar
2335
46- S. multicaulis 49
Lurestan-Oshtoran kuh
1750
47- S. multicaulis 50
West of Azerbayjan- Miyaneh
1200
48- S. multicaulis 51
Fars- Kazeroun
2250
49- S. multicaulis 52
Isfahan- Semirom, Cheshme naz
2270
50- S. nemorosa 19
Ahvaz- Izeh
2000
51- S. virgata 20
Gorgan- Gonbad-e Kavous
1085
52- S. virgata 21
Chahrmahal va Bakhtiari- Dastgerd
2000
53- S. hydrangea 26
Chahrmahal va Bakhtiari- Tangeh sayad- koh-e 2400
Shor shor
5
Table 2: The quantitative morphological characters studied in Salvia
species.
1- calyx length (mm)
2- calyx spin length (mm)
3- bract length (mm)
4- bract width (mm)
5- calyx length/bract length
6- corolla length (mm)
7- bract length/ corolla length
8- theca length (mm)
9- style length (mm)
10- filament length/theca length
11- nutlet length (mm)
12- anther length (mm)
13- filament length/corolla length
14- nutlet width (mm)
15- filament length/style length
16- style length/corolla length
17- corolla tube length (mm)
Table 3: The qualitative morphological characters studied in Salvia species.
1- leaf form: pinnatisect, pinnatifid,
oblong,
linear-oblong,
oblonglanceolate, ovate, broadly ovate, ovateoblong,
ovate-lanceolate,
elliptic,
broadly elliptic, sub-orbicular, linear,
linear-lanceolate
8calyx
form:
campanulate,
campanulate-infundibular,
tubular,
tubular-campanulate, broadly tubular,
ovate-campanulate, broadly campanulate
2- leaf base form: cordate, sub-cordate,
cuneate, narrowed, oblique, rounded
9- corolla tube form: invaginate and
squamulate, non-invaginate and nonsquamulate
3- leaf margin form: entire, sub-entire,
crenulate,
serrate,
serrate-erose,
serrulate, erose, crenate, lobate, sublobate, dentate
10- style apex form: simple, thin
dichotomous, broad dichotomous
4- leaf apex form: acute, obtuse, subobtuse, rounded
11- stamen type: type A, type B
5- bract form: ovate, broadly ovate
12- nutlet form: spherical, sub-spherical,
rounded-trigonous, ovoid, broad ovoid
6- bract apex form:
acuminatespinulose, acuminate, cuspidate
13- nutlet color: light brown,
brown, yellow, light gray, black
7- bract color: green, green-yellow,
green-white, pink, violet
6
dark
Table 4: The data matrix of qualitative morphological characters studied in Salvia species.
Ch./sp.1
1
2
leaf form
Ovate-oblong,
elliptic, ovate
Ovate, broadly Ovate
elliptic, ovateoblong, broadly
ovate
leaf base form
Rounded,
cordate,
cordate
leaf margin form
Sub-entire,
serrate, lobate
leaf apex form
Obtuse,
rounded
bract form
Broadly ovate
bract apex form
Sub-cordate,
sub- cuneate,
rounded,
cordate
3
Rounded
Entire, erose, Sub-entire,
sub-entire,
serrate
dentate
4
5
6
Ovate-oblong, Oblongbroadly ovate, lanceolate
oblong
Cordate,
cordate
sub- Cordate,
cordate
7
8
9
Ovate,
ovate- Linear,
linear- Pinnatifid
oblong,
ovate- oblong, elliptic,
lanceolate
linear-lanceolate
sub- Cordate
Oblique, cuneate
Elliptic,
orbicular
Narrowed
10
sub- Pinnatisect
11
12
Broadly ovate
Ovate, ovateoblong,
broadly ovate
Cordate,subcordate
rounded
Oblique,
rounded
Narrowed
Cordate
Erose,
sub- Crenate,
entire,
serrulate
crenulate,
serrate
Erose, serrulate
Erose,
lobate, Entire, sublobate
sub-entire,
crenate, serrate
Crenulate
Entire
Erose,
lobate
Acute, obtuse
Acute, obtuse, Acute
rounded
Acute, obtuse
Obtuse
Obtuse
Acute
Acute, obtuse
Obtuse subobtuse, acute
Broadly ovate
Ovate
Ovate
Ovate
Ovate
Broadly
ovate
Ovate
Broadly
ovate, ovate
Acuminate
Acuminatespinulose
Acuminate
Acuminate
Acuminate
Acuminate
Acuminate
Cuspidate
Acuminate
Acuminate
Acuminate
Acuminate,
cuspidate
bract color
Green-yellow,
pink
Green-yellow,
pink, green
Green
Green
Violet
Green-white
Green, pink
Green
Green, pink
Green
Green
Pink,
green-white
calyx form
Tubular
Broadly tubular Tubular
Tubularcampanulate
Tubularcampanulate
Tubular
Campanulateinfundibular
Ovatecampanulate
Broadly
campanulate
Campanulateinfundibular
Campanulate
Ovatecampanulate
corolla tube form
Non-invaginate
Non-invaginate Non-invaginate Non-invaginate Non-invaginate Non-invaginate
Invaginate
and
non- and
non- and
non- and
non- and
non- and
non- squamulate
squamulate
squamulate
squamulate
squamulate
squamulate
squamulate
style apex form
Broad
dichotomous
acute, Acute, obtuse
Simple, broad Broad
dichotomous
dichotomous
Thin
dichotomous
Thin
dichotomous
Broad
dichotomous
7
Obtuse
ovate, Broadly
ovate
Broad
dichotomous
and Invaginate
squamulate
ovate, Ovate, broadly Ovate
ovate
sub-
Crenate,
erose,
serrate-erose
and Non-invaginate Non-invaginate
Invaginate and Invaginate
and
non- and
non- squamulate
and
squamulate
squamulate
squamulate
Broad
Broad
dichotomous, thin dichotomous,
dichotomous
simple
Thin
dichotomous
Broad
dichotomous
Thin
dichotomous
Table 4: continue
stamen type
Type B
Type B
Type B
Type B
Type B
Type B
Type B
Type B
Type A
Type A
Type B
Type B
nutlet form
Broad ovoid
Roundedtrigonous,
spherical
Ovoid
Ovoid
Ovoid
Roundedtrigonous
Ovoid
Spherical
Ovoid,
roundedtrigonous
Sub-spherical,
Ovoid
Roundedtrigonous,
spherical
Light brown
Light brown
nutlet color
Light brown
Light brown, Light brown
dark
brown,
light gray
Black,
brown
dark Black,
brown
dark Yellow
Yellow,
brown
light Black
1: 1- S. macrosiphom, 2- S. spinosa, 3- S. sharifii, 4- S. virgata, 5- S. nemorosa, 6- S. syriaca, 7- S. atropatana, 8- S. ceratophylla, 9- S. multicaulis, 10- S. hydrangea, 11- S. limbata, 12- S. sclarea.
8
roundedtrigonous
Light brown, Light brown
dark brown
90 Results
As the results of this study show, the quantitative morphological
characters such as the calyx length, bract length, bract length/ corolla length,
calyx length/bract length, corolla length, corolla tube length, filament length,
filament length/theca length, filament length/style length, style length and style
length/corolla length are the most appropriate taxonomical characters. Among
the qualitative morphological characters we found the best to be; leaf form,
margin leaf form, bract form, bract colour and bract apex form.
Based on ANOVA analysis, bracteole length (sig. = 0.003), corolla length
100 (sig. =0.00), bract length/ corolla length (sig. =0.002), filament length (sig.
=0.001), filament length/theca length (sig. =0.047), filament length/style length
(sig. =0.039), style length (sig. = 0.018) and style length/corolla length (sig. =
0.025) display significant differences (P< 0.05).
The highest morphological variability was found in theca length (C.V. =
81.4) and the lowest was found in filament length/ theca length (C.V. = 10.8)
(Fig. 1). The morphological variability among the Salvia accessions showed that
the highest variations were related to the theca length (C.V. = 98.3, 90.2; S.
atropatana, S. ceratophylla, respectively), anther length (C.V. = 97.7; S.
nemorosa), filament length/corolla length (C.V. = 92.8, 92.3, 71.4; S. sclarea, S.
macrosiphon, S. spinosa, respectively), filament length/theca length (C.V.=
92.1; S. syriaca), nutlet length (C.V. = 91.6; S. sharifii), calyx length/bract
length (C.V.= 90.6; S. virgata), corolla length (C.V. = 83.8, 80; S. multicaulis,
110 S. hydrangea respectively) and calyx spin length (C.V. = 51.4; S. limbata).
The lowest variations were found in calyx length (C.V. = 11.6, 8.9, 7.26, 5.98,
5.3, 4.5, 3.12; S. spinosa, S. syriaca, S. macrosiphon, S. sclarea, S. ceratophylla,
S. sharifii, S. hydrangea respectively), style length (C.V. = 10.4; S. virgata),
nutlet length (C.V. = 9; S. multicaulis), nutlet width (C.V. = 5.3; S.
ceratophylla), corolla tube length (C.V. = 1.27; S. limbata), calyx spin length
(C.V. = 1.2; S. atropatana) and bract length/ corolla length (C.V. = 1.6; S.
nemorosa) (Fig. 2 and 3 ). The Pearson correlation coefficient displayed that the
characters such as bract length and bract width (0.790), bract length and anther
length (0.655), corolla length and style length/corolla length (0.659), corolla
length and filament length/style length (0.637), corolla length and corolla tube
length (0.814), filament length/theca length and corolla length (0.692), style
length and corolla tube length (0.833), nutlet length and nutlet width (0.857),
filament length/corolla length and filament length/style length (0.726), style
length/corolla length and corolla tube length (0.652), and filament length/style
length and corolla tube length (0.694) have significant correlations (0.01 and
0.05 levels).
We obtained the dendrogram shown in Figure 4. The distribution of the
morphological characters show how these are used for the taxonomic
differentiation of the groups studied. In cluster analysis using the quantitative
120 and qualitative morphological characters, we distinguish five clusters
including: group 1) S. sharifii, S. macrosiphon and S. spinosa, group 2) S.
limbata and S. atropatana, group 3) S. multicaulis, S. sclarea, S. ceratophylla, S.
9
hydrangea and S. atropatana group 4) S. nemorosa, S. virgata, and S. syriaca
and group 5) S. spinosa (Fig.1). We found that S. multicaulis accessions
comprised four groups in cluster 3, which clustered with S. hydrangea, S.
sclarea and S. ceratophylla. Moreover, S. nemorosa and S. virgata were mainly
grouped. S. syriaca, S. ceratophylla, S. sclarea and S. macrosiphon contained
two groups in clusters 4, 3, 3 and 1 respectively, S. sharifii, S. atropatana and S.
spinosa comprised two groups in clusters c1, c2-c4 and c1-c5 respectively
which displayed high diversity among their accessions (Fig. 4).
130 Using quantitative and qualitative morphological characters and 12
Salvia species and 52 accessions, the factor analysis (PCA) confirmed the
cluster analysis results. In this case five groups comprised. S. limbata and S.
atropatana were definitely distinct from S. sclarea and S. ceratophylla. Despite
the high similarity between S. nemorosa and S. virgata, these species are
definitely distinct. Moreover, S. spinosa and S. macrosiphon were closely
grouped but definitely distinct (Fig. 5).
10
Figure1: Mean, standard deviation and coefficient of variation in
quantitative characters studied in Salvia species.
cal: calyx length, casp.l: calyx spin length, b.l: bract length, b.w: bract width, cal/bl: calyx length/bract length, col:
corolla length, brl/col: bract length/corolla length, thecl: theca length, fil/thecl: filament length/theca length, stl: style
length, antl: anther length, nutl: nutlet legth, nutw: nutlet width, fil/col: filament length/corolla length, stl/corl: style
length/corolla length, fil/stl: filament length/style length, cot: corolla tube length
11
Figure 2: The variability of quantitative morphological characters (C.V.)
among the accessions of Salvia species in S. macrosiphon (mac), S. spinosa
(spin), S. sharifii (sha), S. virgata (virg), S. syriaca (syr).
12
Figure 3: The variability of quantitative morphological characters (C.V.)
among the accessions of Salvia species in S. atropatana (atr), S. ceratophylla
(cer), S. multicaulis (mult), S. limbata (lim), S. sclarea (scl).
13
Figure 4: Dendrogram of cluster analysis using morphological characters
and Salvia accessions. mac: S. macrosiphon, spin: S. spinosa, sha: S. sharifii, virg.: S. virgata, syr.: S. syriaca, atr: S.
atropatana, cer: S. ceratophylla, mult: S. multicaulis, hyd: S. hydrangea, limb: S. limbata, scl: S. sclarea. nem: S. nemorosa.
14
Figure 5: Factor analysis in 52 Salvia accessions using morphological
characters.
Discussion
140 As the results of the morphological studies demonstrate, most of the
Salvia species studied have been discriminated by calyx form, calyx length,
corolla length, corolla tube length, bract length, bract length/ corolla length,
filament length and style length, which are in accordance with Kahraman and
Dogan (2010), Kahraman et al. (2010b), Ozkan and Soy (2007) and Reals et al.
(2004). S. spinosa is closely related to S. macrosiphon, but it differs in
diagnostic characters such broader leaves and calyx, which is based on the
Kharazian (2009) results. Moreover, in our results S. nemorosa and S. virgata,
which have a high similarity in morphological characters, are diagnosed by
bract colour, corolla length, filament and style length. As the results of statistical
150 analysis show, the best morphological characters were selected to evaluate
15
the taxonomic position. Thus, the characters relating to quality and quantity of
calyx, corolla, bract, stamen and style are introduced as appropriate
morphological characters and are used in the taxonomic status of this genus
(Tab. 2 and 3). Moreover, Kahraman et al. (2010b), Kahraman et al. (2009) and
Kaya et al. (2007) reported that the stem indumentums, corolla length, bract
length and stamen type are of sufficient taxonomical significance to identify
some Salvia species. Ryding (1994) proved that the length of hairs in the bract
and bracteole margin can be applied to taxonomical studies. This evidence is not
in agreement with our morphological studies in each Salvia species.
160 According to Hedge’s classification (1982a), the Salvia species have
been divided into five groups. S. multicaulis, S. hydrangea, S. ceratophylla were
categorized in a group with simple, pinnatisect and pinnatifid leaf, biennial and
perennial herbaceous, suffruticose or fruticose stem, large and non-convoluted
leaf and corolla length 8-40 mm. Moreover, S. multicaulis was divided into
group with fertile pollen, anther- like lower theca and calyx clearly expanded in
fruit or scarcely expanded. S. syriaca, S. nemorosa, S. virgata, S. macrosiphon,
S. spinosa, and S. sharifii were in a group including corolla tube not-invaginated
and not- squamulate and inside of corolla tube not perfectly or perfectly
annulated. S. sclarea, S. atropatana, S. ceratophylla and S. limbata were in a
170 group including invaginated and squamulate corolla tube, and inside of
corolla tube glabrous (Hedge, 1982a).
In cluster and factor analyses, S. multicaulis and S. hydrangea were in
accordance with Hedge’s classification (1982a), S. ceratophylla accessions were
clustered in different groups such as S. multicaulis and S. sclarea which was in
agreement with Hedge's taxonomy (Fig. 1 and 2). Obviously, based on
qualitative and quantitative characters, S. multicaulis comprised different groups
which are nearly in concurrence with Hedge’s treatment (1982a) (Fig. 1). Hedge
(1982a) only reported the variation of leaf and stem indumentums in this
species. In our research, these variations are generally connected to the
indumentums of stem, leaf, petiole, calyx and inflorescence axis, leaf form,
calyx apex, calyx color and bract form. It appears that morphological variations
are closely related to the varieties, forms or the polymorphism characters for this
180 species. In our research using AFLP molecular markers, we concluded that
S. multicualis and S. hydrangea were mainly clustered. In addition, using this
method S. multicaulis comprised one group (Sajadi et al., 2010), which has been
partially confirmed by morphological characters and cluster analysis (Fig. 1;
cluster c3).
As mentioned above, most of the species which were in groups with
corolla tube not-invaginated and not- squamulate have been confirmed by the
clustering and factor analysis of this study (Fig. 1 and 2). In cluster analysis, S.
190 macrosiphon accessions were in two different groups in cluster c1 (Fig. 1).
Owing to the hybridization and introgression of S. macrosiphon with other
species, such as S. moorcroftiana Wall. Ex Benth. and S. reuterana Boiss, it can
also be considered as variation patterns in this species (Hedge, 1990,1982a). In
addition, this variability was observed in Sajadi et al. (2010). In this research,
most of the variations were in leaf indumentums, leaf form, leaf base, leaf
16
margin, bract indumentums, corolla color, corolla tube length, calyx length,
calyx apex and inflorescence indumentums (Kharazian, 2008).
In the clustering results, S. spinosa and S. macrosiphon were closely
grouped in cluster c1. As previously mentioned these two species are extremely
200 similar but were distinguished using diagnostic characters (Kharazian,
2009). Moreover, the high variability of S. spinosa accessions (including two
groups) seems to either show the high hybridization and introgression with S.
macrosiphon or prove the variation of this species in Iran (Kharazian, 2009).
Additionally, these results are in accordance with our molecular marker research
(Sajadi et al., 2010). The morphological variations among the S. spinosa
accessions were in leaf form, leaf margin form, leaf indumentums, stem
indumentums, inflorescence indumentums, bract indumentums, bract
dimension, bract color, calyx indumentums, calyx dimension, corolla
indumentums and corolla length (Kharazian, 2009).
210 It has been noted that based on the quantitative and qualitative
findings, S. sharifii accessions showed different groups, which is in agreement
with Sajadi et al. (2010). This variation is related to the stem, leaf and bract
indumentums. In most cases, S. sharifii was grouped with S. macrosiphon (Fig.
1) which is based on the findings of Sajadi et al. (2010). Some of the S. sharifii
accessions belonging to south and south-east regions of Iran are related to S.
macrosiphon (Hedge, 1982a), confirming our results (Fig. 1). In addition, S.
sharifii and S. macrosiphon are morphologically closely related. It can be
concluded that the morphological characters such as bract length and corolla
length are diagnostic features among these two species.
220 In factor analysis, S. nemorosa was strongly separated from S. virgata
(Fig. 2), which is in accordance with Sajadi et al. (2010), but in cluster analysis,
were closely clustered (Fig. 1). Based on Hedge’s classification (1982a), these
two species were diagnosed using bract color and corolla length. As previously
mentioned in our results, these are also separated through bract, calyx, filament
and style features. According to Kaya et al. (2007), some of these characters are
well-documented taxonomic characters in Salvia genus.
Furthermore, using cluster analysis S. syriaca was found to comprise of
two groups in cluster c4 and mainly grouped with S. nemorosa and S. virgata,
230 including the group with corolla tube not- invaginated and not- squamulate
(Hedge, 1982a). The high morphological variability in S. syriaca is due to the
stamen features (Fig. 1). According to Ozkan et al. (2009), stamen feature in
Salvia species represents the morphological diversity. This diversity was also
displayed in molecular markers (Sajadi et al., 2010).
In relation to the group with invaginated and squamulate corolla tubes, S.
atropatana accessions were found to mainly consist of two different groups,
which were related to the high polymorphism characters among the accessions
(Kharazian, 2012). In cluster analysis, S. atropatana was clustered with S.
limbata, which is in agreement with Hedge’s classification (1982a) and in 240
another case, clustered with S. sclarea, which is in accordance with Sajadi et al.
240 (2010) (Fig. 1). These variations are in the stem and leaf indumentums, leaf
17
form and leaf margin form, inflorescence indumentums, bract indumentums,
pedicel indumentums, corolla and calyx length, corolla and calyx indumentums,
corolla tube indumentums and style length. Hedge (1982a) stated that this
species displays variability only in leaf features. In our AFLP molecular marker
results, we observed one group of this species (Sajadi et al., 2010) which was
grouped with S. limbata. Consequently, the AFLP marker partially confirmed
these results. In this regard, Reals et al. (2004) found a relationship between the
environment and some of the morphological characters within Salvia
accessions.
250 In our results, S. limbata mainly showed one group and seems to be a
different species, which is confirmed Sajadi et al. (2010). Using clustering and
factor analyses, S. limbata was shown to differ from S. ceratophylla and S.
sclarea, which is not confirmed by Hedge’s classification (1982a) (Fig. 1 and
2). Furthermore, S. sclarea and S. ceratophylla are strongly grouped, which is
also observed using AFLP molecular markers (Sajadi et al., 2010). Ozdemir and
Senel (1999) also showed the morphological properties of S. sclarea in Turkey,
which has some similarities and differences compared to other findings in
taxonomic literature. In our results, some accessions of S. sclarea displayed
different groups, which is probably due to the morphological variations or
ecological adaptations. It seems that these taxonomic differentiations were due
260 to polymorphism in the morphological characters, hybridization between
species and geographical distribution (Hedge, 1982a). S. sclarea has variability
in terms of the bract color, bract length, corolla upper lip color, leaf form and
leaf margin. Based on our findings in AFLP results, S. sclarea accessions were
did not display variability (Sajadi et al., 2010). In the same way, Kahraman et al.
(2010b) and Kaya et al. (2007) revealed that the morphological features of
Turkish S. macroclamys Boiss. & Kotschy and S. halophila Hedge such as
petiole length, bract and flower dimension, stem indumentums, leaf length,
calyx length, corolla length and nutlet dimension provide some additional data
to that reported by Hedge (1982b).
270 Conclusion
As a final point, we conclude that the morphological character studied
here appear to be the appropriate features in the taxonomy of Salvia genus. The
qualitative characters and quantitative characters definitely separate the Salvia
species. It can be assumed that the phenotypic variations observed in the Salvia
species might have arisen due to segregation, recombination, reproductive
system and adaptation against adverse environmental conditions (Aktas et al.,
2009; Baran et al., 2008; Haque, 1983; Wang et al., 2007). In some way, the
morphological characters seem to be appropriate features to display the
accessions variability and taxonomic levels.
280 Acknowledgement
The author is thankful to Mr. H. Fatahi and Mrs. F. Hasanzadeh for kindly
helping with this research. This study has been supported by the Research
Deputy of Shahrekord University, Shahrekord, Iran with No. 1978.
18
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Figure1: Mean, standard deviation and coefficient of variation in
quantitative characters studied in Salvia species.
1
2
Figure2: The variability of quantitative morphological characters (C.V.)
among the accessions of Salvia species in S. macrosiphon (mac), S. spinosa
(spin), S. sharifii (sha), S. virgata (virg), S. syriaca (syr.).
3
4
5
Figure 3: The variability of quantitative morphological characters (C.V.)
among the accessions of Salvia species in S. atropatana (atr), S. ceratophylla
(cer), S. multicaulis (mult), S. limbata (lim), S. sclarea (scl).
6
7
8
Figure 4: Dendrogram of cluster analysis using morphological characters
and Salvia accessions.
9
10
Figure 5: Factor analysis in 52 Salvia accessions using morphological
characters.
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12
13
14
15
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