The comparative pollen morphology
of genera Matricaria L. and
Tripleurospemum Sch. Bip. (Asteraceae) in
Turkey
Talip Çeter, Nur Münevver Pinar,
Hüseyin İnceer, Sema Hayirlioğlu-Ayaz
& Ahmet Emre Yaprak
Plant Systematics and Evolution
ISSN 0378-2697
Volume 299
Number 5
Plant Syst Evol (2013) 299:959-977
DOI 10.1007/s00606-013-0776-z
1 23
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Author's personal copy
Plant Syst Evol (2013) 299:959–977
DOI 10.1007/s00606-013-0776-z
ORIGINAL ARTICLE
The comparative pollen morphology of genera Matricaria L.
and Tripleurospemum Sch. Bip. (Asteraceae) in Turkey
Talip Çeter • Nur Münevver Pinar •
Hüseyin İnceer • Sema Hayirlioğlu-Ayaz
Ahmet Emre Yaprak
•
Received: 27 January 2013 / Accepted: 25 February 2013 / Published online: 20 March 2013
Ó Springer-Verlag Wien 2013
Abstract Pollen morphology of four Matricaria species
and 28 Tripleurospermum species was investigated with
light microscopies (LM) and scanning electron microscopies (SEM). Pollen slides were prepared using Wodehouse technique. Measurements were based on 20 or more
pollen grains per specimen. For SEM studies, dried pollen
grains were transferred on aluminum stubs and coated with
gold for 4 min in a sputter-coater. The pollen grains of
Matricaria and Tripleurospermum are radially symmetric
and isopolar. The pollen grains of the Matricaria are
oblate-spheroidal with the polar axes 16.6–31.2 lm and the
equatorial axes 18.7–23.9 lm. Tripleurospermum is oblatespheroidal, suboblate and prolate-spheroidal with the polar
axes 15.6–32.2 lm and the equatorial axes 17.7-38.5 lm.
The pollen grains of Tripleurospermum are operculate and
tricolporate. Matricaria is operculate and usually tricolporate or rarely syncolporate, tricolpate and tetracolporate.
The pollen grain of both taxa shows echinate ornamentation. The spines are commonly conical with a broadened
base and a tapered apical portion. The spine length varies
between 1.8–4 lm in Tripleurospermum and 2.3–3.3 lm
in Matricaria. The width of spines varies between
2.8–4.6 lm in Tripleurospermum and 2.4–3.6 lm in
T. Çeter (&)
Department of Biology, Faculty of Arts and Science,
Kastamonu University, Kastamonu, Turkey
e-mail: talipceter@hotmail.com
N. M. Pinar A. E. Yaprak
Department of Biology, Faculty of Science,
Ankara University, Ankara, Turkey
H. İnceer S. Hayirlioğlu-Ayaz
Department of Biology, Faculty of Science,
Karadeniz Technical University, 61080 Trabzon, Turkey
Matricaria. Inter-spinal area shows granulate–perforate,
reticulate–perforate, rugulate–perforate ornamentations
and the tectum surrounding the spine base is micro perforate. Overall exine thickness ranges from 2.8 to 4.8 lm in
Tripleurospermum, 3.6 to 5.2 lm in Matricaria. Intine is
thicker under pores in Tripleurospermum (0.3–0.62 lm)
than in Matricaria (0.6–0.8 lm). Inter-spinal ornamentations, pollen shape and the numbers of perforations at the
spin base have been observed as important morphological
characters.
Keywords Asteraceae Anthemideae
Tripleurospermum Matricaria Pollen morphology
Turkey
Introduction
Matricaria L. with about seven taxa, and Tripleurospermum Sch.Bip. with about 40 taxa are two closely related
genera in the tribe Anthemideae of the Asteraceae family.
Both genera are widespread in Europe, Central Asia, North
America and North Africa (Oberprieler et al. 2007). In
Turkey, Tripleurospermum and Matricaria are represented
by 30; 14 endemic and six taxa, respectively (Inceer et al.
2012).
Taxonomic problems of these genera cannot be ignored.
Species of Tripleurospermum and Matricaria are similar to
each other in their morphological characteristics such as
floral architecture and leaf shape. Therefore, they have
been confused both taxonomically and nomenclaturally
with each other (Jeffrey 1979; Xifreda 1985; Kerguélen
et al. 1987; Applequist 2002; Hansen and Christensen
2009; Inceer and Ozcan 2011). The taxonomy of these
genera continues to be subject of much confusion mainly
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960
T. Çeter et al.
Table 1 The collections data of the investigated Matricaria and Tripleurospermum
Taxon
Locality
Voucher
Matricaria aurea (Loefl.) Sch. Bip.
C6 Gaziantep/Şanlıurfa: between Nizip and Birecik, Dutlu, roadsides, near
cultivated area, 440 m a.s.l., 08.v.2007
Inceer
322
M. chamomilla L. var. chamomilla
C1 Muğla: Marmaris, between Marmaris and Köyceğiz, roadsides, 20 m
a.s.l., 18.iv.2007
Inceer
305
M. chamomilla L. var. recutita (L.) Fiori
C1 Muğla: Marmaris, between Kizilkaya and Fethiye, roadsides, 24 m a.s.l.,
18.iv.2007
Inceer
307
M. matricarioides (Less.) Porter ex Britton
A9 Kars (Ardahan): between Ardahan and Göle, roadsides, 1,800 m a.s.l.,
18.vii.2007
Inceer
420
Tripleurospermum baytopianum E. Hossain
A1 (E) Tekirdağ: Between Şarköy and Gölcük, slopes, meadows and
roadsides, 250 m a.s.l., 17.iv.2008
Inceer
508
T. callosum (Boiss. & Heldr.) E. Hossain
A7 Gümüşhane: Keçikaya village, roadsides, 1,494 m a.s.l., 04.vii.2007
Inceer
380
T. caucasicum (Willd.) Hayek
A8 Rize: Ayder, Yukari kavrun, meadows, streamsides, 2,333 m a.s.l.,
23.vii.2008
Inceer
683
T. conoclinium (Boiss. & Bal.) Hayek
B2 Izmir: Boz Dağ, cultivated fields, meadows and pastures, 1,178 m a.s.l.,
07.iv.2008
Inceer
478
T. corymbosum E. Hossain
B9 Ağrı: Suluçem (Musun), Balık Gölü, meadows, cultivated fields, 2,098 m
a.s.l., 11.vii.2008
Inceer
612
T. decipiens (Fisch. & Mey) Bornm.
B3 Eşkişehir: Han, Midas road, among gardens, 1,290 m a.s.l., 28.vi.2007
Inceer
375
T. disciforme (C. A. Meyer) Sch.Bip.
B2 Izmir: Boz Dağ, roadsides, water meadows, 1,021 m a.s.l., 06.vii.2008
Inceer
592
T. elongatum (Fisch. & Mey.) Bornm.
A7 Giresun: Between Şehitler pass and Şebinkarahisar, meadows, roadsides,
1,317 m a.s.l., 21.vii.2008
Inceer
664
T. fissurale (Sosn.) E. Hossain
A8 Artvin: Between Yusufeli and Ispir, among stones, 653 m a.s.l., 31.v.2008
Inceer
533
T. heterolepis (Freyn & Sint.) Bornm
A7 Gümüşhane: Keçikaya Village, roadsides, 1,618 m a.s.l., 04.vii.2007
Inceer
382b
T. hygrophilum (Bornm.) Bornm.
B1 Izmir: Yamanlar Dağı, above Karagöl, meadows, 820 m a.s.l., 14.iv.2007
Inceer
273
T. inodorum (L.) Sch. Bip
A9 Erzurum: Between Pasinler and Horasan, near Horasan, Köprü village,
roadsides, 1,600 m a.s.l., 11.vii.2008
Inceer
600
T. kotschyi (Boiss.) E. Hossain
T. melanolepis (Boiss. & Buhse) Pobed.
C5 Niğde: Ulukışla, Bolkar mountains, near Karagöl, 2,600 m a.s.l.,
29.vii.2008
A7 Gümüşhane: Torul, roadsides, 1,100 m a.s.l., 09.vi.2002
Inceer
702
Inceer
152
T. monticolum (Boiss. & Huet) Bornm
B8 Erzurum: Palandöken mountain, 2,907 m a.s.l., 13.vii.2008
Inceer
639
T. microcephalum (Boiss.) Bornm.
B8 Muş: Fallow fields, banks, roadsides, 1,323 m a.s.l., 09.vii.2008
T. oreades (Boiss.) Rech. f. var. oreades
A7 Giresun: Kümbet yaylasi, roadsides, meadows, 1,719 m a.s.l., 21.vii.2008
Inceer
594
Inceer
658
T. oreades (Boiss.) Rech. f. var. tchihatchewii
(Boiss.) E. Hossain
A8 Artvin: Şavşat, above Sahara National Park, damp alpine pastures,
2,185 m a.s.l., 17.vii.2007
Inceer
414
T. parviflorum (Willd.) Pobed.
B2 Izmir: Boz Dağ, rocky places, cultivated fields, roadsides, 1,178 m a.s.l.,
07.iv.2008
A2 Bursa: Uludağ, meadows, damp woods, near hotels, 1,828 m a.s.l.,
11.vi.2008
Inceer
479
Inceer
553
T. repens (Freyn & Sint.) Bornm.
A7 Gümüshane: Gezge village, meadows, 1,987 m a.s.l., 08.vii.2007
Inceer
385
T. rosellum (Boiss. & Orph.) Hayek var. album E.
Hossain
T. sevanense (Manden.) Pobed.
A3 Bolu: Near Abant Lake, meadows, 1,331 m a.s.l.,, 12.vi.2008
Inceer
555
Inceer
369b
T. pichleri (Boiss.) Bornm.
123
B3 Eskişehir: Çatacık, near Pinus forest, roadsides, 1,304 m a.s.l., 27.vi.2007
Author's personal copy
The comparative pollen morphology of Matricaria L. and Tripleurospemum Sch. Bip.
961
Table 1 continued
Taxon
Locality
Voucher
T. tempskyanum (Freyn & Sint.) Hayek
A2 Bursa: Uludağ, near hotels, meadows, open places, 1,900 m a.s.l.,
27.vi.2007
Inceer
361
T. tenuifolium (Kit.) Freyn
A2 Bursa: Uludağ, near hotels, meadows, open places, 1,690 m a.s.l.,
27.vi.2007
Inceer
353
T. transcaucasicum (Manden.) Pobed.
B8 Erzurum: Palandöken mountain, 2,946 m a.s.l., 13.vii.2008
Inceer
638
T. subnivale Pobed.
A8 Rize: Ikizdere, above Ayder, grassy stream banks, stony pastures on
limestone, 1,600 m a.s.l., 20.vi.2001
Inceer
118
T. ziganaense Inceer & Hayırlıoglu-Ayaz
A7 Gümüshane: Zigana mountain, between Zigana Pass and Torul, 1,300 m
a.s.l., 22.vii.2008
Inceer
666
Fig. 1 a Triplurospermum for P., b Matricaria for P., c Triplurospermum for E, d Matricaria for E; P polar axes, E equatorial axes
123
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962
T. Çeter et al.
because of the approaches to species delimitation that have
been employed, resulting in varying numbers of recognized
species. Initially, Tripleurospermum was assigned to the
genus Matricaria but later was recognized as a separate
genus on the basis of the different structure of its achenes
and the occurrence of a tetrasporic embryo sac (Harling
1951). However, Rauschert (1974) and Kay (1976) misapplied the name Matricaria to refer exclusively to the
species of Tripleurospermum (Bremer and Humphries
1993). In addition, Oberprieler (2001) showed that Tripleurospermum is closely related to Anthemis in the strict
sense and not to Matricaria. This is supported by the tetrasporic embryo sac shared by Tripleurospermum and
Anthemis (versus monosporic in Matricaria and other
Anthemideae genera).
Cytological studies conducted in Matricaria and Tripleurospermum have concentrated on the chromosome count,
with little work focusing on detailed caryological criteria
for taxonomic purposes (Watanabe 2009). All the members
of the genera show a base chromosome number of x = 9,
the most common basic number in the tribe Anthemideae
and the family Asteraceae (Inceer and Hayırlıoglu-Ayaz
2010). To date, one ploidy level (2x) in Matricaria and four
ploidy levels (2x, 3x, 4x, 5x) in Tripleurospermum have
been reported from Turkey, which is regarded as one of the
main centers of diversification and speciation (Inceer and
Beyazoglu 2004; Inceer and Hayırlıoglu-Ayaz 2010). The
diploid and tetraploid levels are more common than the
triploid and pentaploid levels in Tripleurospermum. The
stability of ploidy level in Matricaria is noteworthy in
Turkish populations (Inceer and Hayırlıoglu-Ayaz 2010).
Pollen morphology has provided an approach to the
systematic relationships among the genera of the Asteraceae (Wagenitz 1955; Stix 1960; Erdtman 1969; Skvarla
and Larson 1965; Blackmore 1982, 1990; Pinar and Oybak
Dönmez 2000; Pinar and İnceoğlu 1996; Pinar and
Adigüzel 1998; Punt and Hoen 2009). Stix (1960) studied
pollen morphology of Matricaria chamomilla L. and
placed it into the Anthemis type. Beug (2004) described a
Matricaria type. Pollen morphology of M. maritima subsp.
inodora, M. maritima subsp. maritima, M. matricarioides
and M. recutita were examined by Punt and Hoen (2009).
They placed it into Anthemis arvensis type. There are only
a few studies conducted on the pollen morphology of
Tripleurospermum. Inceoglu and Karamustafa (1977)
defined pollen morphology of T. elongatum (Fish. & Mey.)
Bornm.
In this study, the pollen grains of Matricaria and
Tripleurospermum showing morphological similarities
were investigated with LM and SEM so that palynological
comparisons could be made and inter and intra-generic
relationships based on pollen morphological data could be
discussed. This study attempts to clarify the systematics of
these genera.
Materials and methods
Plant materials
Materials used for this study were collected from wild
populations. Collectors and localities are shown in the
specimens investigated below. The specimens of the plants
are deposited in the Karadeniz Techinal University Herbarium (KTUB).
The list of investigated species of the Matricaria and
Tripleurospermum taxa are given below. The order of the
species was adapted by Grierson (1975), Enayet Hossain
(1975) and Inceer and Hayırlıoglu-Ayaz (2008) (Table 1).
Palynological analysis
Pollen slides were prepared using the Wodehouse (1935)
technique. Pollen grains were stained with glycerin-jelly
Table 2 Four palynological characters to distinguish the 32 taxa of the genara Matricaria and Tripleurospermum
Taxa/character states
T1
T2
T3
T4
T5
T6
T7
T8
T9
T10
T11
T12
T13
T14
T15
T16
Pollen shape
0
0
1
1
1
0
1
1
1
0
1
1
1
1
1
1
Orn bet. spin
0
0
0
0
2
2
1
2
2
2
2
1
2
2
2
1
Perf. number
22
45
15
15
35
24
14
33
45
28
35
15
45
18
35
16
Exine (lm)
2.8
5.1
3.6
3.6
3.6
4.2
2.8
3.2
4.7
3.6
3.8
3.2
4.2
3.8
3.2
3.75
Taxa/character states
T17
T18
T19
T20
T21
T22
T23
T24
T25
T26
T27
T28
M1
M2
M3
M4
Pollen shape
1
0
2
1
0
1
0
0
0
0
1
0
1
1
1
1
Orn bet. spin
1
1
1
2
2
1
1
2
2
2
1
1
3
3
3
3
Perf. number
19
13
45
28
10
15
28
38
40
25
25
38
12
13
12
14
Exine (lm)
2.8
4.4
3.6
2.3
3.1
4.8
3
3.8
2.8
4.7
3.1
4.2
5.2
3.6
3.6
3.9
123
Taxa
Polar axis (P) (lm)
Equatorial axes
(E) (lm)
Min
Max
Mean
Min
Max
Mean
T. caucasicum (T1)
18 or 36 (2x or 4x)
20.8
28.1
24.2
26
32.2
28.3
0.80
Suboblate
2.8
T. melanolepis (T2)
18 (2x)
20.8
28.1
24.2
26
32.2
28.6
0.85
Suboblate
5.1
T. oreades var. oreades (T3)
T. oreades var. tchihatchewii (T4)
36 (4x)
36 (4x)
21.8
20.8
28.4
27
24.3
23.9
23.9
24.1
31.2
28.9
26.7
26.9
0.91
0.89
Oblate-spheroidal
Oblate-spheroidal
T. rosellum var. album (T5)
36 (4x)
20.8
27
23
22.9
27
24.9
0.92
T. hygrophilum (T6)
18 (2x)
22.9
30.2
25.2
24.5
31.2
27.5
T. baytopianum (T7)
18 (2x)
19.8
25.9
22.4
20.8
28.1
24.6
T. elongatum (T8)
18 (2x)
19.8
25.9
22.6
20.8
27
T. parviflorum (T9)
18 (2x)
22.7
28.1
25.8
26
T. inodorum (T10)
36 (4x)
23.9
30.2
25.9
T. kotschyi (T11)
36 (4x)
21.8
28.1
T. conoclinium (T12)
18 (2x)
19.8
27
T. tenufoliaum (T13)
18 (2x)
20.8
T. pichleri (T14)
36 (4x)
T. sevanense (T15)
P/E
Pollen shape
Exine (lm)
İntine (lm)
Colpus
(lm)
Pore
(lm)
Clt
Clg
Plt
Plg
0.32
6.5
14.6
8.3
8.3
0.52
6.1
16.4
8.2
8.1
3.6
3.6
0.4
0.41
4.4
4.1
12.7
14.3
5.2
5.2
5.2
5.2
Oblate-spheroidal
3.6
0.3
5.6
14.2
6.4
6.3
0.92
Suboblate
4.2
0.35
5
15.2
6.2
6.1
0.91
Oblate-spheroidal
2.8
0.3
5.8
12.3
8.2
8.1
24.7
0.91
Oblate-spheroidal
3.2
0.48
5
12.4
5.8
6
31.2
28.2
0.92
Oblate-spheroidal
4.7
0.53
4.8
17.2
5.6
5.7
27
34.3
30.1
0.86
Suboblate
3.6
0.5
4.8
15.3
6.2
6.2
24.5
22.9
30.1
26.3
0.93
Oblate-spheroidal
3.8
0.3
5.9
16.2
6.5
6.5
23.7
20.8
30.1
26.1
0.91
Oblate-spheroidal
3.2
0.31
5.8
11.4
6.9
6.9
27
25
23.9
28.1
27.1
0.93
Oblate-spheroidal
4.2
0.52
4.2
12.5
5.2
5.2
22.9
32.2
27.9
24.1
34.3
30.3
0.92
Oblate-spheroidal
3.8
0.4
5.3
16.5
6.7
6.7
36 (4x)
15.6
28.1
21.8
17.7
32.2
23.6
0.93
Oblate-spheroidal
3.2
0.54
3.7
13.8
4.5
4.5
Tipleurospermum
T. callosum (T16)
36 (4x)
19.8
28.1
23.1
22.9
30.1
26.4
0.88
Oblate-spheroidal
3.75
0.34
6
13.1
8.1
8.1
T. corymbosum (T17)
27 (3x)
19.6
27
23.2
20.8
28.1
24.4
0.95
Oblate-spheroidal
2.8
0.3
5.2
14.4
6.2
6.2
T. heterolepis (T18)
36 (4x)
20.8
28.1
25.6
22.9
32.2
27.7
0.92
Suboblate
4.4
0.4
5.1
15.1
6.1
6.1
T. transcaucasicum (T19)
T. repens (T20)
18 (2x)
36 (4x)
21.8
17.7
31.2
28.4
26
22.6
20.8
19.8
28.1
31.2
23.9
23.1
1.09
0.99
Prolate-spheroidal
Oblate-spheroidal
3.6
2.3
0.62
0.32
4.4
4.7
20.6
12.8
5.4
5.8
5.4
5.8
T. fissurale (T21)
18 (2x)
20.7
25.9
23.1
22.9
30.1
26.3
0.88
Suboblate
3.1
0.34
4.3
14.2
7.4
7.2
T. monticolum (T22)
36 (4x)
20.5
27
24.3
21.8
28.9
25.6
0.95
Oblate-spheroidal
4.8
0.52
5.2
16.8
6.3
6.1
T. decipiens (T23)
18 (2x)
20.8
28.1
24.2
24.5
34.3
30.1
0.80
Suboblate
3
0.3
5.8
15.8
7.1
7
T. microcephalum (T24)
?
16.6
22.9
19.6
19.8
27
22.9
0.86
Suboblate
3.8
0.47
3.3
13.4
4.3
4.2
T. disciforme (T25)
18 (2x)
15.6
21.8
18.3
17.7
26
23.7
0.77
Suboblate
2.8
0.3
4
10.9
5.1
5.1
T. subnivale (T26)
42–48 (5x)
22.9
32.2
28.9
24.1
38.5
32.7
0.88
Suboblate
4.7
0.78
6.2
17.7
7.3
7.3
T. tempskyanum (T27)
36 (4x)
20.8
27
24.9
21.8
30.1
27.4
0.91
Oblate-spheroidal
3.1
0.52
4.2
14.6
5.2
5.2
T. ziganaense (T28)
18 (2x)
18.7
28.1
22.7
20.8
31.2
27
0.84
Suboblate
4.2
0.42
5.7
20.8
7.3
7.3
Matricaria
18 (2x)
16.6
20.8
18.7
18.7
21.8
20.3
0.92
Oblate-spheroidal
3.6
0.62
3.1
10.7
4.2
4.2
M. chamomilla var. chamomilla (M2)
18 (2x)
18.7
24.1
21.8
21.8
28.1
25
0.96
Oblate-spheroidal
5.2
0.8
4.4
12.5
5.6
5.6
M. chamomilla var. recutita (M3)
18 (2x)
20.8
27
23.9
22.9
28.1
25.5
0.94
Oblate-spheroidal
3.6
0.62
5.6
10.7
6.8
6.8
963
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M. aurea (M1)
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Chromosome
number (2n)/ploidy
level (x)*
The comparative pollen morphology of Matricaria L. and Tripleurospemum Sch. Bip.
Table 3 Pollen measurements of different taxa of Tipleurospermum and Matricaria
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Table 3 continued
Taxa
M. matricarioide (M4)
Taxa
Chromosome
number (2n)/ploidy
level (x)*
Polar axis (P) (lm)
Equatorial axes
(E) (lm)
Min
Max
Mean
Min
Max
Mean
18 (2x)
20.8
31.2
24.8
23.9
32.2
27.2
Aperture type
P/E
0.9
Pollen shape
Oblate-spheroidal
Exine (lm)
3.9
Spine
Length
(lm)
Width
at base (lm)
Perforation
number at base
İntine (lm)
0.62
Colpus
(lm)
Pore
(lm)
Clt
Clg
Plt
Plg
5.7
14.5
6.8
6.8
Ornamentation
Ornamentation
of inter-spinal area
Tipleurospermum
Tricolporate
Tricolporate
4
3.3
4.2
4.2
18–25
30–60
Echinate
Echinate
Granulate–perforate
Granulate–perforate
T. oreades var. oreades (T3)
Tricolporate
2.7
3.5
10–20
Echinate
Granulate–perforate
T. oreades var. tchihatchewii (T4)
Tricolporate
2.8
3.6
10–20
Echinate
Granulate–perforate
T. rosellum var. album (T5)
Tricolporate
4
4.4
20–50
Echinate
Reticulate–perforate
T. hygrophilum (T6)
Tricolporate
2.8
3.4
12–35
Echinate
Reticulate–perforate
T. baytopianum (T7)
Tricolporate
2.8
3.5
10–18
Echinate
Granulate–perforate
T. elongatum (T8)
Tricolporate
3.2
4.1
20–45
Echinate
Reticulate–perforate
T. parviflorum (T9)
Tricolporate
3.2
3.8
30–60
Echinate
Reticulate–perforate
T. inodorum (T10)
Tricolporate
3.7
4.2
15–40
Echinate
Reticulate–perforate
T. kotschyi (T11)
Tricolporate
4
4.6
20–50
Echinate
Reticulate–perforate
T. conoclinium (T12)
Tricolporate
2.7
3.3
10–20
Echinate
Reticulate–perforate
T. tenufoliaum (T13)
Tricolporate
3.4
4.3
30–60
Echinate
Reticulate–perforate
T. pichleri (T14)
Tricolporate
2.1
2.4
10–25
Echinate
Reticulate–perforate
T. sevanense (T15)
Tricolporate
2.5
3.6
20–50
Echinate
Reticulate–perforate
T. callosum (T16)
T. corymbosum (T17)
Tricolporate
Tricolporate
2.1
3.4
3
4
12–20
12–25
Echinate
Echinate
Granulate–perforate
Granulate–perforate
T. heterolepis (T18)
Tricolporate
3.1
2.8
5–20
Echinate
Granulate–perforate
T. transcaucasicum (T19)
Tricolporate
2.6
4.2
30–60
Echinate
Granulate–perforate
T. repens (T20)
Tricolporate
2.4
2.8
15–40
Echinate
Reticulate–perforate
T. fissurale (T21)
Tricolporate
1.8
2.8
5–15
Echinate
Reticulate–perforate
Tricolporate
2.5
3.4
10–20
Echinate
Granulate–perforate
T. decipiens (T23)
Tricolporate
2.5
4.1
15–40
Echinate
Granulate–perforate
T. microcephalum (T24)
Tricolporate
2.4
3.1
25–50
Echinate
Reticulate–perforate
T. disciforme (T25)
Tricolporate
2
3.7
30–50
Echinate
Reticulate–perforate
T. subnivale (T26)
Tricolporate
3.6
4
15–35
Echinate
Reticulate–perforate
T. tempskyanum (T27)
Tricolporate
3.5
4.2
15–35
Echinate
Granulate–perforate
T. ziganaense (T28)
Tricolporate
3.1
3.7
25–50
Echinate
Granulate–perforate
T. Çeter et al.
T. monticolum (T22)
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T. caucasicum (T1)
T. melanolepis (T2)
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Rugulate–perforate
Rugulate–perforate
Echinate
Numerical analysis
Echinate
2.5
Clg colpus length, Clt colpus width, Plt pore width, Plg pore length
* Watanabe 2009; Inceer and Hayirlioglu-Ayaz 2010
2.3
2 % tetracolporate, 5 % syncolporate,
93 % tricolporate
M. matricarioide (M4)
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with safranin, and slightly heating the slide and then a cover
slip was placed on it. The prepared slides were studied under
the light microscope. Their photographs were taken with the
Leica DM3000 digital photomicrograph system (Germany).
Measurements were based on 20 or more pollen grains per
specimen. For scanning electron microscopy (SEM) studies,
dried pollen grains were transferred on aluminum stubs and
coated with gold for 4 min in a sputter-coater (Pinar et al.
2009b; Altuner et al. 2012). Morphological observations
were made in a Jeol JSM 6490LV Scanning electron microscope at TPAO Research Center SEM Laboratory.
Terminology was adopted from Faegri and Iversen
(1975), Salgado-Labouriau (1982), Mesfin et al. (1995) and
Punt and Hoen (2009) and shape classification follows that
of Erdtman (1969) based on P/E ratio in Table 3.
10–18
Rugulate–perforate
Echinate
10–16
3.6
2.4
Tricolporate
M. chamomilla var. recutita (M3)
2.4
Tricolporate
M. chamomilla var. chamomilla (M2)
3.3
8–15
Rugulate–perforate
Echinate
3.2
1 % tricolpate, 2 % syncolporate,
97 % tricolporate
M. aurea (M1)
2.3
Length
(lm)
Matricaria
Taxa
Table 3 continued
Aperture type
Spine
Width
at base (lm)
8–15
Perforation
number at base
Ornamentation
of inter-spinal area
Ornamentation
The comparative pollen morphology of Matricaria L. and Tripleurospemum Sch. Bip.
The Simpson and Roe graphical test (Van der Pluym and
Hideux 1997) was used for statistical calculations. Pollen
characters of the taxa, coefficient of correlation were
determined, and they were grouped using the clustering
analysis method (UPGMA, dissimilarity, standardized
variable) as well as ordination based on principal component analysis (PCA) (Fig. 1).
Four palynological (consisting of binary nominal, multistate nominal and qualitative) characters were selected to
distinguish the 32 taxa (OTUs) of the genara Matricaria and
Tripleurospermum (Table 2). Four morphological character
states and their values or scales are given at Table 2. A
primary mixed data matrix was created for 32 taxa (OTUs)
and four palynological characters (Table 2) for the analysis.
Since Gower’s formula (Gower 1971) modified by Podani
(1999) allows the inclusion of ordinal variables and missing
scores in the data matrix, it was used to calculate the primary mixed data for dissimilarities. Unweighted pair group
method using arithmetic averages (UPGMA) was selected
because it is the most commonly used method (Mohammadi
and Prasanna 2003) and it has advantages to other methods
in: accurate reflection of the similarity matrix as measured
by the co-phenetic correlation coefficient of Sokal and
Rohlf (1962), symmetrical hierarchical structure [the
‘‘structural value’’ concept of McNeill (1979)], and congruence with classification derived by traditional methods
(Ward 1993). All computations were made by the SYNTAX 2000 software (Podani 2001).
Results
Detailed pollen morphological features of the investigated
taxa are summarized in Table 3 and representative pollen
grains are illustrated in figures.
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Fig. 2 SEM microphotograph of Tripleurospermun. 1, 2 T. caucasicum; 3, 4 T. melanolepis; 5, 6 T. oreades var. oreades; 7, 8
T. oreades var. tchihatchewii; 9, 10 T. rosellum var. album; 11, 12
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T. Çeter et al.
T. hygrophilum; 13, 14 T. baytopianum; 15, 16 T. elongatum; 17, 18
T. parviflorum; 19, 20 T. inodorum
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Fig. 3 Light microscope microphotograph of Tripleurospermun. 1–4 T. caucasicum; 5–8 T. melanolepis; 9–12 T. oreades var. oreades; 13–16
T. oreades var. tchihatchewii; 17–20 T. rosellum var. album
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T. Çeter et al.
Fig. 4 Light microscope microphotograph of Tripleurospermun. 1–4 T. hygrophilum; 5–8 T. baytopianum; 9–12 T. elongatum; 13–16
T. parviflorum; 17–20 T. inodorum
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The comparative pollen morphology of Matricaria L. and Tripleurospemum Sch. Bip.
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Fig. 5 SEM microphotograph of Tripleurospermun. 1, 2 T. kotschyi; 3, 4 T. conoclinium; 5, 6 T. tenufoliaum; 7, 8 T. pichleri; 9, 10;
T. sevanense; 11, 12 T. callosum; 13, 14 T. corymbosum; 15, 16 T. heterolepis; 17, 18 T. transcaucasicum; 19, 20 T. repens
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T. Çeter et al.
Fig. 6 Light microscope microphotograph of Tripleurospermun. 1–4 T. kotschyi; 5–8 T. conoclinium; 9–12 T. tenufoliaum; 13–16 T. pichleri;
17–20 T. sevanense
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Fig. 7 Light microscope microphotograph of Tripleurospermun. 1–4 T. callosum; 5–8 T. corymbosum; 9–12 T. heterolepis; 13–16
T. transcaucasicum; 17–20 T. repens
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The comparative pollen morphology of Matricaria L. and Tripleurospemum Sch. Bip.
Fig. 8 SEM microphotograph of Tripleurospermun. 1, 2 T. fissurale;
3, 4 T. monticolum; 5, 6 T. decipiens; 7, 8 T. microcephalum; 9, 10
T. disciforme; 11, 12 T. subnivale; 13, 14 T. tempskyanum; 15, 16
T. ziganaense; 17, 18 M. aurea; 19, 20 M. chamomilla var.
chamomilla; 21, 22 M. chamomilla var. recutita; 23, 24 M.
Matricarioide
Size, symmetry and shape
The pollen grains of Matricaria and Tripleurospermum are
radially symmetrical and isopolar. The pollen grains of the
Matricaria are oblate-spheroidal with the polar axes
16.6–31.2 lm and the equatorial axes 18.7–23.9 lm.
Tripleurospermum is oblate-spheroidal, suboblate and
prolate-spheroidal with the polar axes 15.6–32.2 lm and
the equatorial axes 17.7–38.5 lm (Fig. 1). Their dimensions are smaller in T. disciforme and M. aurea, and larger
in T. subnivale and T. pichleri. Both of their outlines are
elliptic in equatorial view and triangular in polar view: amb
intersemiangular. (Table 3; Figs. 2, 3, 4, 5, 6, 7, 8, 9, 10).
Apertures
The pollen grains of Tripleurospermum are operculate and
tricolporate. Matricaria is operulate and usually tricolporate or rarely syncolporate, tricolpate and tetracolporate.
Some species have shown heteromorfic characteristics. For
example; 1 % tricolpate, 2 % syncolporate and 97 % tricolporate in M. aurea and 2 % tetracolporate, 5 % syncolporate and 93 % tricolporate in M. matricarioides.
Colpus is short or long (10.4–20.8 lm) and narrow or
broad (2.3–6.5 lm) and ora is circular or lalongated in
Tripleurospermum. The colpus of Matricaria is short
(10.9–14.5 lm) and narrow (3.6–5.2 lm) and ora, circular.
The highest values were observed in T. transcaucasicum
and T. ziganaense. M. aurea and M. chamomilla var.
recutita have smallest values of colpus. Margins distinct
are regular and ends are acute in both of them. Colpus
membrane is more or less granulate (Table 3; Figs. 2, 3, 4,
5, 6, 7, 8, 9, 10).
Exine
The overall thickness of stratified exine ranges from 2.8 to
4.8 lm in Tripleurospermum, 3.6 to 5.2 lm in Matricaria.
Ectexine is thicker than endexine without costae and cavea.
Intratectal columellae are very distinct under spines, but
indistinct in inter-spinal region. The spines are commonly
conical with a broadened base and a tapered apical portion.
The spine length varies between 1.8–4 lm in Tripleurospermum and 2.3–3.3 lm in Matricaria. The width of
spines varies between 2.8–4.6 lm in Tripleurospermum
and 2.4–3.6 lm in Matricaria. The base of the spines in
almost all species studied has irregular 1 (T. fissurale,
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T. oreades var. oreades and T. ziganaense), 2 (T. pichleri,
M aurea, M. chamomilla var. chamomilla, M. chamomilla
var. recutita, M. matricarioides), 3 or 4 seriate perforations
with the larger holes often found distally. The number of
cavities is 5–60 in Tripleurospermum, 8–18 in Matricaria.
Intine is thicker under pores in Tripleurospermum
(0.3–0.62 lm) than in Matricaria (0.6–0.8 lm) (Table 3;
Figs. 2, 3, 4, 5, 6, 7, 8, 9, 10).
The pollen wall is provided with spines and it is either
granulate–perforate, reticulate–perforate or rugulate–perforate (Matricaria spp.). In all the species, the tectum
surronding the spine base is microperforate. Table 3 provides a summary of the tectal morphology in Tripleurospermum and Matricaria.
In Matricaria and Tripleurospermum, numerical analysis of the differential palynological characters, which
became evident during the course of our investigations, led
to the realization of a dendrogram. This dendrogram shows
the similaries or dissimilarities which exist among the taxa
being studied. A dendrogram of cluster analysis of Turkish
Matricaria and Tripleurospermum taxa based on 4 character states of 32 taxa (OTUs) has been constructed. To
evaluate the correlation between the dendrogram and the
distance matrix, the cophenetic correlation coefficient was
measured: the higher the correlation, the better the representation of distances in the hierarchy. If the value is higher
than 0.9, the correlation is high; if the value is lower than
0.74, the correlation is not significant. The cophenetic
correlation coefficient of 0.7946 shows a significant correlation between the dendrogram and the distance matrix,
but the correlation is not high (Fig. 11).
Discussion
The grains of the taxa of Matricaria can be ascribed to the
‘‘Anthemis’’ type of Stix (1960), Matricaria type of Beug
(2004) and ‘‘Anthemis arvensis’’ type of Punt and Hoen
(2009), but Tripleurospermum cannot also be classified by
any authors.
The general pollen characteristics found in the Matricaria taxa are the same as for the Tripleurospermum taxa.
The dimensions (P and E) and the thickness of exine and
intine are almost similar. (Table 3; Fig. 1). Similarly,
Inceer and Ozcan (2011) found that the leaf morphologies
and anatomical structures of Matricaria and Tripleurospermum basically resemble each other.
Some of the taxa of Tripleurospermum have 2n = 18
and 2n = 36 chromosomes and some of the taxa of
Matricaria have 2n = 18 chromosomes (Inceer and
Beyazoglu 2004; Inceer and Hayirlioglu-Ayaz 2010).
Stoma and vascular bundle can be used as an anatomical
marker to distinguish diploid from polyploid taxa in a
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T. Çeter et al.
Fig. 9 Light microscope microphotograph of Tripleurospermun. 1–4 T. fissurale; 5–8 T. monticolum; 9–12 T. decipiens; 13–16
T. microcephalum; 17–20 T. disciforme; 21–24 T. subnivale
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The comparative pollen morphology of Matricaria L. and Tripleurospemum Sch. Bip.
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Fig. 10 Light microscope microphotograph of Tripleurospermun and Matricaria. 1–4 T. tempskyanum; 5–8 T. ziganaense; 9–12 M. aurea;
13–16 M. chamomilla var. chamomilla; 17–20 M. chamomilla var. recutita; 21–24 M. Matricarioide
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T. Çeter et al.
Fig. 11 Dendrogram showing dissimilarity distance of the examined taxa
Matricaria and Tripleurospermum (Inceer and Ozcan
2011). Also, Chatuverdi et al. (1990) and Brochman
(1992) reported that pollen grain size strongly correlates
with the level of polyploid, but the data presented here
does not show such a correlation. Mean values for P and
E diploid and poliploid species are very similar (Table 3;
Fig. 1). Similarly, great variations in the values of P and
E in diploid, triploid and tetraploid species of section
Onorbyoidei of Astragalus have not been observed by
Pinar et al. (2009a, b).
The position and size of the basal cavities are speciesdependent (Salgado-Labouriau 1982; Mesfin et al. 1995).
Observations using LM and SEM methods show that the
number of the basal cavities and seriate values found in
Tripleurospermum are highest, and thus the Matricaria
taxa had smaller values. Mesfin et al. (1995) stated that the
ornamentations between spines are an important characteristic for Asteraceae. Ornamentations between spines are
granulate–perforate or reticulate–perforate in Tripleurospermum, and rugulate–perforate in Matricaria.
The general aperture form is tricolporate, but M. aurea
(1 % tricolpate, 2 % syncolporate and 97 % tricolporate)
and M. matricarioides (2 % tetracolporate, 5 % syncolporate and 93 % tricolporate) show considerable aperture
type variation (Table 3; Figs. 8, 10). Variations in pollen
size and aperture type were attributed to heteromorphy in
pollen grains by Nair and Kaul (1965) and Inceoglu (1973).
123
Cluster analysis divided taxa into three main groups,
namely cluster A, B and C; Cluster A includes: T. caucasicum, T. melanolepis, T. decipiens, T. ziganaense, T. heterolepis, T. transcaucasicum; B1 includes T. oreades var.
oreades, T. oreades var. tchihatchewii, T. conoclinium,
T. callosum, T. baytopianum, T. corymbosum, T. tempskyanum, T. monticolum; B2 only includes Matricaria
namely: Matricaria chamomilla var. chamomilla,
M. chamomilla var. recutita, M. aurea, M. matricarioides.
Cluster C1 includes T. rosellum var. album, T. sevanense,
T. elongatum, T. kotschyi, T. repens, T. pichleri, T. parviflorum, T. tenufoliaum; Cluster C2 includes T. hygrophilum, T. subnivale, T. inodorum, T. microcephalum,
T. disciforme, T. fissurale. Results presented according to
palynological data in this study showed that all Matricaria
are clustered together but are not separated from
Tripleurospermum.
Acknowledgments The authors thank Scientific and Technological
Research Council of Turkey (TUBITAK, TBAG Project No.
106T162) for financial support.
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