Fruit and seed morphology of the Fumaria L. species (Papaveraceae) of Iran

F. EBRAHİMZADEH ARAII, M. KESHAVARZI, M. SHEIDAII, P. GHADAM
167
Turk J Bot
35 (2011) 167-173
© TÜBİTAK
doi:10.3906/bot-0909-160
Fruit and seed morphology of the Fumaria L.
species (Papaveraceae) of Iran
Fatemeh EBRAHIMZADEH ARAII1, Maryam KESHAVARZI1,*, Masoud SHEIDAII2, Parinaz GHADAM1
1
Biology Department, Faculty of Science, Alzahra University, Vanak, Tehran - IRAN
2
Shahid Beheshti University, GC, Faculty of Biological Sciences, Tehran - IRAN
Received: 20.09.2009
Accepted: 08.11.2010
Abstract: The macro and micro fruit and seed morphology and surface ornamentations of 21 populations of 6 Fumaria
L. species were investigated using stereomicroscope and scanning electron microscopy. These data are shown to support
data from the general morphology. The results indicate that the fruit and seed characters of the genus Fumaria are
valuable for taxonomic applications and are useful for classification. F. officinalis show a different shape in their fruit.
The close relationships are observed for F. parviflora and F. vaillantii. F. indica, as a hybrid between F. asepala and F.
parviflora, shows intermediate micro-morphological features.
Key words: Fumaria, scanning electron microscopy, systematic, seed, fruit.
Research Article
* E-mail: neshat112000@yahoo.com
Introduction
The genus Fumaria L. (Papaveraceae) comprises
60 species, most of which grow around the
Mediterranean region. In total, 8 Fumaria species
have been reported from Iran. Wendelbo (1974)
reported 7 species from the country and recently
Lidén (2000) reported F. officinalis L. as a new species
for the flora of Iran.
In the Lidén Monograph (Lidén 1986) the genus
Fumaria has been divided into 2 sections; most of
the species growing in Iran belong to the section
microsepala. The identification of Fumaria species
is difficult due to the variability present in their
vegetative and reproductive features, possibly due
to the occurrence of inter-specific hybridisation
(Murphy, 2009).
Characteristics such as sepal size, upper
petal shape, and dry fruit shape are important in
distinguishing these taxa. The best condition to
identify a Fumaria species is to study fresh material,
as many changes occur in the herbarium specimens
during drying, and significant changes in flower
colour occur after drying.
Fumitory species grow mainly in the temperate
and cooler regions of the old world, often as weeds
(Jafri, 1974). Many authors have considered the
fruit and seed ornamentations as a useful tool
for taxonomic considerations (Sheikh Akbari &
Azizian, 2006; Kaya & Dirmenci, 2008; Pınar et al.,
2009; Bayrakdar et al., 2010). The morphological
characters of the seed and fruit have been considered
an essential aid in the taxonomic treatment of
Papveraceae (Lidén, 1986). Fruit surface, seed-coat
development, and structure as well as seed anatomy
are some of these informative characters. Fukuhara
(1992) examined the development and structure of
Fruit and seed morphology of the Fumaria L. species (Papaveraceae) of Iran
168
the seed-coats in 16 species of Corydalis and 2 species
of Dicentra. Fukuhara (1995) studied the vascular
patterns in the fruit of Trigonocapnos and Discocapnos
(Papaveraceae-Fumarioideae). Seed-coat anatomy
has been described in 122 species of Fumarioideae,
which represent all the genera, subgenera, and most
sections (Fukuhara & Lidén, 1995a; Fukuhara,
1995). Fukuhara and Lidén (1995b) studied the
pericarp anatomy in Fumariaceae-Fumarioideae,
while Fukuhara (1999) studied the seed morphology
of Fumariaceae-Fumarioideae. However, similar
studies have not been carried out on the Fumaria
species of Iran. Therefore, the objective of this paper
is to provide a detailed account of the macro and
micro seed and fruit morphology in the Fumaria
species of Iran and to determine the extent to which
such data can be used in the taxonomy of the genus.
This paper presents a detailed account of the seed and
fruit morphology of 6 species of Fumaria collected
from Iran for the first time.
Methods and materials
Plant materials
Twenty-one populations of 6 Fumaria growing
in Iran, namely 1- F. asepala Boiss., 2- F. densiflora
DC., 3- F. indica (Hausskn.) Pugsley, 4- F. officinalis
L., 5- F. parviflora Lam. and 6- F. vaillantii Loisel.
were studied. The details of the voucher specimens
and their localities are given in Table 1. The voucher
specimens are deposited at the Herbarium of Alzahra
University. The specimens were collected from
nature.
For numerical taxonomy analyses, 7 qualitative
and quantitative seed and fruit characteristics were
studied (Table 2).
Samples were studied by a Dino-Lite pro hand
stereomicroscope at first. For SEM studies, the
samples were suspended in a drop of water and
directly transferred by fine pipette to a metallic stub
using double-sided adhesive tape and coated with
gold in a sputtering chamber (Sputter Coater BALTEC, SCDOOS). The coating was restricted to 100
Å. The SEM examination was carried out on a Philips
XL30 microscope, and the measurements carried out
were based on 10 to 20 readings from each specimen.
Statistical analysis
To reveal species relationships we used cluster
analysis and principal coordinate analysis (PCO)
plotting. For multivariate analysis, the mean
of the quantitative characters was used, while
qualitative characters were coded as binary/multistate characters. Standardised variables (mean = 0,
variance = 1) were used in the statistical analysis. The
average taxonomic distances and squared Euclidean
distances were used as dissimilarity coefficients in
the cluster analysis of morphological data. SPSS ver.
9 (1998) and NTSYS ver. 2.02 (1998) were used for
statistical analysis. Cophenetic correlations were
determined for the fit of the dendrograms obtained.
Results
Morphological observations
Our observations indicated that the general shape
of the seed is somehow similar in different species of
studied Fumaria. The seed is spherical to ellipsoid
and has an apical pore and rib. The fruit is spherical to
elliptic and is pointed in all studied Fumaria species
except for F. officinalis, which has cordate fruits with
emarginated tips.
The seed shape in Fumaria species is determined
by the ratio of a seed’s vertical diameter to a seed’s
horizontal diameter. Therefore, the seed shape was
spherical in F. asepala, and F. vaillantii, elliptical in
F. parviflora and F. densiflora, and elliptic-lanceolate
in F. officinalis. The maximum vertical diameter
and apical pore depth is seen in F. officinalis (509.74
and 282.91 Mm). The minimum values of the same
parameters were observed in F. asepala (237.79 and
133.9 Mm).
Seed color is a diagnostic character in Fumaria
species as well. The seed color is grey to gold in F.
asepala, brown in F. densiflora, green to gold with red
spots and dots in F. officinalis, green in F. parviflora,
and green with red stripes in F. vaillantii (Figure 1).
Seed surface ornamentations are of diagnostic
value in the Fumaria species of Iran. F. asepala show
scaly-form ornamentation with round borders,
while scaly-form right angled ornamentations with
gland appendage are observed in F. densiflora. The
seed surface shows scaly-form ornamentations
on a wrinkled substrate in F. officinalis, but the
wrinkled substrate is somehow different in F.
parviflora populations. The seed surface in F. indica
is smooth or plicate. The Yazd and Fassa populations
F. EBRAHİMZADEH ARAII, M. KESHAVARZI, M. SHEIDAII, P. GHADAM
169
Table 1. Voucher details of Fumaria sampled in this study.
Vouchers Species
Mazandaran, Gadook, Keshavarzi, 8612 (Herb. of Alzahra Univ.) Fumaria vaillantii
Mazandaran, on the road of Karaj to Chalous, Pole Zanguleh, 2400 m, Ebrahimzadeh 8613 (Herb.
of Alzahra Univ.) F. vaillantii
Tehran, Jajrood, Ebrahimzadeh 8614 (Herb. of Alzahra Univ.) F. vaillantii
Tehran, Baraghan, Keshavarzi 8620 (Herb. of Alzahra Univ.) F. vaillantii
Tehran, Moderiat, Ebrahimzadeh 8626 (Herb. of Alzahra Univ.) F. vaillantii
Hamedan, Heidareh, Keshavarzi 8628 (Herb. of Alzahra Univ.) F. vaillantii
Tehran, Abali, Mobarak abad, Nataj 8639 (Herb. of Alzahra Univ.) F. parviflora
Golestan, Golestan park, Ebrahimzadeh 8641 (Herb. of Alzahra Univ.) F. parviflora
Lorestan, Dasht Chegene, Derekvandi 8642 (Herb. of Alzahra Univ.) F. parviflora
Lorestan, Garesan, Derekvandi 8643 (Herb. of Alzahra Univ.) F. parviflora
Fars, Fassa, Rastipisheh 8646 (Herb. of Alzahra Univ.) F. parviflora
Yazd, Yazd, Keshavarzi 8647 (Herb. of Alzahra Univ.) F. parviflora
Yazd, Taft, Keshavarzi 8648 (Herb. of Alzahra Univ.) F. parviflora
Kermanshah, Ostandari park, Gholame 8649 (Herb. of Alzahra Univ.) F. parviflora
Tehran, Cheitgar park, Ebrahimzadeh 8635 (Herb. of Alzahra Univ.) F. indica
Charmahal Bakhtiyari, Borojen, Yazdanbakhsh 8652 (Herb. of Alzahra Univ.) F. asepala
Fars, Kakan, Yazdanbakhsh 8654 (Herb. of Alzahra Univ.) F. asepala
Tehran, Taleghan, Falatory 8657 (Herb. of Alzahra Univ.) F. asepala
Mazandaran, Kelardasht, Ebrahimzadeh 8659 (Herb. of Alzahra Univ.) F. densiflora
Mazandaran, Namakabrood, Ebrahimzadeh 8660 (Herb. of Alzahra Univ.) F. densiflora
Mazandaran, Galoogah, Nataj 8661 (Herb. of Alzahra Univ.) F. officinalis
Table 2. Morphological characters
Depth of seed apical gap (mm)
Ratio of first diameter to second diameter of seed
Ratio of first diameter to second diameter of seed apical gap
Seed color: green with red lines = 1, green = 2, ochre-golden = 3, brown = 4, golden green with red spots = 5
Seed shape: spheroid = 1, ellipsoid = 2, elongated ellipsoid = 3
Seed surface ornamentation pattern: scale form = 1, semi smooth and undulating = 2, low walled scales = 3,
round angled scales = 4, right angled scales with tuberous extensions = 5, scales on a wrinkled substrate= 6
Fruit surface ornamentation pattern: highly crowded protruding with velutinus appearance = 1,
wrinkled with prickle base = 2, crowded wrinkle with prickle base = 3, wrinkled granular = 4, fossulate = 5, crowded wrinkled = 6
of F. parviflora show dense and compact forms. F.
vaillantii also shows scaly form ornamentations that
are similar somehow to F. officinalis ornamentations
(Figure 1).
Fruit surface ornamentations are useful in
species identification in the Fumaria populations
of Iran. F. asepala show a wrinkled surface with
compact ornamentations. F. densiflora has a granular
and wrinkled fruit surface. The fruit surface
ornamentations in F. officinalis show fossulate
patterns with deep gaps (Figure 2).
The fruit surface in 3 different populations of
F. parviflora show wrinkled patterns with prickle
shapes. F. indica shows the same pattern, which is
Fruit and seed morphology of the Fumaria L. species (Papaveraceae) of Iran
170
Figure 1. Stereomicroscope and scanning electron micrographs of Fumaria species seeds. 1
and 4- F. asepala, 5 and 8- F. densiflora, 9 and 12- F. officinallis, 13 and 16- Cheitgar
population (F. indica), 17 and 20- Yazd population (F. parviflora), 21 and 24- Fassa
population (F. parviflora), 25 and 28- F. vaillantii. Magnification of 1st column from
left 170× and the 2nd column 230×.
F. EBRAHİMZADEH ARAII, M. KESHAVARZI, M. SHEIDAII, P. GHADAM
171
Figure 2. Scanning electron micrographs of Fumaria species fruit. 1 and 3- F. asepala,
4 and 6- F. densiflora, 7 and 9- F. officinallis, 10 and 12- Cheitgar population
(F. indica), 13 and 15- Yazd population (F. parviflora), 16 and 18- Fassa
population (F. parviflora), 19 and 21- F. vaillantii.
somehow more compact. F. vaillantii has a scabrate
and wrinkled fruit surface. In this species, its
ornamentations with 500 magnification show a velvet
texture on the fruit surface (Figure 2).
Results of statistical analysis
Statistical analysis by cluster analysis method
(UPGMA) based on 7 qualitative and quantitative
micro-morphological characters of the fruit and seed
Fruit and seed morphology of the Fumaria L. species (Papaveraceae) of Iran
172
surface (Figure 3) revealed the presence of 3 major
clusters. F. asepala stands separate from the other
species in the first cluster, while F. densiflora and F.
officinalis comprise the second major cluster. The
other species studied show similarity and form the
third major cluster. F. parviflora takes an intermediate
position between the members of second and third
major clusters. In general, the closer affinity between
F. densiflora and F. officinalis as well as F. vaillantii
and F. parviflora is concordant with their general
morphology. PCO plotting based on fruit and seed
micro-morphological characters (Figure 4) also
supports this clustering result.
Discussion
Our results support the taxonomic treatment
of the genus in the Flora Iranica as species of F.
parviflora, F. indica, and F. vaillantii have been
considered close to each other and F. asepala and F.
densiflora provide a separate position. F. officinalis is
not mentioned in the Flora Iranica, and so our results
about the position of this species cannot be evaluated
with this reference.
The Cheitgar population of F. indica shows some
differences in its seed and fruit surface with the other
populations. Although there are a lot of similarities
between these 2 taxa (F. indica and F. parviflora), it
appears that seed and fruit surface ornamentation is
a very useful tool in species separation. Jafri (1974)
in the Flora of Pakistan mentioned that F. indica
should be considered as a hybrid between F. asepala
0.01 0.01 0.02 0.01 0.03
Coefficient
F. asepala
F. officinalis
F. densiflora
F. parviflora
F. indica
F. parviflora
F. vaillantii Moderiat
Yazd
Cheitgar
Fassa
Kelardasht
Galogah
Taleghan
Figure 3. UPGMA dendrogram based on the seed and fruit morphology of Fumaria species.
Figure 4. PCO ordination of the Fumaria species based on seed
and fruit morphology.
Taleghan
F. asepala
Galogah
F. officinalis
Fassa
F. parviflora
Yazd
F. parviflora
Kelardasht
F. densiflora
Moderiat
F. vaillantii
Cheitgar
F. indica
0.00
-0.01
-0.03 -0.02 -0.01 0.00 0.01
Dim-1
Dim-2
0.00
-0.00
-0.00
F. EBRAHİMZADEH ARAII, M. KESHAVARZI, M. SHEIDAII, P. GHADAM
173
and F. parviflora. It is morphologically very similar
to F. parviflora (Wendelbo, 1974). Our previous
palynological and morphological studies confirmed
the separate position of the Cheitgar population as F.
indica. Due to the micro-morphological differences
between the fruit and seeds of F. parviflora accessions
in Iran, it seems that there are some subspecies in F.
parviflora.
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