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THE JOURNAL OF TROPICAL LIFE SCIENCE OPEN ACCESS Freely available online
VOL. 5, NO. 2, pp. 98-104, May, 2015
Gametophyte Morphology and Development of Six Species of
Pteris
(Pteridaceae)
from Java Island Indonesia
Dwi Sunarti Puspitasari1, Tatik Chikmawati2*, Titien Ngatinem Praptosuwiryo3
1Plant Biology Graduate Program, Department of Biology, Faculty of Mathematics and Natural Sciences,
Bogor Agricultural University, Darmaga Campus, Bogor, Indonesia
2Department of Biology, Faculty of Mathematics and Natural Sciences Bogor Agricultural University,
Darmaga Campus, Bogor, Indonesia
3Center for Plant Conservation- Bogor Botanical Gardens, Indonesian Institute of Sciences, Bogor, West Java, Indonesia
ABSTRACT
The morphology of sporophyte, the type of reproduction, and cytology of
Pteris
had been reported, while
the gametophyte morphology of
Pteris
in Java island has not been studied yet. The objective of this study was to
describe the gametophyte morphology and development of
P. biaurita, P. ensiformis, P. exelsa, P. longipinnula, P.
tripartita
, and
P. vittata
in Java island. Spores were obtained from fertile leaves of
Pteris
plants originated from
several locations in Java island. The number of spores per sporangium was counted from fresh fertile leaves with
mature sporangia. As much as 0.002 g spores was sown in a transparent box with sterile medium contain of ver-
miculite, sphagnum moss, and perlite with ratio 2:2:1. The gametophyte development of each species was observed
under a microscope every 7 days. The spores of
P. ensiformis
were germinated faster, ten days after sowing, while
the spores of
P. longipinnula
were germinated slower, 18 days after sowing. The pattern of spore germination is
Vittaria
-type. The development of gametophyte is
Ceratopteris
-type in common, but in a few cases is the
Adi-
antum
-type. The gametophyte development of observed
Pteris
species is varied in six characters including the
number of filament cell, germinated time, the formation time of notch and gametangia, margin shape, and devel -
opment type.
Keywords:
development, gametophyte, Java, morphology, Pteris
Pteris
L. is a large fern genus belong to the family
Pteridaceae, that are distributed in tropical and sub-
tropical regions [1]. It is estimated about 250
Pteris
species in the world [1,2] and 19 species of them dis-
tributed in Java island, Indonesia [3]. The species of
Pteris
grow in warmer temperature areas, but they also
found in cold temperatures. They grow either terrestri-
ally or lithophytically on rocks in several habitats,
shaded canopy, and open areas, forests, coastal, and
xeric niches [1,4]. Some species also survive in soil
contaminated arsenic or other metals [5].
The
Pteris
species are easily distinguished from
their sori characters. Their sori are linear and located
in marginal of leaves, but are usually not reaching the
apices of segments. A false indusium protected each
sorus [1,6].
Several studies on gametophyte morphology of
Pteris
have been done. The gametophyte development
of several
Pteris
species including,
P. vittata, P. finotii,
P. fauriei, P. exelsa, P. wallichiana, P. ensiformis, P.
cretica, P. multifida, P. deflexa, P. denticulata, P. tris-
ticula, P. faurirei, P. incompleta, P. berteroana, P.
chilensis,
and
P. tripartita
were reported having some
unique characters [7-13]. The similarity of these species
was on spore germination, the development gameto-
phyte, and gametangia type. Among these species are
differed in some gametophytic characters such as the
number cell of the filament, germinated time, the for-
mation time of notch, the formation time of gamet-
angia and type of gametophyte development.
Pteris
is taxonomically very interesting taxon since
it is a species complex [14]. The morphology of the
sporophyte, the type of reproduction and cytology of
some
Pteris
species in Java island such as
P. biaurita,
JTLS | J. Trop. Life. Science 98 Volume 5 | Number 2 | May | 2015
INTRODUCTION
*Corresponding author:
Tatik Chikmawati
Department of Biology, Faculty of Mathematics and Natural
Sciences, Bogor Agricultural University, Bogor, Indonesia
E-mail: tchikmawati@yahoo.com
Gametophyte Morphology and Development of Six Species of Pteris
P.ensiformis, P. multifida, P. vittata
, and
P. tripartita
,
were reported by several authors [15-19], while the ga-
metophyte morphology of
Pteris
has not been studied
before. The information on gametophyte phase is im-
portant to study the evolution, phylogeny and repro-
ductive biology of ferns [20,21]. Therefore, it is neces-
sary to examine the development and morphology of
fern gametophyte, especially on the genus
Pteris
.
The purpose of this study is to describe the gameto-
phyte morphology and development of six species of
Javanese
Pteris
,
P. biaurita, P. ensiformis, P.exelsa, P.
longipinnula, P. tripartita
, and
P. vittata
.
Spores were obtained from fertile leaves of
Pteris
plants originated from several locations in Java island
(Table 1). Fertile leaves were put in paper envelopes
under the dry condition to release spores from spora-
ngia. After 6-7 days, the contents of the envelopes were
sifted to eliminate sporangial fragments and other de-
bris [22].
The number of spores per sporangium was counted
from fresh fertile leaves with mature sporangia, and
five to 10 sporangia were observed for it [23]. Spo-
rangium with 64 normal spores were treated as sexual
reproduction type while the sporangium with 32 spores
treated as apogamous one [14].
As much as 0.002 g spores was sown in a transpar-
ent box with sterile medium contain of vermiculite,
moss and perlite with ratio 4:4:2. Medium were
covered with paper filter [24]. Before planting, the
medium was soaked in hot water for a day. All cultures
were maintained at the temperature ranged from 27-
30°C. The gametophyte development of each species
was observed under a microscope Olympus Stemi 1000
and Nikon Eclipse E100 every 7 days. The photograph
was documented using Optilab Advance.
Data of cell growth was analysis with One-way
Analysis of Variance (ANOVA) followed by Duncan
test on the α<0.05.
Reproduction type and spore morphology of Pteris
Among six
Pteris
species that have been observed,
two species (
P. ensiformis
and
P. tripartita
) have a sex-
ual reproduction type and four others (
P. biaurita, P.
exelsa, P. longipinnula
, and
P. vittata
) have apogamous
reproduction type (Table 2).
Pteris exelsa
has 64 spores per sporangium but are
classified into apogamous type because it has various
spore shape and size (Figure 1). The number of 64
spores per sporangium with various shapes and sizes
have also been found in
P. vittata
[19]. Apogamous
type is affected by the abnormal sporogenesis and spo-
rangium that undergoes the abnormal process, thus, it
produces variation in the number of spores, the size
and shape of spores per sporangium [25].
Most
P. biaurita
have apogamous reproduction type
than sexual types. Previous research reported that
among 90 of individuals
P. biaurita
observed, found 78
individuals have an apogamous type, and 12 individu-
als have mixture type, but the sexual type was never
found [15]. Sexual reproduction type in
P. biaurita
are
relatively few in Bogor and never found in Taiwan
[26,27]. The regulation the reproduction type of fern is
influenced by environmental factors such as light, alti-
tude, and temperature of the area [28]. The ethylene
gas, succinic acid, naphthalene acetic acid (NAA), gib-
berellic acid, high phosphorus concentrations, particu-
lar wavelengths of light, and drought can induce
apogamous type [29].
Sexual type on
Pteris
especially
P. vittata
and
P. en-
siformis
were most often found in Java. Among 14 in-
dividuals of
P. ensiformis,
13 individuals were the sex-
ual type, but one individual has apogamous type [18].
JTLS | J. Trop. Life. Science 99 Volume 5 | Number 2 | May | 2015
RESULTS AND DISCUSSION
MATERIALS AND METHODS
Figure 1. Spores of two fern reproduction types. A. Normal
spores of sexual type in
P. tripartita
, B. Abnormal
spores of Apogamous type in
P. exelsa
Table 2. Spore size and reproduction type of six
Pteris
species
Table 1. Collection site of observed
Pteris
Dwi Sunarti Puspitasari et al., 2015
A previous study reported among 37 individuals of
P.
vittata
in Java, 35 individuals have a sexual type, and 2
individuals were apogamous [19].
The spores of all species are trilete (Figure 2), ex-
cept in
P. exelsa
have various shapes from triangles,
rectangles, and ellipses.
Pteris
spore is triangular to rec-
tangular [1]. Spore size, length polar and the equatorial
diameter varies among species (Table 2).
Pteris longi-
pinnula
has the biggest spore sizes of the different
types. The most size variation spores found in
P.
exelsa
. Spore color is also varied,
P. biaurita, P.
longipinnula
, and
P. tripartita
have brown spore,
P.
ensiformis
has dark brown spore,
P. exelsa
has blackish
brown spore, and
P. vittata
has whitish-brown spore.
Gametophyte Morphology and Development of Pteris
Spore germination
The observed
Pteris
spores were germinated in 10
to 18 days after sowing (DAS) (Figure 3). Comparing
to other observed
Pteris
spesies, the spores of
P. ensi-
formis
were germinated faster, 10 DAS, while the
spores of
P. longipinnula
were germinated slower, 18
DAS. Spore germination type of all spesies is
Vittaria
type, with the first cell, emerged from the spores is per-
pendicular to the first rhizoid [20].
The filamentous stage of each
Pteris
species is var-
ied in the cell number. The filament of
P. ensiformis
has the shortest filament formed of 2-4 cells while
P.
longipinnula
had the longest range of filamentous sizes
(5-30 cell).
Pteris tripartita
had short filamentous size
(2-5 cells), but the filamentous stage of other observed
Pteris
are consisted of 5-9 cells long (Table 3). The fila-
mentous size of Javanese
Pteris
,
P. ensiformis, P. vit-
tata
, and
P. exelsa
, are differed to those described by
Zhang et al. (2008) [10], which have wider size varia-
tion (Table 3). The differences of this result may be
due to Zhang et al. (2008) [10] grew spores in the
mixture of black soil and sand.
The growth rate of
Pteris
gametophyte is varied
among observed species in every week (Figure 4) and
were significantly different among species based on
ANOVA and Duncan test (Table 4). The growth rate
of
Pteris
gametophyte began to differ among species on
the second week, and then the gametophyte growth
was continuously differed by the gametophyte age.
Pteris biaurita
did not grow until the second week.
Pteris vittata
showed the fastest growth rate during the
fourth until the eighth week. On the eight-week, the
growth of
P. ensiformis
gametophyte showed the slow-
est rate while that of
P. tripartita
showed the fastest.
On the ninth week, the growth of
P. longipinnula
ga-
metophyte showed the slowest rate while that of
P. tri-
partita
showed the fastest. On the tenth week,
P. vit-
tata
grew the fastest while
P. ensiformis
grew the
slowest.
JTLS | J. Trop. Life. Science 100 Volume 5 | Number 2 | May | 2015
Figure 3. Comparison of gametophyte development time among
Pteris
spesies. Germinated time ( ), formation
time of laminar ( ), formation time of gametangia
( )
Table 3. Gametophyte development of observed
Pteris
and a
previous study [10]
Table 4. Average of cell number
Pteris
species for 10 week
Figure 2.
Pteris
spores. A).
P. biaurita;
B).
P. ensiformis;
C).
P.exelsa;
D).
P. longipinnula;
E).
P. tripartita;
F).
P.
vittata
Gametophyte Morphology and Development of Six Species of Pteris
Laminar phase
The type of gametophyte development varies within
the genus
Pteris
, type
Ceratopteris
,
Adiantum
, and
modifications of the two kinds (Figure 5). However,
previous studies had reported that the gametophyte de-
velopment in
Pteris
genus has
Ceratopteris
-type [20].
The gametophyte development of all
Pteris
species
is the Cerato
pteris
-type, except
P. ensiformis
and
P. tri-
partita
. This pattern is similar to that of
P. deflexa, P.
tristicula, P. cretica, P. berteroana, P. fauriei, P. incom-
pleta, P. multifida, P. vittata
, and
P. wallichiana
[7-12].
In this type, the first cell division is in apical and
sometime in subapical, following by repeated division
(Figure 5I). Since the meristem is in lateral position,
the cell differentiation in the laminar stage is
asymmetric. By the time, the activity of meristematic
cells gives rise to form a cordate stage after 15-25 days.
P. ensiformis
has two types of gametophyte devel-
opment, the
Adiantum
-type in the early stage, and the
Ceratopteris
-type in the next phase of its prothallia de-
velopment. During the early phase of this type, the
oblique wall division occurs in a terminal cell of the
filament and was followed by a second oblique wall di-
vision at the right angles. A wedge-shaped then was
formed in an apical region (Figure 5G). By the time,
the activity of meristem cell in lateral position develops
a young asymmetric gametophyte. Previous studies re-
ported that the type of development gametophyte of
P.
ensiformis
follow
Ceratopteris
-type [7,10].
The gametophyte development of
P. tripartita
fol-
lows the
Adiantum
-type as described by Nayar and
Kaur (1971) [20]. In this type, the first division in the
terminal cell is parallel to the long axis of the filament.
The second division is oblique, then was followed by
all cell divisions in the meristematic cells (Figure 5H).
An expanded one-cell-thick of the obovate prothallia
plate is formed by repeated transverse and longitudinal
divisions. The location of the meristematic cell turned
into the notch is in the thallus apex. Among these six
species, the apical notches of
P. tripartita
were formed
earlier than that of the others. Rhizoids were usually
formed on the ventral surface of the prothallus, but
they were sometimes found on the dorsal surface of the
cushion or the wing margins. Results of this study dif-
fer from Ravi et al. (2014) [13] who reported that ga-
metophyte development of
P. tripartita
is
Ceratopteris
-
type.
Mature Gametophytes and Sexual Expression
The shapes of the mature cordate prothalli are var-
ied among all
Pteris
species (Figure 6 D-I). The mature
gametophytes of
P. biaurita, P. longipinnula, P. vittata
,
JTLS | J. Trop. Life. Science 101 Volume 5 | Number 2 | May | 2015
Figure 5. Germination, filamentous and laminar stages. A-C.
Germination. A.
P. ensiformis
; B.
P. tripartita
; C.
P.-
longipinnula.
D-F. Filamentous. D-E. Filamentous of
P. ensiformis
and
P. tripartita
formed of 3 cell; F.
Filamenthous of
P.longipinnula
formed of 13 cell.
G. Laminar with wedge-shaped meristematic cell of
P. ensiformis
. H. Laminar with wedge-shaped meris-
tematic cell of
P. tripartita
. I. Laminar with apical
cells twice devide; J. Young laminar plate with notch
in lateral of
P. ensiformis
. K. Young laminar plate
with notch in apex of
P. tripartita
. L. Young laminar
with a meristematiz zone. W= wedge-shaped meris-
tematic cell, N= Notch pointed by an arrow.
Figure 4. The cell growth of gametophyte
Pteris
,
P. biaurita
( ),
P. ensiformis
( ),
P.exelsa
( ),
P. longipinnula
( ),
P. tripartita
( ),
P. vittata
( )
Dwi Sunarti Puspitasari et al., 2015
and
P. exelsa
are asymetric cordiform, whereas
P. tri-
partita
and
P. ensiformis
are nearly symetric cordiform.
Formation time of sex organ is varied among
species.
Pteris
gametophytes began to produce an-
theridia 40–92 DAS.
Pteris vittata
produced sex organ
(antheridia) the earliest, 40 DAS, while
P. longipinnula
is the last producing sex organ, on 92 DAS (Figure 3).
The hermaphrodite gametophyte produced antheridia
earlier than archegonia. The archegonia were produced
on the ventral surface or notches of the prothalli, 74–
102 DAS. Typically, antheridia were produced on the
ventral surface of the wings, distributed over the dorsal
surface, along the wing margins, or both sides of the
gametophytes. Antheridia consist of a cap cell, a ring
cell, and a basal cell (Figure 6K).
Sex organs of
P. exelsa, P. longipinnula, P. vittata
,
and
P. biaurita
give rise to monosexual/male gameto-
phyte.
P. ensiformis
spores produced 17% of hermaph-
rodite gametophyte and 83% of the male gametophyte
while
P. tripartita
produced 27% of hermaprodite and
73% of the male gametophyte (Figure 7).
Apogamous types of
P. exelsa, P. biaurita, P.
longipinnula
, and
P. vittata
produced only the func-
tional antheridium. The same evident also found in
P.
cretica, P. pellucidifolia
, and
P. wulaensis
[30]. How-
ever,
P. wulaensis
produced only archegonium, and the
embryo appeared from the gametophyte cells indicat-
ing that it has apogamous reproduction type. Laird and
Sheffield (1986) [31] reported that apogamous
P. cret-
ica
is hermaprodite, but the archegonia had lost func-
tion because of the failure of the neck canal to open.
Results of this study differ from the previous study
on
P. exelsa, P. ensiformis,
and
P. vittat
a that produces
100% gametophyte hermaphrodites [10]. The differ-
ences of this result may be due to physical factors such
as nutrition, density gametophyte, the influence of
light, and the interaction between the gametophyte [32,
33].
Spore germination of
Pteris
genus is the
Vittaria
type.
Pteris
spores were germinated in 10 to 18 DAS.
The spores of
P. ensiformis
were germinated faster, 10
DAS while the spores of
P. longipinnula
were germi-
nated slower, 18 DAS. The number of cells in each
week of gametophyte growth were significantly differ-
ent among species based on ANOVA and Duncan test.
The gametophytes among
Pteris
species are differed in
the number of filament cell, germinated time, the for-
mation time of notch and gametangia, margin shape,
and the development type. Gametophyte morphologi-
cal characters can be used as a genus characteristic.
The author expresses the deepest appreciation to
Indonesian Government through the Directorate Gen-
eral of Higher Education for providing financial sup-
port for her research, Dr. Wen-Liang Chiou, Cibodas
JTLS | J. Trop. Life. Science 102 Volume 5 | Number 2 | May | 2015
ACKNOWLEDGMENT
CONCLUSIONS
Figure 6. Development stages of the gametophyte and sex or-
gans of
Pteris
. A-C Young gametophyte A.
P. ensi-
formis
; B.
P. tripartita
; C.
P.longipinnula
. D-I Ma-
ture Gametophyte, D. Asymetric cordate of
P. ensi-
formis
; E. Symetric cordate of
P. tripartita
; F. Asy-
metric cordate of
P.longipinnula
; G. Asymetric cor-
date of
P. biaurita
; H-I Asymetric cordate of
P. ex-
elsa
and
P. vittata
; J. Top view of the archegonia
P.
tripartita
; K. Side view of antheridium
P. exelsa
with
a cap cell (C), a ring cell (R), and a basal cell (B); L.
Top view of Antheridia. AR= Archegonium, AN=
Antheridium. B, C, R, AR are pointed by an arrow.
Figure 7. Appearance percentage of sexual expression, male ga-
metophyte ( ) and hermaphrodite gametophyte
( ).
Gametophyte Morphology and Development of Six Species of Pteris
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