全 文 ：Received 23 Jan. 2003 Accepted 2 Apr. 2004
Supported by the National Natural Science Foundation of China (39970407).
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Acta Botanica Sinica
植 物 学 报 2004, 46 (8): 988-996
Ultrastructural Aspects of Plasmodesmata and Cytoplasmic Bridges
During Spermatogenesis in Funaria hygrometrica
DONG Wen, LI Wei, GUO Guang-Qin*, ZHENG Guo-Chang
(Institute of Cell Biology, Lanzhou University, Lanzhou 730000, China)
Abstract: Cytoplasmic bridge, as a broader cellular connection structure, exists in plants from Volvox to
higher plants, but has been subjected to less investigation as compared to plasmodesmata. It has been
speculated that the structure may be related to the synchronization of cell division and development
during the microsporegenesis and spermatogenesis. During spermatogenesis in bryophytes, the
spermatogenous cells are divided into several domains within an antheridium, and their divisions are
synchronous. However, their cellular connection system has not been investigated systematically. In this
study, we undertook an ultrastructural examination of the structure and dynamics of the intercellular
connection system during the spermatogenesis in Funaria hygrometrica Hedw. The result revealed that
within each individual domain, synchronously dividing spermatogenous cells were connected with each
other by numerous cytoplasmic bridges, which were absent in the walls between different domains. The
plasmodesmata connected spermatogenous cells with the cells of jacket layer, and also existed between
the jacket layer cells, but absent in the walls between the developing spermatogenous cells. At the late
stage of the antheridial development, as the cell wall began to degrade, all of the spermatid cells within an
antheridium seem connected with each other by the expanded cytoplasmic bridges. The cytoplasmic
bridges retained to the late stage of spermatid’s differentiation, and finally, the spermatids synchronously
differentiated into spermatozoids. The different internal structures, biogenesis mechanisms and distribution
between the plasmodesmata and cytoplasmic bridges suggest that they may play distinct roles during the
development of antheridia.
Key words: cytoplasmic bridges; plasmodesmata; spermatogenesis; Funaria hygrometrica
Plant cells are separated from each other by the cell wall.
Although the substantial extracellular matrix is not
impervious, it is likely to hinder intercellular communication.
Unlike animal cells, plant cells can not migrate during
development, making communication essential for the co-
ordination of plant growth. It appears that plants have sig-
nificantly overcome the disadvantageous aspect of having
a cell wall by forming bridges between cells to allow transit
of signals and other important molecules. The evolution-
ary power had endowed plant cells with two direct commu-
nicational apparatus, plasmodesmata and cytoplasmic
bridges (also termed “intercellular bridge” or “cytoplasmic
channel”). Plasmodesma is a cytoplasmic strand delimited
by the plasma membrane that is continuous from one cell to
another with an appressed endoplasmic reticulum cylinder
in its center, interconnects cells and form an intercellular
communication network within a plant body. This struc-
ture can be formed at cytokinesis by incorporating the en-
doplasmic reticulum into the forming cell plate or de novo
across existing cell walls. It can also be modified to reduce
or enhance intercellular transport or allow plasmodesmata
to acquire new transport functions (Hepler, 1982; Robards
and Lucas, 1990; Ding et al., 1999). The plasmodesmata
were reported to be highly dynamic in their structure. In
recent years, the significant progress in this field has been
made. It is found that plasmodesmata can mediate intercel-
lular trafficking of protein and RNAs. Researchers convinced
that cell-to-cell communication via the plasmodesmata is
vital to coordinate the cellular processes that lead to cell
differentiation, morphogenesis, development, and growth
of multicellular plant (Ding et al., 1992; Ding, 1998; Ding et
al., 1999; Zambryski and Crawford, 2000; Wu et al., 2002).
Cytoplasmic bridge is a pore between two conjoint cells,
lined by plasma membrane that is continuous from one cell
to another. Unlike plasmodesmata, there has no appressed
endoplasmic reticulum cylinder in its center. Although this
structure is conserved from lower plants such as Volvox to
higher plants (Green et al., 1981; Kwiatkowska and
Maszewski, 1986; Wang et al., 1998; Pan et al., 2002), its
function is still unclear; it even was considered as plas-
modesmata by some scientists (Kwiatkowska and
Maszewski, 1976; Kwiatkowska and Maszewski, 1985;
DONG Wen et al.: Ultrastructural Aspects of Plasmodesmata and Cytoplasmic Bridges During Spermatogenesis in
Funaria hygrometrica 989
Kwiatkowska and Maszewski, 1986; Fraceschi et al., 1994;
Ding et al., 1999; Kwiatkowska et al., 2003). It was specu-
lated that the cytoplasmic bridge (cytomictic channel) might
play important roles in the development of pollen mother
cell of higher plants. Based on the fact that the cytoplasmic
bridges coexist with the synchronous division of pollen
mother cells of higher plants, it was believed that cytoplas-
mic bridge might contribute to this process (Guo and Zheng,
2004). The bryophytes have an important status in plant
evolution: their life cycle is dominated by a photoau-
totrophic haploid gametophytic generation, the relatively
simple and mainly heterotrophic diploid sporophyte were
supported on it. The spermatogenesis of moss has been
elaborated at light microscopic level. The initial of an
anteridium is a superficial cell at the apex of a stem or branch.
This cell divides to form five to fifteen regularly arranged
segments. One of the segments divides in a diagonally ver-
tical plane. One daughter cell is a jacket initial, while other
cell divides into another jacket initial and a primary sper-
matogenous cell. Each of the primary spermatogenous cells
divides and redivides to form a large number of spermatid
mother cells and then completed its multiplication stage.
The blocks of the spermatogenous cells derived from the
various primary spermatogenous cells may be distinguished
from one another by their arrangement and each formed an
individual domain. In the last mitosis each of the spermatid
mother cells divides to form two spermatid cells, which meta-
morphose into spermatozoid finally, and complete its dif-
ferentiation process (Smith, 1938). A very interesting phe-
nomenon during spermatogenesis is that within an indi-
vidual domain the spermatogenous cells, which probably
all come from an individual primary spermatogenous cell,
divide synchronously. This phenomenon was described
more then 60 years ago at light microscopic level (Smith,
1938), but the related intercellular connection system has
not been investigated systematically. In this study, we un-
dertook an ultrastructural examination of the structure and
dynamics of intercellular connection system during the sper-
matogenesis in Funaria hygrometrica Hedw. The result
indicated that the cytoplasmic bridges existed between its
spermatogenous cells. Since plasmodesmata and cytoplas-
mic bridges exist simultaneously within an individual
antheridium, we focused on the relationship between them.
Their distribution, structure and possible functions have
been investigated respectively.
1 Materials and Methods
Funaria hygrometrica Hedw. was collected from local
greenhouse, their antheridia were chopped finely from the
apex of fertile male gametophyte under anatomical lens and
fixed immediately. This structure seems difficult to be fix-
ated ideally. A series of combination of fixation fluids have
been used in the present study. The material was prefixed
in 5% glutaraldehyde in 0.1 mol/L phosphate buffer (pH
7.4) containing either 0.3% tannin or 0.5%-1.0% Tween 80
for 3-6 h at 4 ℃. Addition of Tween 80 in the fixative was
necessary for tissue penetration and optimal fixation. Four
percent paraformaldehyde was added in all the fixation flu-
ids mentioned above. The specimens were washed in 0.1
mol/L phosphate buffer (pH 7.4), postfixed in 1% or 2%
OsO4 in the same buffer overnight at 4 ℃, 0.8% or 1.6%
K3Fe(CN)6 have been added respectively or not. The speci-
mens become brittle when they were postfixed by 2% OsO4.
K3Fe(CN)6 did not have distinctive effect on this material.
After several rinse in distilled water and dehydration in a
graded ethanol series, the tissue was embedded in Epon
812 and sectioned with an LKB-8800 ultrathin microtome.
The sections of 70-80 nm thick were collected, double-
stained with lead citrate and uranyl acetate, and examined
under the Phillip EM-400T transmission electron
microscope.
2 Results
2.1 The dynamic of the cytoplasmic bridges in the anthe-
ridial development
There was no cytoplasmic bridge in the cell wall of the
primary spermatogenous cells at the initial stage of the sper-
matogenesis (Fig.1). Along with rapid division, the sper-
matogenous cells within an antheridium were divided into
several distinct domains (Fig.2). The domains can be dis-
tinguished clearly at light microscopic level (Fig.2), some-
times by the synchronous mitotic figure within some of
them (not shown); Within each domain the spermatogenous
cells were connected with each other by numerous cyto-
plasmic bridges (Figs.3-4, 6), which were absent in the
walls between different domains (Fig.3). In both kinds of
walls, no plasmodesma was observed. It appeared that cy-
toplasmic bridges have been blocked by wall material at
some walls within one individual domain, so the number of
the domains increased gradually with the development of
antheridia. The endoplasmic reticulum existed in the form-
ing spermatogenous cell plates (Fig.5). Numerous irregular
cytoplasmic bridges extended across the newly born cell
wall (Fig.6). The endoplasmic reticulum was rarely observed
in the vicinity of those kinds of cell wall. The younger cell
walls have higher density of funnel-shaped cytoplasmic
bridges (Fig.6), whose average diameter in narrowest place
was found to be about 50 nm and ranged from 30 to 100 nm
Acta Botanica Sinica 植物学报 Vol.46 No.8 2004990
(about 11 per mm2). The mean frequency (density
distribution) of cytoplasmic bridges in the longitudinal sec-
tions of newly formed cell wall was about 10 per 3 000 nm of
the cell wall and hence the cell wall occupied by cytoplasmic
Figs. 1-6. 1. Cytoplasmic bridge was absent from the cell wall (arrows) of the primary spermatogenous cells. ×3 900. 2. Longitudinal
section of an antheridium at light microscopic level, the domains can be distinguished clearly. ×330. 3. Spermatogeneous cells within an
antheridium are divided into several different domains by thick walls, which have no cytoplasmic bridge. Within an individual domain
spermatogenous cells are separated from each other by the thin walls, but not isolated as they are connected by many of cytoplasmic
bridges. Cytoplasmic bridges (arrowheads) in the thin wall were sectioned longitudinally. ×62 000. 4. Cytoplasmic bridges were
sectioned transversely, which looked as a hollow encircled by plasmalemma. ×165 000. 5. The forming cell plate of spermatogenous
cells. Endoplasmic reticulum (arrow) participated in the process. ×44 000. 6. Newly formed cell wall. Numerous of funnel-shaped
cytoplasmic bridges span cross it. ×33 000. Abbreviations: CW, cell wall; Ja, jacket layer cells; N, nucleus; Sp, sermatogenous cells; St,
stalk cells; Tk, thick walls; Tn, thin walls.
DONG Wen et al.: Ultrastructural Aspects of Plasmodesmata and Cytoplasmic Bridges During Spermatogenesis in
Funaria hygrometrica 991
bridges can be calculated to be 2%-3%. Along with the
division of the spermatogenous cells, the endoplasmic
reticulum was gradually approaching the cell wall and ar-
ranged along the cell wall finally (Fig.7). The endoplasmic
reticulum excreted the wall materials to the cell walls, which
leads to cell wall thickening (Fig.8). Ultimately, the cyto-
plasmic bridges disappeared at particular wall (Figs.7, 8)，
and the new blocks (domains) formed. At the same time, the
density of cytoplasmic bridges had decreased within one
domain (about 6 per mm2); on the other hand, the remain-
ders were become regular fistulous (Figs.3, 4), then the en-
doplasmic reticulum gradually dispersed into the cytoplasm
again. The spermatogenous cells, by division and redivision,
gave rise to many cubical cells, which became progres-
sively smaller in each succeeding cell generations, and their
protoplasts became condensed. All of those characteris-
tics can help us to easily distinguish different development
stages of the spermatogenous cells.
At the late stage of the antheridial development, as sper-
matogenous cells completed their multiplication, the cell
wall began to degrade. The spermatid cells shrank and be-
gan to round off, to carry out their differentiation stage
(spermiogenesis). At this stage, all of the spermatid cells
within an antheridium seemed to be connected with each
other by the expanded cytoplasmic bridges directly or indi-
rectly (Fig.9). After the thorough degradation of the cell
wall, the spermatids eventually lie within a common cavity
that is embedded by one layer of jacket cells. At this
moment, a number of cytoplasmic bridges encompassing a
spermatid and made it looked multi-protuberant (Figs.9, 10).
The cytoplasmic bridges retained to the late stage of
spermatid’s differentiation. Along with the gradual cyto-
plasmic deletion, the spermatids were shrunken, and the
cytoplasmic bridges break down ultimately and the sper-
matids synchronously differentiated into spermatozoids
(Fig.11).
2.2 The dynamic of plasmodesmata
Plasmodesmata, as another cellular communicational
apparatus in plant, existed at early stages of spermatogen-
esis simultaneously with the cytoplasmic bridges within
one antheridium but distributed differently. The plasmodes-
mata connected spermatogenous cells with the cells of jacket
layer (Fig.13), and also existed between the jacket layer
cells in the antheridia (Fig.12), but absent in the walls be-
tween the developing spermatogenous cells in whole pro-
cess of spermatogenesis. Along with the degradation of
the wall of the spermatogenous cells, the plasmodesmata
between the jacket layer cells and the spermatogenous cells
were break down. This may contribute to the differentia-
tion of the spermatid cells. Interestingly, there was a high
density of plasmodesmata between the stalk cells (Fig.14).
The density of plasmodesmata in the longitudinal sections
of those cells wall was about four per mm of the cell wall.
2.3 Ultrastructure of cytoplasmic bridges and plasmodes-
mata
In the longitudinal sections, the cytoplasmic bridges in
the newly formed androgonial cell wall could be seen as
funnel-shaped cannels which widen out towards the inside
of the cell (Fig.6). Their average diameter in narrowest place
(middle lamella) was found to be about 50 nm and ranged
from 30 to 100 nm. As the cell wall became thicker, the cyto-
plasmic bridges turned into open barrel-like structure (Fig.
3). Their diameter was approximately 50 nm. The cytoplas-
mic bridges looked as a hollow encircled by plasmalemma
in the transverse section (Fig.4). It was important to note
that the endoplasmic reticulum was never found to span
cross the cytoplasmic bridges at this stage (Figs.3, 4). After
the thorough degradation of the cell wall, elongated and
expanded cytoplasmic bridges could be observed (Figs.9,
10). Their diameter ranged from 100 nm to 350 nm. The di-
ameter of the cytoplasmic bridges could reach its broad-
est to 700-800 nm between the spermatids (Fig.10).
The ultrastructure of plasmodesmata in the F.
hygrometrica was similar to not only the other member of
this family but also the seed plants (Cook et al., 1997).
Contrast to intercellular bridge, both in the longitudinal
sections and in the transverse sections, configuration of
appressed endoplasmic reticulum cylinder could be ob-
served across the plasmodesmata (Figs.16, 17). The diam-
eter was similar to that in higher plant, approximately 30 nm.
Figs. 7-11. 7. Endoplasmic reticulum (arrows) approached the cell wall and arranged along it. Part or all of the cytoplasmic bridges have
been grandly blocked at particular cell walls. ×9 000. 8. The endoplasmic reticulum excreted the walling materials (arrows) to the cell
wall. ×36 000. 9. The elongated cytoplasmic bridges (arrowheads) between spermatids. ×14 000. 10. The diameter of the cytoplasmic
bridges between the spermatids could reach 700-900 nm (arrowhead). ×9 300. 11. Along with the gradual cytoplasmic deletion, the
spermatids were shrunken, and the cytoplasmic bridges break down ultimately and the spermatids differentiated synchronously.
×5 400. Abbreviations: CW, cell wall; ER, endoplasmic reticulum; F, flagella; G, Golgi body; N, nucleus; P, plastid.
→
Acta Botanica Sinica 植物学报 Vol.46 No.8 2004992
DONG Wen et al.: Ultrastructural Aspects of Plasmodesmata and Cytoplasmic Bridges During Spermatogenesis in
Funaria hygrometrica 993
3 Discussion
The concept of cytoplasmic bridge as a special commu-
nication canal in plat has not been fully accepted by plant
biologist. In some cases, it is even confused with
plasmodesmata, examples include the cytoplasmic bridges
during the spermatogenesis of Chara. We doubt whether
those opened tubular structure can be named as plasmodes-
mata since no appressed ER existed in its center
(Kwiatkowska and Maszewski, 1986; Kikuyama et al., 1992).
Some authors named it as “simple plasmodesmata”
(Fraceschi et al., 1994; Ding et al., 1999). In the present
Figs. 12-16. 12-14. The plasmodesmata system during development of the antheridia. 12. Plasmodesmata (arrows) exist in the cell
wall between jacket layer cells. × 22 000. 13. Plasmodesmata (arrows) existed in the cell wall between the jacket layer cell and the
spermatogenous cell. ×25 000. 14. There have a high density of plasmodesmata between the stalk cells. ×15 000. 15, 16. Ultrastruc-
ture of plasmodesmata in the antheridia of Funaria hygrometrica, which was similar to it in the higher plants, but branched plasmodes-
mata has not been found in this species. 15. Transversal section of plamodesmata with the appressed endoplasmic reticulum in its center.
×65 000. 16. Longitudinal section of plasmodesmata with endoplasmic reticulum (arrows). ×57 000. Abbreviations: Chl, chloroplast;
CW, cell wall; Ja, jacket layer cells; N, nucleus; P, plastid; Sp, sermatogenous cells.
Acta Botanica Sinica 植物学报 Vol.46 No.8 2004994
study, cytoplasmic bridges and plasmodesmata were ob-
served to exist within one antheridium simultaneously dur-
ing the spermatogenesis of F. hygrometrica, but have dif-
ferent structures, distributions and dynamics as described
above. This implies that these two different intercellular
connection structures may play different roles during the
development of antheridia.
In spite of the diversity in diameter and shape, cyto-
plasmic bridges exhibited similar structures as hollow plasma
membrane-limited cannels connecting two adjacent cells.
Its plasma membrane was continuous from one cell to
another. Unlike the plasmodesmata, there is no appressed
endoplasmic riticulum cylinder in the center of the cyto-
plasmic bridge, which was in many cases much wider than
the former. The difference in structure between plasmodes-
mata and cytoplasmic bridges may determine the differ-
ence in their transport functions. Although some small
molecules could diffuse via plasmodesmata unselectively,
they were selective for certain ions and molecules, espe-
cially the macromolecules such as transcription factors,
mRNA, endogenous proteins, viral proteins and viral ge-
nomes (Ding, 1998; Ding et al., 1999; Wu et al., 2002). The
plasmodesmata connected not only the jacket layer cells
with spermatogenous cells but also the jacket layer cells.
Since the spermatogenous cells have no fully developed
chloroplast, they are unable to synthesize nutrients through
photosynthesis; therefore, the jacket cells may transport
some nutrients and/or signaling molecules through the plas-
modesmata to spermatogenous cells. In this way, plas-
modesmata can make two different kinds of cell separated
from each other, but not isolated, so keeping their differen-
tiation states (Ding, 1998; Ding et al., 1999; Zambryski and
Crawford, 2000; Wu et al., 2002). Cytoplasmic bridges, as
an open structure, nonselective transport maybe its major
mechanism of symplastic transport: most of the macromol-
ecules and even the organelles can be shared between cells
(Zhang et al., 1990; Cooley and Theurkauf, 1994; Cooley
and Cooley, 1998; Wang et al., 1998; Woodruff and Tilney,
1998; Wang et al., 2002; Zhang, 2002). It was believed that
the cytoplasmic bridges may play important roles during
the spermatogenesis of animals for they ensure that the
haploid spermatids have access to the products of post-
meiotically expressed X-linked genes during the complex
morphological changes of spermatogenesis in mammals
(Braun et al., 1989; Caldwell and Handel, 1991; Morales et
al., 1998; Morales et al., 2002). However, cytoplasmic
bridges also exist in haploid gametophytes of F.
hygrometrica during its spermatogenesis, where cell divi-
sion is just mitotic and thereby no genetic segregation,
raising the problem of their special function in this process.
Maybe it was essential to the synchronous development
of the spermatogenous cells. Maybe the process of syn-
chronous division of spermatogenous cells were controlled
by related genes, but the intercellular coordination was
indispensable. Spermatogenous cells are “stick together
through thick and thin” and each making up the other’s
deficiency from its own surplus through the cytoplasmic
bridges. The spermatogenous cells are highly coordinated
on almost all aspects of the cellular activities in development,
producing many basically if not absolutely identical func-
tional spermatids at the same time. This may contribute to
successful fertilization. Although other functions of cyto-
plasmic bridges during the spermatogenesis of this spe-
cies are waiting to be investigated, our results show that
cytoplasmic bridge is different from plasmodesmata in func-
tional aspects. We speculated that plasmodesmata, with its
selectivity, communicate cells with different fate while the
cytoplasmic bridges made cell synchronously to develop
during the spermatogenesis of F. hygrometrica.
Based on the fact that the newly formed cell wall has a
higher density of cytoplasmic bridges than older one and
along with the development of the antheridia the number of
domain gradually increased, we suppose that within one
domain of the F. hygrometrica antheridium, the cytoplas-
mic bridges formed as a result of incomplete cytokinesis
and some of them may have been blocked by the deposi-
tion of wall material in the process of the cell wall
development. Endoplasmic reticulum existed in the forming
cell plate, but not in the center of newly formed cytoplas-
mic bridges, suggesting that the endoplasmic reticulum was
participated in the formation of cell plate but not related to
the formation of the cytoplasmic bridges, which was basi-
cally different from the formation of plasmodesmata (Hepler,
1982). The cytoplasmic bridges have been blocked com-
pletely at some specific cell wall, increasing the number of
d o mains wi thin o ne an the r id ium d ur ing the
spermatogenesis. Why the part of cell wall was blocked
completely to form different domains and by what mecha-
nisms this can be achieved is still enigma. Maybe it con-
tributed to the proper coordination of the cells within one
domain by restricting number of the cells in an acceptable
limitation.
As the cell wall starts to disintegrate, cytoplasmic
bridges seem to connect all the spermatid cells. We specu-
late that part of the cytoplasmic bridges may be formed
secondarily. It is believed that the land plants, including
the bryophytes, appear to be a monophyletic group that
arose from an ancestor held in common with certain mod-
DONG Wen et al.: Ultrastructural Aspects of Plasmodesmata and Cytoplasmic Bridges During Spermatogenesis in
Funaria hygrometrica 995
ern charophycean green algae (Graham et al., 1991;
McCourt et al., 1996). So it is no wonder that a similar phe-
nomenon also exists during the spermatogenesis of Chara
where cells within a single filament are also divided into
two or more synchronous segments, which was caused by
“plugging” of “plasmodesmata” between different seg-
ments by the osmiophilic substance. (Kwiatkowska and
Maszewski, 1976; Kwiatkowska and Maszewski, 1985;
Kwiatkowska and Maszewski, 1986; Kwiatkowska, 2003).
These kinds of plugged “plasmodesmata” in the walls ad-
joining asynchronous groups of cells within a single fila-
ment and between the basal cells of adjacent antheridial
filaments can be opened if the substance plugging “plas-
modesmata” disappears. Then the process of developmen-
tal synchronization of antheridial filaments extended from
the region of one filament to all the filaments developed
from the same capitular cell (Kwiatkowska and Maszewski,
1986). The three-dimensional cytoplasmic bridge systems
of F. hygrometrica within its antheridium are more complex
than that in Chara, but they are continuous in evolution.
So it is not proper to name the open bridges in the Chara as
plasmodesmata. Whether the cytoplasmic bridges connect
all of the spermatic mother cells or the spermatids directly
or indirectly within an individual antheridium still need to
be confirmed by 3-D reconstruction. The biogenesis mecha-
nism of those “secondary” cytoplasmic bridges between
the spermatid mother cells and spermatid cells is still to be
investigated.
Acknowledgements: We thank Mr. LU Wei and Miss
WANG Dai-Si for their help in electron microscopic
observation; Dr. Rajesh Kumar Tiwari for critical reading of
the manuscript; and numerous colleagues for suggestions
and helps with the manuscript.
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