Download Development of secretory cells and crystal cells in Eichhornia

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DOI 10.1007/s00709-010-0157-1
ORIGINAL ARTICLE
Development of secretory cells and crystal cells
in Eichhornia crassipes ramet shoot apex
Guo Xin Xu & Chao Tan & Xiao Jing Wei &
Xiao Yan Gao & Hui Qiong Zheng
Received: 4 February 2010 / Accepted: 23 April 2010
# Springer-Verlag 2010
Abstract The distribution and development of secretory
cells and crystal cells in young shoot apexes of water
hyacinth were investigated through morphological and
cytological analysis. The density of secretory cells and
crystal cells were high in parenchyma tissues around the
vascular bundles of shoot apexes. Three developmental
stages of the secretory cells can be distinguished under
transmission electron microscopy. Firstly, a large number of
electron-dense vesicles formed in the cytoplasm, then fused
with the tonoplast and released into the vacuole in the form
of electron-dense droplets. As these droplets fused together,
a large mass of dark material completely filled the vacuole.
To this end, a secretion storage vacuole (SSV) formed.
Secondly, an active secretion stage accompanied with
degradation of the large electron-dense masses through an
ill-defined autophagic process at periphery and in the
limited internal regions of the SSV. Finally, after most
storage substances were withdrawn, the materials remaining
in the spent SSV consisted of an electron-dense network
structure. The distribution and development of crystal cells
in shoot apical tissue of water hyacinth were also studied by
light and electron microscopy. Crystals initially formed at
one site in the vacuole, where tube-like membrane
structures formed crystal chambers. The chamber enlarged
as the crystal grew in bidirectional manner and formed
Handling Editor: Friedrich W. Bentrup
Electronic supplementary material The online version of this article
(doi:10.1007/s00709-010-0157-1) contains supplementary material,
which is available to authorized users.
G. X. Xu : C. Tan : X. J. Wei : X. Y. Gao : H. Q. Zheng (*)
Institute of Plant Physiology and Ecology, Shanghai Institutes for
Biological Sciences, Chinese Academy of Sciences,
300 Fenglin Road,
Shanghai 200032, China
e-mail: [email protected]
needle-shaped raphides. Most of these crystals finally
occurred as raphide bundles, and the others appeared as
block-like rhombohedral crystals in the vacuole. These
results suggest that the formation of both secretory cells and
crystal cells are involved in the metamorphosis of vacuoles
and a role for vacuoles in water hyacinth rapid growth and
tolerance.
Keywords Water hyacinth . Shoot apex . Secretory cells .
Crystal cells . Vacuole
Introduction
Water hyacinth [Eichhornia crassipes (Martus) Solms] is
one of the most productive plants in the world. The growth
of this plant is indeterminate, and the major way of its
reproduction is vegetative (Spencer and Bowes 1986). It
produces long stolons with rooted rosettes (ramets) at the
nodes. Each ramet can immediately produce other stolons
from any axillary meristems at the basal bract, even before
the root formation. The capacity of water hyacinth to
produce new clonal plants through stolon buds has been
reported in previous studies (Lugo et al. 1998; Kathiresan
2000; Simpson and Sanderson 2002), but there are few data
available about the developmental anatomy of the ramets
with emphasis on secretory cells and crystal cells, which
might be important to water hyacinth for its rapid growth
and adaptation to a wide range of environmental conditions.
Secretory cells, which have been found in almost all
plant organs, are specialized structures filled with secretion
products, such as tannic acid, resin, polysaccharides, pectin,
salts, and calcium oxalate crystal (Ciccarelli et al. 2001;
Mastroberti and Mariath 2003; Plachno and Swiatek 2008;
Paiva et al. 2008, 2009). The contents of secretion
G.X. Xu et al.
substances varied with the species. The functions of
secretory cells are related to the secretion products. For
examples, the secretion products of floral nectars contain
sugar, which can attract insects to visit and pollinate the
flowers. Mastroberti and Mariath (2008) suggested that a
role of the secretory cells (also called mucilage cells) in
young leaves of Araucaria angustifolia could be in
translocation and water storage of solute. The deposition
of secretion was observed at interface between the
plasmalemma and the cell wall (Klein et al. 2004; Paiva
et al. 2008), in the reduced portion of cytoplasm
(Mastroberti and Mariath 2008), or the central vacuole
(Fahn and Shimony 1998). Endoplasmic reticulum (ER)
has been considered to play an important role in the
development of secretory cells. According to Benayoun and
Fahn (1979), ER produces secretion substances and transports them out of cells. Langenheim (2003) also reported
the central role the ER played in transporting terpenoid
resin components from intracellular synthesis sites into the
lumen of an endogenous secretory structure. They assumed
that ER could fuse with membranes of other organelles and
form vesicles that move through the cell to vacuoles. For
example, plastids are considered as the site where
terpenoid resin are synthesized (Dell and McComb 1978;
Lichtenthaler et al. 1997) and fuse with ER to export the
production to vacuoles (Dell and McComb 1978; Fahn
1988; Carmello et al. 1995). Vacuoles are important
intracellular endpoints of secretion pathways in plants, but
mechanism of the transformation of vacuoles of secretory
cells is unknown.
Ca oxalate (CaOx) crystal is one of the most common
storage materials that can be found in most tissues and
organs of photosynthetic plants, such as Pistia stratiotes,
Morus alba, and grapevine, as an intra- or extracellular
deposit (Franceschi et al. 1993; Katayama et al. 2007;
Storey et al. 2003; Li et al. 2003). Intracellular crystals
often occurred within vacuoles of cells specialized for
crystal formation, called crystal idioblasts (Franceschi and
Nakata 2005). Studies on the CaOx crystal idioblast
formation in developing tissues suggested that a primary
function of crystal cells may be to serve as a strong
localized Ca sink to reduce the apoplastic Ca concentration
around adjacent cells, allowing them to develop normally
(Franceschi and Nakata 2005). The crystal cells were also
suggested to work as sinks for deposition and compartment
of toxic metals to reduce physiological damage (Franceschi
and Nakata 2005). Water hyacinth can absorb and accumulate large amounts of toxic substances such as heavy metal
ions and pollutants from water without damage (Mahamadi
and Nharingo 2010; Agunbiade et al. 2009; Rajan et al.
2008; EI-Khaiary 2007). CaOx crystal, which binds heavy
ions such as Cd and Pb, was also observed in water
hyacinth leaf cells (Mazen and Maghraby 1997), but little
information is available for the formation of CaOx
idioblasts in water hyacinth. In the present study, the
process of vacuole metamorphosis during development of
both secretory cells and crystal cells in water hyacinth shoot
apexes was examined, and its possible relevance to water
hyacinth tolerance is discussed.
Materials and methods
Plant material collection and culture
Water hyacinth (E. crassipes Solms) plants were collected
from a river at Jiading in Shanghai. The plant samples
were inserted in an upright position in plastic boxes of
40×40×40 cm3 containing 50 L Hoagland nutrient culture
solution (Hoagland and Arnon 1938) and grew in a
greenhouse (25–30°C) as described by Zheng et al.
(2006). Light intensity was about 120 µmol m−2 s−1, and
the period was 16 h light/8 h dark.
Transmission electron microscopy
Water hyacinth rosette shoot apexes were cut into small
blocks (about 2×2×2 mm3) and fixed for 12 h at 4°C in 2%
glutaradehyde and 2.5% paraformaldehyde in 50 mM
PIPES buffer (pH 7.2), washed by 50 mM PIPES buffer
(pH 7.2), then incubated in 2% osmium tetroxide in 50 mM
PIPES buffer (pH 7.2) for 2 h at room temperature. After
being washed by 50 mM PIPES buffer (pH 7.2) and
dehydrated with an ethanol series, the samples were
embedded in Epon 812 resin. The specimens were
sectioned with a diamond knife, and the thick sections
(5 µm)were stained with 0.1% toluidine blue and examined
under light microscopy (Leica DMLB).The ultra-thin
sections (about 100 nm) were stained with 1% (w/v) uranyl
acetate (aqueous) and 1.5% (w/v) alkaline lead citrate
(aqueous) and examined with a Hitachi 7650 TEM.
Light microscopy
Freehand cross sections were cut from fresh rosette shoot
apexes and put in a glass plate with distilled water. The
thinner sections (about 70 µm thick) were selected and
examined under a light microscopy (Leica DMLB).
Isolation of crystal protoplasts
Isolation of crystal protoplasts was according to the method
described by Franceschi et al. (1993).Water hyacinth rosette
shoot apexes were cut into small blocks (6∼8 mm3) and
homogenized in four volumes of water. The homogenate
was filtered with 200- and then 70-µm nylon nets and
Development of secretory cells and crystal cells in Eichhornia crassipes ramet shoot apex
rinsed with distilled water twice, and then the isolated
crystal protoplasts were collected and examined under light
microcopy (Leica DMLB).
network structure (Fig. 5d). Finally, after the SSVs were
exhausted, the cells lost the ability of secretion.
Development of crystal cells in water hyacinth apexes
Results
Development of secretory cells in water hyacinth
shoot apexes
Water hyacinth produces long stolons with rooted rosettes
(ramets) at their nodes. Each rosette shoot has leaves at the
apex and adventitious roots at the node end (Fig. 1a, b).
Serial sections through a rosette shoot apex showed three
distinguished tissues including epidermis, cortex, and
vascular cylinder. A number of vascular bundles were
distributed in the parenchyma tissue of the vascular
cylinder (Fig. 1b, c). The tissues in the rosette shoot apical
area displayed a glorious pink color (Fig. 1b), which was
due to a lot of pink secretory cells dotted among the
parenchymal tissue in vascular cylinder (Fig. 1d–f). The
distribution density of secretory cells apparently decreased
at rooted end of the shoot (Fig. 1b). The secretory cells in
shoot apical tissues displayed a heavy staining black color
in glutaraldehyde-osmium fixed sections and were distributed around vascular bundles (Fig. 2a, b), corresponding to
the observation of secretory cells in the fresh sections
(Fig. 1d–f). In addition, most of secretory cells were
adjacent to xylem cells of vascular bundles (Fig. 2c) or
crystal cells (Fig. 2d), which we will discuss later.
The results from the electron microscopy showed that a
large number of electron-dense vesicles formed in the
cytoplasm of developing secretory cells (Fig. 3a, b). These
dense vesicles then fused to tonoplast (Fig. 3c) and
deposited the storage materials into the vacuole, where a
large number of electron-dense droplets were presented
(Fig. 3d). As development of the cells, these dark droplets
gradually filled the vacuole (Fig. 3e) and merged together
to form a huge secretion storage vacuole (SSV), which
occupied almost the whole cell (Fig. 3f). At this stage, a lot
of mitochondria in the cytoplasm (Fig. 4a) and many small
globoids containing heavy staining electron-dense substances in the vacuole matrix were observed (Fig. 4b). Several
electron-dense areas appeared at the periphery of the SSV
and the degradation began at those areas (Fig. 4b) with an
ill-defined autophagic process (Fig. 4c, d), where the
electron-dense vesicles were released to cytoplasm
(Figs. 4d and 5a). In the same time, the breakdown contents
in a limited region of globoids led to form a large number
of small electron-transparent holes in the SSV matrix
(Fig. 5b, c).The volume of these holes increased with
secretory cell senescence, and the materials remaining in
the spent matrix of the SSV consisted of an electron-dense
Figure 6a showed that there were a large number of crystal
cells in the water hyacinth apical tissues. The distribution
pattern of crystal cells is similar to that of the secretory
cells, which we have described above (Fig. 1d). Both
crystal and secretory cells occur in high frequency in the
parenchyma tissue around vascular bundles in the vascular
cylinder of the rosette shoot (Fig. 2a, b). The crystal cells
are apparently larger than its neighboring parenchyma cells
and secretory cells (Fig. 6b). The morphology of crystals
detected in isolated protoplasts of water hyacinth apexes is
raphide bundles (Fig. 6c) or block-like rhombohedra
(Fig. 6d). Most of crystals in the cells of this tissue were
raphide bundles, while few of them were block-like
rhombohedra (Fig. 6d).
Crystals appeared first in one site of the central vacuole
(Fig. 7a, d) and then increased by adding new growing
crystals at the peripheral region of the crystal forming area
(Fig. 7b, e). As the crystal cell developed into the mature
stage, the number of crystals in the vacuole extremely
increased and finally filled the whole vacuole (Fig. 7c, f).
When the developing crystal cells were examined under
transmission electron microscopy, a large amount of ER
surrounded by vesicles throughout cytoplasm (Fig. 8a) and
many tube-like structures, measuring 8–10 nm in diameter,
in the matrix of the vacuole were observed (Figs. 8b, c and
9a, b). These tube-like structures might function as
chambers of crystals (Fig. 8c). The volume of the small
tube-like structure obviously increased when the crystal
were initiated in its lumen (Fig. 8d, e). The chamber grew
as the crystal grew in bidirectional manner and the shape of
chamber changed from oval at the beginning (Fig. 8e, f) to
rhombic at the mature stage (Fig. 8g, h). The size of a
mature crystal cell is usually three to four times larger in
length than that of parenchyma cells or secretory cells
around it (Fig. 7c).
Discussion
The growth rate of water hyacinth seems to exceed that of
any other aquatic or cultivated plant because its shoot has a
strong ability to produce new clonal plants (Gopal 1987). In
addition, it can tolerate relatively large amounts of toxic
substances, such as heavy metals in aqueous environment.
A detailed investigation of the water hyacinth shoot apex
development is needed to fully elucidate its abilities of
rapid reproduction and toxic substance tolerance. The
experiments in this study have focused on the development
G.X. Xu et al.
Fig. 1 Developmental anatomy of water hyacinth shoot and the
distribution patterns of secretory cells in a shoot apex. a A stolon bud.
b A longitudinal section through the shoot apex of a stolon bud. Note
the apical area in pink color (arrow points). c A cross section through
the shoot apex. d–f Optical micrographs of freehand sections through
Fig. 2 Optical micrographs of
sections through glutaraldehydeosmium fixed water hyacinth
shoot apexes. a Longitudinal
section through the shoot apex.
b Cross section through the
shoot apex. c The secretory cell
adjacent to a crystal cell. d The
secretory cell adjacent to a xylem cell. SC secretory cell, Cr
crystal cell, X xylem cell. Bars
50 µm in a, b; 20 µm in c, d
the shoot apex. e, f Enlarged view of the shoot apical tissues. SH
shoot, AR adventitious root, SS stolon shoot, SC secretory cell, Cr
crystal cells, Ep epidermis, Co cortex, Vc vascular cylinder, Vb
vascular bundle. Bars 5 mm in a; 2 mm in b, c; 0.1 mm in d; 0.05 mm
in e, f
Development of secretory cells and crystal cells in Eichhornia crassipes ramet shoot apex
Fig. 3 Electron and optical micrographs of developing secretory cells
in water hyacinth shoot apex. a Developing secretory cell with several
dark droplets in the vacuole. b An analogous autophagic process
appeared in the cytoplasm during secretory vesicle formation.
Substances with high electron density surrounded tonoplast and
secretory vesicle. c A secretory vesicle is fusing with the vacuole. d
Early stage of the developing secretory cell with a number of dense
droplets in the vacuole. e Dark droplets with dense secretory
substances fill the vacuole. f Dark droplets fused together and formed
a secretion storage vacuole. V vacuole, SV secretory vesicle, DP
droplet, AV autophagic vesicle, SER smooth endoplasmic reticulum, N
nucleus. Bars 5 µm in a, 500 nm in b, 200 nm in c, 10 µm in d–f
of secretory cells and crystal cells, which may play an
important role in promoting the growth rate and stress
tolerance of the water hyacinth.
Secretory cells widely exist in plant tissues and organs,
such as root, shoot, leaf, flower, and fruit. The functions of
secretory cells are various in different organs and species
(Dell and McComb 1978; Paiva et al. 2008; Paiva 2009).
The gland or epidermal hairs that consisted of secretory
cells were often observed in the apical meristem tissue of
young shoot and the epidermal tissues of leaves (Klein et
al. 2004; Mastroberti and Mariath 2008). According to the
observation in this study on the abundance of secretory
cells in water hyacinth shoot apex and the previous reports
on the rapid vegetative reproduction of this tissue, we
assume that secretory cells in the shoot apex might function
as a storage compartment to store and transfer nutrient
elements to meristem cells in vigorous growth stage.
The autophagic procedure has been interpreted as
catabolic activity, which was regarded as a step in the
destruction of specific metabolic machinery leading to the
establishment of a new one (Kupila-Ahvenniemi et al.
1978). Krasowski and Owens (1990) considered that the
autophagy resulted from nutrient deficiency caused by lack
of photosynthesis in apical meristematic cells of coastal
Douglas fir during embryonic shoot development. Vacuolar
autophagy in plant cells have been widely found in
different tissues, such as developing seeds, old, and disease
stressed leaves (Bassham et al. 2006), but detailed research
on autophagic procedure in the formation of secretory cells
has not been reported. In the present study, the autophagic
procedure appeared in the vacuoles, where reserve substance began to be degraded. Thus, autophagic effect might
play an important role in the transformation of secretory
cells from the storage stage into the active secretion stage.
A heavy deposit of crystalline material, which was
identified as CaOx, has been found in the water hyacinth
leaves in a previous study (Mazen and Maghraby 1997).
Results of our research show a dense distribution of crystal
G.X. Xu et al.
Fig. 4 An ill-defined autophagic process appeared in secretory cells during the degradation
of storage substances in the
vacuole. a A secretory cell with
dense matrix in the vacuole and
a lot of mitochondria in cytoplasm. b Degradation in the
vacuole begins with erosion at
the periphery and globoids in
the matrix. c An intermediate
secretory cell. d Enlarged view
of the collapsed matrix in the
peripheral area of vacuole. V
vacuole, GL globoid, M mitochondria, W cell wall, SV secretory vesicle, AV autophagic
vesicle. Bars 500 nm in a, b,
and d; 2 µm in c
Fig. 5 Degradation processes of
storage substances in the vacuole of a secretory cell. a High
magnification electron micrograph of secretory vesicles in the
cytoplasm and globoids in the
vacuole matrix. b Globoids
appear in the heavy staining
vacuole matrix. Note that the
degradation is limited in a
certain region of the globoids.
c A secretory cell at the active
degradation stage. d A secretory
cell at the late degradation stage.
V vacuole, SV secretory vesicle,
M mitochondria. Bars 1 µm in
a, b; 5 µm in c, d
Development of secretory cells and crystal cells in Eichhornia crassipes ramet shoot apex
Fig. 6 Crystal cells in water
hyacinth shoot apex. a, b Optical micrographs of cross sections through a fresh shoot apex
show distribution of crystal cells
in the tissues. c Isolated crystal
protoplasts with raphide-bundle
crystals. d Isolated crystal
protoplasts with block-like
rhombohedral crystals. Cr
crystal, X xylem. Bars 100 µm
in a, b; 50 µm in c, d
cells in the rosette shoot apexes. The objective of this study
was to investigate the metamorphosis of vacuole during the
process of crystal formation. Tube-like structures, which
might serve as crystal chambers and determine crystal
morphology in the cells, have been found in the complex
crystal vacuole systems in developing crystal cells of water
hyacinth shoot apexes. Similarly, formation of crystals in
chambers has been observed in plastids (Li and Franceschi
Fig. 7 Optical and electron micrographs of developing crystal cells in
water hyacinth shoot apex. a–c Phase contrast image of longitudinal
sections through developing raphide crystal cells. d–f Electron
micrographs of cross sections through developing raphide crystal
cells. Note that short needle-shaped crystals appear in crystal cell
vacuole (a, d), then elongate (b), and finally occupy the whole cell (c,
f). Cr crystal, V vacuole, N nucleus. Bars 10 µm in a; 20 µm in b, c;
5 µm in d, f; 1 µm in e
G.X. Xu et al.
Fig. 8 Ultrastructural images of
crystal formation in the vacuole.
a The interface between vacuole
and cytoplasm in a developing
crystal cell. b A group of growing crystals in vacuole. c Tubelike structure in vacuole. d A
crystal chamber develops from
tube-like structure. e–g Crystals
are growing in the chambers.
h Mature crystals. ER endoplasmic reticulum, M mitochondria,
VC secretory vesicle, DV dense
vesicle, Cr crystal, V vacuole,
TU tube-like structure, iCr
initial crystal chamber. Bars
500 nm in a, b, and h; 100 nm
in e–g; 20 nm in c, d
1990) and vacuoles (Horner and Whitmoyer 1972;
Kostman and Franceschi 2000) in other plants, but the
actual role of these tubules in crystal formation requires
further research. It has been suggested that the tubules were
involved in material transportation from the cytoplasm to
the crystal formation site in the vacuole (Frank and Jensen
1970). The tubules had also been considered directing both
the orientation of the developing crystal chambers and the
Fig. 9 High magnification of ultrastructure of the developing crystal
cells. a The interface between vacuole and cytoplasm of a primary
crystal cell. Note abundance of ER in the cytoplasm and tube-like
structures in the matrix of vacuole. b A number of tube-like structures
in various orientations are visible in the crystal formation region of the
vacuole. ER endoplasmic reticulum, VC secretory vesicle, V vacuole,
TU tube structure, iCr initial crystal chamber, Cr crystal. Bars 100 nm
Development of secretory cells and crystal cells in Eichhornia crassipes ramet shoot apex
movement of the various vacuolar structures (Horner and
Whitmoyer 1972). Results of ultrastructural study in the
present research showed that crystals formed in the lumen
of the tubules, which might act as the chambers of crystals.
CaOx crystals may be involved in the detoxification of
toxic heavy metals such as lead, cadmium (Cd), and copper
(Mazen and Maghraby 1997; Franceschi and Nakata 2005).
Different tissues of water hyacinth plant have different
abilities in accumulating heavy metals when it was grown
in the medium with different concentrations of metals
(Mazen and Maghraby 1997). To test if the abundance of
crystal cells in water hyacinth shoot apexes is related to
the heavy metal tolerance, the amount of crystal cells in
shoot apexes of plants grown on the medium containing
different concentrations of Cd was investigated. Figure S1
shows that there is almost no Cd to be transported to the
shoots and leaves, and most of Cd retains in roots under
low concentration Cd (less than 10 mg/L) conditions, but
content of Cd apparently increased in shoot apexes and
leaves under higher concentration Cd (more than 10 mg/L)
conditions. In contrast, the amount of crystal cells did not
significantly change in shoot apexes under both low and
high concentration Cd conditions (Fig. 2S A and B). In
addition, Cd, even at high concentration, could not induce
the formation of crystal cells under conditions of Ca
deficiency (Fig. 2S C). Thus, the mechanism of heavy
metal tolerance in water hyacinth might not depend on
increasing the amount of crystals in shoot apical tissues,
but involve the sequestration of hazardous metals in the
existing CaOx crystal cells as described by previous
studies (Mazen and Maghraby 1997; Franceschi and
Nakata 2005).
In summary, the formation of both crystal cells and
secretory cells in water hyacinth shoot apexes are involved
in the metamorphosis of vacuoles. However, the relationships between these two kinds of cells in the rapid growth
and the pollutant tolerance of water hyacinth and whether
ion channels or transporters in tonoplast are involved in
regulating the formation of these special cells are still
obscure. Further work is being carried out to clarify these
points.
Acknowledgment This work was supported by the Shanghai
Science and Technology Committee (072312031).
Conflict of interest The authors declare that they have no conflict of
interest.
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