Plant Physiol, December 2001, Vol. 127, pp. 1339-1345
SCIENTIFIC CORRESPONDENCE
Exploring Bioinorganic Pattern Formation in Diatoms. A Story
of Polarized Trafficking
Chiara
Zurzolo and
Chris
Bowler*
Dipartimento di Biologia e Patologia Cellulare e Molecolare,
Università Federico II di Napoli, Naples, Italy (C.Z.); and
Laboratory of Molecular Plant Biology, Stazione Zoologica "Anton
Dohrn," Villa Comunale, I-80121 Naples, Italy (C.B.)
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INTRODUCTION |
The world's oceans cover 70% of the surface of our
planet. The photosynthetic organisms living within
its photic zone are responsible for about
one-half of global primary productivity. The most successful organisms
are thought to be photosynthetic prokaryotes (cyanobacteria and
prochlorophytes) and a class of eukaryotic unicellular algae known as
diatoms (Norton et al., 1996
; Van Den Hoek et al., 1997; Falkowski et
al., 1998).
Diatoms are likely to have arisen around 280 million years ago
following an endosymbiotic event between a red eukaryotic alga and a
heterotrophic flagellate related to the Oomycetes (Medlin et al., 1997,
2000). As a consequence, their only phylogenetic similarity to green
algae and higher plants is derived from the primary endosymbiotic
event, which is thought to have occurred at least 700 million years ago
(Kowallik, 1992). Therefore, diatom cells have a range of features that
make them highly divergent from the classical cellular structure of
higher plants, including:
(a) The use of the brown carotenoid pigment fucoxanthin for light
energy transfer within the light-harvesting complexes of photosystems I
and II.
(b) The presence of four membranes around their plastids. The inner two
membranes are equivalent to the membranes that normally surround higher
plant chloroplasts, whereas the second membrane (as counted from the
outside) is thought to be derived from the endosymbiont's plasma
membrane, and the outer membrane is continuous with the endoplasmatic
reticulum of the host cell.
(c) The presence of a rigid cell wall composed largely of amorphous
silica (i.e. glass). The exquisite lacework-like patterning of diatom
cell walls (see example in Fig. 1) is
reproduced with high fidelity from generation to generation and is
species specific. For these reasons, it has been used since the last
century for taxonomic classification.
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Figure 1.
Electron micrograph of the diatom
Campylodiscus sp. at 890× magnification. Photograph
courtesy of Masahiko Idei.
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Current phylogenetic trees place diatoms close to Alveolata lineages
and far from the green and red lineages of other photosynthetic eukaryotes (Baldauf et al., 2000). This has been further confirmed by the analysis of diatom expressed sequence tags (ESTs), although more similarity than expected was found with Metazoan genes (S. Scala,
N. Carels, A. Falciatore, M.L. Chiusano, and C. Bowler, unpublished
data). The EST program has revealed the presence of genes encoding
enzymes involved in cAMP metabolism, as well as genes encoding the
components of the animal extracellular matrix, such as fibronectins,
elastins, and tenascins, none of which appear to be present in higher
plants. As a consequence, one could almost consider diatoms as
photosynthetic animals rather than unicellular plants!
The study of diatom biology therefore promises to reveal many novel
aspects (Scala and Bowler, 2001), and now that so much information has
been generated about the "conventional" metabolism of model
organisms such as yeast (Saccharomyces cerevisiae),
Caenorhabditis elegans, mouse (Mus
musculus), and Arabidopsis, it is possible to divert some
attention to more recalcitrant experimental systems. Given the
extreme ecological importance of diatoms, they should come close to the
top of the list of priorities for plant biologists, and could become
the system of choice for studying phytoplankton interactions with the
marine environment. The range of molecular-level technologies that have
now been established, such as genetic transformation (Dunahay et al.,
1995; Apt et al., 1997; Falciatore et al., 1999; Fischer et al., 1999),
protocols to study gene expression (Leblanc et al., 1999), and the
availability of several reporter genes (Falciatore et al., 1999;
Zaslavskaia et al., 2000) make them all the more attractive.
It is not surprising that the study of silica cell wall biogenesis has
been a major focus of diatom research for the last 150 years. However,
most information is descriptive, being based on microscopic
observations, and only recently have biochemical and molecular
techniques been incorporated, due largely to the pioneering work of
Nils Kröger and colleagues (for review, see Kröger and
Sumper, (1998)). The current review aims to summarize the basic aspects
of the silica biomineralization process and to indicate the major gaps
in current understanding that can now be addressed using knowledge and
tools derived from better studied organisms.
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SILICA AND THE DIATOM CELL CYCLE |
Diatoms lie within the Heterokont division of the class
Bacillariophyceae (also known as Stramenopiles). They usually exist as
single cells of between 5 µm and 5 mm, depending on the species, although some can form chains or colonies (Van Den Hoek et al., 1997;
Lee, 1999). Each cell is surrounded by a unique type of cell wall
(known as frustule) which consists of two halves of amorphous
polymerized silica resembling a box with an overlapping lid (Fig.
2). The inner frustule is known as the
hypotheca and the outer one is denoted the epitheca. In addition to the
main valves (hypovalve and epivalve), each frustule often contains several ring-like silica structures denoted girdle bands (Fig. 2).
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Figure 2.
Schematic overview of the siliceous components of
diatom cell walls. Drawing by Ian Nettleton.
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There are two major diatom groups: the centric and the pennate diatoms.
These can be most simply distinguished from each other on the basis of
cellular symmetry: Centric diatoms are radially symmetrical (resembling
a petri dish), whereas pennate diatoms are elongated and bilaterally symmetrical.
Diatom cell division typically proceeds through asexual mitotic
divisions. However, because the rigid siliceous cell walls largely
preclude cell growth through expansion (except unilaterally by the
addition of new girdle bands), the two daughter cells must be formed
inside the parent cell (Fig. 3;
Pickett-Heaps et al., 1984, 1990; Van Den Hoek et al., 1997). One
sibling cell uses the epitheca of the parent cell as a size guide to
generate a new hypotheca, whereas the other uses the parental
hypotheca, which therefore becomes the epitheca of the daughter cell
(Fig. 3). As a consequence, mitotically dividing populations decrease in mean size over time. In most species, size restoration occurs through sexual reproduction once a critical size threshold (typically 30%-40% of the maximum size) has been reached (Mann, 1993; Van Den
Hoek et al., 1997).
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Figure 3.
Schematic overview of mitotic cell division and
hypovalve and girdle band formation. For further details see text. N,
Nucleus; MC, microtubule center; SDV, silica deposition vesicle.
Drawing by Ian Nettleton.
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The strict requirement for silica in frustule formation has led to the
evolution of silica-dependent checkpoints in diatom mitosis, which
presumably ensure that cell division does not occur unless there are
sufficient bio-available silica for frustule formation. Checkpoints
have been found to occur in diatoms at both the G1/S and G2/M
transitions (Brzezinski et al., 1990; Martin-Jezequel et al., 2000) and
it has been speculated that diatom DNA polymerases may be silica
dependent. This has not yet been confirmed at the molecular level.
It is known that diatoms possess silica uptake transporters that
are able to accumulate silica at intracellular concentrations up to 250 times higher than in the surrounding media (Martin-Jezequel et al.,
2000). Where it is localized intracellularly is still open to debate
(see "Transport to the SDV"). These transporters have novel
primary structures, and by expression in Xenopus
laevis oocytes it has been found that they are highly
selective for the soluble form of silica, Si(OH)4
(Hildebrand et al., 1997, 1998). Homologous sequences do not exist in
the Arabidopsis genome, although it is possible that they will be found
in rice, which is known to have silicified hairs (Raven, 1983).
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FORMATION OF A NEW FRUSTULE |
Following mitosis, two daughter cells form inside the parent cell,
one of them bound by the parent epitheca on one side and the other
bound by the hypotheca on the other side (Fig. 3). Each daughter cell
must then synthesize a hypotheca ex novo before they can separate. This
process has been observed extensively in numerous diatom species at the
ultrastructural level, such that a rather complete description of the
process is now available (Pickett-Heaps et al., 1990). The key events
are shown in Figure 3 and can be summarized as follows:
(a) The nucleus of each daughter cell moves to the side of the cell
where the hypotheca will be formed.
(b) A microtubule center (MC) positions itself between the nucleus and
the plasma membrane above which the hypotheca will eventually be placed.
(c) A specialized vesicle known as the silica deposition vesicle (SDV)
forms between the MC and the plasma membrane in a region that becomes
the "pattern center."
(d) The SDV elongates into a tube and then spreads out perpendicularly
to eventually form a huge vesicle along one side of the cell.
(e) A new valve is formed within the SDV by the targeted transport of
silica, proteins, and polysaccharides. During this process, the SDV
becomes acidic as a result of the silica polymerization process
(Vrieling et al., 1999). Some of the organic components eventually
form a coat around the silica framework, whereas others are involved in
silica deposition.
(f) Once valve biogenesis is complete, it is exocytosed
by fusion of the SDV membrane (the silicalemma) with the plasma
membrane. As a consequence, the inner face of the silicalemma is
thought to become the new plasma membrane.
(g) Following separation, the daughter cells can expand
unidirectionally along the cell division axis by the biogenesis of girdle bands. These structures are also formed within SDVs in a manner
analogous to that described above.
These events are very similar in both pennate and centric diatoms,
although the timing can be different (Pickett-Heaps et al., 1990; Van
Den Hoek et al., 1997). Very little is known about the underlying
mechanisms controlling these events. Most intriguing is how such
intricate structures can be generated from a shapeless inorganic
substrate. Although it has been proposed that much of the early
biomineralization process can proceed via physico-chemical space
filling of silica (Gordon and Drum, 1994), this is certainly not
sufficient to explain the exquisite species-specific designs that are
ultimately generated. The fact that frustule design is faithfully
reproduced from parent to daughter cells indicates that there is a
significant genetic basis underlying bioinorganic pattern formation.
One strategy that appears to be important in pattern formation is known
as macromorphogenesis, whereby silica deposition is "molded" into a
pattern by the presence of organelles such as mitochondria spaced at
regular intervals along the cytoplasmic side of the SDV (Schmid, 1994).
Therefore, these organelles are thought to physically restrict the
targeting of silica from the cytoplasm, to ensure the laying down of a
correctly patterned structure (for models, see Schmid, 1994).
The importance of macromorphogenesis will only be clear when it is
known how silica and silica-associated proteins and polysaccharides are
deposited into the SDV. This is thought to occur, at least partially,
by their transport to the SDV in vesicles, which is described as
membrane-mediated morphogenesis (Pickett-Heaps et al., 1990).
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ORGANIC COMPONENTS OF DIATOM CELL WALLS |
Much of the biochemical studies of frustule composition have been
done in the pennate diatom Cylindrotheca fusiformis
(Kröger and Sumper, 1998). This work has led to the discovery of
novel peptides known as silaffins that may participate in the basic biomineralization process within the SDV (Kröger et al., 1999). These cationic peptides of various sizes are generated from precursor polypeptides and are characterized by the presence of Lys-Lys repeat
elements that are covalently modified by the posttranslational addition
of novel chemical units, such as oligo-N-methyl propylamines (Kröger et al., 2001). It is interesting that silaffins can
promote the formation of nanoscale silica spheres in vitro
(Kröger et al., 1999).
Other major organic constituents of diatom biosilica are
putrescine-derived long-chain polyamines. Like the silaffins, these can
also induce rapid silica precipitation in vitro (Kröger et al.,
2000), forming spheres between 100 nm and 1 µm depending on the
polyamine used. Different diatoms have different complements of
silaffins and frustulins, which confer species-specific differences to
in vitro silica precipitation. It is remarkable that some of these
combinations generate silica blocks in addition to silica spheres. This
observation infers that silaffins and polyamines therefore may be
involved in generating the basic building blocks that are then modeled
into diatom frustules, and that combinatorial interactions between them
may be responsible for the underlying genetic basis of species-specific
pattern formation. However, the fact that they are both bound tightly
to the silica scaffold of diatom cell walls begs the question: "How
did they get there?" If they are bound to a preformed silica
framework, then how was it formed? On the other hand, if silaffins and
polyamines are responsible for silica pattern formation, how are they
themselves directed into a network that determines the final pattern?
To find out, it is necessary to understand the mechanisms underlying the targeting of silaffins, polyamines, and silica to the SDV.
Other proteinaceous components of diatom cell walls include frustulins
and pleuralins (formerly denoted HEP proteins; Kröger et al.,
1997; Kröger and Wetherbee, 2000). Like the silaffins, pleuralins
are also tightly bound to silica and can only be removed from diatom
cell walls following the solubilization of silica with hydrogen
fluoride. Pleuralins are encoded by a small multigene family and are
characterized by the presence of repeated amino acid motifs. It is
interesting that the localization of one of them, pleuralin-1, is
precisely restricted to the most terminal girdle band (known as the
pleural band) of the epitheca (Fig. 2), in the region of overlap with
the hypotheca. During cell division it also becomes associated with the
pleural band of the hypotheca, at a time when the parental hypotheca is
functionally converted into an epitheca of one of the daughter cells
(see Fig. 3; Kröger and Wetherbee, 2000). This is a very
significant observation, because it demonstrates that
hypotheca-epitheca differentiation is under strict developmental control.
Pleuralin-1 is not targeted to the SDV but is directly secreted into
the cleavage furrow that forms between the two daughter cells
(Kröger and Wetherbee, 2000). Association with the terminal girdle band of the hypotheca therefore occurs in the extracellular space. Secretion is thought to occur by general mechanisms of exocytosis, but it is nonetheless an intriguing example of polarized transport specifically toward the cleavage furrow. It will be interesting to determine how many other wall-associated proteins avoid
the SDV during their secretion and incorporation into diatom frustules.
Frustulins are much more loosely associated with diatom cell walls than
are silaffins and pleuralins, and can be extracted with EDTA. To date,
five different frustulins have been described, all of which are
glycoproteins able to bind calcium due to the presence of EF hands
(Kröger et al., 1994). They also contain characteristic acidic
Cys-rich domains, the function of which is not yet known. Frustulins
are not thought to be involved in silica deposition, but constitute the
outermost protein coat of the cell wall (van de Poll et al.,
1999).
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TRANSPORT TO THE SDV |
Both the silaffins and the frustulins must be targeted to the
SDVs. Because the SDV is such an unusual but fundamental structure for
the diatom cell, understanding its biogenesis and dissecting the
targeting mechanisms for silica and protein import are of major
biological interest. Furthermore, because the frustule is formed on
only one-half of the cell, it is a dramatic example of cell polarity.
Silaffins, frustulins, and pleuralins are all synthesized as precursor
proteins containing amino-terminal presequences that resemble typical
signal sequences for the co-translational import of proteins into the
endoplasmatic reticulum. Other unidentified sequences are likely to be
present within the silaffin and frustulin precursors that target them
from the Golgi apparatus to the SDV. The silaffin precursor is cleaved
into specific peptides that are found associated with silica in the
frustule (Kröger et al., 1999). Therefore, it is conceivable that
this maturation event occurs in a post-Golgi compartment (e.g. within
the transport vesicles or in the SDV itself after specific targeting of
the precursor protein to the SDV).
Bearing in mind the above considerations, it seems likely that the
Golgi apparatus is connected to the SDV via transport vesicles. Such a
system would also provide a convenient and economical means for
silicalemma expansion. Although clouds of vesicles emanating from the
Golgi have often been observed during cell wall deposition (Pickett-Heaps et al., 1990), vesicle fusion to the SDV has not been
clearly established. However, because many specific mechanisms of
vesicle targeting to organelles have been studied intensively in other
eukaryotes, parallels can be easily searched for. One approach would be
to look for the presence of specific protein pairs such as V-SNARE and
T-SNARE, which are known to mediate vesicle docking (Chen and Scheller,
2001; Pelham, 2001). Furthermore, the use of drugs such as brefeldin A,
which blocks forward vesicle trafficking from the Golgi apparatus
(Lippincott-Schwartz, 1983; Pelham, 1991), could clarify the role of
Golgi vesicles in SDV formation.
We envisage two possible mechanisms of vesicle targeting from the Golgi
apparatus to the SDV. Analysis of the silaffin and frustulin sequences
reveals stretches of amino acids highly enriched in acidic residues,
which is also typical of granins, secretory proteins that accumulate in
post-trans-Golgi network (TGN) secretory granules in
neuroendocrine cells (Huttner et al., 1991). Therefore, these
SDV-targeted proteins could follow a pathway similar to regulated
secretion occurring at the plasma membrane of specialized secretory
cells (Miller and Moore, 1990; Tooze, 1998). In this case, peptides
would accumulate in the Golgi-derived vesicles by a process requiring
protein aggregation, due to acidic and Pro-rich amino acid sequences
(Benedum et al., 1987; Castle et al., 1992; Rindler, 1998), and would
then be targeted to the SDV in response to a specific signal in a
manner analogous to the regulated secretory pathway of mammalian cells.
A report of small vesicles surrounding the nascent SDV, but not yet
fusing (Li and Volcani, 1985), might support this model.
Another possibility would be a mechanism similar to the Man 6-phosphate
receptor-mediated pathway that hydrolytic enzymes follow from the TGN
to the lysosomes (von Figura, 1991). In this case, a transmembrane
receptor protein should be present in the TGN, where it would bind to
signals within the SDV-targeted proteins separating them from other
proteins in the lumen and concentrating them in coated vesicles that
would then be specifically targeted to the silicalemma. The fact that
some Golgi-derived vesicles in diatoms seem to possess a coat (Gordon
and Drum, 1994) could support this hypothesis.
Conversely, how silica is targeted to the SDV is also a mystery. In
principle, it could follow the same route followed for cell
wall-associated proteins or could be targeted independently. It is not
known if it is already complexed with organic molecules during its
transport through the cell or even whether it is sequestered into
vesicles. The existence of silica transport vesicles has been proposed
(Schmid and Schulz, 1979), although evidence is poor. What is clear is
that if silica was already precipitated inside targeting vesicles, it
would have been observed in electron micrographs. The fact that it has
not (Pickett-Heaps et al., 1990; Martin-Jezequel et al., 2000)
indicates that silica is only likely to encounter silaffins and
polyamines once inside the SDV. Furthermore, if silica is packaged into
vesicles, it must first be targeted into them. There is no evidence
that this happens. Although both silica transporters and ionophores
have been identified in diatoms (Bhattacharya and Volcani, 1983;
Martin-Jezequel et al., 2000) it is not known whether they are
localized on vesicles inside the cell. Furthermore, it is not clear why
a specific vesicle transport mechanism should be needed to transport
silica to the SDV because the presence of silica transporters on the
silicalemma could be sufficient. The availability of antibodies against
the silica transporters would make it possible to determine whether they are present on the silicalemma as well as on the plasma membrane. This is one of the most urgent questions that requires an answer.
If silica transporters are present on the silicalemma, they could be
targeted to it by endocytic vesicles derived from the plasma membrane.
This process would both increase the size of the SDV and create the
conditions for concentrating silica within this organelle. Fusion of
Golgi-derived vesicles carrying silaffins and polyamines with the SDV
would then initiate the process of silica deposition.
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SDV FORMATION |
Based on the above considerations, it is possible that the SDV has
an endocytic origin similar to the early endosomal compartment present
in mammalian cells (Woodman, 2000). The initial formation of this
organelle could be strictly linked (or driven) by the positioning
of the MC between the nucleus and the plasma membrane immediately after
cytokinesis. The fact that microtubule depolymerization affects valve
formation supports a role for microtubules in SDV formation (see
Pickett-Heaps et al., 1990, and refs. therein).
The observation that the acidity of the SDV increases with silica
deposition (Vrieling et al., 1999) can be paralleled with the
maturation hypothesis of mammalian cells, which postulates that late
endosomes/lysosomes derive from maturation of early endosomes (Mullins
and Bonifacino, 2001). The identification of markers specific for early
and late endosomes and lysosomes (e.g. Rab5, Rab7, and Rab9,
respectively; Zerial and McBride, 2001) on the silicalemma therefore
could provide some clues to the origin of the SDV.
An additional, albeit speculative, connection between silica
polymerization and lysosomes comes from the recent finding that a
lysosomal cathepsin L-like hydrolase is the major silica
binding protein within the silica-rich spicules of sponges (Shimizu et al., 1998).
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EXOCYTOSIS |
The final stage of the valve formation process is exocytosis of
the SDV. There are at least four models for how this could occur
(Pickett-Heaps et al., 1990; van de Poll et al., 1999). It is most
likely that the SDV fuses at specific sites, perhaps the valve edge. To
drive fusion at specific sites, landmarks for vesicle docking must be
present. Furthermore, timing must be precise. In the case of mammalian
and plant cells, specific vesicle fusion is driven by the pairing of V-
and T-SNAREs (Chen and Scheller, 2001; Pelham, 2001). However,
additional factors define cognate fusion and docking sites. One example
is represented by the exocyst in yeast, a multiprotein complex involved
in vesicle targeting and docking at the plasma membrane (TerBush et
al., 1996). The exocyst is specifically localized to sites of active
exocytosis and its proper localization is thought to be important for
spatial regulation of secretion in yeast and mammalian cells (TerBush et al., 1996; Zahraoui et al., 2000). It has been found recently that
the small GTP-binding protein Rho1 is involved in regulation of exocyst
localization at the plasma membrane (Guo et al., 2001). It would be
interesting to analyze whether a similar multiprotein complex exists at
specific sites of the SDV or plasma membranes of diatoms.
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FUTURE PROSPECTS |
There is clearly a great need for the development of
pharmacological, biochemical, molecular, and genetic tools to address the novel aspects of diatom frustule biogenesis such as SDV formation, targeting to the SDV, silica biomineralization, bioinorganic pattern formation, and exocytosis. A major bottleneck has been the inability to
purify the SDV. However, a technique for fluorescently labeling the SDV
in vivo has been described using rhodamine 123, which binds silica and
which fluoresces brightly at the acidic pH of the SDV (Li et al., 1989;
Brzezinski and Conley, 1994). It is possible that such labeling
combined with modern fractionation techniques could be a useful
approach. Furthermore, the use of green fluorescent protein to
fluorescently tag SDV-destined proteins such as frustulins could reveal
the fundamental features of their intracellular transport, and could
reveal where different silica transporters are localized and whether
they are mobile during SDV formation and silica deposition.
Of major importance is the identification of other components
regulating SDV biogenesis, frustule formation, and exocytosis. One
extremely valuable approach is the random sequencing of expressed genes
to generate ESTs. Several thousand ESTs have been generated in the
pennate diatom Phaeodactylum tricornutum, and sequences encoding proteins homologous to a range of GTP-binding proteins such as
Rabs and Rhos have already been identified, as have COP coatomer
proteins, dynamin, cathespsins, and clathrin adaptor proteins (S. Scala, N. Carels, A. Falciatore, M.L. Chiusano, and C. Bowler,
unpublished data). Therefore, these provide important new substrates
for initiating molecular and cellular studies in diatoms.
The species-specific patterns of silica nanofabrication indicates that
there is a considerable genetic basis underlying pattern formation. The
isolation of pattern mutants will be an important approach to develop
insights into how this works. The two diatom species for which most
molecular tools have been developed, P. tricornutum and
C. fusiformis (Scala and Bowler, 2001), represent simple
experimental systems that can be used for such approaches.
The eventual elucidation of the mechanisms used by diatoms to transform
soluble silica into sturdy intricate structures at ambient temperatures
and pressures that way exceed current human capabilities could
eventually allow materials scientists to generate micrometer scale
silica structures for a whole range of nanotechnological applications
(Mann and Ozin, 1996; Morse, 1999; Parkinson and Gordon, 1999). This,
combined with the intrinsic scientific interest of understanding such a
process, makes diatom cell wall biogenesis an attractive research topic
that is in desperate need of intensive molecular and cellular-based studies.
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ACKNOWLEDGMENTS |
We would like to thank Angela Falciatore for critical reading of
the manuscript and Ian Nettleton for the illustrations. We apologize
that due to size restrictions it has not been possible to discuss all
the original work relating to diatom cell wall formation.
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FOOTNOTES |
Received August 10, 2001; returned for revision August 21, 2001; accepted August 27, 2001.
*
Corresponding author; e-mail chris{at}alpha.szn.it; fax
39-081-764-1355.
www.plantphysiol.org/cgi/doi/10.1104/pp.010709.
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INTRODUCTION
SILICA AND THE DIATOM...
