Download Cell division in the green microalga Marvania

231
Ada
801. Neerl. 36
November
(3-4),
231-245
1987, p.
division in the green
Cell
Marvania
geminata:
role of coated
autosporogenesis,
pit-microtubule
systematic
H.J.
1
2
1
Sluiman
Rijksherbarium,
Universite de
and
complexes,
significance
2
and O.L.
P.O. Box
Reymond
2300 RA
9514,
Institut
Lausanne,
microalga
semi-exogenous
Leiden,
The Netherlands.
d’Histologie et d’Embryologie, Rue
du
Bugnon 9,
CH-1005
Lausanne, Switzerland.
SUMMARY
Cell
division
electron
the cell
in
the unicellular
microscopy. Unlike
has
part of the
intact. The
expanded
appears
a coated
and in
at the
break
spindle
is not associated
site at the
before division is initiated.
pit-like
septum. Cells
original
the cell
cleavage
furrow.
after the
During mitosis
events, in
be
may
seem
is marked
grow
by
near
a
to be
wall
particular
considered
as
a
the
absent
along
escape
of
envelope remains
throughout
with
invaginates
the short
the cell
is broken
of
a
forms
a
at the
broadly
to form
microtubule,
furrowing mechanism,
member
not before
the
cortical microtubule which
daughter cell
layer
transmission
occurs
involves
the nuclear
short
with
mitosis
the microtubule
inward
common
studied
algae,
expansion
After furrowing, each
old,
It is concluded
geminata
Cell
centrioles, which
membrane
septum. A model explaining cytokinetic
that M.
volume.
The plasma membrane
separate
has been
geminata
wall.
The latter continues to
structure.
effect constitutes the
new
in
M.
in other coccoid green
cycle
with
plasma
alga
green
about twice its
protoplastthrough a
The division
cycle.
until
coccoid
the division
wall
level
layer
of the
is presented.
conceived
order
Chlorococcales.
1.
INTRODUCTION
features of the external
Light microscopical
zation of the
a
plant body (including
dominantrole in
tion of green
current
text
algae (example:
non-flagellated forms
are
its
book
Ettl
morphology
presentations
1980).
For
generally assigned
few will doubt that the order thus conceived is
not
be defined
held
by sharp,
those coccoid
Especially
together
due
which results in
trate
the
complexity
to
the
more
difficulty
what appears
The
to
be
of
a
unambiguous
green
persistence
or
forms and those with
to
to
the
continue
higher-level
unicellular and colonial
order
Chlorococcales,
artificial, heterogenous,
products
and
or
yet
can-
1983).
of cell division
of extra-cellular substances
discrete
play
to
classifica-
criteria (cf., Komarek & Fott
virtual continuum of
of how
of the
example,
in which the
less coherent tissue-
establishing
among the green
question
algae
and the cellular organi-
reproductive structures)
filament-like
complexes,
illus-
morphological categories (taxa)
increasing
are
(mucilage, walls)
levels of
in
morphological
algae.
distinguish
higher grades
between multicellular chlorococcalean
of organization
like filaments and tissue-like
232
H.
has led Bold and co-workers
complexes
systematic value of the patterns
This resulted in the
‘desmoschisis’,
include
to
to
be capable
cell
basic
two
division,
and
as
‘eleutheroschisis’,
well
critical
The
taxonomic
problematic
filamentous green
The
‘filament’
algae
The
spherical
assigned
to
summ-
and Ettl & Komarek 1982 for
a
the
special
in
to
occur
for that
cell
in
case
(Hindak
microalga
green
point
sense,
as
diad-forming
view,
Marvania geminata Hin-
that illustrates the
mentioned
problems
suggest
an
affinity
with chlorococ-
mode of cell division
only
1976; Heynig 1980; Reymond
in any member of the
Chlorococcales,
nor
involving
al.
et
in
any
can
should be
be
produced
classified,
at
led Hindak
least
(1976,
tentatively,
1978)
a
1986)
other
The fact that under certain conditions linear
matter.
complexes
geminata
the inabi-
more on
considered to be filamentous in Hindak’s
are
characteristic and
is
ment-like)
(e.g.,
cell division patterns.
specific
broad
a
truly
Hindak
the taxonomic delimitation of the order Chlorococcales. The
mechanism
alga,
of
occurrence
by
in the order Ulotrichales.
budding-like
known
Ulotrichales
primitive
of the Chlorococcales is based
obviously applied
was
algae, yet its
that M.
on
cell features of Marvania obviously
vegetative
green
be
a recent
natural link between Chlorococcales and
unicellularnon-motile
concerning
calean
1982,
of the so-called
position
a
concept
placed
dak 1976, presents
above
non-vegeta-
or
to
has been discussed in various papers
like Elakatothrix
and therefore are
not
as
form filaments than
term
green
algae)
His
1962,1978,1982).
to
algae.
discussion.)
(which might be regarded
lity
potential
and that those known
would have
separate order Chlorosarcinales (see Bold & Wynne 1985 for
ary, and Silva 1982, Tschermak-Woess
a
the
types of cell division exist, viz.
by eleutheroschisis,
desmoschisis
by
to
that the order Chlorococcales would be restricted
proposed
divide
to
that
that divide solely
algae
as
a
was
focus their attention
to
REYMOND
of cell division that occur in coccoid green
recognition
vegetative
or
tive division. It
J, SLUIMAN AND O. L.
(fila-
conclude
to
in the order Ulotri-
chales.
It
now seems
‘natural’
higher
ral and
al.
(1986),
a
features and
biochemical,
preliminary
et
doubt that for the establishment of
green
micro-algae,
taxonomic levels, it is essential
reproductive
cally
beyond
classification of
at
to
study
of M.
geminata
seemingly exotic
a more
stable and
intermediate and
morphological
markers,
both
was
undertaken
by
and
structu-
reason,
a
Reymond
method of cell division is basi-
Our present report examines the ultra-
autosporogenesis.
structural aspects of cell division in M.
2.
gross
search for novel taxonomic
who found that its
form of
de-emphasize
at
cellular and macromolecular levels. For this
ultrastructural
special
to
especially
geminata
in
more
detail.
MATERIALS AND METHODS
A strain of Marvania geminata
Bratislava, Czechoslovakia)
Hole MBL
medium
2 mM HEPES
Hindak, (nr.
was
following
grown
as a
Nichols
1978/21, isolated by
unialgal
(1973),
Dr. F.
Hindak,
culture in aerated Woods
with TR1S
being replaced by
(N-2-hydroxyethylpiperazine-N’-2-ethanesulfonic
acid)
at
16 °C
CELL DIVISION IN MAR VANIA
Fig. 1.
new
Marvania
(inner)
x51000.
wall
233
GEMINATA
geminata. Advanced
layers clearly
visible.
stage of cell
expansion prior
to cell
division,
with
C, chloroplast; G, Golgi body; M, mitochondrion;N,
old
and
nucleus,
234
H.
under
16 h
a
numbers of
the
at
light:
3500
cells
dividing
for 5
rpm
in
30- 50
noted
being
at
followed
followed
that the
by
during
that the
in agar
(galloyl glucose,
in medium. The
acidified
a
took
distilled
MW 1701.21,
electron
(Lausanne)
at
table
a
of the
using
centrifuge
(1 % glutaralde-
temperature for
room
cells in
pelleted
3
mm
taken
As
(3)
and 0.05%
blocks,
were
embedded in
using Philips
at room
warm
temperature
in method
(1), except
in medium, and that
in method
glutaraldehyde,
Polysciences)
in c. 8
cut
As
(2)
glutaraldehyde
of 0.2%
2,4-dimethoxypropane,
photographs
in
4 ml fixative
c.
highest
the sixth h of light)
samples
7.2)
water.
Reichert Ultracut-E microtome and
made and
in
pH
after osmication.
place
specimens,
cultures
light period (the
1 % aqueous Os0 4 for 90 min
wash in
fixative consisted
primary
10 ml
by embedding
fixative consisted of 0.2%
primary
embedding
in
thorough
a
L. REYMOND
of the immobilized cells in medium containing 0.1
repeated washing
postfixation
the
approximately
M HEPES,
AND O.
Exponentially growing
by resuspension
0.1
containing
min; centrifugation
M HEPES;
using
followed
min,
medium
1.5% agar;
3.
photoperiod.
following protocols. (1) Centrifugation of
hyde
or
8 h darkness
for electron microscopy
sampled
were
J. SLUIMAN
(2), except
0.2% tannic acid
saponin (Polysciences)
dehydrated
Spurr’s resin,
with
acetone
and sectioned
diamondknife. Observations
a
EM-300
(Leiden)
were
and Zeiss EM-10
microscopes.
RESULTS
The
ultrastructure of M. geminata has been the
general
study (Reymond
will focus
a
thin wall is
plast.
The
wall in
deposited
less
with the
the
‘isthmus’
cell has reached
having
the
nucleolus
the
occurs,
(MT)
to
indicate the
not
was
than 5
or
at
a
length
two
presence
a
and
semi-cells
and
short
a
previous
the
at
irregular
plasma
the
out
At the
of the
same
bulging part
chloroplast.
is effected
seemingly
time,
a new
of the proto-
shows
(which
sign
no
By
what
might
After
of
the time
original diameter,
organization
(fig. 2).
the
a
is established,
and
be described
chloroplast
as
has
condensation of chromatin
entering prophase.
membrane (PM) associated micro-
‘isthmus’
transverse
at
passes
expansion
Golgi-body having duplicated,
(fig. 4).
This MT is
visible
sections. Most observations
single cortical MT,
position
As the nucleus
(fig. 1).
position
level of the
one
protoplast
of about twice its
that the nucleus is
the
of
of the
intracellular
central
a
6 consecutive
noted in similar
shown).
of
increase in volume of the
elongating parietal
disappears,
indicating
appears
no more
an
cell, including
symmetrical
assumed
between
in
MT
subject
in the present report which
contains the nucleus
and the
At this first stage of mitosis
tubule
repeated
fashion
initially single mitochondrion
nucleus
patches
yet)
mirror-like
the
cleaved,
be
not
bulging
budding-like
a
expanding cytoplasm
the expanded
or
a
all around the
imminent mitosis
more
will
cell until it has doubled in size. This cell
break in the cell wall and
rigid encasing
an
1986), and
stage of each division cycle involves
initially spherical
by
al.
the details of cell division.
on
The first
et
opposite
but
on one
occasion
side of the nucleus
through prometaphase during
a
seem
second
(micrograph
which
a
much
CELL
Fig.
DIVISION IN
2. M.
chondria
geminata. Cell expansion
(M)
reduced
is
and
bodies
(G)
a
is
completed,
have
and mitosis has been
initiated
duplicated, and chloroplast division
minute indentation or
PM is associated with
particularly
acid is
ing
Golgi
is
a
associated with
a
two
some
a
abluminal
proteins
evidence
MTs instead of
are a
one
MT.
fixative
major
(not shown)
coat
that
52000.
x
the cortical
diameter of less than 50
primary aldehyde
This suggests that
material. There is
with
densely staining
well visible when
employed.
pit
Mito-
(prophase).
underway,
spindle apparatus is developed (figs. 3, 5) the PM subtending
MT forms
pit
235
MARVANIA GEMINATA
nm.
The
(figs. 6-8),
which
containing
tannic
constituentof the
the coated
pit
coat-
may
be
236
H.
M.
Figs. 3,4.
(arrow),
(arrow)
x
geminata. Fig.
40000.
marks the
Fig.
3.
Prophase
4. Cel! at
nucleus in
in
prophase
division site,
presumptive
period,
of the cell
any stage
After
to
of the
by
an
intact nuclear
or
the
now
elongated
PM
furrow,
at
just completed septum with
cytokinetic
1
or
time have
being
are
formed
microtubule
not
observed
most
during
invagination proceeds
an
at
the
front end
associated MT is shown
MTs been observed
during cleavage, apart
2 MTs just described.
of the
Immediately following completion
some
REYMOND
least until about half of the internuclear cytop-
in fig. 9. At
from the
L.
envelope during
coating material/MT complex persists
lasm has been bisected. A
no
microtubules
membrane-associated
Centrioles were
permanently.
of mitosis
inward. The
invagination
not
spindle
plasma
O.
cycle.
completion
grow
if
a
SLUIMAN AND
42000.
x
The mitotic apparatus is enclosed
of the division
which
which
J.
in each
daughter
cell
begins
trans-side, containing amorphous
septum (shown in fig. 10) the dictyo-
release
to
a
steady
flow of vesicles from its
electron dense material. These vesicles mi-
grate towards the septum where the amorphous substance is discharged via
cytosis (figs. 10-13).
wall
the
in the
layer
dictyosomes
tion from
shown in
the
the
a
new
to
septum,
fig.
10
initially
but after
to
a
bi-layer
layers
similar
at
the septum
texture
and
differentiatebetween old and
period
are
has
apparently
not
restricted
a
delicate
exo-
single
wall is formed. The transibeen
captured
activity
to
this
is
most
region
in the cell
evident
at
alone since
continuous with layers deposited elsewhere.
staining properties,
new
of
of intense vesicle traffic from
wall formation
septum, it is certainly
the
development
double-layered
a
(arrow). Although
wall
in the
some
the septum PM
to
single layer
transverse
Due
This results
layers
where
they
however,
are
it
is
difficult
to
closely appressed (fig.
CELL DIVISION
Fig.
5-8. M.
IN
geminata. Fig.
envelope. Furrowing
membrane,
showing
with
coated
advanced coated
237
MARVANIA GEMINATA
one or
by
the formation
two associated
pit (arrow)
pit,
5. The mitotic nucleus
has started
with
in
more
(metaphase?) is
of
microtubules,
detail,
x
80000.
associated microtubule
a
coated
x
47000.
surrounded
Fig.
6.
x
an
60000.
intact nuclear
of the
Enlarged portion
Figs. 7,8. Non-adjacent
(arrows),
by
pit-like invagination
serial
plasma
of
sections
fig. 5,
of
an
238
H.
Figs. 9,10.
after
M.
plane (arrow),
Fig.
body
geminata. Fig.
telophase.
10.
Early
x
A
9. A
just completed, delicate septum
septum-associated
microtubule
can
be
seen
J.
SLUIMAN AND O. L.
spans the intemuclear
about
halfway
across
REYMOND
cytoplasm
the
division
44000.
stage of septum wall
ofeach cell. Part of the
new
formation, with
wall has
wall
precursors
being produced by
already become bi-layered (arrow),
x
35000.
the
Golgi
239
CELL DIVISION IN MAR VANIAGEMINATA
II,
As
inset).
the
wall
two
layers
cell wall that encloses
outer
the
the septum increase in
at
septum (fig. 12-13, arrows). This allows the cells
shape,
4.
and
eventually
to
to
old
level of the
to a more
spherical
separate.
DISCUSSION
4.1.
and
Morphological
taxonomic
On the basis of the present observations
bined with information obtained
the division cycle of this
alga
of the division site
formation of
(5)
site marked
of the
the
now
coated
a
1
or
2 MTs,
MTs other than those
of the
by separation
The
larly
informative
of the
aspects
the
of the
to
as
PM
resulting
new
associated
wall
layers
at
cell division
cell
be
to
appears
expansion
and
more
the
of
al.
of M.
1986). Assignment
be contradicted
cell
cycle
1983).
tion of the
quence is
Cell
geminata
seen:
after
gradual
occurs
at
least
cell
two
period
is
the Chlorococ-
geminata represents
important respects.
expansion,
in the
by
a
of nuclear
an
inactivity,
or
apparently
the
prolonged
followed
after rupture
progeny
However, in M. geminata
some
the
during autospor-
to
within the confines of the mother cell wall
expansion
mother wall.
and
particu-
The over-all
unique although
in Chlorococcales is characterized
cytokinetic inactivity
cleavages occurring
& Fott
are not
algae.
any of the other features listed. Ne-
by
the chlorococcalean pattern in
typical
daughter cells;
two
following cleavage
it is obvious that the cell division mechnism of M.
First,
with
the level of the septum, followed
vertheless,
period
apically
distinct wall layers by
two
its taxonomic affinities among green
to
the
of
septum that separates the
not
seem
MTs;
at
absence of cytokinetic
the formationof walls in Chlorococcales
et
cycle;
cleavage; (7)
cales does
on
membrane
plasma
invagination
in cell
deposition during
ogenesis (Reymond
variation
of the cell
short cortical
cells.
‘budding-like’
same as
(‘bud-
and mito-
prometaphase; (6) following telophase, ingrowth
pit-like
the
rest
two
one or
com-
structural features:
following
details noted in M. geminata and listed above
pattern of cell wall
essentially
at
two
geminata,
it is concluded that
(1986),
mitosis and the
during
prophase by
at
common outer
of the
cytokinetic
al.
chloroplast, Golgi apparatus,
mentioned; (8) deposition
Golgi activity
(9) rupture
at
coated
elongated
co-migrating
enhanced
of the
pit-like invagination
cortical MTs
by
et
is characterized
by the
absence of centrioles
chondrion; (3)
cell division in M.
Reymond
by
ding’); (2) pre-mitotic duplication
(4) marking
considerations
on
of the cell and localized rupture of the cell wall
(1) pre-mitotic expansion
a
the
at
convert
the
thickness,
cells breaks
daughter
two
by
two
or
(Komarek
desintegra-
reversed
beginning
of
se-
a new
division cycle is marked by expansion of the protoplast, causing rupture of the
cell
wall,
with
subsequent
been doubled. This
M.
geminata
cytokinesis
seems to
and in Chlorococcales
A second deviation of M.
pattern is
of
cells
as
are
geminata
the formation of only
multiple daughter
being delayed
indicate that the cell
two
until the cell
cycle
fundamentally
volume has
control mechanisms in
different.
from the usual chlorococcalean division
cells per division cycle.
reported by
Hindak
(1976)
was
(The
not
formation
observed in
240
Fig.
H.
11. M.
geminata.
of wall material via
Inset:
More
advanced
Golgi-derived
Enlarged portion
of
stage
vesicles
of
septum
(arrows).
wall
SLUIMAN AND O.
formation, with
The wall is now
fig. 11, showing the junction
J.
L. REYMOND
continued
excretion
bilayered throughout,
of transverse and lateral walls.
x
39000.
x59000.
CELL DIVISION
IN MARVANIA
241
GEMINATA
Figs. 12,13. M. geminata.Golgi-derived vesicles apparently fuse
thereby discharging
the
13).
septum (asterisk
x
37000,
x
their
in
45000.
electron
fig. 12),
dense
and
contents
(arrows).
their remnants remain
with the
Old
wall
visible
for
septum plasma membrane,
layers
some
break
time
at
the level
(asterisk
in
of
fig.
242
our
H.
This
cultures).
division
resulting
mentous
forms
one
related
Microspora ) closely
of
pair
that appear
grounds (Sluiman
to
well,
for
ment
order,
be
the
expanding
more
If this
to
SLUIMAN AND O.
exist in other
geminata belongs
less
or
with the
simple
this
pseudo-fila-
(Sphaeroplea,
Chlorococcales
more
(which
fila-
loosely organized
or
is taken
as
an
argu-
limits of
morphology-based
accepted
to
in
occurs
Radiofilum, Fusola, Fottea)
currently
REYMOND
structural and ultrastructural
on
affinity
L.
apparent than real. Cell
more
typically
( Cylindrocapsa )
Chlorococcales
to
like Elakatothrix,
it is clear that M.
cells
daughter
1984, 1985).
future EM studies may reveal
ments as
may be
deviation, however,
in
J.
the
conceived order
broadly
Chlorococcales.
On
the basis of all information now available
cell division of M.
paper),
geminata
appears
division patterns of Chlorococcales than initial
(Hindak
1976)
cales is the
M.
would
is
formation of
probably
et
best
spores, the
type
present
the known
observations
in Chlorococ-
division pattern
formation of
‘semi-exogenous
as
1986,
to
light microscopic
multiple
described
al.
similar
more
Whereas thebasic cell division
suggest.
endogenous
geminata
(Reymond
be
to
in
auto-
spore diads’.
4.2.
The role of coated
In M.
pears
geminata,
and
at
electron-dense
of ‘coated
the
same
pits’,
Although
i.e. PM
a
the coated
helpful
Coated
to
sign
of the
arise
in M.
geminata
development
as
a
discussion,
does
not
of coated
its
site ap-
is
highly
give
reminiscent
in the forma-
implicated
see
face with
cytoplasmic
Emons & Traas
rise
to
a
coated
1986).
vesicle,
in other systems
pits/vesicles
of PM
bilayer helps (or, induces)
cytoplasmic vesicle (Darnell
can
believed that the
the
al.
the PM in
cause
predetermined
curve
into
clear,
but the consistent presence
at a
et
along
the
latter
1986;
proteins,
cytoplasmic
to
of
assembly
invaginate
surface
and
Heuser & Evans
to
1980;
1969).
A similar mechanism may
pit
that are coated with
regions
clathrin. It is
lattice of clathrin from triskelions
Kanaseki & Kadota
a
on
structure
that have been
references and
by invagination
phospholipid
bud off
cleavage
understand its role in the process of cell cleavage.
pits
cage-like
cleavage
determination of the
resulting
specializations
pit
a
PM-associated MT is formed. The PM then inva-
a
the best characterized of which is
the
microtubules in
of
time becomes associated
(for
with the
comparison
and
material. The
coating
tion of coated vesicles
be
when
during prophase
ginates
pits
the first visible
site.
of
a
dividing
How this
cells of M.
cleavage
MT before the
pit
site is
has
geminata
fixed is
developed,
to
not
and
its close and persistent association with the coating material suggests that there
is
microtubular involvement in the
a
the
cleavage
formation
at
this
known
tant
site.
According
to
(Ockleford 1981),
specific
site from the
clustering
the membrane
the
protein
subtending
microtuble/monomer interaction,
parts
of the PM, and arrive
of the fluid membrane bilayer.
at
the
of
coat
motility
monomers
cortical
or
pit
may
site
by
protein
monomers
may
be inserted in the PM
cytoplasm through
be
at
model of coated vesicle
incorporated
in
some un-
more
lateral transport in the
dis-
plane
CELL DIVISION
The fact that
rather
persists
sors
the
that MTs
lular
play
a
role in
material. This
stopped
cell.
the
Although
(fig. 9)
may
association
Coated
scribed
graphs
actual
the
be taken
might
pit-like
as
et
al.
In
that in M.
of
material
coat
MT
geminata
at
alongside
the
the presence
by
the
apical
could
not
has
coat
of
to
side of the
opposite
be
observed
just completed septum
a
this site the close
at
subcel-
as a
It is understood that coated
disassembly
coat
a
involved with
clearly
are
coccoid green
plant
visible in
PM/coat/MT-
algae.
also the
figures,
conerning
MT
aeria
(fig.
(MTs?)
cytokinetic
division
to
been de-
11
1-3 in Deason
(figs.
the
not
electron micro-
Tetracystis
pit-associated
useful comparison
a
published
These include
of detailed information
organisms prevents
cell division have
few
a
and Friedmannia israelensis
1979),
of these
some
Lack
present.
in these
process
structures
dividing
1979).
be
The observed co-mi-
with other membranes
fusing
implies
indirect evidence that
in Deason & O’Kelley
to
explained
certain radius
have ended.
before, yet they
of
once a
1981).
of the
integrity
microscope.
the presence of
study,
vesicle but
may be
the addition of new PM precur-
Ockleford
be disassembled before the furrow reaches the PM
in the present
coated
a
and its associated MT into the cell again suggests
maintaining
from
prevented
are
coating
coat
form
to
invagination
has
interrupting
membrane (cf.
PM
PM
assembly
visible in the electron
structure
vesicles
the
apical
narrow
coat
off
pinched
not
without
reached,
invaginating
of the
gration
is
pit
ever-elongating
an
is
curvature
to
the coated
as
that the process of
by assuming
of pit
243
IN MARVANIA GEMINATA
events
seems
process
in M.
gemi-
nata.
It is known that green
plants
cellular division by localized
or
Golgi-derived vesicles),
man
1984).
many green
described in
growth
and is often
any
detail;
in
published
by
on
the
referred
the
particular,
reported
to as
precise
Domozych
through ingression
mechanism in the
cleavage
(1987).
physically
ponent (ER, Golgi apparatus)
furrow whose
apical
presents the first
to
a
green
of PM
cell
evidence of the
been
an
and
detailed
Carteria
were
division is effected
on
the lack of critical
endomembrane com-
M. geminata,
intrinsic,
never
recently,
very
based
membrane-associated
positive
port-dependent invagination
an
has
flagellate
conclusion that
the furrow PM.
be characteristic of
mechanism of membrane
Only
was
(invagination) (Slui-
to
‘furrowing’,
transferred from
PM bears
nizable marker in the form of
therefore,
His
of existing PM into the cell
evidence that membraneis
a
in of lateral PM
which has been
casually
septum membranes during
of endomembraneelements (i.e., ER-
in the furrow has received little attention.
observations
duces
new transverse
by folding
or
The latter process,
algae
form
incorporation
however,
ultrastructurally
coat.
The present
occurrence
during cellular division
in
a
of lateral
green
pro-
recog-
study,
trans-
alga.
ACKNOWLEDGEMENTS
This work
for the
was
made possible with support from the Netherlands
Advancement of Pure Research
(Z.W.O.), grant
Organization
H 86-88. Thanks
are
244
H.
due to Dr. F. Hindak
P.-A.
Dr. B. Hickel
(Bratislava),
Milliquet (Lausanne)
the
(Leiden)
SLUIMAN AND
O. L.
REYMOND
Prof. B. Droz and Mr.
(Pldn),
for their assistance
C. Kalkman and Dr. G. M. Lokhorst
J.
in various ways,
for their
helpful
and
Prof.
to
comments
on
manuscript.
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