Neerl. 37(1), March 1988,
Acta Bot.
p.
3-16
steady-state model for apical wall growth
A
in
fungi
J.G.H. Wessels
Department ofPlant Physiology, Biological Centre, University ofGroningen, 9751,
NN
Haren,
The Netherlands
Introduction
3
General perspective
Structure of
fungal
Biosynthesis
and
Mechanism of
3
walls
6
of the wall
assembly
apical
wall
9
11
growth
Conclusions
13
INTRODUCTION
The
of cell walls makes
presence
Whittaker
dom,
have
certain
a
1969)
degree
plants
have evolved
of
mobility
immobile but
due to
the
as
in
while
colonizing
and
parasitic
These activities
fact that fungi
1981), they
fungi
This
a
cells in
at
(saprotrophs)
in relation
prominent
plant pathogens (Dickinson
all land
nearly
plants (Harley
in
man)
& Smith
plants
apex
of
is
growing fungal hyphae.
GENERAL
Many
and
1986).
on
the
It is
only
knowledge
hypotheses
a
the
hyphae
manifested
publication
at
away from its
original
to
plants,
as
evidenced
the
by
& Lucas
in
that
fungi
of the
1982)
their
and
is
colonizing ability
for the continuous extension
emerging
e.g.
view of
wall
to
now
1986).
It should be noted, however, that
a
form
they
the association
root
apical
structure.
be similar in
some
hairs, pollen tubes,
wall extension
It is
and
can
be
possible, however,
cells of
apically growing
details would be different because of differences in the
PERSPECTIVE
notable is
wide
moves
polymers.
of the basic observations
various
ofa
Consequently,
living organisms (biothrophs)
1983). Although
limited,
growth by apical extension,
fungi although
of wall
substrates.
immuno-compromised patients (Chandler
that the principles involved may ultimately prove
and
separate king-
the main decomposers of the lignocellulosic plant cell wall (Crawford
show intrusive
(Schnepf
chemistry
or
a
mycelial colony, consisting
through
is concerned with the mechanisms responsible
formulated based
both
and
as
the presence of cell walls,
associations.
particularly
healthy animals (including
the
plants
rhizoids
are
problem
paper
of the wall
symbiotic
over
fungal mycelium constantly
dead substrata
also the main
with
with
becoming
are
are
mycorrhizae
of
of the
actively growing part
The
apical growth.
system of branched hyphae, may thus grow
position
fungi (defined
organisms which, despite
as
the
of
apical
from 1892
Peziza
apices
on
wall
then put forward
of
by
species
growth
to
were
explain
made in the nineteenth
century
apical growth
still
survive.
Most
Reinhardt in which he described experiments
showing
hyphae. Many
that
disturbances of
of these observations
were
growth
later
were
repeated
with
first
and
β-glucan,
chitin, fungal cell wall,fungalhypha, Schizophyllum commune,wall growth.
Key-words: apical growth,
3
4
J. G. H.
Fig.
the
1. The rate of expansion of any point at the apex is proportional to the cosine of the angle
tip
is
hemispherical (a),
extended
Robertson
by
hemispherical
to
to the
or
of
origin
curvature
the evidence that
(1892)
of
A
(1958 1965).
half-ellipsoids
by Trinci & Saunders(1977),
hairs
root
at
extension
of
when
in the
change
the
shape
of the
tip
when the
a
is half
rate
shape
of
ellipsoid (b).
of the apex from
shape
increasing growth
the apex and
more or
less
noted
(Fig. 1), as
the surface
on
sativum.
validity
together
these observations
the apex. Direct observations
at
occurs
Lepidium
confirmed the
(Castle 1958)
a
also observed by Reinhardt. In addition, he noted that the
was
the displacement of particles
on
made with
angle
of revolution with
was
hyphae
hyphal
of the
co-tangent
WESSELS
could
during apical growth
Similar
with
experiments
of his conclusion that
provided
Reinhardt
by
extend
fungal hyphae
be
only
fungal
a
system
at
their
apices.
With
wall
regard
area as
while
new
a
a
theory
elastic
because it
inadequate
in the
in
change
Trinci &
zone.
A
which
wall
thickness.
Collinge
change
is
1975)
in the
suggested
unlikely by
caused
quality of the
by
of the wall
recent
bursting
strength
was
work
one
over
the
intussusception
1972,
low osmotic
due
to
zone.
potential,
occurred
by
Fig. 2).
later
zone.
con-
As he puts it, such
increase in wall thickness
no
or
by
evidence for
Bracker
that
just
precisely
increase in
swelling
or
maximally
cytoplasm
by
from the
the
hydrostatic
bursting
at
in the wall increases.
a
1970,
at
grow
the
by plastic
extreme
tip
growth
apical
at
the
the apex
pressure,
extreme
cylindrical
as
tip.
form
Subapical swelling
must
expansion.
and
change
considered
1958, 1965, Bartnicki-
investigators (Robertson
not
the kind of
under the apex where the
stress
resulted in cessation of
D’Arcy
an
is
(see below) —was
Reinhardt concluded that the wall
declining
have uniform
He
by applying
was
proposed
to zero
at
the
solutions of
interpreted
as
being
wall, thus interrupting the organized
cytoplasm.
the observations made
considerations of
turgor pressure
increase in mechanical
an
The fact that reliefof turgor pressure,
of new wall material
Disregarding
form,
see
of wall material
detachment of
delivery
laboratory
our
expect
whole apex and does
base of the extension
of the
However, he
1969, Grove &
molecules—which
from
would
bursting
also observed
Lippman
require
proportional
with water, would result in
Instead he observed that
Garcia &
would
to
dis-
(1892)
also found that wall thickness remains uniform in the extension
is attained and where the circumferential
and
a
due
expands
intussusception.
or
investigators (Girbardt
Later
Reinhardt. Thus
by flooding
wall
Reinhardt
regarded enlargement
molecules that make up the wall. He found
quality
by
growth,
who
the base of the extension
to
increase in strength could be achieved
change
plastic
or
by apposition
of the wall from the
very apex
strength
an
an
material is added
a
wall
apical
prevailing theory of leading botanists
process in which
wall
sidered such
the mechanisms involved in
to
the then
cussed
by
Reinhardt (1892), and probably
Thompson (1917,
see
Bonner
mathematical models have been put forward
to
1961)
on
describe
the
inspired by
origin
of cellular
apical morphogenesis.
APICAL WALL GROWTH IN
Fig.
2.
acetic
Explosive apical bursting
acid, following
the
located at the base of the
all
They
yield
to
D-1
rely
to
shape
of the
its
apex
of
hyphal
apex when
1).
a
cate
apex
(for
is
to
swell and burst
see
wall from becoming
been
proposed
for the
be
apical
plasm
explain why
may
wall
apex, when turgor is
At the
question
same
the
for
Such models
apically
in
to
with
through
of Dr
0-5%
a
hole
J.H. Sietsma.)
the presence of a
tendency
of the wall
Wolff & Houwink
(de
point
any
a
plastic
at
1954,
through
a test
at
it would
various
to
the base of the
expanding
recently
always
necessary
the
over
to
growing
dome instead of the
none
turgor pressure
cytoskeletal
pressure
tubes
by
burst
at
(Wessels
(Picton
the
1986).
& Steer
underlying
its weakest
of those
has cared
elements in the
1987) protect the newly
internal pressure
not
the
be found for the
must
apical
under
discovered
extending pollen
the wall does
on
make.
to
high hydrostatic
against high
seem
points
dome is
apical
depends
pressure. It is unfortunatethat
wall
the
the
on
dismissed, another explanation
wall in
formed deliThis has also
1982).
Protec-
structured cyto-
point,
i.e.
at
the very
suddenly increased.
of the
of cytoskeletal elements
presence
of mathematical models
may be wrong in
vacuoles,
(Courtesy
decrease in the
a
at
McKerracher & Heath
time, recognition
validity
off(b).
flooding
is extruded
apex is due
hyphal
of the wall
high turgor
to
subject
apical
tion of the
is blown
after
commune
cytoplasm
downwards
tip
difficult
to
theory
review
The
mathematical function which
a
properties
explain subapical bursting. Possibly
hyphal
the
To put these models
subjected
who have advanced
at
expansion
to
measurements are
tips
apical dome
extreme
models
and elastic
theory
Schizophyllum
(1966).
1972, Green 1974, Trinci & Saunders 1977, Saunders & Trinci
all these
(Fig.
such
If Reinhardt’s
extreme
the whole
position, according
plastic
obviously
tendency
In
1982).
by
determinethe
apex;
(a) or
of
of the wall such that there is
Riva Ricci & Kendrick
1979, Koch
hyphae
& Robinson
that extension
concept
plasticity
of Park
turgor pressure from the
determined
to
dome
5
agar-grown
procedure
apical
the
on
in the
gradient
of
FUNGI
is
assuming
uniformly present
assuming expansion
that turgor pressure,
over
the whole
at
the
apex
would
under turgor
pressure.
probably generated
apical
wall
area.
sub-
New models
6
J. G. H.
into
taking
the
in
If there is
the
shaping
concept of
generated
the
account
in
cytoplasm
a
of
presence
hyphal
elements
cytoskeletal
(as already
apex
advocated
might assign
a
WESSELS
role
while
by Reinhardt)
to
the
retaining
deformable wall expanding under the influence of hydrostatic pressure
subapical hyphal parts.
gradient
a
in the
of the
plasticity
wall,
maximal at the very apex and
declining
towards the base of the apical extension zone, then how is this gradient generated? Two
possibilities
and
until it becomes
expands
expand
considered in the nineteenthcentury. Either the wall is
were
until it becomes
rigid
the wall is
or
The first concept
plastic.
synthesized
as
(Nageli)
apposition (Strasburger) (cit: Reinhardt
of the wall after its formation
his
explain
commune
basis
observations
(Wessels
model of
& Sietsma
apical
wall
below)
growth’ (Wessels
lytic
Gooday (1978). Although
balance between wall
rather
uncritically
as
a
lytic
tal
enzymes. For the
STRUCTURE
first
OF
are
for
see
1982,
considered
chitosan)]
alkali-insoluble
(Sietsma
seems
a
role
expand
was
been favoured
experimental
‘steady-state
expressed
a
must
be
century ago by
by Bartnicki-Garcia (1973)
concept,
the conclusion
that,
1986). Lysins
which presumes
1973),
of lysins
in
date,
to
play
is
a
‘delicate
missing,
it is
explain
apical
the evidence for this
role in
no
this model does
sufficient to
not
the
the structural and
wall
growth
preferred
disprove
to
were
a
role for
experimenarise,
e.g.
a
Wessels
much
and
and
1988)
WALLS
bewildering
a
Bartnicki-Garcia
number of
1968, Wessels
when
1986). However,
more
simple picture
basidiomycetes mainly
(chitin)
and
wall
is
solely
(1 ->4)-P-D-glucosamino-
wholly deacetylated
There
responsible
com-
The alkali-insoluble wall
emerges.
or
1981a, Bartnicki-
the alkali-insoluble
consist of
partially
and constituent
polymers
& Sietsma
only
(l-»3)-p-D/(l->6)-P-D-glucan.
portion of the
& Wessels
molecular and
lysis’ (Bartnicki-Garcia
1984,
it
glycans, [poly-A-acelylglucosamine
(e.g.
to
to
this would necessitate modification of the model.
portions of ascomycetes
tives
1965)
Schizophyllum
and has been named the
1893)
growth. However,
FUNGAL
(for reviews
Garcia & Lippman
ponents
come to
walls contain
sight fungal
monomers
a
in
biogenesis
rigidification
(1958,
The alternative concept that the wall
in order
wall
wall
this concept
al.
recently
(Wessels
moment
data. If hard evidence
on
Robertson
fact in many research papers and textbooks. I have critically
thin indeed
through genetic studies,
At
and
model of apical wall
steady-state
et
1986).
more
examined the evidence and have
concept is very
Work
direct evidence for this
synthesis
cited
in formulations by
given
enzymes
Marchall-Ward (1888) and has
and
has
1981b, Wessels
loosened by
continuously
implicit
living hyphae.
on
be discussed
(to
was
cannot
by intussusception
was
This concept of
1892).
and
in the nineteenth
generally accepted
was
century; controversies mainly concerned whether wall addition
or
originally plastic
rigid entity
a
for
is
evidence
hyphal
deriva-
that
this
morphogenesis
and for the sake of the present discussion the
alkali-soluble
components of the wall will therefore be largely ignored.
In order
to
observations,
tions,
have been made
1981a).
wall
reveal the molecular architecture of the hyphal wall, electronmicroscope
combined with the
as
on
On the basis of such
a
co-axially
use
of
the walls of
layered
more or
a
observations,
structure.
As
Hunsley
Burnett
understood that the co-axially arranged regions
into each other. Wessels & Sietsma
less
specific enzymic
variety of fungi (lit.
are
& Burnett
(1979)
not
(1981a), however,
has
cit.
or
chemical
in Wessels
(1970)
have modelled the
pointed out,
supposed
to
noted that the
extrac-
& Sietsma
it
should be
be discrete but grade
techniques
used
can
APICAL WALL GROWTH
Fig.
3. Model
of the mature
chitin
hydrogen-bonded to
contains
amino acids with
(1 -*6)-P-linked glucose
(1
-*6)-P
form
linked
s-glucan) (f)
(1 ->3)-P-glucan
excreted into
easily
to
(c)
or
to
(Adapted
applies
aerial
to
3
where
depicts
integrating
(Wessels
the
a
outside
insoluble
of
just
one
on
(I->6)-P-linked
attached
to
or
a
to
branches
(I ->3)-P
branched
or
chains
outer
They
forming
(g)
layers
may
be
linked
and carry
are
also
as a
layer. Free
present
in
glucose
water-soluble
most
published
studies
(l-»4)-P-linked
with
layer,
This
layers.
some
components
model
simple
basidiomycete Schizopyllum
and
a
Both
In
this
these chains
Other
and
commune
ultrastructural analyses
a
layer
which contains
complex
thus
some
the
case
a
resemble the
(1->3)-P-linked
chains
glucan
through
an
alkali-
chains
are
of the chains, branches
types of branched glucans
glucosaminoglycan
only
water-insoluble but alkali-soluble
branches attached. In
residue and
more
specialized structures, e.g. spores and
the outside of
complex.
the outside of the hyphae.
branches.
one
chemical, enzymic
at
may
the wall and may be
1977,1979, vanderValk etal. 1977). In this
accumulate
single
present.
wall of the
number of
are
alternatively, (1 -»3)-P and
(l->3)-P glucan segments
considered
extra
the walls of
hyphal
(a)
1981b.)
form essentially
not to
(1 ->6)-p-linked
glucan
sparsely
structure.
apparently
and
genuine
results of
with
are
chitin
coupling fragment (b)
glucannetwork. Crystalline (1 -*3)-a-glucan fibrils (alkali-
gel-like (1 ->3)-(3-/(l -»6)-P-glucan
(1 -»3)-P-linked
chains
chains. The
and accumulate at the outer surface
of wall
glucosaminoglycan-glucan
accumulating
P-glucan
from Wessels & Sietsma
modelof the
(1 ->3)-ct-glucan (s-glucan)
consist
of the
etal. 1972, Sietsma & Wessels
water-soluble
The
Partially crystallized
p-glucan
modelof the wall in which the various wall components are
vegetative hyphae
hyphae,
Figure
the
of lysine.
strength
closely associated with each other
at
linked
longer(I ->6)-p-linked glucan branches (d)
misinterpretations
a
commune.
covalently
single (1 ->6)-P-linked glucose
be in agreement with
accumulating
Schizophyllum
carry
throughout the wall
chains with
7
Some unsubstituted
which add to the
the medium.
lead
which
high proportion
branches
occur
FUNGI
wall of
hyphal
chains
glucan branches (e).
triple helices (h)
soluble
a
IN
gel-like glucan
chains
are
their
carry
thought
reducing
longer
to
be
ends via
J. G. H.
8
Table
1.
Solubilization of non-aminoglycans by
Nitrous acid
Nitrous
S.
depolymerization
of aminoglycans*
Chitinase
Chitinase
treatment
WESSELS
treatment
Aminoglycan
Non-aminoglycan
Aminoglycan
Non-aminoglycan
degraded
released
degraded
released
98
98
88
88
48
10
10 (95-4)f
(95 4)t
(100)t
—(100)t
commune
—
A.
A. bisporus
hisporus
Vegetative mycelium
M.
M.
mucedo
*In
S.
commune
insoluble
to
wall
the percentages
A.
and
fraction
of
94
79
79
100
bisporus figures refer
treatments
wall
to the
in water and
and
aminoglycan
alkali-insoluble
on
tNitrous
67
41
becoming soluble
treatment. Nitrous acid
done
38
19
19
41
41
Fruit-body
Fruit-body stipe
stipe
glycuronan
done
were
56
—
—
percentages
of
aminoglycan
and
glucan
alkali after the treatments. In M. mucedo
in
the whole
wall
which
soluble
were
before exposure of the walls to alkali.
in
heating
partially hydrogen-bonded
chains of
in
X-ray analysis
acid breaks the
linked
10
the wall fraction in
The
specific
linkages
chains
aminoglycan
M
NaOH to
is
the
(Datema
et
jV-acetylglucosamine)
et
al.
1
of
shows
1979)
all the
and
hand,
solubilizing
is
very
the
residues in the
data
is less
soluble in
break
to
shown
the very
cerevisiae
must
and chitin.
and
glucan
water
in
& Feather
to
residues
break
occur
stretches
homopolymer
of
alkali-insoluble P-glucans
small
be held
glucos-
alkali after
or
nitrous acid
glucosamine
and ascomycetes
even
hydrolyses (1 ->6)-P-
polymers (Stagg
solubilize all the
to
found that
bonds
seen
with hot dilute
& Wessels
(Sietsma
amount
of
1981;
glucosamino-
responsible for keeping
the
alkali-insoluble form (Mol & Wessels 1987).
is first
two
basidiomycetes,
In
is
degrading
occur
nitrous acid
released
by
In
a
&
(Sietsma
the first
species
(from
Serratia marcescens),
on
acetylated glucosaminoglycan (chitin)
this
in
commune
unpublished).
and nitrous acid has littleeffect unless the
Chitinase
Agaricus bisporus
glucosaminoglycan
Schizophyllum
& Wessels
acetylated
deacetylated.
effective in
effectively
and
triple
reflections
hydroglucans
between
where non-acetylated
basidiomycetes
we
complex
are
unsub-
hydrogen-bonded
depolymerizations (employing
chitinase
been
for
P-glucan.
glucan
linkage
chains become
Agaricus bisporus (Mol
extensively degraded by
glucan
Such
Saccharomyces
an
postulating
glucan
glucosaminoglycan
glucosaminoglycan
other
and
have
and
reflections of
(acetyl)glucosamine-containing
1979).
number of
in the wall in
Table
Wessels
of
for
of
hydroglucan
Treatment of the
sharp X-ray
to
evidence
1988). Recently
in the wall
glycan
P-glucan
nearly
a
the
were
chains
of hydrogen-bonded
presence
glucosaminoglycan
leading
that the
1977b)
from the wall of
The
glucan complex.
glucosaminoglycans
al.
after
water
deacetylate chitin.
consisting
inferred from the weak
was
between
depolymerization
bonds in
Mol
chains
Sietsma & Wessels
1973,
microfibrillarchitin
of the chitin
important
most
to
poly-TV-acetylglucosamine.
glucan
chains thus
glucan
alkali-
fractions.
acid treatment after
helices among the
the
figuresrefer
Chitinase treatments
amino acids, particularly lysine. Probably these substituted glucosaminoglycan
stituted
in
the
,
however,
a
deacetylated
releasing P-glucan
chitinase but
a
large
number of
glucosamine
form because the
into solution.
the
and
is
polymer
Consequently,
nitrous acid treatment, followed
the
by
a
chitinase treatment, effectively brings all the P-glucan into solution (Mol & Wessels 1988).
Table 1 also shows data derived from
1977b).
In this zygomycete
an
even
a
study
larger
on
the wall of Mucor mucedo (Datema
fraction of the
glucosamine
et
al.
residues of the
APICAL WALL GROWTH
Fig.
4. Possible
bonding
is
cetes
and
The
and
can
two
an
acid
glucuronic
)
and
(I-*3)-p-glucan (~) involving hydrogen
anionic
(5:1:1:6
also be extracted
is
polymers
by
in
a
poly-cation.
heteroglucuronan
on
molecular
a
containing
basis).
strong salt solutions and
ionic and
probably
not
covalent,
of this
Depolymerization
fucose,
Since in this
the
the
partly by alkali,
as
mannose,
case
non-
linkage
surmised in the ascomy-
basidiomycetes.
of the
linkage
mycetes and
0-glucan
basidiomycetes
combination with
highly
glucosaminoglycans (
deacetylated resulting
releases
glucosaminoglycan
aminoglycan
9
heterologous chains.
glucosaminoglycans
between the
FUNGI
interactions between
between
galactose
IN
chains
not
only
hydrogen-bonding
cross-linked
complex
as
to
glucosaminoglycan
leads
to
between
shown in
Fig.
chains in the walls of
insolubilization of the
homologous chains,
3. This may,
glucan
ascoco-
chains
but,
may also result in
however, represent
in
a
an extreme
case.
Figure
4
schematically depicts
interactions
between
some
wall
glucosaminoglycan
structures
and
which may
(1 ->3)-p-glucan
actually
chains.
arise from the
Included
are
possible interactions between homologous chains involving hydrogen bonds leading
the formationof chitin microfibrils in the
helices in the
case
of
of the
of acetylated
(l->3)-P-glucans (Jelsma
situation in which all the chains
chitin microfibrils
depicted (Fig. 4a-e)
case
may
are
involved in
covalently
actually
bind the
&
Kreger
glucosaminoglycans
1975). Figure
hydrogen bonding
glucan
chains. In
fact,
to
triple
4e thus shows
while the
outer
all the
be present in the wall and contribute
and
to
a
chains
structures
its mechanical
properties.
BIOSYNTHESIS AND
Most evidence
chains
are
membrane
(Vermeulen
made
at
protein,
acetylglucosamine
1976)
are
the
et
outer
chitin
at
ASSEMBLY
the
al.
THE WALL
1979 and references cited
surface of the
synthase,
cytoplasmic
minivesicles which
OF
probably
plasma
that accepts
therein)
indicates that chitin
membrane probably
the
an
integral
precursor
side of the membrane. Chitosomes
act as
by
(Bracker
conveyers for inactive chitin synthase
et
al.
en route
J. G. H.
10
the
to
the discoverers of these chitosomes still entertain the
plasma membrane, although
that chitosomes themselves
possibility
Herrera
1984).
In
plasma
from Cabib’s
come
(Bartnicki-Garcia
laboratory (Cabib’s
cations have arisen after the gene for this chitin
in vitro
et
al.
thus
by
insertion,
The gene
far in
vitro but
another
enzyme
vivo with
can
an
1986).
1977).
to
In this
replace
did
affect
not
glucan
cit: in
the ultimate product
the
product
be
may
the
al.
et
been
et
al.
et
al.
1983),
(indicated
Because the
nature
results in
in
Fig.
Fig. 4b-e)
of the
enzymic
by
al.
et
a
might
then
recall the
addition,
occur
matrix of animals
in
occurring
cell
all take
residues attached
enzymically
Amadori
glucan
Irrespective
biological
1981)
or
to
by
the
et
with
end
1984).
on
the
the
that lead
fungi (lit.
the
plasma
outer
plasma
of
(Wilson
glucan
shown in
residues
are
ends of
can
be
chains
we
com-
envisage
amino-
to
analogy
an
we
may
in the extracellular
residues in extensin
may
forming
directly
a
cannot
as
in
Fig. 4,
that the
Fig.
4a has visco-elastic
properties
composite
structures shown in
Fig.
4c-e
and
non-
Schiff base and
reducing
ends of
be excluded.
glucosaminoglycans
envisaged
coupling
1986). Alternatively, lysine
Fry
depicted
wall.
glucan
reacting
attached
Also direct interactions of the
as
and
P-glucans. Coupling
occurring
as
glucosaminoglycans
it
two
enzyme. Rather
an
glucosaminoglycans
of
wall, such
instance,
of the
tryptophane
&
cross-linked wall
domain of the
the mechanism of
nature
collagen
glucosaminoglycan
to
glucosaminoglycan
reducing
of the type of cross-links between the
transitions within the
the
at
oxidases in the wall. As
within the
al.
amino-groups
structure
associated
fungi,
phenolic
cross-linking
plants
reducing
with the
whereas the cross-linked
of
the
or
aminosugars
consequences. For
wall
lysine
and/or
as
of vascular
products (Monnier
chains with
post-synthetic
cursor
to
interact
(1->3)-(3-d-
from
S. cerevisiae has the
within the
place
polymeric
between lysine residues in
(Hay
in
of the individual
and may differ among
via radicals produced
walls
only
residues
the processes
because of the
glucosaminoglycans
cross-linking
but
after
water-insoluble and alkali-insoluble product
synthesis
4a)
must
scheme in which amino acids such
sugars within the
in
Wessels
(chitin),
immediately
preparations
(partially)
ponents it is unlikely that the coupling itself is mediated by
a
commune
glucosaminogly-
alkali-soluble
an
but
1985)
be
to
of
synthesis
membranous
coupling fragment between
chains is insufficiently known,
remains elusive. In
shown
it follows that after
in
catalysed by
S.
der Valk &
deacetylation
of the W-acetylglucosamine
immediately
(3-glucan chains (indicated
structures
apparently
(van
studied
synthase
mainly poly-A'-acetylglucosaminc
to
inactivated
1980).
the polymerization
membrane surface
and
cloned,
by
compli-
1984).
1985; Szaniszlo
rigorously
membrane (Shematek
(Wessels
vivo,
membrane
plasma
was
uridine-diphosphate-glucose
synthase
Since
1984)
has shown that akali-insoluble
subject
& Bartnicki-Garcia
Sonnenberg
glucan
but
et
allele by transformation (Bulawa
of chitin in
Numerous studies have demonstrated the
from
of chitin
the appearance of the chitin
synthesis
outside
synthesized just
synthesis (Davis
wild-type
1984, Ruiz-
al.
had been
synthase
the
through
synthesis
(Orlean 1987). However, autoradiography after labelling
case
cases
the
replacement abolished
tritiated-JV-acetylglucosamine
is indeed
in other
and used
& Bracker
cerevisiae evidence for vectorial
Saccharomyces
membranes has
chitin after their extrusion
synthesize
membrane into the domain of the wall
plasma
WESSELS
and
may have
P-glucans,
important
highly hydrated
and
can
display
be
pre-
deformed;
various
degrees
rigidity.
The evidence collected with S.
commune to
and
assembly of wall components with
can
be summarized as follows.
an
support such
a
two-step process of synthesis
accompanying change
in mechanical
properties
APICAL
1.
WALL GROWTH
IN FUNGI
11
Water-soluble and alkali-soluble (l-»3)-(3-glucans
the alkali-insoluble
both with
(Wessels
al.
formed
polyoxin D, protoplasts
chitin and alkali-insoluble
then
can
another
alkali-soluble
be linked
not
(Sonhenberg
remain soluble
nikkomycin,
of
by pulse-chase
radioactivity
and with growing
1982)
into
(l->3)-(3-glucan
1975,
hyphae
(I ->3)-a-glucan
are
normally
glucosaminoglycan
and thus
al.
et
have shown that
(1987)
inhibits the conversion of
synthase,
glucan
der Valk &
van
precursor molecules
Elorza
1982). Similarly,
alkali-insoluble
an
wall made of
a
& Wessels
alkali-insoluble
to an
inhibitor of chitin
specific
glucan
al.
et
form
can
(de Vries
glucan
the soluble
1976). Although
they
al.
et
the precursor molecules for
are
shown
1983).
2. In the presence of
Wessels
was
regenerating protoplasts (Sonnenberg
et
without
in the wall. This
P-glucans
on
regenerating
an
of
protoplasts
Candida albicans.
3.
shows
Autoradiography
synthesized
at
the
extreme
ent
is found for water-soluble
the
extreme
apex. While
apex
4.
the
Electron
(Vermeulen
the
et
al.
of shadowed
microscopy
& Wessels
have ceased
to
their
walls.
apical
and
apex
5.
grow
after
growing hyphae
these
not
shearing
are
it
a
apically
forces
chains
Fig.
in
the
hyphae
et
linkage
be
highly
serves
zone,
and
complex
as
pressure of the
subapical
appositional
and
to
cytoplasm.
direction
glucosaminoglycans
chains.
Hyphae
that
a
time
gap
exists
between
1986).
hyphae through
X-press,
an
and
glucan.
in
polymers, present subapically
chase,
not
are
removed
have
we
glucan chains present
show
to
at
by
the tip
in the matured wall.
the basis for the
individual
area
and
maximal
They
form
As
by growth,
a
are
zone
a
occurs
at
to a more
as
at
extreme
the
apex
in accordance with autoradio-
(Gooday
that
visco-elastic wall segment
moves
model
(1 ->3)-P-glucan
the
1971,
chains extruded into the wall
visco-elastic wall
it also
and
probably polymerized
deposition
of labelled precursors
P-glucan
steady-state growth
glucosaminoglycan
by apposition.
incorporation
glucosaminoglycan
hydrated
at
APICAL WALL GROWTH
into the wall
estimates of
The
the whole
chitinase and hot dilute
glucosaminoglycan
after the
growing
not
and then declines towards the base of the extention
1983).
not occur
autoradiography
al. 1983). This is the only direct evidence
membrane-wall interface. Per unit
graphic
to
glucan
to
in vitro
pulse-labelled
glucosaminoglycan
5. In the extension
deposited
are
over
glucosaminoglycans
apex the
growing
the passage of
generated by
The evidence summarized above
shows in
the
few minutes these labelled
(Wessels
OF
at
shown that also
was
differs from the cross-linked
MECHANISM
combined with
susceptible
still available for
remove
that the mixture of individual
mechanically
become insoluble
seen to
at
extension in the absence
of the chitin chains (Vermeulen & Wessels
as
and
chase of
or
during
have alkali-insoluble glucan but also microfibrillarchitin in
only
Recently,
tips
a
be
preparations
evidence that
as
High shearing forces,
However,
can
non-fibrillar and very
are
crystallization
disrupt growing
direction
shown that the alkali-insoluble
1984) has
yet crystallized and
synthesis
subapical
become alkali-insoluble. If extension does
glucans
mineralacid. This is taken
not
a
gradi-
1983).
growing hyphal
have
in
maximally
are
direction. A similar
subapical
but very little alkali-insoluble glucan is present
the water-soluble glucan
chase,
(Wessels
apex
glucosaminoglycans
in
decreasing
0-glucan
displaced
of label, the water-soluble
during
that alkali-insoluble
hyphal
expands
Wessels
are
et
al.
supposed
to
under the
is stretched and
internal
displaced
in
external side of the wall because
addition of visco-elastic wall material on the inside continues so that uniform
12
J. G. H.
Fig.
5.
while
model
Steady-state
being displaced
extension
ceases
in
a
of apical wall
subapical
the interactions
growth. Glucosaminoglycan (
direction.
occur over
displaced
internal pressure
and
the
interactions between the
cation,
ing
branches
as
very
scarce
the
are
continue
an extent
(Fig. 5d)
but
that is
al.
et
that the final wall
highly regular
in
very
little
structures
crystallinity
as
chains with
depicted
in
in
the
outer
The
quently
above
hardened
into
by
the
is
and
c
to
However,
in
the
the
further rigidifi-
(Wessels
(1 ->6)-(3 linkages
It is also
structure
are
to
possible
the
are
et
al.
appear-
initially
that
they
probably deviates from
actually
be
are
glucosaminoglycan
the alkali-insoluble
may
complex
the
shows
of various
made up
the water-soluble (1-»3)-p-glucan
residues attached which
Consequently,
freely
occur
in the wall
which accumulates
the whole apex
the apex then assumes the
The
1984, Sietsma
et
al.
1985).
continued extension
in the wall. The
rate
cross-linking (rigidification)
ceases
experimental
cross-linking
and
of extrusion of wall
are
supposed
stiffening
will
to
be
occur
evidence does indeed show that the wall
same structure as
(l->6)-(3-linked glucose
because
visco-elastic wall material which is subse-
process
of
when growth
over
(Fig. 5).
rate
model
steady-state
a
cross-linking
the wall and the
over
of
chains
to
glucose residues
or
partly crystalline (1 ->3)-a-glucan (s-glucan)
the continuous extrusion of the
independent.
ance
0-glucan
chains
between
point
longer yields
lead
1985).
fact,
In
shown
not
no
At
surfaces of the wall.
on
polymers
4. Also
single (1 ->6)-P-linked glucose
model described
depends
X-ray diffraction
Fig.
and the alkali-solubleand
at
5d.
chains.
probably
hooked up
secondarily
Fig,
externally
when the wall matures, eventually
appear
chains. It should also be stressed
depicted
and
subapically
is attained.
hyphae
and
chains. Such
rapidly
(1 ->3)-P*linkages (Sietsma
structure
interact
subapically. When
appear
of covalent bonding
that the wall
(1 -»6)-[3-linked glucan
glucan
mixed-linkage glucan
a
such
(1 ->3)-P-linked glucan
in the insoluble
outnumbering
part of
the
on
5d
Fig.
(I ->-3)-P-glucan ( ~)
homologous
deduced from continued insolubilization of
as
Also shown in
1983).
to
because
maximal diameter of the
polymers
and
time the
same
between
hydrogen bonding
5 these processes have advanced
Fig.
At the
1974).
undergoes rigidification
chains and
heterologous
)
residues also
the whole
apex.
wall thickness is maintained (Green
wall segment
(1 -*6)-p-linked glucose
WESSELS
in
subapical parts, including
residues and chitin microfibrils
(Vermeulen
the appear& Wessels
APICAL WALL GROWTH
to
With respect
explains
IN FUNGI
observations with
do
why hyphal tips
Instead the model
implicated.
the
living hyphae,
when
lyse
not
13
growth
because
of the
predicts rigidification
model of wall
steady-state
ceases
tip
lytic
no
wall which would
why extension becomes irreversibly blocked when growth is interrupted for
Robertson
(Reinhardt 1892,
1958).
In
addition,
Trinci
1975)
variety
of deformations of
with the
rise
homologous
when
as
congo red
which interferes with the
branch
lysins would still
specific
enzymes
be
for
may
to
et
be
generation
al.
1984,
initiate the
process.
example,
the
essence,
scheme
ascomycetes in general
give
may
associations such
for the formationof various
of bulbous
from
However,
be induced
can
& Wessels
For
1986).
matured wall segment,
a
lysine
such
break the cross-links between
tips
Wessels, unpublished)
(Vermeulen
above
suggested
but
details may
may
be
could be
quite
and
glucosaminoglycan
applicable
differ. It is
tempting
zygomycetes the role of the chitin-glucan linkages is played
partially deacetylated
depolymerization
of
chitin and
in zygomycetes
Table
1). Deacetylation
causes
at
These in
glucuronans.
process
at
occur
the apex could lead
turn
may be
in the visco-elastic
linkages
shortly
of the
properties
a
after
the
0-glucans by
et
al.
chitin
1977a,
synthesis
& Bartnicki-Garcia
(Davis
in
between
partially deacetylated
of the
1984).
of the cationic groups
by
chains
by
glucosaminoglycan
among themselves. Thus the
hydrogen-bonded
of deacetylation of chitin at the apex of
significant change
the ionic
generation
cross-linking
that
speculate
glucuronans (Datema
occurred
the apex, the
to
of the
in the wall
seems to occur
has
by
and
basidiomycetes
to
to
Similar to the solubilizationof
solubilization of
crystallization
that these processes
deacetylase
the
of chitin
chitin chains and before
Assuming
glucuronans.
chitin, specific depolymerization
chains
acidic
a
chains.
glucan
the
of
rate
Steele &
produce
in the wall
symbiotic
Vermeulen&
extending tip
an
1892;
process could
polymers
In
responsible
the
of chitin chains
of
generation
required
that,
(Pancaldi
crystallization
i.e. the
formation,
host tissue,
Experimentally,
1986).
explain
substances that interfere
produced
interactions between
in blastic conidia (Cole
produced by
substances such
In
as
(Reinhardt
cross-linking
hyphal tips. Endogenously
heterologous
or
infection structures.
fungal
Interference with the
envisaged.
bulbous cells such
to
substances,
by
be
can
zone
are
short time
a
between the
positive relationship
a
hyphal growth and the length and width of the extension
growth
enzymes
zygomycete hypha could also lead
to a
of the wall.
CONCLUSIONS
Growth of the
wall
which
properties
at
the
contrast
hyphal
with
apex
the
requires
requirement
that-the wall in this
of
widely held view involves the participation
of
the apex and
be inserted. As
allow
to
new
model is discussed based
holds
that
However,
the
this
assemblage
various individual
subapical
made
on
on
assemblage
direction
wall material
to
wall-lytic
enzymes
an
polymers
develops
synthesized
at
the
alternative,
apex
in
rigidity by interactions,
polymers present
while the
during elongation.
assemblage
This model
seems to
in
the
is
essence
wall,
A
at
steady-state
a
this model
inherently
the
plastic
hypha.
the wall
plasticize
to
observations in the author’s laboratory. In
of
has
region
elsewhere
rigidity
plastic.
between
is stretched and
moves
the
in
a
fit many of the observations
living hyphae.
ACKNOWLEDGEMENTS
I would like
to
thank Drs J.H. Sietsma and C.A. Vermeulen for
experiments and
in the
development
of ideas
expressed
in this
joining
paper.
me
in
many of the
14
J. G.
H.
WESSELS
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