ACTIN-CYTOSKELETAL CONTROL OF GRAVITY SENSING AND GRAVITY-ORIENTED TIP GROWTH
Markus Braun, Brigitte Buchen and Andreas Sievers
Botanisches Institut, Universität Bonn, Bonn, Germany
ABSTRACT
Gravity-sensing and gravity-oriented polarized growth of
characean rhizoids and protonemata are dependent on the actin
cytoskeleton. The multiple functions and dynamic nature of the
actin cytoskeleton are conferred by the concerted action of a
variety of actin-binding proteins. Monomer actin-binding
profilin, actin-depolymerizing factor (ADF) and spectrin-like
proteins concentrate in a central prominent spot in the apex of
both cell types, where they colocalize with a dense, spherical
actin array and a unique aggregate of endoplasmic reticulum
(ER), which represents the structural center of the
Spitzenkörper1. Spectrin-like proteins are suggested to be
involved in stabilizing the ER aggregate by forming crosslinks
between ER membranes and actin filaments. The apical actin
filaments radially assemble from the center of the Spitzenkörper,
where actin polymerization might be under local control of ADF
and profilin. Distinct actin filaments extend into the outermost
tip and form a dense meshwork in the apical and subapical
region, before they are incorporated into thick bundles that
generate rotational cytoplasmic streaming in the basal region of
both cells. The actomyosin system not only mediates the
transport of secretory vesicles to the growing tip and controls the
incorporation pattern of cell wall material, but also coordinates
the tip-focused distribution pattern of calcium channels in the
apical membrane which establish the tip-high calcium gradient,
the prerequisite for exocytosis. Microgravity experiments have
added much to our understanding that both cell types use an
efficient actomyosin-based system to control and correct the
position of their statoliths and to direct sedimenting statoliths to
confined graviperception sites at the plasma membrane. Actin´s
involvement in the graviresponses is more indirect. The upward
growth of negatively gravitropic protonemata was shown to be
preceded by a statolith-induced relocalization the calcium
gradient to the upper flank that does not occur in positively
gravitropic (downward growing) rhizoids, in which statolith
sedimentation is followed by differential flank growth.
Combining these results, it is evident that the spatiotemporal
control of actin polymerization and dynamic actin remodeling is
fundamental for the process of gravity sensing and gravityoriented polarized growth in characean rhizoids and
protonemata.
INTRODUCTION
Gravity-oriented growth and gravity-modulated developmental processes have been investigated for more than a
century, but the underlying molecular and cellular
1
Spitzenkörper (apical body): a tip-growth organizing ‘compartment’ in
characean rhizoids and protonemata that comprises a central ER
aggregate, an accumulation of secretory vesicles and an extensive actin
organisation.
____________________
* Correspondence to: M arkus Braun
Botanisches Institut, Universität Bonn
Venusbergweg 22, D-53115 Bonn, Germany
Email: [email protected]
Phone: 49 228 732686; FAX: 49 228 732677
mechanisms are still enigmatic. Gravity sensing and
gravitropic orientation of most higher and lower plant
cells and organs are based on the positioning and gravityinduced displacement of sedimentable particles, so called
statoliths. There are a number of studies proposing that
elements of the cytoskeleton, highly dynamic filamentous
networks of microtubules and actin filaments which are
regulated by a great number of associated proteins, are
involved in gravitropism, but its role in the different
phases of the gravitropic signaling pathways is still
intensely debated and the findings are sometimes
contradictory (Kiss, 2000; Blancaflor, 2002; Sievers et
al., 2002). Tip-growing rhizoids and protonemata of the
characean green algae increasingly receive attention since
they represent favorable model cell types for studying
several aspects of gravitropism (Sievers et al., 1996;
Braun and Wasteneys, 2000). They are generally more
easily accessible for experimental approaches than higher
plant organs. In both cell types, the complete signaltransduction pathway is short and limited to the apical
region.
In positively gravitropic (downward growing) rhizoids
and negatively gravitropic (upward growing) protonemata, microtubules maintain the prominent polar
cytoplasmic zonation and organelle distribution, but they
are not present in the apex and are not involved in the
primary steps of the gravitropic signaling pathway. In
contrast, actin filaments provide the basis for a variety of
motile processes, such as cytoplasmic streaming in the
basal zone, transport of secretory vesicles to the tip, the
only growing part of the cell. Inhibitor treatments have
shown that actin also regulates the positioning of the
BaSO4-crystal-filled vesicles which serve as statoliths,
whose gravity-induced sedimentation initates the
reorientation of the growth direction in both cell types
(Sievers et al., 1979, 1991; Hejnowicz and Sievers, 1981;
Braun and Sievers, 1993).
Experiments performed on clinostats, centrifuges and
in microgravity (<10-4g) during several sounding rocket
flights (TEXUS, MAXUS) and during the Space-Shuttle
missions, IML-2 and S/MM05, have added to the
conclusion that actin and the motor protein myosin
(Braun, 1996a) are key players in the gravisensing
mechanisms (Buchen et al., 1993, 1997; Cai et al., 1997;
Braun et al., 1999; Braun, 1996b, 2002). In characean
rhizoids and protonemata, the natural position of statoliths
close to the cell tip is highly coordinated by actomyosin
forces compensating the statoliths´ weight in their original
position (Braun et al., 2002).
In this paper, we outline the results of experiments that
have been performed in microgravity, on centrifuges, on
clinostats and on ground to reveal the organization and
the function of actin and its associated proteins in the
processes of gravity-sensing and the gravity-response
mechanisms in characean rhizoids and protonemata.
Gravitational and Space Biology Bulletin 17(2) June 2004
39
M. Braun, B. Buchen, A. Sievers – Actin-Cytoskeletal Control of Gravitropic Tip Growth
CONSTANT POLYMERIZATION AND DYNAMIC
REMODELING OF ACTIN FILAMENTS IN THE
EXTENDING TIP IS FUNDAMENTAL FOR
GRAVITY SENSING AND GRAVITY-ORIENTED
POLARIZED GROWTH
In contrast to other tip-growing cell types (Geitmann
and Emons, 1999; Hepler et al., 2001), an extensive array
of distinct actin filaments is found in all regions of
rhizoids and protonemata including the continuously
extending, extreme apex. The arrangement of the actin
cytoskeleton is very similar in both cell types and reflects
the cells’ polar cytoplasmic organization. Fine actin
bundles focus in a spherical actin area in the center of the
Spitzenkörper (Braun and Wasteneys, 1998) that contains
a prominent aggregate of endoplasmic reticulum (ER)
(Bartnik and Sievers, 1988). This area is surrounded by an
accumulation of secretory vesicles. The position of the
ER aggregate defines the center of maximal growth, the
plasma membrane area at the tip, where incorporation of
cell wall material is maximal (Hejnowicz et al., 1977;
Sievers et al., 1979; Braun, 1996b).
The dynamic nature and the multiple functions of actin
in both cell types, including cytoplasmic streaming,
polarized growth, gravity sensing and gravitropic growth
responses, are regulated by the concerted action of
numerous actin-binding proteins. Experiments with actin
inhibitors and calcium ionophores have shown that the
structural integrity and the function of the Spitzenkörper
is controlled by the calcium-dependent activity of
actomyosin and a number of actin-binding proteins
(Braun and Richter, 1999; Braun, 2001). Actindepolymerizing factor (ADF), profilin and spectrin-like
epitopes are concentrated in the center of the
Spitzenkörper and colocalize with the ER aggregate.
Spectrin-like proteins are suggested to be involved in
stabilizing the cisternae of the ER aggregate by forming
crosslinks between the membranes and the actin
microfilaments. In animal cells, these proteins are also
able to provide a mechanism for recruiting specific
subsets of membrane proteins and to form microdomains
and, thus, might
help to create the particular
physiological apical conditions for the mechanism of
gravity-oriented tip growth. The accumulation of actin
monomer-binding proteins, ADF and profilin, in the
center of the Spitzenkörper indicates very high actin
turnover rates and an actin polymerizing function of this
area (Braun et al., 2003). Strong evidence comes from
cytochalasin D-induced disruption of the actin
cytoskeleton which causes a complete dissociation of the
center of the Spitzenkörper. Immunofluorescence
localization of actin, ADF, profilin and the ER aggregate
dissipate and tip growth stops. After removing the
inhibitor, the reorganization of the actin cytoskeleton
starts with the reappearance of a dense actin array in the
outermost tip. As soon as actin filaments start to radiate
out, this actin array rounds up and is repositioned in the
center of the apical dome, accompanied by the
reorganization of the ER aggregate, the reappearance of
40
Gravitational and Space Biology Bulletin 17(2) June 2004
ADF and profilin and followed by the resumption of tip
growth (Braun et al., 2003).
The results suggest that this central area of the
Spitzenkörper represents an amazingly localized apical
polymerization site for actin filaments that has not been
found in any other tip-growing cell types examined to
date. It is tempting to speculate that the complexly
coordinated actin architecture in the apex is functionally
related to the fundamental role of the actomyosin system
in the different phases of the gravitropic signaling
pathways and polarized growth.
ACTOMYOSIN FORCES KEEP STATOLITHS IN A
DYNAMICALLY
STABLE
EQUILIBRIUM
POSITION
The microgravity environment of the parabolic flights
of sounding rockets (TEXUS, MAXUS) and SpaceShuttle missions (IML-2, S/MM05), as well as simulated
weightlessness, provided by a three-dimensional and a
fast-rotating clinostat, were used to study the actincoordinated regulation of statolith positioning in both cell
types (Buchen et al., 1993; 1997; Cai et al., 1997; Hoson
et al., 1997; Braun et al., 2002). Individual acropetal and
basipetal movements of statoliths indicate that statoliths
interact with axially oriented apical and subapical actin
filaments with opposite polarities. Gravity is an additional
passive transport component that contributes to the
positioning of statoliths mainly in the statolith region
basal to the apex. When statoliths have been centrifuged
into the subapical region, a statolith retransport can be
observed that is not notably influenced by gravity (Sievers
et al., 1991; Braun and Sievers, 1993). The retransport
occurs along axially oriented actin microfilament bundles,
and statoliths do not sediment onto the lower flank until
they have reached the statolith region near the tip, where
statoliths sedimentation is not constrained by
microtubules (Braun and Sievers, 1994).
In the downward-growing rhizoids, the statoliths are
actively kept in an area 10–35 µm basal to the tip.
Actomyosin forces prevent statoliths from settling into the
tip by excerting net-basipetal forces. In upward growing
protonemata, actomyosin prevents statoliths from sedimenting towards the cell base by acting net-acropetally
(Hodick et al., 1998; Braun et al., 2002). When the
influence of gravity was abolished during the
microgravity periods of parabolic flights of sounding
rockets (TEXUS, MAXUS) (Buchen et al., 1993) and
during rotation on the three-dimensional and the fastrotating clinostat (Hoson et al., 1997; Braun et al., 2002),
actomyosin forces generated a displacement of statoliths
against the former direction of gravity. Thus, in the
statolith region of normal, vertically-oriented rhizoids and
protonemata, the statoliths are under control of
actomyosin forces that exactly compensate the effect of
gravity.
During long-term microgravity experiments without
any directing gravitational acceleration, the statoliths
became non-random within both cell types. Instead, after
an initial basipetal transport at the beginning of
M. Braun, B. Buchen, A. Sievers – Actin-Cytoskeletal Control of Gravitropic Tip Growth
microgravity, the statoliths stopped before leaving the
statolith region; they remained there or were retransported
towards their original position (Braun et al., 2002).
Displacing statoliths into other regions (except the basal
region) of the cell by centrifugation or laser-tweezers
micromanipulations resulted in an actin-mediated retransport of statoliths towards the statolith region (Braun,
2002). Thus, by acting differently in the different regions
of the cells, actomyosin forces actively control and
rearrange the original functional position of the statoliths,
where they can respond to acceleration stimuli and trigger
the gravitropic reorientation of the tip.
Figure 1. Actomyosin and gravitational forces acting on
statoliths in the different apical regions of normal vertically
oriented, inverted and horizontally positioned Chara
rhizoids (a-c) and protonemata (d-f). The gravity force is
indicated by truncated arrows, basipetal and acropetal
actomyosin forces by arrows with black and white arrowheads,
respectively. The resulting force acting on the statoliths is
indicated by the white arrows with black outlines. Brackets
indicate confined graviperception sites. The diameter of the cells
is 30 µm. Illustration was modified after Braun et al. (2002).
ACTOMYOSIN FORCES PROVIDE A SENSITIVE
GUIDING
SYSTEM
FOR
DIRECTING
SEDIMENTING STATOLITHS TO SPECIFIC
GRAVIPECEPTION SITES
The actomyosin forces acting oppositely on statoliths
in rhizoids and protonemata have important implications
on statoliths´ sedimentation. Upon gravistimulation,
statoliths are directed to distinct statolith-sensitive plasma
membrane areas, the graviperception sites. Forcing statoliths to sediment outside these areas did not result in a
gravitropic response (Braun, 2002).
Microgravity experiments (Buchen et al., 1997) and
earlier optical tweezer experiments (Leitz et al. 1995)
have shown that, in lateral direction, the statolith position
is only weakly controlled by the actomyosin system; the
force needed to move statoliths towards the apex is
greater than the force to move the statoliths towards the
flank. Thus, after reorienting rhizoids by 90o, the
sedimenting statoliths mainly follow the gravity vector
(they are slightly shifted basipetally) and settle onto the
lower cell flank of the statolith region, where
graviperception takes place and the graviresponse is
initiated. However, when cells were rotated in angles
different from 90o, statoliths did not simply follow the
gravity vector (Hodick et al., 1998). Instead, even in
inverted cells, statoliths were actively redirected against
gravity towards the small gravi-sensitive plasma
membrane area of the statolith region (10-35 µm from the
tip). Only when statoliths are fully sedimented within that
small area of the plasma membrane graviperception takes
place (Braun, 2002) leading to differential flank growth
by a locally limited reduction of the rate of exocytosis at
this site (Sievers et al., 1979).
Gravistimulation of protonemata causes an actinmediated acropetal displacement of sedimenting statoliths
into the apical dome where they sediment very close to
the tip (Hodick et al., 1998). In contrast to rhizoids, the
graviperception site in protonemata is limited to a plasma
membrane area 5-10 µm basal to the tip (Braun, 2002).
During the upward bending of protonemata, the
actomyosin system periodically allows statoliths to leave
the graviperception site - which is reflected by phases of
straight growth - before they are actively pushed back
again.
ROLE OF ACTIN AND CALCIUM IN THE
GRAVITROPIC
RESPONSE
–
THE
REORIENTATION
OF
THE
GROWTH
DIRECTION
There is experimental evidence that one major
difference between protonemata and rhizoids is the fact
that the growth center in protonemata can be easily
displaced by statoliths, which are moving by both
sedimentation and active transport. Asymmetric statolith
movement against the apical cell wall and displacement of
the Spitzenkörper occur naturally in protonemata but
require considerable centrifugal force to happen in
rhizoids. Rhizoids can be forced to respond to some
extent like protonemata, but only when centrifuged or by
pushing statoliths aymmetrically into the apical dome
with optical tweezers (Braun, 2002). There is evidence
from centrifugation experiments (Braun, 1996b; Hodick
and Sievers, 1998) and from attaching particles to the
surface of bending rhizoids (Sievers et al., 1979) that the
position of the growth center at the cell tip is relatively
stable and that the Spitzenkörper is more tightly anchored
in rhizoids than in protonemata.
The idea that the degree of Spitzenkörper anchorage is
mediated by properties of the actin cytoskeleton and the
activity of calcium-dependent, actin-binding proteins is
supported by recent experimental data (Braun and
Richter, 1999). Immunofluorescence of spectrin in
graviresponding cells labels the ER aggregate in the
center of the Spitzenkörper. The symmetrical position of
the spherical labeling pattern was drastically displaced
towards the upper flank, the site of future outgrowth,
during initiation of the graviresponse in protonemata,
clearly before curvature was recognizable by the
formation of a bulge on the upper flank (Braun, 2001). In
contrast, the same labeling in rhizoids remained
Gravitational and Space Biology Bulletin 17(2) June 2004
41
M. Braun, B. Buchen, A. Sievers – Actin-Cytoskeletal Control of Gravitropic Tip Growth
symmetrically positioned in the apical dome throughout
the graviresponse, confirming that a repositioning of the
ER aggregate is involved in the negative graviresponse of
protonemata, but not in the positive graviresponse of
rhizoids (Braun, 2001).
Figure 2. Gravitropic responses of Chara rhizoids (a) and protonemata (b). In tip-downward growing rhizoids (a), the statolith (St)
position results from net-basipetally acting actomyosin forces (Factin) compensating gravity (Fgravity). Upon reorientation, statoliths
sediment onto the lower cell flank. The Spitzenkörper (Spk) remains arrested at the tip and the calcium gradient (indicated by darker and
lighter grey dotted area) is always highest at the tip. Statolith sedimentation causes a local reduction of cytosolic Ca2+ that results in
differential extension of the opposite cell flanks (double-headed arrows). In upward growing protonemata (b), net-acropetally acting forces
mediated by the actin microfilaments (MFs) compensate gravity. Upon horizontal positioning, statoliths settle near the growth center at the
tip by gravity-induced and actomyosin-generated movements. This causes a drastic shift of the calcium gradient and then of the
Spitzenkörper towards the upper flank and the new outgrowth occurs at that site. Until the protonema reaches the upright position, the
statoliths are sporadically pushed upward towards the growth center and fall back again. The white arrows point to the area of maximal
calcium influx. MT, microtubule; Spkc, center of the Spitzenkörper.
Further evidence comes from calcium imaging, which
demonstrates a drastic shift of the calcium gradient from
the tip towards the upper flank during initiation of the
graviresponse in protonemata, but not in rhizoids (Braun
and Richter, 1999). In accordance with this observation,
dihydropyridine-fluorescence,
which
indicates
a
symmetrical distribution of putative calcium channels at
the tip of normal vertically growing cells, was also found
to be displaced towards the upper flank only in
graviresponding protonemata (Braun and Richter, 1999).
These results suggest that the early asymmetric
repositioning of the calcium gradient in protonemata may
result from statoliths-induced displacement or, more
likely, from statoliths-induced differential activation or
inhibition of apical calcium channels. The asymmetric
influx of cytosolic Ca2+ in turn may mediate the
repositioning of the Spitzenkörper and of the growth
center by differentially regulating the actin-anchorage or
the activity of actin-associated proteins along the shifting
calcium gradient.
The tendency for protonemata to reorient towards the
former growth axis after a short gravistimulation indicates
that the new growth axis induced by the upward shift of
the Ca2+ gradient is rather labile and may require actin
cytoskeletal anchorage to stabilize the new growth
direction (Braun and Richter, 1999; Braun, 2001).
Altogether, the experimental approaches reveal that actin
is fundamentally, but also very differently involved in the
positive and negative gravitropic response mechanisms.
42
Gravitational and Space Biology Bulletin 17(2) June 2004
Recent advances in molecular genetics have provided
new innovative approaches for the characterization and
identification of actin-associated proteins and other
essential components of gravitropic signaling pathways.
Molecular studies are currently under way that promise to
further increase our body of knowledge on the
cytoskeleton-mediated mechanisms of plant gravity
sensing and gravity-oriented growth responses.
ACKNOWLEDGEMENTS
We thank Christoph Limbach, Jens Hauslage and
Simone Masberg for their dedicated contributions. We are
also grateful to the crew members of STS 65 and 81, the
teams of Astrium (former ERNO, now EADS), Dornier
(now EADS), Kayser-Threde, DLR, MUSC, NASA, SSC
and ESA for their engineering contributions, their
provoking questions and inspiring conversations. This
work was financially supported by Deutsches Zentrum für
Luft- und Raumfahrt (DLR) on behalf of the
Bundesministerium für Bildung und Forschung
(50WB9998).
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