Plant Physiol. (1999) 119: 645-650
Curvature Induced by Amyloplast Magnetophoresis in Protonemata of
the Moss Ceratodon purpureus1
Oleg A. Kuznetsov,
Jochen Schwuchow,
Fred D. Sack, and
Karl H. Hasenstein*
Biology Department, University of Southwestern Louisiana,
Lafayette, Louisiana 70504-2451 (O.A.K., K.H.H.); and Department of
Plant Biology, The Ohio State University, Columbus, Ohio 43210 (J.S.,
F.D.S.)
 |
ABSTRACT |
After gravistimulation of
Ceratodon purpureus (Hedw.) Brid. protonemata in the
dark, amyloplast sedimentation was followed by upward curvature in the
wild-type (WT) and downward curvature in the wwr mutant
(wrong way response). We used ponderomotive forces induced by high-gradient magnetic fields
(HGMF) to simulate the effect of gravity and displace the presumptive
statoliths. The field was applied by placing protonemata either between
two permanent magnets at the edge of the gap, close to the edge of a
magnetized ferromagnetic wedge, or close to a small (<1 mm) permanent
magnet. Continuous application of an HGMF in all three configurations
resulted in plastid displacement and induced curvature in tip cells of
WT and wwr protonemata. WT cells curved toward the HGMF,
and wwr cells curved away from the HGMF, comparable to
gravitropism. Plastids isolated from protonemal cultures had densities
ranging from 1.24 to 1.38 g cm
3. Plastid density was
similar for both genotypes, but the mutant contained larger plastids
than the WT. The size difference might explain the stronger response of
the wwr protonemata to the HGMF. Our data support the
plastid-based theory of gravitropic sensing and suggest that
HGMF-induced ponderomotive forces can substitute for gravity.
| |
INTRODUCTION |
The force exerted by gravity is proportional to an object's
volume and density. Therefore, objects denser than the surrounding medium fall or sediment. Much evidence suggests that gravity sensing in
higher plants depends on the sedimentation of dense, starch-filled amyloplasts inside specialized cells, so-called statocytes (Sack, 1991
,
1997; Kuznetsov and Hasenstein, 1996, 1997b; Balu
ka and Hasenstein, 1997).
Dark-grown protonemata of the moss Ceratodon
purpureus are tip-growing cells that are negatively
gravitropic, i.e. they grow upward (Fig. 1). The wwr mutant
(wrong way response) of
C. purpureus is positively gravitropic, with reaction
kinetics similar to the WT (Wagner et al., 1997). In horizontal WT
(Fig. 1) and wwr protonemata, amyloplasts sediment in a
specific zone located behind the apical dome. Plastid sedimentation is
probably responsible for gravity sensing in both genotypes because it
precedes curvature and because the recovery of gravitropism after
basipetal centrifugation correlates with the return and sedimentation
of amyloplasts (Walker and Sack, 1990, 1991; Wagner et al., 1997; Sack
et al., 1998).
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| Figure 1.
Gravitropic curvature and amyloplast sedimentation
(arrowheads) in WT protonemata of C. purpureus that were
rotated from the vertical to the horizontal 4 to 5 h before
fixation.
|
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To study further the possible role of amyloplast sedimentation in
gravity sensing, it is helpful to displace amyloplasts without reorienting the cell in the gravitational field. This can be achieved by exposing cells to an HGMF, thereby inducing the intracellular magnetophoretic displacement of starch-containing plastids (Kuznetsov and Hasenstein, 1996, 1997a, 1997b).
Dense plastids such as amyloplasts and the cytoplasm differ in
their chemical composition and physical properties, including their
magnetic characteristics. When subjected to a nonuniform magnetic field, magnetically heterogeneous systems experience ponderomotive forces that depend on their relative magnetic
susceptibilities (Kuznetsov and Hasenstein, 1996). Therefore, a
magnetic field of sufficient intensity and gradient should be able to
displace plastids inside the cell and provide an excellent test for
plastid-based gravity sensing.
If gravity sensing is plastid dependent, negatively gravitropic WT
protonemata should curve toward stronger field intensities. In
contrast, wwr cells should curve toward lower field
intensities or in a positive gravitropic sense, similar to previous
experiments with positively gravitropic roots (Audus, 1960; Kuznetsov
and Kuznetsov, 1989; Kuznetsov and Hasenstein, 1996) and negatively gravitropic shoots (Schwarzacher and Audus, 1973; Kuznetsov and Hasenstein, 1997b). These experiments suggest that intracellular magnetophoresis is equivalent to plastid-based gravity sensing. However, these experiments were performed with higher plant organs, where the sites for perception and response are different, rather than
with single cells that are capable of both sensing and responding to
gravity. Moreover, the small size of moss protonemata and the availability of genotypes with opposite gravitropic responses warrants
the use of HGMFs to study the possible involvement of plastid-based
sensing in C. purpureus. If gravitropic sensing depends on
the amyloplast sedimentation, then exposure to a magnetic field should
induce both amyloplast displacement and the curvature of the tip cells
in directions that are genotype dependent.
This hypothesis was tested using several configurations to produce
magnetic fields of different intensities and geometries. We report here
that exposure to HGMF caused magnetophoretic displacement of
amyloplasts and induced curvature in both WT and wwr
protonemata in the predicted directions.
| |
MATERIALS AND METHODS |
Plant Material
WT (strain "WT3") and wwr protonemata of
Ceratodon purpureus (Hedw.) Brid. were vegetatively
propagated from stock cultures (Walker and Sack, 1990). Protonemata
were transferred onto nutrient medium overlaid with cellophane in
35-mm-diameter plastic Petri dishes (Schwuchow and Sack, 1993). The
dishes were sealed with Parafilm and the protonemata were kept in
darkness for 5 d with the surface of the agar in a vertical
position. After several days the protonemata were oriented parallel to
the agar surface due to upward growth of the WT and downward growth of
the wwr mutant. Cultures were transferred to the
experimental systems under dim green light (<2 µmol
s1 m2).
For gap experiments, we transferred 5-d-old cultures to plastic sheets
(56 × 30 × 0.8 mm) with an opening of 35 × 16 mm,
both sides of which were taped with cover glasses. Agar medium
(0.35 mL) was spread onto the inner surface of the first cover glass to
a thin film. A cellophane strip with protonemata was placed on top and
a second cover glass was taped to the frame to provide an enclosed
chamber.
For experiments with a ferromagnetic wedge, we filled plastic chambers
(24 × 8 × 4 mm) with nutrient medium and cultures on cellophane. The chamber was covered with a slitted lid to allow the
wedge to be in close proximity to the protonemata without making
contact.
We applied magnetic particles to WT and wwr cultures growing
in 35-mm Petri dishes containing growth medium; we placed the particles
on top of the agar about 4 mm from the tips of the protonemata and then
arranged the dishes vertically so that the cells would grow toward the
magnetic particles.
Magnetic Systems
We used three types of magnetic systems to generate an HGMF with
the required parameters (Fig. 2). The
first system employed an HGMF at the edge of a 1.2-mm gap between two
50- × 50- × 12.5-mm neodymium iron boron magnets that generated a
magnetic field of 8 kOe (Fig. 2A), producing a ponderomotive force for
plastids equivalent to about 0.1g (Kuznetsov and Hasenstein,
1996) directed away from the gap. The cuvette with the cultures was
inserted into the gap between the two magnets and positioned such that the protonemata were oriented parallel to the edge of the magnets (Fig.
2B) so that most protonemata were exposed to the HGMF. Control protonemata were placed either in the gap between two nonmagnetic plates or in a uniform magnetic field. Both cultures exposed to HGMF
and controls were rotated on a 1-rpm clinostat with the protonemata growing perpendicular to the horizontal axis of rotation.
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| Figure 2.
Magnetic systems generating HGMF. Bold arrows
indicate the direction of force acting on diamagnetic substances. A,
HGMF at the edge of a gap between two magnets or magnetic poles repels
diamagnetics from the gap. The dispersion of the magnetic field at the
edge of the gap between two magnets results in a decrease of field
intensity. The field in the depth of the gap reached 8 kOe, the dynamic
factor  (H2/2) at the edge of the gap was estimated to be
5.3 × 108 Oe2 cm1
(Kuznetsov and Hasenstein, 1996). B, Position and the predicted
curvature of wwr protonemata near the edge of the gap
between two magnets. C, The field in the vicinity of a ferromagnetic
wedge between two magnets concentrates the field near its protruding
edge such that LH is directed toward the edge. Therefore, diamagnetic
plastids experience a force that is directed away from the wedge.
L(H2/2) in close proximity of the edge can exceed
1010 Oe2 cm1. D, Relative
position of the magnetized wedge and protonemata with the projected
curvature of the WT. E, Gradient of the field around a spherical magnet
is directed toward the particle, hence diamagnetic particles will be
repelled from it. Near a small (<1 mm) but strong magnet, the dynamic
factor of the field L(H2/2) can exceed 109
Oe2 cm1.
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The second system (Fig. 2C) used a ferromagnetic wedge that was
magnetized by a uniform magnetic field (4.5 kOe) in an 8-mm-wide gap
between two permanent magnets (see Kuznetsov and Hasenstein, 1996,
1997b). The dynamic factor (H2/2) of HGMF
around the wedge tip was approximately 109 to
5 × 1010 kOe cm1
within the cylinder of a diameter of 0.2 to 0.3 mm around and along the
edge of the wedge and generated a force on plastids of about
1g. Outside this volume, the dynamic factor of the field decreased by 2 orders of magnitude over the next 1 mm. A
nonferromagnetic, plastic-coated brass wedge of the same shape was used
as a control. Chambers containing the protonemata were mounted in the
gap between the two magnets so that the filaments were oriented
parallel to and in close proximity to the wedge edge (Fig. 2D). The
magnets with the cultures were rotated on a 1-rpm clinostat with
protonemata oriented perpendicular to the horizontal axis of rotation.
The third configuration (Fig. 2E) used small permanent magnets
(SmCo5, diameter < 0.6 mm) coated with
plastic or nonmagnetic brass particles as controls. The protonemata
were allowed to grow toward the particles without clinorotation. The
experiments were terminated by fixing the cultures after the
protonemata reached the vicinity of the particles.
Documentation
Protonemata were fixed in darkness for 45 to 90 min by dropwise
application of fixative (1% paraformaldehyde, 2% glutaraldehyde, and
5 mM CaCl2 in 50 mM
sodium cacodylate buffer, pH 7.1). Starch was stained with IKI (1%
iodine in 2% potassium iodide) and cells were photographed on a light
microscope. The negatives were digitized and the tip angles were
measured using the Optimas image analysis program (version 5.2, Media
Cybernetics, Silver Spring, MD). All possible cells within 0 to 0.6 mm from the wedge were measured and average values (±SE)
were calculated for 0 to 0.2, 0.2 to 0.4, and 0.4 to 0.6 mm.
Determination of Amyloplast Size and Density
We isolated the intact plastids from 5- to 6-d-old dark- and
light-grown protonemata, and determined their density by centrifugation in metrizamide solutions (Kuznetsov and Hasenstein, 1997a). We used
microscopy to find the diameter of the IKI-stained amyloplasts.
| |
RESULTS |
Magnetophoretic Curvature of WT and wwr Mutants
Cultures exposed to an HGMF and rotated on a clinostat showed both
amyloplast displacement and curvature (Fig.
3). WT cells curved toward the HGMF and
wwr cells curved away from it, in the direction of
amyloplast displacement (Fig. 3, compare with Fig. 2B). The angles of
curvature of cultures exposed to the HGMF in the gap for 12 (WT) and
15 h (wwr) were 41% and 40%, respectively, of the
curvature of the controls after horizontal orientation for the same
time period (Fig. 4).
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| Figure 3.
Photographs of clinorotated protonemata in the
gap. Bars = 50 µm. In A to D the direction of the magnetic force
is toward the bottom of the micrographs. The arrowheads in B to D
indicate HGMF-induced amyloplast displacement. A, wwr
cells curving toward the outside of the gap after 24 h in the
HGMF, in a pattern similar to Figure 2B. B, WT protonema curving toward
the inside of the gap after 12 h in the HGMF. C,
wwr tip cell in the gap for 6 h. D,
wwr tip cell in the gap for 5 h. E,
wwr control cell inside the gap between the magnets for
5 h. Cells were exposed to a uniform magnetic field (about 8 kilo-oersteds), but not to an HGMF. Plastids were distributed
symmetrically around the longitudinal axis of the cell and no curvature
was observed. F, WT control cell after 12 h outside the gap, away
from an HGMF. No lateral amyloplast displacement or curvature occurred.
Fm, magnetic force.
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| Figure 4.
Curvature of WT and wwr protonemata
after magnetophoresis or gravistimulation. After 8 h the curvature
in the wedge system equaled that of protonemata that were
gravistimulated for the same time period. The HGMF-induced curvature
(stippled bars, 8 h WT) decreased with the distance from the wedge
edge (bar a, 0-0.2 mm; bar b, 0.2-0.4 mm; bar c, 0.4-0.6 mm). The WT
control was rotated on a clinostat (1 rpm) without a magnetic field.
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In both the WT and wwr protonemata, tip-cell amyloplasts
were displaced toward the outside of the gap (arrowheads in Fig. 3,
B-D, direction of arrow in Fig. 2A). HGMF-induced plastid displacement occurred in the same subapical sedimentation zone where amyloplast sedimentation occurred after a 90° reorientation in the gravity field
(Fig. 1). Although cells exposed to an HGMF exhibit opposite curvature
in WT and in wwr, the direction of plastid displacement is
the same, emulating the gravitropic phenotypes of the WT (Fig. 1) and
the wwr cells (Wagner et al., 1997). However, the extent of
amyloplast displacement by HGMF was less obvious compared with the
horizontally placed controls, presumably because of a weaker force
acting upon the plastids. This force was estimated to be only
0.1g.
Controls inside the gap in the area of homogenous field density showed
no plastid displacement or curvature (Fig. 3E). Controls rotated on a
clinostat in the absence of a magnetic field also showed no
preferential curvature or lateral displacement of plastids (Fig. 3F).
The angles of tip cells from controls rotated on a clinostat exhibited
much greater variability than vertical, stationary controls, regardless
of the presence or absence of a magnetic field.
As in gap experiments, exposure of protonemata to a magnetized wedge
also induced curvature. wwr protonemata close to the edge
curved away from the wedge (data not shown), and WT cells curved toward
the wedge (Figs. 2D and 5A). The extent of curvature increased with the
proximity of protonemata to the wedge (Fig. 5A), so that some WT protonemata not only
curved on the plane of the agar, but upward, away from the
agar surface toward the wedge. The angle of curvature of WT cultures
exposed to the HGMF in the area less than 0.2 mm from the wedge (where
the ponderomotive force is comparable to gravity) was similar to the
curvature of the controls that were kept horizontally for the same time
period (Fig. 4). The curvature of protonemata decreased with
increasing distance from the wedge edge to negligible values at
distances greater than 0.4 mm (Fig. 4). Controls placed near a
nonmagneticwedge showed neither lateral amyloplast displacement nor
curvature.
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| Figure 5.
Protonemata growing in the presence of magnetized
wedges and magnetic and nonmagnetic particles. A, WT cells exposed to
an HGMF for 8 h on a clinostat curve toward the wedge from both
sides, as in Figure 2D. The projection of the wedge edge is shown as a
long, horizontal line. Note that curvature decreases with increasing
distance from the wedge edge. B, WT protonema curving around a magnetic
particle. The protonemal culture was not clinorotated and curvature is
thus the result of the magnetic force and gravity. C, Control
wwr protonemata grow downward and are not influenced by
the presence of a nonferromagnetic, brass particle. Arrows in B and C
indicate the g vector. Bars = 200 µm.
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HGMF derived from magnetic particles also induced curvature. Dark-grown
tip cells of WT protonemata curved toward the magnetic particle (Fig.
5B) and eventually grew around it. Nonmagnetic particles did not induce
curvature (Fig. 5C).
Density and Size Distribution of Plastids
The densities of IKI-stained plastids isolated from WT and
wwr protonemal mats ranged from 1.24 to 1.38 g
cm3 and 1.26 to 1.38 g
cm3, respectively. In contrast, amyloplasts
from flax, corn, barley, and tomato showed a narrower range of
densities (1.36-1.39 g cm3 [Kuznetsov and
Hasenstein, 1997a]). The larger density range indicates higher
variability in plastid composition of moss plastids. The densities of
plastids from light-grown WT and wwr cells did not differ
measurably from those of dark-grown cultures.
The diameter of plastids from WT and wwr protonemata ranged
from 1 to 5 µm (Fig. 6). The average
diameter (±SE) of dark-grown wwr
plastids (1.97 ± 0.03 µm) was slightly larger than that of WT
plastids (1.74 ± 0.03 µm).
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| Figure 6.
Distribution of sizes of amyloplasts isolated from
WT (open) and wwr (stippled) mutant protonemata.
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| |
DISCUSSION |
This study shows that an HGMF induces protonemal curvature and
amyloplast displacement that mimics gravitropism in the moss C. purpureus. Such effects can be attributed to the ponderomotive force rather than to the presence of a magnetic field, because protonemata failed to curve in a uniform magnetic field. These data
provide significant support for plastid-based gravitropic sensing in
C. purpureus. The pattern of magnetophoretic displacement was comparable to the location of amyloplast sedimentation in horizontal tip cells of C. purpureus (Walker and Sack,
1990).
Amyloplasts were displaced away from the HGMF in both the WT and
wwr mutant protonemata, yet the WT curved toward the field and wwr curved away, similar to the direction of gravitropic
curvature in both genotypes (Wagner et al., 1997). Thus, exposure to
magnetic gradients does not impede the directionality of the growth
response. Because amyloplasts were likely to be the major intracellular component displaced by the HGMF and because this displacement correlates with the correct sense of curvature for each genotype, our
data strongly suggest that amyloplast displacement is important for
gravity sensing.
Despite the correct direction of curvature, the extent of curvature due
to the HGMF in a gap system was less than gravity-induced curvature for
a comparable period of exposure (Fig. 4). This is probably due to the
reduced force of approximately 0.1g that is experienced by
the plastids. Because the HGMF-induced force in a wedge system can
reach 1g within less than 0.3 mm of the wedge, the rate of
curvature should be stronger than in the gap system. This reasoning is
confirmed by the stronger curvature obtained from 8 h in the wedge
system compared with the curvature after 12 h in the gap design
(Fig. 4). The stronger curvature in the more effective HGMF suggests
that gravitropic sensing relies on a force exerted by amyloplasts on
some structure. The gravitropic receptor in moss protonemata is
unknown, but candidates include the ER and microtubules (Schwuchow et
al., 1990; Walker and Sack, 1995; Sack et al., 1998).
The importance of a force exerted by plastids is also supported by the
more reliable and stronger response of the wwr protonemata compared with the WT (Fig. 4). Although plastid density was comparable in the two genotypes, wwr protonemata contained more and
13% larger amyloplasts than the WT. The size difference suggests that
the forces produced by the displacement of amyloplasts by HGMF would be
stronger in wwr than in WT protonemata. This observation
conflicts with data showing that WT and wwr protonemata
respond gravitropically at the same rate (Wagner et al., 1997), and
suggests a rate-limited response mechanism in either system for a
1g stimulus. The differential response to HGMF may be due to
a reduced force that did not saturate the sensing mechanism. The
difference in the directions of curvature of WT and wwr
protonemata probably resulted from transduction events downstream of
sensing rather than from differences in the mechanism of sensing itself
(Wagner et al., 1997; Sack et al., 1998).
An alternate hypothesis of gravitropic sensing is based on pressure
exerted by the mass of the entire protoplast on tension- or
compression-sensitive components of the plasma membrane and cell wall
(Wayne et al., 1992; Staves et al., 1997). If this hypothesis were true
for moss protonemata, then an HGMF should produce curvature in the
direction opposite to that observed. The polysaccharide-rich cell wall
has a magnetic susceptibility comparable to starch. The cell itself
(the protoplast) has a much lower magnetic susceptibility because most
of its volume is filled with cytosol, which has a magnetic
susceptibility close to that of water (Audus, 1960). Thus, an HGMF
would repel the cell wall more than the cell, and the cell membrane
would be compressed to the cell wall closer to the HGMF and would be
under tension on the side away from the HGMF. If the pressure of the
cell mass functioned in gravitropic sensing, then the WT should curve
toward the weaker part of the field (away from the gap), and the
wwr mutant should curve toward the inside of the gap.
However, Kuznetsov and Hasenstein, (1996, 1997b) found the reverse in
this and previous studies using roots and shoots of higher plants.
In experiments with magnetic particles, the moss protonemata were
exposed to an HGMF and gravity field without clinostat rotation. The
protonemata did not curve toward the particle but curved around it,
presumably because of an equilibrium between the stimuli of gravity and
ponderomotive forces. As the protonema leaves the vicinity of the
magnetic particle, the HGMF weakens and the tip begins to curve upward
(Fig. 5B). Because magnetophoresis initiated strong curvature and
because the HGMF repelled the amyloplasts, the results from the
particle studies also support plastid-based rather than
whole-cell-based gravity sensing.
Collectively, these HGMF data extend previous evidence consistent with
the importance of the plastid mass in gravitropic sensing in moss
protonemata (Sack et al., 1998) and in higher plants (Sack, 1991,
1997). Our work also shows that an HGMF can substitute for gravity in
inducing differential growth in a single cell.
| |
FOOTNOTES |
1
This research was supported by the National
Aeronautics and Space Administration (grant nos. NAG10-0179 to F.D.S.
and NAG10-0190 to K.H.H.).
*
Corresponding author; e-mail hasenstein{at}usl.edu; fax
1-318-482-5834.
Received July 29, 1998;
accepted October 25, 1998.
| |
ABBREVIATIONS |
Abbreviations:
HGMF, high-gradient magnetic field.
Oe, oersteds.
WT, wild-type.
| |
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Top
Abstract
Introduction
