Download Cell Elongation and Revolving Movement in Phaseolus vulgaris L

Plant Cell Physiol. 39(9): 914-921 (1998)
JSPP © 1998
Cell Elongation and Revolving Movement in Phaseolus vulgaris L. Twining
Shoots
Anne-Frangoise Care, Leonid Nefed'ev, Bernard Bonnet, Bernard Millet and Pierre-Marie Badot'
Sciences Vdgetales, Laboratoire de Biologie Ecophysiologie, University de Franche-Comte, Place Leclerc, F-25030 Besancon Cedex,
France
In Phaseolus vulgaris L., the shoot displays a revolving movement that occurs rhythmically in a highly regular
manner. Previous data led to think that revolving movement is driven by turgor and volume changes in the epidermal cells of the bending zone. To document this hypothesis, the time course of in situ cell length variations in the
bending zone was measured during the movement of the
shoot and related to the phase of the revolving movement.
Each ten minutes, a photograph of cells was taken and the
revolving movement was simultaneously recorded using
time-lapse microphotography and video-monitoring. In the
moving part of the shoot, epidermal cells displayed partly
reversible length variations during their growth. Data were
processed by Fourier analysis to determine whether or not
a periodicity exists. Rhythm in cell length variations was
evidenced only when initial cell lengths were ranged between 60 and 120 fan. In this case, the period corresponds
to that of the revolving movement.
Thus, revolving movement is related to partly reversible length variations in the cells of the bending zone. These
results agree with the hypothesis of an involvement of
turgor mediated volume changes in the revolving movement.
Key words: Cell elongation — Circumnutation —
Phaseolus vulgaris L. — Revolving movement — Turgor
changes.
The French bean (Phaseolus vulgaris L.) twining
shoots display a revolving movement, usually known as a
circumnutation movement (Darwin 1865, Baillaud 1958,
Johnsson 1979). This movement takes place in the terminal
part of the shoot just below the apical bud. The moving
zone consists of a linear horizontal apical part and a curved
part. The trajectory of the apex is more or less helicoidal
(Millet et al. 1984). The period of the movement is about
90 minutes at 25°C. The direction is constant and positive
(counterclockwise).
The revolving movement occurs as a result of the bending of the upper regions of the shoot. Each time the shoot
1
To whom correspondence should be adressed. (fax 33 3 81 66 56
98, email: [email protected])
914
ceases to move, the curvature disappears. For a long time,
it was thought that the curvature was the consequence
of unequal growth on the opposite sides of the shoot
(Baillaud 1958). The side with the highest growth rate becomes convex; the side with the lowest becomes concave.
Thus, the revolving movement has usually been considered
as a growth movement. However, Millet et al. (1988) noted
a discrepancy between this theory and experimental facts.
A calculation of the required growth rate was done using
shoot geometry and the movement period. This theoretical
growth rate was compared to the measured one showing
that the daily enlargements of the bending zone are much
lower than expected. It was concluded that the revolving
movement mechanism could not be limited to rhythmic
variations in cell elongation and might involve other processes such as turgor and volume changes. Scanning electron micrographs of the bending zone showed that epidermal cells appeared fully turgid with smooth walls when
located in the convex side. On the other hand, when they
were located in the concave side, epidermal cells showed
transverse folds suggesting a lower turgor pressure. Other
observations show that the relative water content was
higher in the convex side than in the concave one (Badot
1987). Changes in osmotic potential and ion distribution
were also evidenced during circumnutation (Badot et al.
1990). These previous data imply that partly reversible cell
volume variations must be responsible for the revolving
movement. The movement cannot be restricted to a growth
phenomenon (irreversible cell volume variations), but must
involve a reversible component such as turgor-driven
changes.
Other cells are known to undergo turgor changes that
generate movement. Stomatal guard cells, for example,
display large and reversible volume variations due to
changes in cellular osmotic potential that are converted
into turgor pressure modifications (Gorton 1990, Meidner
and Bannister 1979). The leaf movement also originates
from turgor-driven volume variations of the pulvinus parts
usually denned as extensor and flexor (Mayer et al. 1985,
Freudling et al. 1988).
Estimations of cell volume changes in the bending
zone would allow us to describe the revolving movement
through the successive swelling and shrinking of cells.
Changes in cell volume can be evaluated by measuring cell
length variations. In this way, simultaneous recordings of
Cell growth and revolving movement in bean
915
cell length variations and movement could help us to evidence that revolving movement originates in partly reversible volume variations of the cells in the bending zone.
Thus, the aim of this paper is to investigate in situ cell
growth in the moving part and to measure cell length variations in the bending zone of a revolving bean shoot.
In other plant materials, estimations of variations in
cell volume were often obtained indirectly from length
measurements of shoot segments. Most of these previous
results concerned the whole plant or part of it (Michelena
and Boyer 1982, Luthen and Bottger 1992). In the same
way, Baskin et al. (1985) analyzed the elongation pattern of
small areas of maize coleoptile epidermis from time-lapse
photomicrographic records. Other workers have used more
direct ways to record cell volume changes. For example,
Omasa et al. (1983) used an image instrumentation system
to observe the stomatal response of plants to environmental changes. In this study, we intend to determine the in situ
variations of cell elongation and to establish a clear relationship between it and the revolving movement of bean
shoots.
Materials and Methods
Plant material and growth conditions—Phaseolus vulgaris
L., cv. Blanc de Juillet seeds were provided by S.P.G. (Avignon,
France). Plants were planted in 175-ml pots filled with vermiculite
and watered with tap water. They were grown under constant conditions of light (40 W m~ 2 ), relative humidity (65±5%) and temperature (25 ± 1°C) as previously described by Millet et al. (1988).
Fig. 1 A photo-micrograph of the surface of a Phaseolus
vulgaris L. bean shoot. This is a printed example of one of the negatives from which the measurements were made. The four dye
droplets delimit the three cells whose elongation was measured.
These cells are located along the same generating line (arrowheads). The horizontal bar represents 100 nm.
The plants were analyzed at the age of 12 d. At this stage of development, the shoots were 26-cm-long and the revolving movement
Fig. 2 A schematic representation of the experimental setup built to measure in situ variations of the cell length in a Phaseolus vulgaris
L. bean shoot, and to simultaneously record the apex revolving movement. 1, video camera; 2, French bean shoot; 3, green light (cold
light source); 4, colored ball; 5, horizontal inverted microscope; 6, stand; 7, micro-manipulator; 8, camera; 9, video monitor.
Cell growth and revolving movement in bean
916
had already started.
Measurement of mean cell length along the shoot—Cell
lengths were measured along the shoot of 6 different 12-day-old
bean plants. Microphotographs of illuminated cells were taken
every 1.5 cm along the 13.5 first cm of the shoot at a 250-fold
magnification (Leica, Wild MPS 48). After calibration, 50 cells
were measured at each level. Mean lengths, ± the standard deviation (SD) for p=0.05 were calculated.
Measurement of cell elongation—The bean plant was put into
a test tube so that the roots were placed in distilled water. Then,
the tube was fixed to a holder and layed on a microscope stage.
Epidermal cells in the beginning of the bending zone (6+1.5 cm
from the apex) were marked with a micro-instrument made in the
following way: a micropipette was pulled from a 1 mm outer diameter capillary with a Sutter Instruments Co. puller (Novato,
Californie, U.S.A.). Then, the tip was closed by flame so that its final diameter was about 100 fim. It was coated with a viscous dye
made up of a mix of honey and neutral red. The micropipette was
fixed on a Leitz micromanipulator and observed with a microscope at a 100-fold magnification. A dye droplet of about
in diameter was left at each end of an epidermal cell. One to three
cells were marked on the same plant (Fig. 1). Afterwards, the tube
was placed on a micromanipulator in the viewing field of a Leica
inverted microscope (Fig. 2). A black and white photograph of the
marked cells (Leica, Wild MPS 48) was taken every ten minutes at
a 40-fold magnification (objective lens magnifying 10-fold, with a
numerical aperture of 0.2 and a working distance of 2.3 cm). Time
intervals were measured with a stopwatch. To increase illumination, a cold light source (Schott Glaswerke, KL 1500, Wiesbaden,
Germany) with a green filter lit the shoot. The time course of cell
length variations was then measured using an enlarger (Durst D
659, Bolzano-Bozen, Italy) to obtain an image that was magnified
280-fold. Data calibration was carried out as follows: at the beginning and at the end of each experiment, the distance between two
droplets was measured with an ocular micrometer. The measurements of cell elongation were carried out with 38 cells, which were
from 40 to 150//m long.
Movement monitoring—At the same time, the revolving
movement of the bean shoot was monitored with a video camera
(Burle, Lancaster, U.K.) placed above the shoot. The obtained im-
Orientation of the plane
containing shoot curvature
before (a,b and d) and after
(c) device rotation
Schematic representation o(
the shoot seen in cross
section before (a.b and d)
and after (c) device rotation
Schematic representation
the same shoot after device
rotation
Orientation of the plane
containing shoot curvatun
after device rotation
<•")
(b")
(d")
Measurement of the
distance between two
dye droplets
Fig. 3 Bean shoot seen from above at the beginning of the experiment (t0), after ten (t o +10) and twenty minutes (t o +20). The shoot is
drawn in the bending zone where some cells were marked. The black point on the shoot epidermis represents a dye droplet. The half part
of the shoot seen from above and coloured in grey with a bold surface corresponds to the convex side (ex). The other is the concave one
(cv). The shoot displays a counterclockwise revolving movement. The plant is placed in the viewing field of an inverted microscope. At to,
in (a), the plane which contains the shoot curvature was perpendicular to the optical axis. In such a configuration, it was not necessary to
rotate the tube-plant device (a'). At t o +10, in (b), the convexity moved around the shoot. In order to avoid any geometrical mistake of
the distance measured between the two marks (see "Methodological precautions"), the tube-plant device was rotated (manual rotation)
to restore the perpendicular between the curvature and the optical axis (b'). The new position of the shoot was represented in (c). At t o +
20, in (d), the curvature moved again around the shoot and the tube-plant device was rotated once again to take a photograph at this
time (d'). (a"), (b") and (d") display the way to measure the distance between the two dye droplets (cell length). They show that the angle
between the optical axis of the objective and the plane which contained shoot curvature was always 90°.
Cell growth and revolving movement in bean
age was observed on a monitor (Electrohome LTD., Kitchener,
Ontario, Canada). The position of the apex was recorded on
screen every time a photograph was taken using the orthogonal
projections (Tronchet 1942). These data were digitized according
to Millet et al. (1984).
Methodological precautions—When several cells were marked
on the same shoot, they were always located along the same
longitudinal line. Before taking each photograph, the tubeplant device was rotated so that the plane, which contained the curvature, was perpendicular to the objective axis. Indeed, the bending of the plant moved the surface of interest out of the plane
perpendicular to the optical axis, and this was a source of error.
This movement caused a projection of the length to be recorded.
Figure 3 explains the geometrical relations between optical axis
and the plane containing the curvature during the measurement.
The rotation of the device allowed us to avoid any geometric
mistake of the distance measured between the two marks: this
distance was always set perpendicular to the optical axis at the time of the measurement. This implied locating the exact position
of the system at each data point before rotating. Four coloured
balls were placed on the tube and their position was systematically
noted each ten minutes. Thus, it was possible to determine the
apex relative position in relation to the tube, and therefore, in relation to the plant base even if rotations were necessary for the cell
length measurements. The recording of movement and cell elongation began after a stabilization period of ninety minutes to rule
out the disturbances due to handlings.
Mathematical data processing—The possible periodicity of
cell length variations was checked by a mathematical processing of
the data using a method adapted from Assaad (1985). First, trend
(growth) was eliminated by the least squares method. Then, data
were processed by the Fourier spectral analysis. A time form y =
f(t), where t is the time passing, was converted into a frequential
form y=f(v), where v is a time frequency. The Fourier theorem explains that a periodic function can be split up into a sine and
cosine sum for successive harmonics of the basic frequency
(Brillouin 1939):
917
different shoots are shown in Fig. 4. Signals digitized from
the revolving movement of these shoots are given in
Fig. 5a, 6a, and 7a after elimination of the trend by the
least squares method. Fig. 5b, 6b, and 7b show the signals
issued from the corresponding cell length variations after
the same mathematical treatment. The experimental conditions were in such a way that maxima in signal digitized
from revolving movement were observed when the marked
cells were located in the concavity (Fig. 5a, 6a, 7a); on the
contrary, minima were noted when these cells were located
on the convex side. Corresponding power spectra obtained
after data processing by the Fourier analysis are shown in
Fig. 5c, 6c, 7c, and 5d, 6d, 7d.
For the entire experimental duration, the 55 jum long
cell elongated in a linear way and measured 85 //m at the
end of the experiment (Fig. 4). Moreover, reversible and
transient changes in cell length were observed. They increased with time from 2fim for the four first hours and
later increased to 8 ^m. No periodicity was shown after processing by the Fourier analysis (Fig. 5d). In that case, cell
elongation displayed no rhythmicity. The period of the
corresponding shoot revolving movement was 75 min
(Fig. 5c).
In Fig. 4, another cell elongated from HO^/m to 160
/im in 8 h. As in the case of the shorter cell, its elongation
was not completely linear. The variations of cell length
were only partly irreversible and displayed oscillations. Six
cycles, and consequently 6 higher cell lengths, were recorded (lh, 2h30, 3hl0, 4h40, 6h, 7h20). Cell length was observed in relation to its position in the bending zone (con-
1
where vo=—
F(t)=Ao+ Z (An
l
The Fourier coefficients—AQ, An and Bn—represent the successive
sine and cosine amplitudes of the periodic function F(t) to the nlh
value of a whole number. These coefficients are calculated as
follows (Crawford 1972):
F(t)dt
An = 2v o l
F(t)sin 27TVontdt
for any to, value of t
B n =2v 0 (
°F(t)cos 27tV(,ntdt
K
Results are expressed in terms of a frequency spectrum that
decomposes into an amplitude spectrum a(n) and a phase spectrum (n).
I o(n) | =
x
o
si
tfn)=Arctg( - | j
Results
Representative examples for the time course of length
variations of three cells with different initial lengths (55
pm, WOfim and 140 fim) in the bending zone of three
Fig. 4 Time course of length variations for three representative
epidermal cells with different initial lengths (55 fim, 110/<m and
140/<m).
918
Cell growth and revolving movement in bean
PERIODS (min)
Ill-Ill.
••—
irt-OHi^vomiTfl-'tnnc
PERIODS (min)
Fig. 5 (a) Successive orthogonal projections of the apex movement during 8 h. (b) Time course of elongation for an epidermal cell with
an initial length of 55 //m. (a) and (b) were calculated after mathematical processing of the rough data by the least squares method (trend
out). When minima were recorded on curve (a), the marked cell was located on the convex side (dotted line), (c) and (d) The power spectra obtained from (a) and (b), respectively, after processing them with the Fourier spectral analysis.
vexity, concavity). The 110-/vm cell was longer when it was
located in the convexity (dotted lines in Fig. 6a, b). On the
other hand, in the concavity, the cell was shorter. The
shoot revolving movement occurred with a 75-min period
similar to that of cell elongation (Fig. 6c, d).
During the recording, the longer cell (140 /an) elongated linearly for the most part (Fig. 4). It measured 205 fun
after 8 h. Cell length varied with a low amplitude. In that
case, the Fourier analysis showed no periodicity for cell
length (Fig.7d), although the shoot revolving movement
completed rhythmic cycle every 80 min (Fig. 7c).
The elongation pattern of thirty-five cells on fourteen
different shoots and their corresponding revolving movement were recorded and processed in the same way as the
previous ones. The periods, when detected by the Fourier
analysis, and initial length of the corresponding cells were
reported in Fig. 8. The cells that were marked in the beginning of the bending zone measured from 45 to 150/an.
However, no rhythmicity of cell elongation was shown for
the cells between 45 and 65 fxm, and for the ones longer
than 120 fim (white circles). Cell length variations were periodic for most of the cells from 65 to 120 fim. Moreover, the
difference between the cell length variations period and the
corresponding apex revolving movement period is no
15
PERIODS (min)
PERIODS (min)
Fig. 6 (a) Successive orthogonal projections of the apex movement during 8 h. (b) Time course of elongation for an epidermal cell with
an initial length of 110 fim. (a) and (b) were calculated after the mathematical processing of the rough data by the least squares method
(trend out). When minima were recorded on curve (a), the marked cell was located on the convex side (dotted line), (c) and (d) The power
spectra obtained from (a) and (b), respectively, after processing them with the Fourier spectral analysis.
Cell growth and revolving movement in bean
§?
3 w
15-
a q
/
/
32
-5-15-
V1
i
\
/^
F\
T\
/V
/ V
\ /r V\ f\
919
?R ft
\ // \\ // \ '
V w w \/\/
1
'
3
4
1
5
i
r
PERIODS (min)
TTMEQi)
60
iL.-.i.-i.Ji-i.i.
PERIODS (min)
Fig. 7 (a) Successive orthogonal projections of the apex movement during 8 h. (b) Time course of elongation for an epidermal cell with
an initial length of 140 ftm. (a) and (b) were calculated after the mathematical processing of the rough data by the least squares method
(trend out). When minima were recorded on curve (a), the marked cell was located on the convex side (dotted line), (c) and (d) The power
spectra obtained from (a) and (b), respectively, after processing them with the Fourier spectral analysis.
greater than 15 min (black plots joined by a dotted line). A
statistical correlation was evidenced between the two kinds
of periods (correlation coefficient R 2 =0,921). Among these
twenty-one cells, only four were found to elongate in a
non-rhythmic way.
Fig. 9 allows us to estimate the mean cell length versus
the distance from the apex. Along the 11 first cms, growth
appears regular. Then, it ceases and the maximum length
statistically evaluated for the epidermal cells is 160//m. At
130
120
.=
•
*
110 -
Q
o
2
Discussion
In the course of their growth, most of the cells in the
bending zone of the bean shoot display partially reversible
length variations (Fig. 8). These changes are rhythmic. All
the cells that elongate in a partly reversible and rhythmic
way had initial lengths from 65 fim to HO^m. Otherwise,
our results show that some cells in the bending zone do not
display reversible length variations or elongate in a partially reversible, but unrhythmical way. Among these cells, we
• Cell elongation
o • Revolving movement
•
the distance chosen for cell labeling, cells are found to
measure statistically from 57±SD to 90±SD. An individual variability is observed in cell length for a particular distance from the apex. Thus, the cells randomly chosen
for cell labeling are sometimes longer or shorter than the
statistical means.
IOO.
o oooo#
*§• *
90-
E
a
80-
s
70
40
150-
60
80
100
120
140
160
INITIAL LENGTH OF CELLS dim)
Fig. 8 Periods of cell elongation (•) and shoot revolving movement (o, •) versus the initial length of the cells. Periods of the
movement represented with white circles correspond to records
without periodicity for cell length variations. Cell length and
revolving movement periods represented in black differ from less
than fifteen minutes. The dotted lines join the coupled plots corresponding to the same record.
I
t
100-
50-
DISTANCE FROM THE APEX (cm)
Fig. 9 Variations of cell length (mean ± SD; n = 50; p=0.05) versus the distance from the apex in six different bean shoots.
920
Cell growth and revolving movement in bean
find all the cells with an initial length lower than 65 #m and
higher than 110 //m. On the other hand, all the cells with initial lengths from 65 to 110/rni do not inevitably undergo
partly irreversible and/or periodic length changes. Some of
them do not exhibit any reversibility of length variations.
Others elongate in a partly reversible way but their length
changes display no periodicity. The shortest cells are preferentially located in the upper part of the shoot (Fig. 9) and
are the youngest ones. The longest cells are preferentially
found below the curvature and are statistically the oldest
ones. Thus, it seems that along the time, cells are first unable to display partly reversible length changes, then they
become able to express this behaviour when located in the
curvature. Afterwards, they lose this feature when they become older. However, individual variability of cell length
explains that some of the shortest and the longest cells
measured in these experiments may be found in the curvature. In this part of the shoot, the proportion of very
short and long cells is low as observed in data given in
Fig. 9. If we explain the twining movement by the alternative swelling and shrinking of the cells on opposite sides
of the bending zone, it seems difficult to understand how
some of these cells do not undergo any reversible nor
rhythmic length variation. In that case, no revolving movement would occur. From a methodological point of view,
we may attribute a part of these particular results to disturbances due to cell labeling. Indeed, touching cells and
epidermal hairs with a micro-instrument, even without any
visible damage, could have affected some of them and
caused a mechanical stress. This one seems to have disturbed only the reversible part of cell length variations and not
the growth. Previous experiments requiring growth measurements were usually performed with ink (Kutschera and
Kohler 1994, Pfeiffer and Kutschera 1995) or with a black
sheep hair placed directly on the coleoptile to provide a
standard length (Baskin et al. 1985). These works did not intend to record one single cell elongation in situ, but the
growth rate of shoot segments. Thus, it is not surprising
that the disturbances due to labeling did not affect the
results at the whole organ level. Moreover, the mathematical processing used in the present study is very discriminating. The Fourier analysis is strict, and therefore,
does not allow for any irregularity. It implies a number
of constraints such as a minimum and a whole number
of periods. The signal has to be as regular as possible
before processing. This could partly explain why some cells
were not found to elongate in a periodic way. For the
shortest ones, amplification of cell length variations could
be too low to have been detected by the Fourier analysis.
These methodological considerations tend to prove
that the most significant results are the rhythmic pattern in
cell elongation displayed by most of the studied cells. The
cells in the bending zone of the bean shoot show rhythmic
and partly reversible length variations (Fig. 6). Growth
oscillations have already been observed in stems or other
plant materials. Kristie and Joliffe (1986) used a high-resolution transducer system to obtain a continuous record of
stem elongation rate in seedlings of different plant species.
In most cases, they observed short period oscillations of
growth and suggested that they were caused by synchronized variations in the rate of cell elongation. Other results
deal with the so-called pulsatory growth of pollen tubes
(Derksen 1996 and references therein). After short phases
of rapid extension (10-20 s long), growth of the tubes is interrupted for long periods (up to minutes long). However,
no reversible variation in cell length was reported by these
authors. In bean shoot, the partly reversible variations of
cell length could be a key component of the revolving movement mechanism. Cell elongation on the opposite sides
of the bending zone runs in an opposite, but coordinated
way. Cells exhibit a maximum length on the convex side,
whereas they display a minimum on the concave side. Moreover, the period of the cell length variations corresponds to
that of the apex revolving movement. If reversibility occurs
in cell length variations, it means that cell elongation, i.e.
growth is not the only phenomenon involved in the revolving movement mechanisms. To explain the reversibility
component of the cell length variations pattern, we have to
take into account reversible phenomena such as turgor
variations. This fully agrees with the theoretical calculations from Millet et al. (1988) who showed that revolving
movement could not be limited to a growth movement.
Periodic volume—and therefore turgor—variations could
successively affect the cells all around the shoot in the
curvature and, thus could be partly responsible for the revolving movement of twining shoots. During one revolution, cells in the bending zone alternatively swell and
shrink. Whether or not these volume changes are due to
osmotic changes or to cell wall loosening is still unknown.
Badot (1987) measured osmotic potential on bean epidermal
strips taken from the concave and convex sides of the curvature zone and found that cell osmotic potential displayed
periodical changes. The relationships between cell volume,
turgor pressure, and osmotic potential variations are insufficiently investigated and remain unclear in our material.
Changes in cell length evidenced in twining shoots could be
correlated to concomitant variations in cell turgor as observed in sunflower hypocotyls (Kutschera and Kohler
1993). Turgor pressure is generally conceived as the driving
force for wall yielding and extension (Cosgrove 1987).
When turgor exceeds a yield threshold, cell wall extends
(Passioura and Fry 1992) and this may result in cell growth.
Previously, Millet et al. (1988) observed a stratification of
the wall in the epidermal cells of twining shoots and hypothesized that this corresponds to intense polysaccharides
deposits on microfibrils. Thus, previous and present results
are consistent to the hypothesis that revolving movement is
due to an alternative swelling and shrinking occuring in
Cell growth and revolving movement in bean
growing epidermal cells.
The present observations demonstrate that the revolving movement could be an interesting model system to investigate the relationships between cell elongation and
turgor changes. Biochemical and cytological studies have
to be undertaken to explain how the wall materials of
the cells are successively stretched then cleaved by wall-loosening enzymes. The involvement of expansins in the responses of walls and their regulation (McQueen-Mason et
al. 1992, McQueen-Mason and Cosgrove 1995, Cosgrove
1997) have also to be investigated in bean cells. On the
other hand, direct measurements of turgor pressure in the
epidermal cells of the bending zone with a pressure probe
would be the best way to confirm the present results.
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(Received September 16, 1997; Accepted June 18, 1998)