Download Gravitropism in Leaves of Arabidopsis thaliana (L.) Heynh.

Plant Cell Physiol. 47(2): 217–223 (2006)
doi:10.1093/pcp/pci237, available online at www.pcp.oupjournals.org
JSPP © 2006
Gravitropism in Leaves of Arabidopsis thaliana (L.) Heynh.
Eriko Mano 1, Gorou Horiguchi 2, 3 and Hirokazu Tsukaya 1, 2, 3, 4, 5, *
1
Department of Biosystems Science, School of Advanced Sciences, The Graduate University for Advanced Studies, Shonan Village, Hayama,
Kanagawa, 204-0193 Japan
2
Department of Basic Biology, School of Life Science, The Graduate University for Advanced Studies, Shonan Village, Hayama, Kanagawa, 2040193 Japan
3
National Institute for Basic Biology/Okazaki Institute for Integrative Bioscience, 38 Nisigonaka, Myodaiji, Okazaki, Aichi, 444-8585 Japan
4
Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, 606-8502 Japan
;
Roberts and Gilbert 1992, Poff et al. 1994, Kaufman et al.
1995).
Gravity perception is generally associated with the sedimentation of amyloplasts located in starch sheath cells that
surround the phloem in shoots (Fukaki et al. 1998, Moctezma
and Feldman 1999, Kiss 2000, Weise and Kiss 1999) and in
cells of the root cap (Sack 1991). Studies of the model plant
Arabidopsis thaliana (L.) Heynh. (Arabidopsis, hereafter) have
supplied vast knowledge on the mechanisms of gravitropism in
stems and roots from mutational analyses (Okada and Shimura
1992, reviewed by Fukaki et al. 1996a, Tasaka et al. 1999,
Terao-Morita and Tasaka 2004).
The graviresponse is not always independent of other
environmental factors in plants. Light is known to modulate
gravitropism in roots, stems, apical hooks and secondary stems
(Myers et al. 1994). For example, red light induces positive
gravitropism in the roots of Zea mays L. variety Merit, which is
mediated exclusively by phytochrome (Feldman and Briggs
1987). Gravitropism is enhanced by red light in various plant
species (Brits and Galston 1982, Woitzik and Mohr 1988).
However, the gravicurvature of pea epicotyls decreases with
red light irradiation (McArther and Briggs 1979).
Like other organs, leaves also respond to various environments (e.g. Kozuka et al. 2005, reviewed in Kim et al. 2005,
Tsukaya 2005). However, our knowledge on the nature or
mechanism of gravitropism in leaves is lacking. Indeed, we
have little knowledge of how leaves position the angle of the
leaf petiole relative to the shoot axis, which appears to vary
among species. For example, leaf petioles of Oxalis corniculata
L. elongate parallel to the direction of gravity (our preliminary
observations), while those of Arabidopsis show a typical rosette
form, expanding radially and parallel to the ground plane.
Moreover, how the rosulate form of leaf arrangement is controlled in such rosette plants is not well understood. How is the
positioning of leaves determined? Is gravitropism responsible?
To answer these questions, we analyzed the response of
rosette leaves in Arabidopsis by changing the direction of
gravity against the axis of the plant, as a first step toward
understanding gravitropism in leaves.
In higher plants, stems and roots show negative and
positive gravitropism, respectively. However, current
knowledge on the graviresponse of leaves is lacking. In this
study, we analyzed the positioning and movement of rosette
leaves of Arabidopsis thaliana under light and dark conditions. We found that the radial positioning of rosette leaves
was not affected by the direction of gravity under continuous white light. In contrast, when plants were shifted to
darkness, the leaves moved upwards, suggesting negative
gravitropism. Analysis of the phosphoglucomutase and
shoot gravitropism 2–1 mutants revealed that the sedimenting amyloplasts in the leaf petiole are important for gravity
perception, as is the case in stems and roots. In addition,
our detailed physiological analyses revealed a unique feature of leaf movement after the shift to darkness, i.e. movement could be divided into negative gravitropism and
nastic movement. The orientation of rosette leaves is
ascribed to a combination of these movements.
Keywords: Amyloplast — Arabidopsis thaliana — Gravitropism — Petiole — Shoot axis dependent.
Abbreviations: N-position, normal position; R-position, reversed
position.
Introduction
Plants respond sensitively to many environmental stimuli,
such as light, temperature, nutritional conditions and gravity.
Such environmental responses are exhibited as plasticity of
growth and development, and different organs exhibit different
responses to given environmental stimuli. For example, stems
show negative gravitropism, whereas roots show positive
gravitropism in general. Additionally, lateral branches and lateral roots demonstrate plagiogravitropism, and stolons show
diagravitropism (Stockus 1994). The gravitropic response
mechanism can be separated into three steps, i.e. gravity perception, signal transduction and asymmetric growth response
by differential cell elongation (Feldman 1985, Pickard 1985,
5
*
Present address: Graduate School of Science, University of Tokyo Science Building #2, 7-3-1 Hongo, Tokyo 113-0033 Japan.
Corresponding author: E-mail, [email protected]; Fax, +81-564-55-7512.
217
218
Gravitropism in leaves of Arabidopsis thaliana (L.) Heynh.
Fig. 1 Position of rosette leaves under
continuous light. Plants grown for 4
weeks in a normal position (A), and after
a 90° rotation (B) or inversion (C) under
continuous light. An arrow shows the
direction of gravity. Light was irradiated
from omnilateral directions. Note the
transparency of the medium on which
plants were grown.
Results
Positioning of leaves is stable in Arabidopsis
First, we examined whether the positioning of rosette
leaves is dependent on gravity, by growing plants in an inverted
position or rotated 90° under continuous light conditions. As
shown in Fig. 1, the positioning of the rosette leaves, in terms
of the angle of the leaf petioles against the shoot axis, was not
affected even after 4 weeks of the repositioned cultivation. All
five individuals examined maintained the radial pattern of leaf
arrangement, irrespective of the difference in the direction of
gravity against the axis of the plant shoot (Fig. 1). Thus, we
concluded that the rosette arrangement of the leaves was regulated in a gravity-independent and shoot axis-dependent manner under continuous light conditions.
the leaves reached a plateau at 9 h after the shift to darkness
(Fig. 3, open circles). Thus, the treatment period was fixed for
9 h of dark adaptation for further analysis. Then, we analyzed
age dependency in the response of the first pair of true leaves
against the dark shift treatment (data not shown). We found that
14-day-old seedlings were suitable for further analysis since
the first pair of true leaves at this stage responded well to the
dark treatment and were large enough to capture the clear
images of petioles. Fig. 4 shows the changes in the angle
between the first pair of true leaves in response to changes in
light condition. When 14-day-old plants were shifted to
Leaf movement under dark conditions
Do leaves not exhibit gravitropism at all? When
Arabidopsis plants are placed in darkness, the petioles of
rosette leaves bend upwards (Hangarter 1997). A typical example of such leaf movement is shown in Fig. 2. In darkness, the
petiole bent up at its proximal part rather than along the entire
petiole axis. This phenomenon could be interpreted as negative
gravitropism of the leaves. Alternatively, it could be considered gravity-independent, nastic movement parallel to the shoot
axis. We analyzed darkness-induced leaf movement in detail. A
kinetic study on 21-day-old plants showed that movement of
Fig. 2 Movement of rosette leaves after a shift to darkness. (A)
Before shift to the dark condition. (B) At 9 h after shift to the dark
condition. Bars represent 5 mm.
Fig. 3 Time course of dark-induced leaf movement. Plants were
shifted to darkness in a normal position or an inverted position, and
photographs were taken every 30 min after the shift. Open circles
show mean data for plants in a normal position; black circles show
mean data for upside-down plants. As depicted in the insert, movements of leaves relative to the position of leaves at zero time were
measured. Leaf movements toward or away from the shoot axis are
expressed as positive and negative angles, respectively. The vertical
error bars represent the SE. More than nine plants were examined for
each group.
Gravitropism in leaves of Arabidopsis thaliana (L.) Heynh.
Fig. 4 Time course of leaf movement in response to multiple dark
treatments. Wild-type plants were grown under continuous white light
for 14 d and shifted to darkness in a normal position for 9 h (dark 1).
These plants were returned to continuous light and grown for 24 h
(light). After that, plants were shifted to darkness again (dark 2). In
each condition, photographs were taken every 1 h. As depicted in the
inset, the angle between the first pair of true leaves was measured. Vertical error bars represent the SE (n = 3).
darkness, the leaves bent up. After 9 h of dark treatment, these
plants were shifted to the light condition and grown for 24 h.
During this light treatment, the leaf angle returned to the initial
position. When these plants were again shifted to darkness,
leaves bent up over the 9 h of dark treatment. This repeatable
leaf movement seems to be independent from circadian rhythm,
since the second dark treatment in Fig. 4 is out of 24 h phase.
Gravitropism of leaves
As shown in Fig. 2–4, Arabidopsis wild-type leaves were
confirmed to move after being placed in the dark. Plants were
placed upside-down under dark conditions to determine
whether the darkness-induced movement of rosette leaves was
based on gravitropism. When plants were put in a normal position (hereafter, N-position), the difference in the angle before
and 9 h after the dark treatment was about 23°, while the difference in the angle was only about 15° for plants that were
placed upside-down (hereafter, R-position, Fig. 3). Since in
both the N- and R- positions, leaves were bent against the
direction of gravity, this movement is very likely to have
resulted from gravitropism. However, the extent of leaf
movement in the R-position is smaller than that in the N-position, suggesting that a movement toward the shoot axis counteracted the gravity-dependent movement. Therefore, the
observed movement of leaves in darkness can be divided into
negative gravitropism and nastic, gravitropism-independent
219
movement of the leaves (see Fig. 5D). Moreover, our kinetic
analysis showed that leaf movement began just after the shift to
darkness for plants in the N-position, but the start of the
movement was retarded by approximately 5 h after the shift to
darkness for the R-position (Fig. 3). These differences in the
kinetics of movement between plants in the N-position and
R-position may reflect differences in the nature of darknessinduced movements of leaves. In other words, darknessinduced movements of leaves appeared to be the sum of nastic
movement parallel to the shoot axis that starts just after the
dark shift and negative gravitropism that starts slightly later
than the nastic movement (Fig. 5D).
Next, to determine whether the mechanism of the graviresponse of leaves was the same as that of shoots and roots, we
compared darkness-induced behavior in leaves of two mutants
with a defect of gravitropism, phosphoglucomutase (pgm) and
shoot gravitropism 2–1 (sgr2-1), that had defects in phosphoglucomutase and a phospholipase-like protein, respectively, with that of wild-type Arabidopsis. In this experiment,
14-day-old wild-type, pgm and sgr2-1 were placed in the N- or
R-position with or without light for 9 h. The angles between
the first pair of true leaves were measured after the treatments
(Fig. 5). First, in any plant lines, statistical differences between
N- and R-positions were not found under the light condition
(compare white and hatched bars). In contrast, the dark treatment induced leaf movement toward the shoot axis in wild type
(compare white and gray bars). As expected from Fig. 3, the
dark treatment of the wild type in the R-position results in a
wider petiole angle than that in the N-position (compare gray
and black bars), suggesting that axis- and gravity-dependent
movements counteracted each other. Consistently, the difference in petiole angles between the N- and R-position under
darkness was smaller in the pgm mutant than in the wild type
(approximately 30° and 13° in wild type and pgm, respectively, Fig. 5A, B), indicating that effective petiole movement
against the direction of gravity requires functional phosphoglucomutase activity that is required for full development of
amyloplasts. This result also corroborates the idea that the
darkness-induced movement of Arabidopsis leaves can be
divided into negative gravitropism and nastic movement parallel to the shoot axis.
Similarly, inflorescence stems of the sgr2-1 mutant did
not respond to gravity due to a defect in the signaling of the
graviresponse (Fukaki et al. 1996a, Fukaki et al. 1996b). We
observed that sgr2-1 showed a defect in sedimentation of
amyloplasts in the petiole (Fig. 6F). As shown in Fig. 5C, the
sgr2-1 leaves also bent upwards after a shift to darkness, but
the angles of the N- and R-positions in the dark were not statistically different from each other, suggesting again that the difference in the angle between the N- and R-positions in wildtype leaves is attributable to gravitropism in the leaves.
Finally, we checked if petiole cells have sedimenting
amyloplasts, since amyloplasts play a central role in gravity perception in stems (Fukaki et al. 1998, Moctezma and Feldman
220
Gravitropism in leaves of Arabidopsis thaliana (L.) Heynh.
Fig. 5 Leaf movement in the wild type
(A), pgm mutant (B), and sgr2-1 mutant
(C). Two-week-old light-grown plants
were kept in a normal position (N) or
reoriented upside-down (R) for 9 h with
or without light irradiation. The angle
between the first pair of true leaves was
measured as described in Fig. 4. Vertical
error bars represent the SE (n ≥ 10). (*)
indicates a significant statistictical difference by t-test ( P < 0.05) between the Nand R-position angle for the same light
condition. (#) indicates a significant statistic difference by t-test (P < 0.05)
between the light and dark N-position
angle or R-position angle. (D) Schematic model of leaf movement under
dark conditions (see text for details).
1999, Kiss 2000, Weise et al. 2000) and root cap (Sack 1991).
In the wild type, amyloplasts were observed only in the few
cell layers of cells around the main vasculature of leaves. In the
proximal region of the petiole, amyloplasts were sedimented
according to the direction of gravity (Fig. 6A, C). In the distal
region of the petiole, they were not sedimented but dispersed
(Fig. 6B, D). The pgm mutant lacks starch in all tissues, and
inflorescence stems showed only a weak response to gravity
(Weise and Kiss 1999). We confirmed that the pgm mutant also
lacked starch in the leaf petioles (Fig. 6E) and that amyloplasts
were dispersed within the petiole cells of the sgr2-1 mutant
(Fig. 6F). Thus, the reduced petiole movement against the
direction of gravity in the pgm and sgr2-1 mutants (Fig. 5) correlated with the absence or abnormal distribution of amyloplasts. Similarly, the occurrence of sedimenting amyloplasts in
the proximal but not in the distal part of wild-type petiole correlated with the site of petiole bending (i.e. proximal part, Fig.
2). This suggests that sedimenting amyloplasts in the cell of the
proximal region of the petiole play an important role in gravity
perception.
Discussion
Characteristics of leaf movement in Arabidopsis thaliana
In this study, we analyzed the behavior of leaves under
various environments, and revealed several new findings. First,
we showed that Arabidopsis leaves exhibited little graviresponse under continuous light, and that the leaves expanded
radially perpendicular to the axis of the shoot (Fig. 1). This fact
shows that the ‘rosette’ form of radial leaf arrangement does
not depend on gravitropism, but is determined in a shoot axisdependent manner.
However, when plants were shifted into darkness, the
position of the leaves was altered, as noted previously by
Hangarter (1997). This movement of leaves could have been
gravity-independent nastic movement and/or nyctinasty. Our
results, however, strongly suggest that the observed leaf movement was the sum of the shoot axis-dependent and gravitydependent movements. Under dark conditions, the angle of the
leaves against the shoot axis was decreased in a manner of nastic movement and, simultaneously, the leaves showed negative
gravitropism independent of the nastic movement (Fig. 5D).
This is a very interesting aspect of leaf movement, and the
rosette arrangement of Arabidopsis leaves may be realized by
Gravitropism in leaves of Arabidopsis thaliana (L.) Heynh.
221
Fig. 6 Amyloplasts in leaf petioles.
Leaf petioles of wild type: (A) and (B)
are the leaf petiole of the basal part and
leaf blade side, respectively; (C) and (D)
are amyloplasts in the cell of (A) and (B),
respectively. (E) and (F) are the cells of
the petiole of the basal part in the pgm
and sgr2-1 mutants, respectively. Bars in
(A) and (B) represent 100 µm, and those
in (C), (D), (E) and (F) represent 50 µm.
An arrow shows the direction of gravity.
the suppression of the above two movements by light. Given
that the stem generally shows negative gravitropism, it seems
natural that leaves, which, like stems, are derived from the
shoot apical meristem, have fundamentally the same negative
gravitropism as stems. In the future, it is necessary to perform
experiments of the hypergravity or hypogravity condition to
understand the relationship between leaf movement and gravity further in detail. We will discuss our present understanding
on this matter in the following paragraphs.
To date, only a few attempts have been made to describe
the graviresponse of leaves, and the results were contradictory
between different studies. For example, Hangarter (1997)
found that when light-grown Arabidopsis seedlings were tilted,
leaves were reoriented toward the horizontal direction, as
opposed to the result shown in Fig. 1. This difference could be
attributable to the differences in the growth condition, such as
unidirectional (Hangarter’s experiment) or multidirectional
light illumination (our experiment) or the use of seedlings
grown on opaque soil (Hangerter’s experiment) or on transparent gel (our experiment). On the other hand, Millenaar et al.
(2005) found that tilting the plants 90° downward for several
days did not induce clear petiole movements. This result is
consistent with our observation that gravity-dependent movement is suppressed under light conditions (Fig. 1, 5). Millenaar
et al. (2005) also found that ethylene induces upward bending
of petioles in the light condition. This movement is similar to
that induced by the dark treatment in our study, in relation to its
kinetics and repeatable nature (see below). Interestingly, the
extent of ethylene-induced movement of petioles was little
affected when plants were tilted about 20–30°. Based on these
observations, Millenaar et al. (2005) proposed that hyponasty is
not a readjustment by the leaves to a preferred angle relative to
gravity. In light of our finding that the leaf movement induced
by dark treatment could be divided into negative gravitropism
and nastic movement, the petiole movements induced by
ethylene in the light condition might correspond to the nastic
movement in the dark while negative gravitropism is still
suppressed. The relationship among light, ethylene, nastic
movement and gravity-dependent movement is an important
issue to be addressed in the future.
Is the nastic part of leaf movement nyctinasty? Shifts to
dark conditions may have triggered circadian leaf movement as
reported by Engelmann et al. (1992). However, the circadian
period of the leaf movement has been reported to be approximately 24 h (e.g. Onai et al. 2004). Also, in our system, the
periodical bending up movement of leaves from the lowest to
the highest position takes about 12–14 h under continuous
light, nearly half of the circadian period (data not shown). This
is longer than the observed period required for movement of
leaves to reach a plateau (9 h, Fig. 3). In addition, when we
shift the plants that had bent up their leaves in response to
darkness to continuous light and left them to grow for 24 h, the
leaf angle returned to the initial position. These leaves
responded to a second shift to darkness for 9 h (Fig. 4). Thus,
regardless of expected circadian rhythm that would repeat a
24 h cycle, the leaves bend up whenever they are shifted to
222
Gravitropism in leaves of Arabidopsis thaliana (L.) Heynh.
darkness. These results suggest that the observed leaf movement in response to a shift to darkness is a repeatedly inducible, short-term reaction and may differ from long-term
circadian movements or nyctinasty.
Light-dependent control of the graviresponse has also
been reported for roots and stems (e.g. Brits and Galston 1982,
Feldman and Briggs 1987, Robson and Smith 1996, Correll et
al. 2003). In terms of the light-controlled nature of the movement, the leaf is not unique. However, in contrast to roots and
stems, we revealed that leaf movement in darkness is the sum
of two completely different movements. These features have
retarded the discovery of the unique nature of leaf movement.
Further analyses of the effects and perception of light on the
suppression of leaf movement are currently in progress.
Gravity perception in leaves
The starch–statolith hypothesis, i.e. the idea that starchcontaining amyloplasts function as statoliths in gravity perception, has been strongly supported by a variety of experimental
approaches in various plant species (Kiss et al. 1989, Sack
1997). Also in Arabidopsis stems, sedimenting amyloplasts are
found in the endodermis and are a key factor of gravisensing
(Terao-Morita et al. 2002). In Arabidopsis roots, sedimenting
amyloplasts are found in the root cap (Blancaflor et al. 1998).
In our study of leaves, we found that sedimenting amyloplasts
are developed specifically in the proximal region of the petioles.
Our analyses of gravitropism-impaired mutants strongly
support the idea that the sedimenting amyloplasts are also
important for gravity perception in leaf petioles, as in stems
and roots. Fig. 2 suggests that leaf petioles bend only at the
junctions with stems rather than curving, whereas stems can
bend in all regions (Fukaki et al. 1996a). Since the localization
of amyloplast-accumulating cells and the bending regions overlap in the basal-most part of the petiole, the basal part of the
petiole is strongly suggested to be responsible for the gravity
response in leaves.
Taken together, the fundamental mechanisms of gravitropism, such as the use of amyloplasts for perception in a particular type of cells, seem to be shared among leaves, stems and
roots, but leaves are unique in that light suppresses their movement. To our knowledge, this is the first report of the nature of
the movement and positioning of rosette leaves. Our findings
will supply clues leading to more details on the positioning of
leaves, and photobiological analyses of the suppression of leaf
movement are under way.
Materials and Methods
Plant materials and growth conditions
The Columbia-0 (Col-0) strain was used as the wild-type A.
thaliana (L.) Heynh. in this study. The gravitropism mutants examined, pgm and sgr2-1, in the Col background were a generous gift from
Dr. H. Fukaki of the Nara Institute of Science and Technology
(NAIST), Japan. Except for an aseptic culture, seeds were sown on
rockwool trimmed to a square pyramid shape, moistened with distilled
water and nutrients (Hyponex®, Hyponex Corp., Andover, MA, USA),
and grown under continuous white light (50–60 µmol m–2 s–1) at 22°C
in air-conditioned rooms. Five- to 21-day-old-plants were used for the
assay. For the in vitro culture, seeds were sown on MS plates processed in a square pyramid shape and grown under continuous white
light at 22°C.
Analysis of leaf positioning under continuous light
Seeds were sown on pyramid-shaped, transparent MS medium
solidified with 0.5% Gellan Gum and grown for 7 d; germination containers were then put in a normal position or rotated by 90° or 180°.
Cultures were continued for another 3 weeks at 22°C under continuous light (50 µmol m–2 s–1). Light was carefully arranged to illuminate
the plants equally from all directions.
Graviresponse assays in different light conditions
For the graviresponse assays, we chose plants that had straight
hypocotyls that were elongated parallel to the direction of gravity.
Reorientation of plants was performed by rotating the rockwool cubes
by 180° at 22°C under light or dark conditions. For the time course
assay shown in Fig. 3, the plants were photographed immediately after
the reorientation and every 30 min after the reorientation during the
9 h assay. Leaf movement was characterized by the difference of petiole angle between the initial time point and a subsequent time point.
The movements of leaves toward and away from the shoot axis are
expressed by positive and negative values, respectively.
In the case of the light condition used in Fig. 5, the plants were
irradiated from the direction of the plant apices so that the relative positional relationship between plants and the white fluorescent lamp was
maintained. For the analysis of leaf angles shown in Fig. 4 and 5,
angles between the petioles of cotyledons or those between the petioles
of the first pair of true leaves were measured.
Visualization of starch grains
Leaves were fixed in FAA solution for 2 h. After fixation, leaves
were rinsed in 70% ethanol and placed in a 2% (w/v) iodine potassium iodide (IKI) solution for 1 min. IKI-stained leaf petioles were
cleared in a solution containing 5% (v/v) glycerol and 50% (w/v) chloral hydrate, and observed using a Leica DMRX/E microscope (Leica
Corp., Hamburg, Germany).
Acknowledgments
The authors thank Dr. Hidehiro Fukaki of the Nara Institute of
Science and Technology (NAIST) for providing the pgm and sgr2-1
mutants, Dr. Satoshi Yano of the National Institute for Basic Biology
(NIBB) for image analysis, Dr. Toshiaki Kozuka of Kyoto University
for valuable suggestions, and Mr. Sho-ichi Higashi and Mr. Takanori
Nakamura of NIBB for technical assistance. This study was supported
by a Grant-in-Aid for Scientific Research on Priority Areas from the
Ministry of Education, Science and Culture of Japan and by funds
from the Bio-Design Program of the Ministry of Agriculture, Forestry
and Fisheries, Japan. The study was also conducted as part of the
Ground-Based Research Announcement for Space Utilization promoted by the Japan Space Forum.
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(Received October 31, 2005; Accepted November 29, 2005)