Annals of Botany 84 : 709–714, 1999
Article No. anbo.1999.0963, available online at http:\\www.idealibrary.com on
The Role of Amyloplasts during Gravity Perception in Gynophores of the Peanut
Plant (Arachis hypogaea)
E D G A R M O C T E Z U M A and L E W I S J . F E L D M A N
Department of Plant and Microbial Biology, UniŠersity of California at Berkeley, 431 Koshland Hall, Berkeley,
CA 94720, USA
Received : 15 March 1999
Returned for revision : 26 May 1999
Accepted : 2 August 1999
Gravitropic perception and response are essential for the completion of the reproductive life cycle of the peanut plant
(Arachis hypogaea L.). The developing seeds are buried in the soil by a specialized organ, the gynophore, allowing
the fruit to mature underground. Controversy exists about the site of graviperception in the gynophore : previous
workers suggested that the intercalary meristem was the zone where gravity was perceived. Taking the starch statolith
hypothesis for graviperception as a framework, we explored the possibility that the starch-grain filled plastids
(amyloplasts) in the starch sheath of the gynophore may be acting as gravisensors. We show that these amyloplasts
sediment readily with respect to the gravity vector within 30 min of reorientation, and before there is a measurable
gravitropic response. Gynophore explants were incubated with gibberellic acid and kinetin, in darkness, to remove
starch from the amyloplasts. Destarching the gynophores did not inhibit overall growth of the organ, but reduced
the gravitropic response curvature by 82 % compared to water-treated controls. In addition, gynophores placed on
a rotating clinostat (without hormone treatment) also showed a reduced gravitropic response. In conclusion, the
evidence presented in this work strongly suggests that the amyloplasts of the starch sheath are responsible for
gravitropic perception in the peanut gynophore. A model for graviperception in the gynophore is presented.
# 1999 Annals of Botany Company
Key words : Amyloplast, Arachis hypogaea, gravity perception, groundnut, gynophore, peanut, starch sheath, starch
statolith hypothesis.
INTRODUCTION
Gravity perception and gravitropic response are essential
for the completion of the reproductive cycle of the peanut
plant or groundnut (Arachis hypogaea L.). The peanut plant
produces aerial flowers in the leaf axils of the stem, as in
other angiosperm species. What is unusual about the peanut
plant is that once the ovules are fertilized, they are carried
down into the soil where the fruit develop and mature
underground (Smith, 1950). The peanut carries and buries
its developing seeds into the ground by means of a specialized
organ, the gynophore (Jacobs, 1947). If the peanut
gynophore fails to perceive and respond to gravity, it will
not bury the developing seeds and, as a consequence the
fruit will not develop fully.
The gynophore grows downwards by means of an
intercalary meristem (Fig. 1 A), located proximal to the seed
region (Jacobs, 1947 ; Shushu and Cutter, 1990), which
includes an elongation zone found at 2 to 5 mm from the tip
(Moctezuma and Feldman, 1998). The downwards gravitropic growth of the peanut gynophore consists of three
phases : perception of the gravity stimulus, transduction of
the signal, and the gravitropic growth response (downwards
bending). Thus, to understand the gravitropic response of
the peanut gynophore, it is first necessary to characterize
and understand its mechanism of gravity perception.
Fax (510) 642–4995, e-mail edgar!nature.berkeley.edu ; feldman!
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0305-7364\99\120709j06 $30.00\0
Although graviperception is of upmost importance in the
peanut life cycle, there have been no studies on how the
gynophore perceives the gravity stimulus. Shushu and
Cutter (1990) briefly mention that the intercalary meristem
region may be responsible for the gynophore’s gravitropic
perception. However, they did not provide experimental
evidence to support their statement.
A century ago, the starch statolith hypothesis (SSH) for
gravity sensing was established (reviewed by Sack, 1991).
The SSH states that specific cells in plant organs contain
starch grains (statoliths) that are displaced by the force of
gravity within the cell. The starch grain-filled plastids
(amyloplasts) interact with other cell component(s), and
provide the cell with information about its orientation
(Hart, 1990 ; Sack, 1991).
The SSH has been the object of extensive debate because
most of the evidence to support it is correlative. Although
opponents of the SSH argue that other cellular components
may act as gravity sensors, the amyloplasts remain the main
intracellular elements that readily sediment upon reorientation (Caspar and Pickard, 1989 ; Kiss et al., 1989 ;
Sack, 1991).
In plant shoots, the cells of the starch sheath contain
amyloplasts that readily sediment with the gravity stimulus
upon reorientation (Sack, 1991 ; Fukaki et al., 1998). The
peanut gynophore has a typical shoot anatomy that includes
an amyloplast-filled starch sheath. Despite this typical shoot
anatomy, the peanut gynophore responds positively to
gravity. Thus, the following question arises : does the peanut
# 1999 Annals of Botany Company
710
Moctezuma and Feldman—GraŠity Perception in the Peanut Gynophore
gynophore perceive the gravity stimulus like a typical shoot,
or does it have a different mechanism of graviperception ?
Sack (1997) points out that gravity perception may have
evolved numerous times in different organisms, so the
peanut gynophore could have an unusual graviperception
mechanism. The role of the starch sheath and the amyloplasts of the peanut gynophore in graviperception has not
yet been explored ; it is the topic of the present work.
Studies that have partially elucidated the role of the
starch sheath and its amyloplasts in shoot graviperception
have involved incubating the plants with plant hormones,
in darkness, in order to remove all the starch from within
the amyloplasts (Pickard and Thimann, 1966 ; Iversen,
1969). These destarching experiments have sparked controversy about the validity of the SSH, producing evidence
against and in favour of the hypothesis due to minor
modifications in the destarching protocols.
Using the SSH as a framework, we hypothesize in this
work that amyloplasts in the cells of the starch sheath are
primarily responsible for gravity perception in the peanut
gynophore. Three lines of evidence are presented in this
study : (1) an anatomical analysis of amyloplast sedimentation correlated with the timing of the gravitropic
response ; (2) experiments in which the starch is removed
from the gynophores and the subsequent gravitropic
response measured ; and (3) experiments using a rotating
device (a clinostat) to verify the importance of the
sedimentation of the amyloplasts during graviperception.
MATERIALS AND METHODS
Plant material
Peanut seeds, ‘ Virginia 93B ’, were kindly provided by
Dr W. Mozingo (USDA-AREC, Suffolk, Virginia, USA).
Plants were grown as described in Moctezuma and Feldman
(1998).
Anatomical sections
Peanut gynophores (n l 15) were placed either vertically
or horizontally, excised at 6–8 mm from the tip and fixed
immediately in a formalin-acetic acid-ethanol solution (50 %
ethanol, 10 % formalin, 5 % acetic acid) overnight (16 h) at
4 mC. Of the total samples, 11 were fully developed, fertilized,
vertically growing, 20–40 mm long gynophores. The remaining four samples were of gynophores before fertilization
of the ovules (and before any gravitropic response was
observed). The orientation of the gynophores was maintained during the fixation process by using metal pins to
immobilize the samples inside the fixation vials. The samples
were dehydrated, infiltrated with paraffin (Paraplastj,
Oxford Labs, USA) and sectioned to 10 µm thickness.
Sections were later stained with safranin, tannic acid, iron
alum and Orange G, according to the staining protocol of
Sharman (1943). Using this technique, amyloplasts of the
starch sheath are stained black.
Destarching experiments
It has been demonstrated previously that gynophore
explants can be grown in Šitro (Ziv and Zamski, 1975).
Excised gynophores are able to continue their growth and
gravitropic response in the culture media. The ability of
these gynophore explants to grow in Šitro was used to treat
these organs to similar destarching protocols by Pickard
and Thimann (1966) and Iversen (1969).
Gynophores 20–40 mm long (n l 18) were excised from
the plant, sterilized, recut to 15 mm in length and placed in
sterilized Petri plates containing Murashige and Skoog
media, as in Ziv and Zamski (1975). The vertical orientation
of the samples was always maintained during this process.
Two sets of samples were used. The first set was incubated
at 30 mC in a solution of 1i10−& mol l−" of gibberellic acid
(GA ) and 7i10−& mol l−" of kinetin for 36 h in the dark$
ness. The second set, a control, was kept under the same
incubation conditions as above, except that distilled water
replaced GA and kinetin. After incubation, samples were
$
horizontally oriented for 48 h at 22 mC, and the angles
of curvature measured using a protractor as described in
Moctezuma and Feldman (1998). In addition, the two sets
(hormone-treated and water controls) were further subdivided and gravistimulated either in complete darkness or
daylight. The final length of all gynophores was recorded in
order to determine the overall rates of growth during
treatments.
To determine if any starch remained in the hormonetreated samples Šs. the water controls, a preliminary test for
starch was performed by adding a few drops of iodinepotassium-iodide to freshly cut samples (Glenn et al., 1992).
The hormone treated (destarched) samples showed no
staining, whereas the water controls showed a dark brown
staining, indicating the presence of starch within the tissues.
In addition, some of the destarched and control samples
were fixed, embedded, sectioned and stained with the
Sharman’s staining technique, as above, in order to detect
any starch within the amyloplasts of the starch sheath.
Clinostat experiments
In Šitro-grown gynophores were placed on a rotating
clinostat (Model T, 115V, Hurst Corporation, Princeton,
Indiana, USA) in order to further investigate the relationship
between amyloplast sedimentation and the gravitropic
F. 2. A, Longitudinal section of a vertically oriented, graviresponding gynophore. Notice the sedimenting amyloplasts in the starch sheath cells
(arrowhead). This micrograph is also a water-treated control for the destarching experiments. B, Longitudinal section of a gynophore that has
been oriented horizontally for 30 min. Notice the sedimentation of the amyloplasts to the new lower surface of the endodermal cells (arrowhead).
C, Longitudinal section of a destarched gynophore. Notice the absence of amyloplasts in the cells of the starch sheath (arrowheads). D, High
magnification view of the intact starch sheath cells showing the sedimenting amyloplasts (arrowhead). E, High magnification view of destarched
starch sheath cells, showing the absence of starch-filled amyloplasts (arrowhead). c, Cortex ; p, pith ; vb, vascular bundles ; g and arrow, direction
of the gravity vector. Bars for A–C l 80 µm ; D–E l 20 µm.
Moctezuma and Feldman—GraŠity Perception in the Peanut Gynophore
711
response of the gynophore. The constant rotation [1
revolution per minute (RPM)] of the clinostat is thought to
prevent amyloplasts from sedimenting in a set place within
the cell. Thus, the gynophore perceives an omnilateral
gravity vector, since the rotational movement of the clinostat
will continuously keep changing the direction of the gravity
vector.
Gynophores (n l 15) were cut to 15 mm in length, leaving
the tip and ovule region intact. Samples were immediately
explanted into a glass beaker containing Murashige and
Skoog medium, as in Ziv and Zamski (1975). While some
samples (n l 9) were horizontally oriented and placed in the
central axis of rotation of the clinostat, the remainder were
placed horizontally into a stable (non-rotating) beaker. The
angle of bending after 70 h of gravistimulation was measured
on each of the samples.
RESULTS
F. 1. Anatomical analysis of amyloplasts in the starch sheath cells of
the peanut gynophore. A, Longitudinal section of a peanut gynophore.
Arrowheads indicate the location of the amyloplasts near the elongation
zone, proximal to the intercalary meristem (im) and the seed region (s).
Bar l 0n5 mm. B, Cross section of a peanut gynophore, showing the
amyloplasts of the starch sheath (arrows) surrounding the vascular
bundles (vb). C, Cross section of a destarched peanut gynophore.
Notice the absence of amyloplasts in the starch sheath (arrows). D,
Cross section of a young, unfertilized gynophore. No amyloplasts are
visible in the starch sheath cells (arrows) at this early stage of
development in the peanut gynophore. Bars for B–D l 100 µm.
The starch sheath of the gynophore consists of the innermost
one–three cell layers of the cortex, surrounding the vascular
bundles (Fig. 1 B). Developmentally, the starch sheath is
first observed with starch-filled amyloplasts after the ovules
have been fertilized. Unfertilized gynophores are agravitropic (Shushu and Cutter, 1990), and do not exhibit starchfilled amyloplasts within the starch sheath (Fig. 1 D). The
starch sheath of mature (20–40 mm long) gynophores is
visible approx. 2 to 8 mm from the tip, in longitudinal
section. This area includes the main elongation zone of the
gynophore, which occurs at 2–5 mm from the tip (Moctezuma and Feldman, 1998).
Amyloplasts in the starch sheath of a mature gynophore
sediment readily with gravity. In longitudinal sections of
vertically-oriented gynophores, the amyloplasts always
F. 2. For legend see facing page.
712
Moctezuma and Feldman—GraŠity Perception in the Peanut Gynophore
T     1. Destarching experiments : mean angles (s.e.) of
graŠitropic response after 48 h of graŠistimulation
Water control
Hormone treated
Gravistimulation under continuous
white light, at 25 mC
45n2 (2n7)
Gravistimulation under darkness, at 25 mC
42n5 (7n5)
9n2 (0n6)
7n0 (2n1)
All figures in degrees of curvature, where 0 l horizontal and
90 l vertically downwards.
T     2. Clinostat experiments : mean angles of curŠature
after 70 h of graŠistimulation
Treatment
Mean curvature (s.e.)
Stable controls
Clinostat rotated (1 RPM)
58n2 (3n7)
2n3 (0n4)
All figures in degrees of curvature, where 0 l horizontal and
90 l vertically downwards.
sediment to the lowermost surface of the cell, in the
direction of the gravity vector (Fig. 2 A and D). However,
in gynophores reoriented horizontally for 30 min, the
amyloplasts sediment towards the new lower surface of the
starch sheath cells (Fig. 2 B). It is important to note that the
amyloplasts sediment before a gravitropic response curvature occurs, which is 2 h after reorientation (Moctezuma
and Feldman, 1998).
In destarched gynophores an 82 % decrease in the
curvature angle of the gravitropic response occurs compared
to water-treated controls (Table 1). Amyloplasts are no
longer visible in the destarched gynophores (Figs 1 C, 2 C
and E) because the plastids have been depleted of starch.
Results were not statistically different between gynophores
gravistimulated in light or dark conditions (Table 1).
Both the destarched gynophores and the water-treated
controls continued to grow during the treatments (at approx.
0n03–0n04 mm h−"), indicating that the destarching hormone
treatment did not affect the growth of the samples.
Results of the clinostat experiments indicate that after
70 h of reorientation there was a marked difference in the
gravitropic response between the gynophores placed on the
clinostat Šs. the controls. These experiments corroborate the
hypothesis that the bending response in the horizontallyoriented gynophore is a true gravitropic response. Rotation
in the clinostat prevented the amyloplasts from sedimenting
in a stable place inside the starch sheath cells of the
gynophore, thus resulting in a dramatic decrease (96 %) in
the mean curvature of the gravitropic response. As in the
destarching experiments, these gynophores also continued
their growth in Šitro for the duration of the clinostat
experiments.
DISCUSSION
Anatomical sections of reoriented gynophores show rapid
sedimentation (within 30 min) of the amyloplasts to the new
lower surfaces of endodermal cells. These amyloplasts
appear after fertilization of the ovules, since unfertilized
gynophores do not contain visible amyloplasts (Fig. 1 D) ;
nor do they respond to gravity in the same way as fertilized
gynophores. Thus, in the peanut gynophore, there is a
strong correlation between amyloplast development in the
starch sheath and the onset of the gravitropic response.
Destarching experiments have produced contradictory
results in the past. Pickard and Thimann (1966) first used a
protocol in which coleoptiles were incubated in darkness for
several hours. Although they observed the complete absence
of starch in the samples (under light microscopy), the wheat
coleoptiles were still able to respond to gravity (although at
a slower rate than intact coleoptiles). Iversen (1969) also
performed similar destarching experiments. By raising the
temperature of the incubation period, Iversen (1969) was
able to completely deplete the amyloplasts of starch and to
abolish the gravitropic response of cress roots.
In this paper we used a destarching protocol similar to
that used by Iversen (1969), to fully deplete the amyloplasts of the peanut gynophore of starch. These destarched
gynophores showed an 82 % reduction in the angle of
gravitropic response curvature, compared to water-treated
controls. Destarching protocols have been criticized because
of the possible growth-stunting effects that the hormone
treatments may have on the plant organs as a whole.
However, growth measurements in this study showed that
both destarched and control gynophores continued to grow
in Šitro—only the gravitropic response was inhibited in the
destarched gynophores.
A possible explanation for the results obtained in the
destarching experiments is that the amyloplasts within the
gynophore were depleted of starch, leaving only empty
plastids within the endodermal cells. Previous studies
(Iversen, 1969 ; reviewed by Sack, 1991) have shown that
starch-depleted plastids are less dense than normal, starchfilled plastids, and therefore do not sediment as readily as
the controls. Although the starch-depleted amyloplasts may
have retained some gravity sensing properties (destarched
gynophores did bend slightly), these empty plastids were not
sufficiently dense to produce a full gravitropic response in
the peanut gynophore.
The use of a clinostat for the study of plant gravitropic
sensing has been criticized by many (Moore, 1990), mainly
because of the possible deleterious effects that this device
may have on the plant. However, for the purposes of this
study, the clinostat experiments provided useful data which
corroborated : (1) that the downwards bending of the
gynophore is a true gravitropic response ; and (2) by
preventing the amyloplasts from sedimenting during clinostat rotation, it is possible to reduce gravitropic perception
and, consequently, gravitropic response. The use of the
clinostat provided additional evidence in favour of the
amyloplasts in the starch sheath of the gynophore as the
likely gravity perceptors for the organ. Furthermore, these
clinostat experiments also provide an additional control of
an intact graviresponding gynophore grown in Šitro, to be
compared with hormone-treated and water-treated gynophores used in the destarching experiments.
Shushu and Cutter (1990) suggest that the intercalary
Moctezuma and Feldman—GraŠity Perception in the Peanut Gynophore
A
B
g
Vertically oriented
Horizontally oriented
F. 3. Diagrammatic representation of sedimenting amyloplasts
during gravistimulation. A, Vertically oriented gynophore, with
sedimenting amyloplasts ($) located in endodermal cells. B, Horizontally oriented gynophore. The strategic location of the starch sheath
and the sedimenting amyloplasts produce a structural asymmetry
between the upper and lower halves of the organ. In the upper starch
sheath, the sedimenting amyloplasts are closer to the cells of the
vascular bundles (). The amyloplasts of the lower starch sheath,
however, are in direct contact with the cortex cells of the lower surface.
This structural asymmetry may be important for the upcoming
physiological events that occur during the gynophore’s gravitropic
response. g and the arrow indicate the direction of the gravity vector.
meristem (IM) of the peanut gynophore may be the site for
gravity perception. This statement is only partially true,
since some of the amyloplasts in the starch sheath are
located near the IM of the gynophore (Fig. 1 A). However,
the actual meristematic cells of the IM are unlikely to play
the role of gravity perceptors for the gynophore per se.
Why ? As Bjo$ rkman (1992) calculated in his study, the small
size of meristematic cells does not physically allow them to
perform such a task. In addition, their dense cytoplasmic
content and their lack of sedimenting amyloplasts or other
organelles, make the IM a poor candidate for the site of
gravity sensing in the peanut gynophore.
In conclusion, the evidence presented in this study strongly
suggests that the amyloplasts of the starch sheath are prime
candidates for the role of gravity perceptors in the peanut
gynophore. Recent evidence in other plant systems also provides additional data in support of the starch sheath as the
site of graviperception in plant shoot systems. Kiss et al.
(1997) show that hypocotyls of starch-deficient mutants of
Arabidopsis exhibit reduced gravitropism. Similarly, Fukaki
et al. (1998) provide genetic evidence in favour of the
amyloplasts as graviperceptors, with Arabidopsis mutants
that lack a starch sheath and which fail to perceive and
respond to gravity. In addition, Kuznetsov and Hasenstein
(1997) performed magnetophoresis experiments using barley
coleoptiles in which the amyloplasts of the starch sheath
were displaced by a magnetic field, followed by a bending
response.
Furthermore, the strategic location of the starch sheath
(in a ring surrounding the vascular bundles) may also be
important in the physiological events that occur during the
gravitropic response. The sedimenting amyloplasts create a
structural asymmetry between the upper and lower halves of
the peanut gynophore (Fig. 3). In the upper endodermal
cells, the amyloplasts contact the cells of the vascular
713
bundles, whereas the amyloplasts of the lower starch sheath
are closer to the cells of the cortex. This structural asymmetry
created by the strategic location of the starch sheath cells,
may later translate into a physiological asymmetry, which
would result in an unequal growth response between the
upper and lower surfaces—and the eventual downward
bending—of the gynophore. Many workers (Sack, 1991 ;
Bjo$ rkman, 1992) believe that the contact of the amyloplasts
with the plasma membrane of the starch sheath cells can
mechanically open ion channels in these cells. Calcium and
other molecules (such as plant hormones) may be transported from within the tissues upon opening and closing of
these channels, thus creating physiological differences
between the upper and lower halves. As other studies have
shown (Moctezuma and Feldman, 1996, 1999 ; Moctezuma,
1999), the plant hormone indole-3-acetic acid is redistributed
asymmetrically to the upper surface of a horizontallyoriented gynophore, thus creating a growth asymmetry
between the upper and lower surfaces which eventually
leads to the downwards bending of the organ.
Some final questions still remain open for future study : if
the positively gravitropic peanut gynophore perceives the
gravity stimulus in the same way as a negatively gravitropic
shoot, why does the peanut bend down, while a typical
shoot bends up ? Which step in the transduction process has
to be ‘ switched ’ in the gynophore, in order to obtain an
opposite gravitropic response ? The answers to these and
other questions should provide us with important clues to
elucidate the signal transduction mechanisms that govern
gravitropism in higher plants.
A C K N O W L E D G E M E N TS
We thank Dr Steven Ruzin and Dr Denise Schichnes from
the Biological Imaging Facility for their technical help,
David Welch for help with the images, Dr W. Mozingo
from USDA for providing the Virginia 93B peanut seeds,
and Denise A. Benoit for critically reading this manuscript.
This work was supported by a research fellowship from the
National Aeronautics and Space Administration to E.M.
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