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Developmental Biology and Developmental Genetics |
2Microscopy and Imaging Center, Texas A&M University, College Station, Texas 77843 USA; 3Department of Botany, Oklahoma State University, Stillwater, Oklahoma 74078 USA; 4Department of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada; 5Department of Botany, Miami University, Oxford, Ohio 45056 USA
Received for publication December 4, 2006. Accepted for publication February 14, 2007.
ABSTRACT
Amyloplasts are hypothesized to play a key role in the cellular mechanisms of gravity perception in plants. While previous studies have examined the effects of starch deficiency on gravitropic sensitivity, in this paper, we report on gravitropism in plants with a greater amount of starch relative to the normal wild type. Thus, we have studied the sex1 (starch excess) mutant of Arabidopsis thaliana, which accumulates extra starch because it is defective in a protein involved in the regulation of starch mobilization. Compared to the wild type (WT), sex1 seedlings contained excess starch in cotyledons, hypocotyls, the root–hypocotyl transition zone, the body of the root, root hairs, and in peripheral rootcap cells. Sedimented amyloplasts were found in both the WT and in sex1 in the rootcap columella and in the endodermis of stems, hypocotyls, and petioles. In roots, the starch content and amyloplast sedimentation in central columella cells and the gravitropic sensitivity were comparable in sex1 and the WT. However, in hypocotyls, the sex1 mutant was much more sensitive to gravity during light-grown conditions compared to the WT. This difference was correlated to a major difference in size of plastids in gravity-perceiving endodermal cells between the two genotypes (i.e., sex1 amyloplasts were twice as big). These results are consistent with the hypothesis that only very large changes in starch content relative to the WT affect gravitropic sensitivity, thus indicating that wild-type sensing is not saturated.
Key Words: amyloplast • Arabidopsis thaliana • columella • endodermis • gravitropism • starch excess mutant • statolith
Gravity, a constant and ubiquitous force throughout evolutionary history, has a profound impact on the development and growth of plants. Thus, the nature of the cellular mechanisms of gravitropism is one of the most important and fundamental questions in plant biology. Numerous studies have shown that starch and the total mass of plastids are important in gravity perception (reviewed in Sack, 1997
; Kiss, 2000
). While these previous reports have focused on starch-deficient plants, in this paper we have expanded these studies to include the starch excess (sex1) mutant, which accumulates extra starch in many tissues including the leaves, petals, anthers, and root cap of Arabidopsis thaliana (Caspar et al., 1991
). This phenotype is due to retardation of starch breakdown, resulting from a disrupted water glucan dikinase that is required for the phosphorylation and degradation of starch (Yu et al., 2001
; Ritte et al., 2002
; Sokolov et al., 2006
).
Starchless and starch-deficient mutants have previously been used to study the role of starch in the regulation of photosynthesis (Hanson, 1992
) and to identify enzymes involved in starch biosynthesis and carbon translocation (Caspar, 1994
; Smith et al., 1997
). The sex1 starch degradation mutant provides an opportunity to study tissue-specific regulation of starch biosynthesis and degradation. The sex1 mutation affects starch breakdown but not the synthesis (Caspar et al., 1991
), which results in the starch-excess phenotype. In developing amyloplasts, where starch synthesis prevails and breakdown is negligible, WT and sex1 could be expected to have similar amounts of starch. However, when starch synthesis declines and/or starch degradation increases, sex1 plastids should contain more starch than the WT. Because the rates of synthesis and breakdown may be a function of cell position as well as environmental factors, the sex1 phenotype may vary depending on the tissue and light regime.
As stated, because gravitropic sensing relies upon the mass of amyloplasts that sediment in specialized tissues, such as the endodermis in stems and hypocotyls and the columella of the root cap (Sack, 1997
), starchless or starch-deficient mutants have also been useful in the study of gravitropism (Kiss et al., 1989
, 1997
; Kiss and Sack, 1990
; Vitha et al., 1998
). These reports have shown that starchless mutants are much less sensitive to gravity compared to WT plants. Mutants with intermediate levels of starch are more gravisensitive than starchless mutants but are less sensitive relative to the WT (Kiss et al., 1996
, 1997
). To date, no data are available on whether higher-than-WT starch levels affect the extent of amyloplast sedimentation and gravitropic sensitivity. Here, we analyze whether the sex1 mutation induces excess starch in all tissues, whether it causes increased amyloplast sedimentation, and whether it affects gravitropism of roots and hypocotyls of young seedlings.
MATERIALS AND METHODS
Plant material and cultivation
The sex1 allele used was originally termed TC265, which was reselected from five successive backcrosses of TC26 to the WT (Columbia ecotype; Caspar et al., 1985
). For root gravitropism experiments, seeds were sown in square polystyrene petri dishes (100 x 15 mm) on 1% (w/v) agar containing nutrients supplemented with 1% (w/v) sucrose (Kiss et al., 1996
). The dishes were sealed with parafilm, placed on edge so that the surface of the agar was vertical and kept under continuous illumination (60–80 µmol·m–2·s–1 from 40 W "cool white" fluorescent lamps) for 80–100 h, until the roots were 5–13 mm long. Roots used for microscopy were grown as described, except they were kept at 4°C for 4 d after sowing to promote uniform germination. Seedlings for hypocotyl studies were germinated at room temperature and grown under three different light regimens: "dark-grown" (4 d in the dark, 4D), "light–dark-grown" (2L, 1D), and "light-grown" (7L). For inflorescence stems, plants were grown in plastic pots filled with Promix substrate (Premier Horticultural, Red Hill, Pennsylvania, USA) with a 12-h photoperiod (also 60–80 µmol·m–2·s–1) for approximately 8 wk, until the stems were 11–15 cm long. Plants were used in experiments 6 h after the start of the photoperiod. These light regimens were selected because in preliminary experiments, they affected the starch content in seedlings and plants.
Microscopy
For microscopic studies, seedlings in petri dishes were secured in place by covering them with several layers of gauze. Dishes were then either turned upside down or kept upright for 2.5 h. Petri dishes were then filled with fixative consisting of 3.7% (w/v) formaldehyde and 1% (v/v) glutaraldehyde in phosphate-buffered saline (PBS) buffer (0.14 M NaCl, 2.7 mM KCl, 6.5 mM Na2HPO4, 1.5 mM KH2PO4, pH 7.3), briefly vacuum infiltrated, and maintained in position for 4 h. Seedlings were then rinsed in water, dehydrated in an ethanol series, and flat-embedded in Spurr's resin between two transparent acetate sheets. This ensured the correct alignment of seedlings for longitudinal sectioning of hypocotyls. Longitudinal 3 µm sections of hypocotyls were cut with a glass knife on a Reichert-Jung Ultracut microtome (Vienna, Austria), attached to glass slides, sequentially stained with 1% (w/v) toluidine blue and IKI solution (2% KI, w/v, 1% I, w/v), and viewed with a Zeiss IM35 microscope (Thornwood, NY, USA). Kodak (Rochester, NY, USA) Ektachrome ET160 film was used for photography.
For the analysis of inflorescence stems, pots with plants were turned upside down and kept in darkness for 1 h. Whole stems were then immersed in fixative consisting of 3.7% (w/v) formaldehyde, 40% (v/v) ethanol, 5% (v/v) acetic acid, and dehydrated in ethanol. Stems were maintained in a vertical, inverted orientation throughout. After dehydration, four segments, each 5 mm long, were excised from each stem, from locations at 5, 35, 65, and 105 mm from the stem apex. Segments were then embedded in Steedman's wax as described in Vitha et al. (1997)
. Longitudinal sections (10 µm thick) were cut on a rotary microtome with a steel knife, attached to slides, dewaxed in ethanol, and stained for starch with IKI.
Measurement of plastid size
Plastid area was measured in sections of hypocotyls and inflorescence stems. Bright-field images, focused on the maximum diameter of a plastid, were captured using a 100x oil immersion objective and a Panasonic CCD video camera (Matsushita Electric Industrial Co., Osaka, Japan; model WV-D5100) and a Snappy video capture device (Play, Inc., Rancho Cordova, California, USA). Measurements were performed using NIH Image software as described in Vitha et al. (1998)
on sections from five inflorescence stems and six hypocotyls. The total number of plastids measured was 70 to 103 for each of the two sites in hypocotyls, and 96 to 119 for each of the four segments of inflorescence stems sampled.
In hypocotyls, endodermal plastid size was measured in two locations. The first was in subapical endodermal cells that were not yet elongated, i.e., in the hypocotyl hook (dark-grown seedlings; Fig. 3A) or in the 3–4 endodermal cells closest to the apex (light–dark- and light-grown seedlings, Fig. 3G). The second site measured in hypocotyls was in a more distal segment approximately 0.5 mm long, starting where endodermal cells were at least twice as long as they were wide (indicated by "#" in Fig. 3A, G). Light-grown hypocotyls were not measured in the distal site, because no or very few endodermal amyloplasts could be found at this location.
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Amyloplast size in individual layers of the root columella (L1 to L5) was measured from digitally scanned electron micrographs using NIH image software. Between 14 and 53 plastids were measured for each layer and genotype. Stereological analysis of columella cell size, volume fraction (%) of starch per cell, and electron microscopy were performed as described in Caspar and Pickard (1989)
. For each layer, 18 to 30 cells were analyzed in sections from six WT and five sex1 roots.
Measurement of gravitropism and growth
For hypocotyls, all the growth and gravitropism experiments were performed in the dark, regardless of the light regimen used for cultivation of seedlings. Petri dishes with seedlings were either turned to the horizontal (for measurements of gravitropic curvature) or kept upright (for measurement of growth). Seedlings were intermittently photographed using Kodak T-Max 400 ASA film and illumination with dim green light (irradiance of approx. 0.008 µmol·m–2·s–1 at the level of the hypocotyl) provided by one fluorescent lamp (20 W "cool white") filtered through four layers of a Roscolux (Rosco Laboratories, Port Chester, New York, USA) filter no. 1089 (peak transmission 60% at 526 nm, bandwidth 80 nm) and one layer of no. 1090 (peak transmission 23% at 526 nm, bandwidth 58 nm). Growth rates were measured over 4 h, except for light-grown hypocotyls where growth was measured over 27 h, using digitally scanned photographic negatives and NIH Image software. A total of 26 to 47 hypocotyls were measured for each genotype and cultivation regimen. Gravitropic curvature was measured from photographic prints as an increment over the initial angle of each hypocotyl. Gravitropic sensitivity to a single dose of gravistimulation (presentation time) was measured as described in Kiss et al. (1989)
. The clinostat used in these experiments was custom built, with a horizontal axis of rotation and speed of 1 rpm.
Root growth and gravitropism were measured similarly as for the hypocotyls, except that all experiments were performed in unfiltered "cool white" light (light from above, the same source and intensity as for cultivation). Growth was measured over 4 h. Gravitropic sensitivity was measured by intermittent stimulation or by a single dose of gravistimulation as described by Kiss et al. (1989)
.
RESULTS
Excess starch is present in many tissues in sex1 seedlings
In sex1 roots, excess starch was found in peripheral cells of the cap, in the cortex, in root hairs, and in the root–hypocotyl junction (Fig. 1). In the seedling shoot, excess starch was found in the hypocotyl cortex, throughout the cotyledon, as well as in the seed coat (Fig. 1). The magnitude of these differences between sex1 and the WT depended on the cultivation conditions, but differences could always be detected under all conditions.
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). On a medium without sucrose, the differences between WT and sex1 were visible as well, but the seedlings grew poorly. Thus, for all further experiments, seedlings were grown on a medium with 1% sucrose.
Columella starch and plastid size are equivalent in sex1 and in WT
Amyloplast size is equivalent statistically (Student's t test, 
= 0.05) between sex1 and the WT within each layer (L1 to L5) of the columella (Table 1). Stereological analysis of electron micrographs showed that the volume fraction (%) of starch per cell, columella cell size, and number of plastids per cell were also equivalent in both genotypes (data not shown). Sedimented amyloplasts of equivalent size were found in both sex1 and WT inverted roots in mature columella cells (layers 3 and 4), but not in younger cells (L1 and L2). Sedimentation was absent in layer 5 (in transition to peripheral cells) even though they were larger than the L3 and L4 plastids. Thus, sex1 root cap amyloplasts were larger than WT plastids only in peripheral cells (Fig. 1K, L).
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).
Patterns of hypocotyl starch content vary with light regimen
The amyloplast size in the endodermis of hypocotyls varied within each genotype depending upon the lighting regimen used for cultivation. Endodermal plastids in dark-grown and light-grown hypocotyls were larger than those in light–dark-grown hypocotyls or in inflorescence stems (Fig. 3). Within each genotype, amyloplasts in dark-grown seedlings were somewhat larger in the distal endodermis than in the subapical region, whereas in light–dark-grown hypocotyls, amyloplast size was more or less equivalent in both regions. In the light-grown hypocotyls of both genotypes, the distal endodermis contained no or very few small amyloplasts, and therefore plastid size could not be measured (see Fig. 3K, L, O).
Culture conditions also affected amyloplast size between genotypes. Although dark-grown sex1 hypocotyls had more starch in the cortex than WT hypocotyls (Fig. 1B, G), sex1 endodermal amyloplasts were smaller than the WT (Table 1). In contrast, sex1 endodermal amyloplasts were twice as large as WT amyloplasts in seedlings grown for 7 d in the light. The sex1 mutant also had large amounts of starch in the hypocotyl cortex and epidermis, while these tissues appeared largely devoid of starch in the WT in the light (Fig. 3J–Q). Qualitative observations of light-grown hypocotyls show that sex1 endodermal plastids decrease in size with distance from the apex, while sex1 cortical plastids stay the same size throughout the apical half of the hypocotyl (Fig. 3N, O).
As shown, sex1 seedlings grown for 7 days under continuous light accumulated large amounts of starch in hypocotyls. In about a third of all sex1 hypocotyls assessed, sedimentation of plastids was observed in outer cortical layers. The sedimentation was most apparent at the mid-length of the hypocotyl (Fig. 3Q). Plastid sedimentation was obvious in many, but not all, cells of the cortex.
Differences in gravitropic sensitivity in WT and sex1 seedlings
In the time course of curvature studies, sex1 roots had a greater gravitropism compared to WT roots (Fig. 4A), but this appears to be due largely to the faster growth rate of sex1 roots compared to WT roots (Table 1). Gravitropic sensitivity was equal in roots of both genotypes whether measured by presentation time (Fig. 4B; Table 1) or by intermittent stimulation (Table 2).
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DISCUSSION
Differences in starch content of seedlings between cultivation regimens
In hypocotyls of dark-grown seedlings, endodermal amyloplasts in both genotypes are of similar size, but excess starch is found in various other tissues (see Fig. 1). From the equal size of endodermal amyloplasts in sex1 and the WT, it seems that little or no breakdown of amyloplast starch is taking place in the endodermis. Thus, starch synthesis is occurring largely without breakdown, judging from the large size of these amyloplasts.
Our results also suggest that light causes changes in the starch synthesis and/or breakdown rates. When exposed to light, breakdown of starch in the WT hypocotyls is increased—both in the endodermis and cortex; consequently, starch content in the WT is decreased, as seen in the light–dark and the light-grown material in comparison to the dark-grown hypocotyls. The same decrease of starch content does not occur in sex1 because of a disrupted water glucan dikinase that is required for the phosphorylation and degradation of starch (Yu et al., 2001
; Ritte et al., 2002
). It is not quite clear why the sex1 amyloplasts in light–dark grown hypocotyls are smaller than those in the dark-grown ones. One possibility is that light not only causes increased starch degradation, but also decreases starch synthesis once the seedlings were put into darkness.
The hypocotyls of light-grown seedlings have the most severe starch excess phenotypes: WT hypocotyls have very little starch, while sex1 hypocotyls contain a great excess of starch in cortex and subapical endodermis (Fig. 3). Plastids in the light-grown sex1 mutant are very large, probably due to the combined effect of the inability to degrade starch and the ongoing starch synthesis under continuous illumination. In the WT, the balance of synthesis and degradation is in favor of degradation; therefore, the WT hypocotyls contain very little starch. Interestingly, endodermal amyloplasts in the hypocotyls of light-grown sex1 seedlings decrease in size sharply with their distance from the apex (Fig. 3), but this observation may be due to the fact that hypocotyls are very short and the same absolute distance from the apex spans many more cells than in the dark-grown hypocotyls, which are highly elongated.
In the root columella, WT and sex1 plastids are not of statistically different sizes (Table 1), and this is probably because amyloplasts in columella cells L1–L5 undergo rapid starch accumulation without any starch degradation. Previously, we found that an increase in sucrose concentration in the growth medium increased the starch content in amyloplasts of root columella cells (Guisinger and Kiss, 1999
).
Amyloplast size and sedimentation in gravisensing cells
In the root columella, usually only amyloplasts in cells L3 and L4 are sedimented, but not in L5, even though amyloplasts are larger in this layer. Sedimentation is not dependent simply on amyloplast size but rather on the special properties of the cell itself. For example, cells in L3 and L4 are the most important for Arabidopsis root gravitropism as was shown by Blancaflor et al. (1998)
in laser ablation experiments. Balu
ka et al. (1997)
also found that the central root cap of several species was depleted of endoplasmic microtubules and actin microfilaments and suggested that these properties enhanced plastid sedimentation and the gravity-perceptive function of these cells. In addition, MacCleery and Kiss (1999)
found a correlation between starch content and the magnitude of plastid sedimentation in these columella cells of Arabidopsis.
Similarly as in the root cap, amyloplast sedimentation in the endodermis of inflorescence stems was dependent on cell position rather than just on the amyloplast size (see also Weise et al., 2000
). Plastid sedimentation was observed 5 mm but not 65 mm below the stem apex (Fig. 2), even though amyloplast size was not significantly different between the two sites. In other studies, endodermal cells in inflorescence stems have been shown to play a key role in gravity perception in these organs (Tasaka et al., 1999
; Weise and Kiss, 1999
).
In hypocotyls of the light-grown sex1 mutant, however, plastid sedimentation can occur even in cells that are presumably not specialized for gravity sensing—here in the two outer layers of cortex (Fig. 3Q). In this case, amyloplasts probably reached certain critical mass and could not be held in their place any longer. It is unclear as to whether this type of amyloplast sedimentation plays any role in gravity sensing. In addition, the rate of gravitropic curvature is much greater in inflorescence stems compared to seedlings (Weise and Kiss, 1999
), so further study is needed to understand the role of excess starch in plastids in terms of the kinetics of gravitropism in these organs.
Increases in total mass of plastids cause an increase in gravitropic sensitivity
The vast majority of studies support the hypothesis that amyloplasts function as statoliths in specialized gravity perceiving cells (reviewed in Kiss, 2000
; Blancaflor and Masson, 2003
; Mano et al., 2006
). For instance, in previous studies with starch-deficient mutants, gravitropism improved when there is an increase in the total mass of plastids per gravity-perceiving cells (Kiss et al., 1996
, 1997
). In addition, others have demonstrated that hypergravity treatment causes increased plastid sedimentation in gravity-perceiving cells of both WT and starch-deficient mutants, which, in turn, increased gravitropism in these seedlings (Fitzelle and Kiss, 2001
). In the present study, gravitropism of the WT and sex1 generally correlated with amyloplast size in gravity-sensing cells.
In roots, sex1 and the WT had the same amyloplast size and also the same gravitropic sensitivity. In contrast, dark-grown hypocotyls of sex1 and WT seedlings had similar amyloplast sizes as well as similar gravitropic sensitivities. However, hypocotyls of light-grown seedlings had the greatest and most striking differences in starch content between the genotypes, and, in turn, gravitropic sensitivity as measured by presentation time (Table 1) was also dramatically different. For sex1 hypocotyls, the threshold of gravitropic sensitivity was approximately 6 min, while the hypocotyls of the WT (with low starch) did not produce significant curvature even after 90 min of gravistimulation.
Taken together, these results support the hypothesis that only very large increases or reductions in starch content relative to the WT affect gravitropic sensitivity in plants. This model also is consistent with the reports that higher-level intermediate starch mutants (i.e., 60% of normal starch) have an almost WT level of gravitropism in some assays (Kiss et al., 1996
). In addition, hypergravity has been shown to increase gravitropic sensitivity even in plants with WT levels of starch (Fitzelle and Kiss, 2001
). Thus, it is likely that normally the sensing system is not saturated and instead is optimized to perceive a sufficient signal from integration over time (Sack, 1991
) rather than from the decreasing benefits of still further increases in plastid mass.
FOOTNOTES
1 The authors thank T. Caspar and T. M. Bourett for providing samples for electron microscopy and for helpful discussions. Financial support was provided by the National Aeronautics and Space Administration. 
6 Author for correspondence (e-mail: kissjz{at}muohio.edu
)
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