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Department of Botany, Miami University, Oxford, Ohio 45056
Received for publication December 3, 1998. Accepted for publication March 18, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: amyloplasts • Arabidopsis • columella cells • microgravity • spaceflight • starch • stereology • ultrastructure
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The utilization of the microgravity environment achieved during spaceflight has become important in the elucidation of the role that gravity plays on organisms.
Amyloplasts, starch-filled plastids in root cap columella cells, are believed to act as gravisensors in plants (Salisbury, 1993
; Sack, 1997
). In this study, plastid size and starch accumulation were examined in spaceflight experiments with wild-type (WT), a reduced starch mutant (ACG20), and a starchless mutant (ACG21) of Arabidopsis thaliana (Kiss, Wright, and Caspar, 1996
). Compared to many previous flight experiments (reviewed in Perbal, Legué, and Driss-École, 1996
), the present study has numerous controls that help to distinguish true microgravity effects from indirect or secondary effects due to the spaceflight environment. These conditions include plants being grown: (1) in normal gravity conditions on the ground (termed G-1g), (2) on a 1g centrifuge during spaceflight (F-1g), and (3) in microgravity during spaceflight (F-µg). In addition, we performed another control in which seedlings were grown in elevated ethylene (G-ethylene) since this gas was found to be present in the spacecraft atmosphere.
Results from spaceflight experiments (Volkmann and Sievers, 1979
; Moore et al., 1987
; Kordyum et al., 1997
) have suggested that the amount of starch available in plants was decreased (i.e., both the starch in columella cell amyloplasts and the total starch per plant). Therefore, in these experiments, stereological and morphometric analyses were performed with root caps of seedlings that developed in microgravity on the Space Shuttle and the various controls. The following questions are addressed. (1) Are plastid size and starch accumulation altered in microgravity as compared to Earth's 1g gravitational acceleration? (2) Is the ultrastructure of other cellular and subcellular components altered by microgravity?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and Kiss et al. (1997)
. Mutant ACG21 is starchless in all tissues and is allelic to previously described pgm mutants (Caspar and Pickard, 1989
), while ACG20 exhibits reduced starch in comparison to the WT and is nonallelic to pgm mutants. Upon harvest, the seeds were stored at 4°C for 19 mo prior to their use in these experiments.
Spaceflight and hardware
Seedlings of the three genotypes were flown in space on the Space Shuttle mission STS (Space Transportation System)-84 in May 1997. While on the ground, seeds were sown onto modified "lentil-roots hardware" (described in Katembe et al., 1998
; Kiss, Katembe, and Edelmann, 1998
) in Biorack type I containers (growth chambers). Seedlings were placed on a sterile, gridded, black membrane (cellulose nitrate, catalog number 66266; Gelman Sciences, Ann Arbor, Michigan, USA) atop two layers of sterile Whatman Number 3 paper in containers that are described by Perbal and Driss-École (1994)
. Once in space, seeds and seedlings were kept at a constant temperature of 22°C in the ESA (European Space Agency) Biorack unit.
The flight procedures and time line are outlined in Fig. 1. The seeds were hydrated with 1.3 mL of sterile Arabidopsis growth medium, which consisted of 5 mmol/L KNO3, 2.5 mmol/L Ca(NO3)2, 2 mmol/L MgSO4, 50 µmol/L Fe EDTA, 2.5 mmol/L KH2PO4, and micronutrients (pH 5.5) (Haughn and Somerville, 1986
). Micronutrient solution contained 100 µmol/L H3BO3, 1 µmol/L ZnSO4, 0.2 µmol/L Na2MoO4, 0.2 µmol/L CuSO4, and 0.01 µmol/L CoCl2.
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). The samples that were kept on the 1g flight centrifuge were briefly (10 min) exposed to microgravity during the illumination process. After illumination, specimens were grown for 65 ± 5 h (in darkness), and then they were fixed in 4% (v/v) glutaraldehyde for 5.5 d in 100 µmol/L phosphate buffer at pH 7.2 for the return flight to Earth.
Ground controls
Ground controls were performed at Kennedy Space Center in a Biorack unit. These were identical to the spaceflight experiments in terms of material, hardware, procedures, and time line. Studies on the development of seedlings in the presence of exogenous ethylene were performed as an additional control following the flight. Ethylene gas was added to a chamber to yield the final concentration of 2 ppm. This chamber contained the flight hardware with seeds, and complete flight procedures were replicated.
Light and electron microscopy
Once on the ground following the flight, the glutaraldehyde-fixed flight material was taken to Miami University. Due to flight constraints, seedlings were kept in glutaraldehyde for a total of 5.5 d. However, preliminary studies (Kiss et al., 1999) revealed this did not have a deleterious effect on ultrastructure.
Both ground control and flight seedlings were rinsed several times in buffer and then post-fixed with 2% (w/v) osmium tetroxide for 2–3 h. The seedlings were dehydrated though an ethanol series. They were then transferred to BGE (butyl glycidyl ether) and infiltrated into 80% Quetol 651 resin for 3 d. The resin was polymerized at 60°C for 24 h.
Thick (1 µm) median longitudinal sections and ultrathin (90 nm) median longitudinal sections of root caps were cut using a Reichert Ultracut S microtome. Thick sections were stained with toluidine blue for light microscopy. Ultrathin sections were transferred to formvar-coated grids and were stained with uranyl acetate and lead citrate. These sections then were viewed and photographed at 60 kV on a JEOL JEM-100S transmission electron microscope.
Additional ground-grown seedlings were stained with iodine potassium iodide (IKI; O'Brien and McCully, 1981
) for examination of starch content in whole mounts. They were photographed with an Olympus BH-2 compound light microscope using Kodak Technical Pan film at an ASA of 50 (Number 2415; Eastman-Kodak, Rochester, New York, USA).
Stereology
Data were gathered from transmission electron micrograph (TEM) images. TEM negatives were scanned and analyzed using Image-Pro Plus (version 3.0; Media Cybernetics, Silver Spring, Maryland, USA) on an IBM-compatible computer. For each genotype and control, 8–9 median longitudinal root cap images were randomly chosen. Four cells within each root cap were examined at a magnification of 6200x (Fig. 2).
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. In this study, we used image analysis to calculate organelle and cell areas in order to determine the relative volumes of cell components (i.e., the ratio of the sum of points in the organelle to the sum of points lying within the cell). Organelle outlines were traced by hand using a graphics tablet. Statistical significance was determined by using ANOVA/Tukey test (P < 0.05), or, where ANOVA criteria were not met (i.e., assumption of normality), a Mann-Whitney rank sum test (P < 0.05) was used. All statistical analyses were performed on an IBM-compatible computer using Jandel Sigma Stat (Version 2.0).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Kiss et al., 1997
), morphology and starch content of roots were examined with light microscopy. Growth of seedlings on agar in comparison to growth on the nitrocellulose membrane substrate of the spaceflight containers resulted in an altered root cap morphology. Specifically, while median longitudinal sections of root caps from seedlings grown on agar show three well-developed columella cell stories (see Sack and Kiss, 1989
), membrane-grown seedlings exhibit only two columella cell stories (Fig. 2). Furthermore, the length of the root cap is reduced in seedlings grown in the spaceflight hardware. These findings were consistent for the spaceflight samples (F-µg) (Fig. 2), ground control (G-1g), and in-flight centrifuge control (F-1g) (data not shown).
In these experiments, sucrose was not added to the growth medium to avoid contamination during the spaceflight. [In contrast, in previous gravitropism studies (e.g., Kiss et al., 1997
), growth medium was supplemented with 1%, w/v, sucrose.] Therefore, we examined seedlings stained with IKI and found that starch content in the WT and intermediate-starch mutant was increased in seedlings grown with supplemental sucrose (Figs. 3, 4) in comparison to those grown without supplemental sucrose (Figs. 5, 6). Thus, growth of seedlings on nitrocellulose results in the development of two stories of columella cells, and growth without supplemental sucrose results in decreased starch content in the root cap.
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). For both stories of columella cells, almost all values for relative volumes were not statistically different among growth conditions (Table 3). One exception occurred for story 1 nuclei. Here, F-µg resulted in an increased relative volume of nucleus per cell, statistically different (P < 0.05) from F-1g centrifuge but not from G-1g.
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As a control, cell areas were measured in order to determine the effects of varying growth conditions on cell size. Cell areas for the WT, intermediate-starch mutant, and starchless mutant exhibited slight variations among the treatments (Table 4). For instance, in both stories of the WT, cell areas appeared to be somewhat influenced by the treatments. In contrast, both the intermediate-starch mutant (ACG20) and the starchless mutant (ACG21) showed no significant increases (P > 0.05) among growth conditions. However, taken together, these results indicate that the cell size was not affected by spaceflight.
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In terms of cross-genotype comparisons, the only difference among the structures examined that appeared to be affected by the treatments was that of starch relative volume (Tables 1–3). In story 1, the intermediate mutant had 1.6, 8.8, and 0.9% of the WT starch in G-1g, F-µg, and F-1g, respectively. In story 2, these values were 16, 13, and 7% for G-1g, F-µg, and F-1g, respectively.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Kiss, Wright, and Caspar, 1996
; Kiss et al., 1997
). Seedlings grown on the nitrocellulose membrane of the spaceflight hardware (described in Katembe et al., 1998
) exhibited a "less-developed" root cap compared to the root cap from agar-grown seedlings. Previous studies (Sack and Kiss, 1989
) with Arabidopsis seedlings grown on nutrient enriched agar in petri dishes demonstrated that the root cap consists of three well-developed stories (or rows) of columella cells. In contrast, the root caps of seedlings grown in spaceflight hardware had only two stories of columella cells. This difference in morphology could potentially have arisen from differing moisture exchange on the membrane in contrast to agar. However, it is also possible that given several more days of growth, these seedling root caps would become more like those of seedlings grown in petri dishes.
In this study, four central columella cells were examined, since Blancaflor, Fasano, and Gilroy (1998)
, using laser ablation studies, demonstrated that these cells are the primary cells involved in graviperception. Thus, our study was designed to consider only the cells most active in graviperception, in contrast to other studies (Moore et al., 1987
; Moore, 1990
), which quantified the effects of microgravity on the ultrastructure of columella cells within the entire root cap.
In order to avoid microbial contamination around the spaceflight specimens, we did not use sucrose in the growth medium. Thus, starch content was decreased in the roots of WT and ACG20, as seen in IKI-stained whole mounts of specimens. Kiss, Wright, and Caspar (1996)
found that mutant ACG20 had 50% of WT starch when seedlings were grown on sucrose-supplemented nutrient agar in petri dishes, but in seedlings grown without sucrose, this mutant had only 16% starch relative to the WT.
Effects of spaceflight on general columella cell ultrastructure
As assayed by transmission electron microscopy, the organization of the columella cells within the root cap was not affected by microgravity, and these results correspond to a study by Moore et al. (1987)
. In the ground controls, amyloplasts of the WT seedlings were sedimented towards the basal cell wall, although their position was maintained above the plasma membrane. In microgravity, amyloplasts appeared to be randomly positioned throughout the cell. However, previous quantitative studies have shown that, in microgravity, the three-dimensional position of amyloplasts in columella cells was not truly random (Smith, Todd, and Staehelin, 1997
). The amyloplasts of seedlings grown on the 1g centrifuge control aboard the Space Shuttle were positioned similar to amyloplasts in ground-grown seedlings, and these results are consistent with a previous study conducted by Hilaire et al. (1997)
.
Endoplasmic reticulum (ER), although not quantified, did not appear to be affected by microgravity. Both rough and smooth ER maintained a peripheral location within the cells and did not exhibit (qualitative) alterations in quantity, size, and structure. Nuclei maintained a proximal location in all growth conditions as was found in other spaceflight experiments (Volkmann, Behrens, and Sievers, 1986
; Perbal and Driss-École, 1989
; Moore, 1990
), which suggests that nuclear position is genetically programmed. In addition, mitochondria did not show a specific localization within the cytoplasm and appeared to have a uniform distribution, and they also appeared to have no differences in matrix density and cristae structure.
Effects of spaceflight on relative volumes of starch and cell organelles in columella cells
Relative volumes of starch, plastid stroma, mitochondria, and nuclei were measured as percentages of the cell area for the three strains of Arabidopsis in the three treatments. In the WT, starch was significantly (P < 0.05) decreased in the flight specimens (both F-µg and F-1g) compared to the ground control (G-1g) in both story 1 and story 2 columella cells. Although other groups (Volkmann, Behrens, and Sievers, 1986
; Moore et al., 1987
) have found that growth of seedlings in microgravity leads to an overall decrease in starch accumulation in root cap columella cells, these experiments were not conducted using an on-board flight centrifuge as a control. In addition, other studies (Hilaire et al., 1995
; Smith, Todd, and Staehelin, 1997
), which also did not have centrifuge controls, suggested that starch was not affected by microgravity. In contrast, in a study that did include an in-flight 1-g control, Perbal and Driss-École (1989)
reported that amyloplasts have a greater volume in columella cells of seedlings that developed in microgravity, but this report did not specifically quantify the volume of starch in the plastids. However, based on our arguments presented below, we suggest that in our experiment, spaceflight environmental effects resulted in a decrease in starch in columella cells, and these decreases in starch were not a direct effect of microgravity.
The importance for 1g on-board centrifuges during spaceflight experiments as a control is evident in this study, as well as others (Krikorian, 1996
; Perbal, Legué, and Driss-École, 1996
). A number of stresses during spaceflight (i.e., vibrations, accelerated g forces, cosmic radiation, or lack of convection) could cause developmental changes in plants. Although such changes may be attributed to microgravity, they may be an indirect effect of spaceflight.
Controls for stereological methods
In the above discussion, relative volumes of cell components were represented as percentages of the cell area. In order to establish that variations in cell size did not affect these values, we compared (1) cell areas and (2) organelle areas (i.e., not as relative volumes, or percentages of cell area, but rather as true areas). Even though the WT F-1g was different from other treatments, taken together, these results indicate that the cell size was not affected by spaceflight. All other cell areas were not significantly different.
In order to determine that differences in cell size did not affect relative volume data of starch, plastid stroma, mitochondria, and nuclei, we compared the total areas of these components per cell. Similar to the above relative volume results, starch was decreased in spaceflight (F-µg and F-1g) in comparison the G-1g control, again indicating that some aspect of spaceflight other than microgravity was involved.
Ethylene and other environmental effects during spaceflight
A recent study from our laboratory group (Kiss, Katembe, and Edelmann, 1998
) suggested that ethylene aboard the Space Shuttle may have affected the growth and morphology of these seedlings. Based on air samples taken during the mission, the concentration of ethylene ranged from 1.1 to 1.6 ppm (Kiss et al., 1999). The altered morphology observed in the flight-grown seedlings best fits the triple response associated with high levels of ethylene (Smalle and Straeten, 1997
): (1) an exaggerated hypocotyl hook, (2) inhibition of root and stem elongation often associated with an increase in radial expansion of these organs, and (3) a decrease in the gravitropic response. A recent study has shown that soybean seedlings grown in space produced significantly more ethylene than seedlings grown on Earth, and space-grown plants produced 20–25% less starch in cotyledons than the ground controls (Brown et al., 1995
). In addition, increased ethylene production for plants on a clinostat was noted by Hilaire and coworkers (1996)
.
In the present study, starch in columella cells of both the WT and intermediate mutant decreased in controls in which ethylene was added to seedlings grown on the ground. Based on these results and the fact that elevated ethylene levels were found during the spaceflight, we propose that ethylene aboard the Space Shuttle was responsible for decreased starch in both flight samples (F-µg and F-1g). Indeed, it has been shown by other investigators (Brown et al., 1995
) that plants producing elevated levels of ethylene accumulate less starch. However, it is possible that factors such as cosmic radiation or vibrations other than ethylene associated with spaceflight may also have contributed to the results of the present study.
Given the role of starch in graviperception (Sack, 1997
; Weise and Kiss, 1999
), decreased starch may result in a decreased gravitropic sensitivity of plants grown in space. In contrast, Volkmann and Tewinkel (1996) found that roots grown in microgravity are more sensitive to gravity (as applied by a centrifuge). Nevertheless, issues of gravitropic sensitivity may be relevant to the growth of crop plants in advanced life support systems or in spaceflight (Musgrave, Kuang, and Matthews, 1997
; Salisbury, Gitelson, and Lisovsky, 1997
) and could affect future plans for growing plants in space.
Conclusions
In this study, we found that starch content in root cap columella cells was altered in seedlings grown in spaceflight. Specimens under the conditions of F-µg and F-1g exhibited a decrease in relative volumes of starch in comparison to the G-1g control, indicating that some factor associated with spaceflight, other than microgravity, was responsible for this effect. Adding ethylene to the seedlings also caused a decrease in starch in columella cells of the root cap. Thus, we propose that elevated levels of ethylene aboard the Space Shuttle were responsible for altered metabolism of carbohydrates. This was the first study to use an on-board centrifuge as a control when quantifying starch, and the importance for this control was demonstrated. Furthermore, our results show that ethylene levels must be carefully considered and controlled when designing plant experiments for the International Space Station.
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FOOTNOTES |
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2 Author for correspondence (e-mail: kissjz{at}muohio.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Brown, C. S., E. M. Hilaire, J. A. Guikema, W. C. Piastuch, C. F. Johnson, E. C. Stryjewski, B. V. Peterson, and D. S. Vordermark. 1995 Metabolism, ultrastructure and growth of soybean seedlings in microgravity: results from the BRIC-01 and BRIC-03 experiments. American Society for Gravitational and Space Biology Bulletin 9: 93.
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