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Physiology and Biochemistry |
Department of Botany, Miami University, Oxford, Ohio 45056 USA
Received for publication 15 August 2007. Accepted for publication 30 November 2007.
ABSTRACT
The ability of a plant to respond to gravity is crucial for growth and development throughout the life cycle. A key player in the cellular mechanisms of gravitropism is ARG1 (altered response to gravity), a DnaJ-like protein that associates with components of the vesicular trafficking pathway and carries a C-terminal domain with similarities to cytoskeleton-associated proteins. The arg1–2 mutant of Arabidopsis thaliana has reduced and delayed gravitropism in roots, shoots, and inflorescence stems when grown in the light or dark. We performed light microscopic studies of plastid movement in the gravity-perceiving statocytes (endodermal cells) of hypocotyls of arg1–2 and WT light-grown seedlings following reorientation to better characterize the role of ARG1 in gravitropism. Cryofixation/freeze substitution procedures were used because they provide a reliable indication of rapid cellular events within the statocytes. Our results suggest that ARG1 affects gravitropism by reducing plastid movement/sedimentation, a process known to be essential for early phases of signaling cascades in the statocytes.
Key Words: actin cytoskeleton • Arabidopsis • arg1–2 (altered response to gravity1–2) • endodermis • gravitropism • plastid movement • statocytes
Plants actively sense a number of stimuli in their surrounding environment. These include abiotic factors such as light, wind, water, temperature, and gravity. As a result of responses to these external stimuli, various important metabolic activities occur within the plant cell. Gravity is one key environmental factor for plants, and gravitropism is the directed growth in response to gravity. Gravitropism in plants occurs in three temporal stages—gravity perception, signal transduction, and organ response (Chen et al., 1999
; Kiss, 2000; Blancaflor and Masson, 2003).
Gravity perception in flowering plants is associated with the movement and sedimentation of dense, starch-filled plastids or amyloplasts (reviewed in Sack, 1997; Kiss, 2000). Gravity perception in roots occurs within the central columella cells (Boonsirichai et al., 2002), whereas the perception in stems occurs in endodermal cells (Fukaki et al., 1998; Moctezuma and Feldman, 1999; Weise and Kiss, 1999). In recent studies of Arabidopsis leaves, sedimentation of amyloplasts in the leaf petiole was shown to play an important role in gravity perception (Mano et al., 2006). Most research to date supports the starch–statolith hypothesis for gravity perception (reviewed in Sack, 1997; Kiss, 2000; Vitha et al., 2007).
During the transduction phase, the information produced by the sedimenting amyloplasts is transformed into a cascade of signaling events. In both gravity perception and signal transduction, the cytoskeleton is hypothesized to interact with the sedimenting amyloplasts (Balu
ka and Hasenstein, 1997). Space experiments have suggested that amyloplasts are attached to actin filaments via motor proteins (Perbal et al., 1997). Two models have been proposed to explain the cytosekeletal-based gravity transduction. The actin-tether model proposes that the amyloplasts are anchored to the cytoskeletal components that are in turn connected to plasma membrane receptors and other proteins (Baluka and Hasenstein, 1997). In contrast, the tensegrity model also emphasizes the role of cytoskeleton in transducing the signal generated by the sedimenting amyloplasts in the columella cells of roots (Yoder et al., 2001). According to this model, the actin-based cytoskeletal network is disrupted by the sedimenting amyloplasts that travel through channels in columella cells (Staehelin et al., 2000; Yoder et al., 2001).
Pharmacological studies in plants have demonstrated the function of the cytoskeleton in gravity signal transduction. The disruption of actin cytoskeleton by latrunculin B in the root cap cells of maize enhanced root curvature after a 90° reorientation (Hou et al., 2003). Similarly in inflorescence stems and hypocotyls of Arabidopsis, disruption of actin cytoskeleton resulted in the promotion of gravitropism (Yamamoto and Kiss, 2002). Several studies have suggested that microfilament-associated proteins such as myosins are involved in gravisensing (e.g., Palmieri et al., 2007). In flowering plants, myosin-like proteins are localized at the surface of the sedimenting amyloplasts (Baluka and Hasenstein, 1997; Volkmann and Baluka, 2000; Blancaflor, 2002).
In terms of downstream events, the sedimentation of amyloplasts may result in an increase in cytoplasmic ion levels that triggers signal transduction leading to root curvature, but the precise role of calcium in gravity signal transduction is yet to be resolved (Boonsirichai et al., 2002; Blancaflor and Masson, 2003). Auxin is involved in the response phase of gravitropism and accumulates differentially on either side of the plant organs to result in differential growth leading to curvature (Moore, 2002; Muday and Murphy, 2002; Shin et al., 2005).
The isolation of several mutants has been useful in the study of the cellular mechanisms of gravitropism. For example, the altered response to gravity/root and hypocotyl gravitropism (arg1/rhg) mutants and arg1-like2 (arl2) mutants of Arabidopsis are hypothesized to participate in the early phases of gravity signal transduction (Fukaki et al., 1997; Sedbrook et al., 1999; Guan et al., 2003). The kinetics of root and hypocotyl curvature of arg1 mutants is slower than in the WT, and the mutants lack cytosolic alkalinization of columella cells in the root cap. The ARG1 gene encodes a type II DnaJ-like protein containing a coiled coil region that is homologous to the regions found in cytoskeleton-associated proteins, suggesting the possible interaction of ARG1 with the cytoskeleton during the early phases of gravitropism (Sedbrook et al., 1999). The DnaJ-like proteins act as molecular chaperones that are bound to Hsp70 (heat shock protein 70). Because this protein has a J domain, ARG1 may be involved in the folding of the proteins that interact with the cytoskeleton.
ARG1 also has been shown to be a peripheral membrane protein sharing subcellular compartments involved in vesicular trafficking of PIN proteins (auxin efflux carriers), and it appears to play a role in the trafficking of proteins and vesicles (Boonsirichai et al., 2003). There is also evidence that ARG1 is involved in early gravity signal transduction influencing the pH changes and auxin distribution in the cells. The arg1 mutants have normal phototropism, normal root responses to hormones and inhibitors of auxin transport, and a normal amount of starch in the statocytes (Sedbrook et al., 1999).
In this paper, we examine plastid movement in the endodermal cells of hypocotyls of arg1–2 seedlings. The arg1 mutant was the focus of our studies because this mutant could be used to test the hypothesis that amyloplast movement is related to the actin cytoskeleton in the early stages of gravitropism. Cryofixation was used to capture the rapid events associated with the movement of these statoliths following reorientation of the plants.
MATERIALS AND METHODS
Plant material and growth conditions for seedlings
Seeds of wild-type (ecotype Wassewskija) and the arg1 mutant of Arabidopsis thaliana (L.) Heynh. (Brassicaceae) were obtained from Dr. Patrick Masson (University of Wisconsin). The seeds were surface sterilized in 70% (v/v) ethanol for 5 min followed by 95% (v/v) ethanol with 0.02% (v/v) Triton-X for 2 min. Seeds were rinsed with double-distilled water with 0.02% (v/v) Triton-X and then with double-distilled water 3–4 times. The seeds were then sown in square Petri plates (containing nitrocellulose film placed on solidified nutrient medium; Yamamoto and Kiss, 2002). The nutrient medium contained 1.2% (w/v) agar, half-strength Murashige and Skoog medium, and 1% (w/v) sucrose and 1 mM MES buffer (pH 5.5).
The Petri plates containing seeds were wrapped in black aluminum foil and placed at 4°C for 24 h to facilitate uniform germination of seeds. The plates then were placed under appropriate light and dark conditions depending on the experimental treatment. For light-grown experiments, the plates were placed vertically under white light with a fluence rate of 60–80 µmol·m-2·s-1 for 4 d. Further, the plates were photographed in darkness under dim green light (0.8 µmol·m-2·s-1) at 0, 2, 4, 6, 8, 10, 12, 24, 48 h time intervals using a Nikon (Melville, New York, USA) digital camera.
Culture conditions for studies with inflorescence stems
Experiments were conducted in inflorescence stems using WT and arg1–2 mutants. Seeds were surface sterilized using 30% (v/v) commercial bleach solution containing 0.002% (v/v) of Triton-X for 15 min and rinsed in double distilled water, and the seeds then were sown in pots and grown under white light as described in Kumar and Kiss (2006). When the plants were 21–25 d-old, the pots were reoriented and inflorescence stems were photographed in dim green light at 0, 2, 4, 6, 8, 10, 12 and 24 h intervals using a Nikon digital camera.
Data analyses for growth and culture studies
Growth and curvature measurements of hypocotyls and roots of seedlings and inflorescence stems were obtained using Image Pro Plus software (version 5.1, Media Cybernetics, Silver Spring, Maryland, USA). Both growth and curvature measurements were obtained from the same plants, and seedlings that deviated more than 20° from the vertical were excluded from the studies. Growth and curvature values are increments from the starting values. Statistical analyses were conducted using Sigma Stat software (version 2.03). For pairwise comparisons, a t test was performed, except when the normality test failed (P < 0.05), in which case a Mann–Whitney rank sum test was performed. All growth and curvature experiments were replicated three times, and each replicate consisted of 3–4 experiments.
Cryofixation procedures
Six-d-old seedlings were cryofixed at indicated times (vertical orientation, 0, 0.5, 1, 2.5, 5, 7.5, 10 and 15 min following reorientation) by immersion into liquid propane cooled by liquid nitrogen, and then freeze substituted in 1% (w/v) osmium tetroxide with 100% (v/v) glass-distilled acetone according to Kiss et al. (1990) and Kiss and McDonald (1993). Four to six hours before the experiment, one of the leaves on the right side was cut using a razor blade from these seedlings to mark the side to which the seedling was reoriented. This selective process helped in identifying the direction of reorientation during the processing of plants. The cryofixed seedlings were stored in freeze substitution medium in –80°C refrigerator until further processing.
Specimens were thawed from –80°C to –20°C, then to 4°C (4 h interval at each temperature) and eventually to room temperature (overnight). The specimens were transferred to acetone : ethanol gradients from 4:1, 3:1, 2:1, 1:1, 1:2, 1:3, 1:4 (30 min duration each) and 100% ethanol (2 h duration). The samples were then infiltrated into L. R. White resin according to the following schedule (ethanol: L. R. White) – 3:1. 2:1, 1:1, 1:2, 1:3, followed by two changes in 100% L. R. White resin. The samples were flat embedded in 100% L. R. White Resin by preparing custom molds as described in Palmieri and Kiss (2005). Because the light-grown seedlings are wider than the etiolated seedlings used in our previously published studies, we used polycarbonate sheets with a thickness of 1.55 mm (Cat #85585K14, McMaster-Carr, Cleveland, Ohio, USA) to make the molds deeper. The samples were polymerized at 60°C for 18–20 h. The resin blocks with plant specimens were trimmed, and semithin sections (1 µm) were obtained using a Reichart Ultracut microtome (Leica, Bannockburn, Illinois, USA) and a diamond knife (Diatome, Histo knife, Hatfield, Pennsylvania, USA). The sections were stained in 0.1% (w/v) toluidine blue. These experiments were replicated a minimum of four times.
Light microscopic studies and data analysis
Light microscopy was used to analyze plastid movement/sedimentation in endodermal cells of arg1 and WT hypocotyls in light-grown seedlings following reorientation. The sections were photographed using brightfield optics on an Olympus AX70 microscope (B & B Microscopes, Pittsburgh, Pennsylvania, USA), and plastid displacement was analyzed using Image Pro Plus software (version 5.1, Media Cybernetics, Silver Spring, Maryland, USA). Angular (plastid angle relative to the gravity vector and plastid angle relative to the cell corner) and linear measurements (plastid distance relative to the original cell wall) were obtained from the endodermal cells according to MacCleery and Kiss (1999) as modified by Palmieri and Kiss (2005). Only endodermal cells within the range of 1: 4–1:6 (width : length) ratio were selected for data analyses. Variables measured included cell trace, average cell width, average cell length, cell center, original gravity vector, cell corner, plastid center, and distance of the plastids to the new cell wall.
To quantify any differences in plastid movement, we used the generalized least squares regression (Pinheiro and Bates, 2000) to analyze angular measurements and linear measurements of the plastids over time. This regression is similar to the ordinary least squares regression, except that it allows complex models of the variance structure. For our data, the variance structure was best approximated as a single power function of the fitted values. Hence, larger values (either angles or linear distances) were expected to be more variable. The data were tested for complex curvilinear relations between time and angle or distance. However, in each case, the most parsimonious model included only a linear effect of time, the effect of the mutation, and the time–mutant interaction. Thus, this method was used in Figs. 7–9 to analyze the data on plastid movement.
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The arg1 mutation affects gravitropic curvature and growth rates in seedlings and plants
We conducted time course of curvature studies to confirm and extend the previous studies of gravitropism in WT and arg1 plants (e.g., Sedbrook et al., 1999). In particular, we studied gravitropism in both dark- and light-grown seedlings as well as in adult plants. Gravitropism is greatly reduced in arg1 hypocotyls of the dark-grown seedlings compared to those of the WT (Fig. 1A). For all time points, curvature of the arg1 mutant was significantly less (P < 0.05) compared to WT curvature, and there was little or no gravitropic curvature in the hypocotyls of arg1 mutants. Gravitropism in roots of dark-grown seedlings also was reduced and delayed compared to the WT (Fig. 1B). Gravitropic curvature from 4 h onward was significantly less (P < 0.05) in arg1 compared to WT. For instance, at 24 h in the time course, curvature of the mutant was 29% that of the WT, and by 48 h, it was only 23% that of the WT.
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), this phenomenon was notably absent in the inflorescence stems of the arg1 mutant.
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; Palmieri and Kiss, 2005). Prior to reorientation of seedlings, amyloplasts sedimented toward the original distal end of the endodermal cell in both arg1 and WT (Fig. 5). At 10 min after reorientation, most WT plastids had rounded the cell corner and had sedimented toward the new lower cell wall. In contrast in the arg1 mutant at 10 min, most of the plastids appeared to have sedimented to the end of the endodermal cell toward the original gravity vector (i.e., prior to reorientation). By 20 min, there appeared to be further movement of the arg1 amyloplasts, but sedimentation in the endodermal cells did not appear to be complete relative to the WT.
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; Palmieri and Kiss, 2005), we obtained two sets of angular measurements—plastid angle relative to the cell corner (Fig. 7) and plastid angle relative to the gravity vector (Fig. 8). We also obtained two sets of linear measurements—distance of the plastids relative to the original cell wall (Fig. 9) and distance of the plastids relative to the new cell wall (data not shown).
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8.1°/min) as the mutant plastids (4.3°/min), and there is a significant difference in the regression slopes (95% confidence interval = 2.40 to 5.95). Therefore, the plastids in the WT changed position more quickly over time when compared to the mutant.
Our data indicate that the plastids in both mutant and WT started at a similar angle in terms of the plastid angle relative to gravity (Fig. 8). However, the plastid angle relative to the gravity vector was significantly less in the arg1–2 mutant over time after reorientation when compared to WT (Fig. 8). The WT plastids moved almost twice as fast (6.6°/min) as mutant plastids (3.8°/min); and there is a significant difference in the regression slopes (95% confidence interval = 1.00 to 4.58).
The final variable considered was linear measurement of plastid movement in the endodermal cells (Fig. 9). Linear plastid distance was shorter in arg1 compared to WT over time after the reorientation of the seedlings. Thus, these results also suggest that the plastid movement was slower in arg1 mutants than the WT. The wild type plastids moved approximately twice as fast (1.9 µm/min) as mutant plastids (1.0 µm/min); and there is a significant difference in regression slope (95% confidence interval = 0.506 to 1.401). Taken together, by all three variables tested, the plastids clearly move less in endodermal cells after reorientation of seedlings in the arg1 mutant than in the WT. The rate of plastid movement in the mutant is only half the rate observed in the WT plants. Therefore, both gravitropism and plastid movement in the statocytes are reduced and delayed in the arg1 mutant relative to the WT.
DISCUSSION
Gravitropism is reduced and delayed in arg1
Previous studies have shown that the arg1 mutation affects gravitropism in seedlings and mature plants. Our aim in this study was to confirm and extend this characterization of arg1 in three organs under different culture conditions. For instance, the study by Sedbrook et al. (1999) focused primarily on gravitropism of dark-grown seedlings. In addition, in their experiments these authors used a single time (72 h) as an assay for gravitropism in hypocotyls of dark-grown seedlings. In this paper, we extended their results by studying the time course of curvature up to 48 h (Fig. 1A) and showing a reduced and delayed response in arg1 hypocotyls throughout the time course (Fig. 1A). Gravitropic curvature studies of roots of dark-grown seedlings also had a delayed response in arg1 roots compared to WT (Fig. 1B). Although these results are consistent with previous studies (Sedbrook et al., 1999), we saw a greater difference between arg1 roots and WT roots. For example, at 24 h in the time course, Sedbrook et al. (1999) found that arg1 achieved 56% of WT curvature while we found this value to be only 29%.
There were a number of interesting differences in growth and gravitropism between the current study and the previous research from the Masson laboratory (e.g., Sedbrook et al., 1999; Boonsirichai et al., 2003). Some of these may be due to different types of culture conditions. The most notable differences were agar (1.2% for our studies vs. 0.8% for the Masson group), sucrose (1% vs. 1.5%), and the fact that we used nitrocellulose on top of the agar layer. The growth of the seedlings on the nitrocellulose layer allowed us to avoid the slanting behavior of the roots described by Rutherford and Masson (1996) and to obtain a more accurate assay of tropistic curvature (Ruppel et al., 2001).
In addition to studies of dark-grown seedlings, we also studied light-grown seedlings (Fig. 2A and 2B). Gravitropism of hypocotyls was severely impaired in the arg1 mutant in the latter part of the time course, although in the initial stage the curvature was similar in the WT and mutant (Fig. 2A). Gravitropism in roots of light-grown seedlings (Fig. 2B) seemed even more impaired when compared to dark-grown plants in that by 24 h, arg1 achieved only 15% of WT curvature in light-grown (compared to 29% in the dark). Taken together, our data show a more drastic impairment of arg1 gravitropism curvature in light- compared to dark-grown conditions.
In addition to assaying gravitropism in seedlings, we also examined gravitropism in inflorescence stems of mature plants (Fig. 3). Gravitropic curvature was reduced and delayed in inflorescence stems as well as in seedlings, but the relative magnitude of inhibition was less in inflorescences compared to seedlings. For instance, in hypocotyls, the arg1 mutants had as little response as 15% of WT curvature, but in inflorescence stems, the greatest inhibition of arg1 relative to WT was 63%. In addition, the arg1 mutant lacked the typical "overshoot" response typically found in WT inflorescence stems (Fukaki et al., 1996; Weise and Kiss, 1999).
Plastid movement in statocytes is reduced and delayed in arg1
Because plastids are known to play an important role during early phases of gravitropism, we investigated whether ARG1 participates in the gravisensing mechanism in plants (Kiss, 2000; Blancaflor and Masson, 2003). Therefore, we studied the kinetics of plastid movement in the statocytes (i.e., endodermal cells) of hypocotyls of the arg1 mutant and compared this variable with that of the WT seedlings. Cryofixation and light microscopic studies revealed that the amyloplast movement is reduced and delayed in arg1 statocytes when compared to those of the WT (Fig. 5). This delay is not due to plastid mass since Sedbrook et al. (1999) showed a similar starch content in statocytes (roots and hypocotyls) of arg1 and the WT.
The angular measurements and linear distance measurements of the plastids were measured as done previously (MacCleery and Kiss, 1999; Palmieri and Kiss, 2005). The results from these variables—plastid angle relative to the cell corner (Fig. 7), plastid angle relative to gravity (Fig. 8), and linear distance moved by plastids (Fig. 9)—showed that plastid movement in the endodermal cells of the arg1 mutant is reduced relative to the WT.
Role of cytoskeleton in the gravitropism
On the basis of the structural homology of ARG1 protein with other cytoskeleton-interacting proteins such as myosin, we hypothesize that ARG1 might be associated with the actin cytoskeleton (Sedbrook et al., 1999). The ARG1 protein consists of 450 amino acids with a J-domain at the N-terminal followed by a hydrophobic region in the center and a coiled coil domain at the C terminus (Sedbrook et al., 1999; Boonsirichai et al., 2003). The DnaJ-domain proteins interact with heat shock chaperones involved in a variety of functions such as protein folding and trafficking (Perrin et al., 2005). ARG1 and ARL2 are two paralogous proteins that seem to function similarly and are required for normal root and hypocotyl gravitropism in dark-grown seedlings (Guan et al., 2003). Our study suggests that ARG1 may modulate plastid movement through its interaction with the cytoskeleton. Although we do not know exactly how ARG1 interacts with the cytoskeleton and directs plastid movement, our results suggest that ARG1 plays a role in plastid movement that is important in gravity perception.
It is well established that the cytoskeleton plays an important role in the mechanisms of gravitropism (Volkmann and Sievers, 1979; Sack 1991; Sack et al., 1984; Blancaflor 2002; Yamamoto and Kiss, 2002; Palmieri and Kiss, 2005; Perrin et al., 2005). Amyloplasts may interact directly or indirectly with the cytoskeleton during the sedimentation process in gravisensing statocytes. Two models have been proposed to explain the role of the cytoskeleton and statoliths in the gravity perception mechanism—the restrained model and the unrestrained model (Baluka and Hasenstein, 1997). According to the restrained model, the organelles within a cell are physically restricted by the cytoskeleton and are not free to move within the cell. When the cell is gravistimulated, the organelles are proposed to exert pressure on the cytoskeleton and the membrane receptors because they are interconnected. According to the unrestrained model, when the cytoskeleton is not robust, the sedimentation of statoliths occurs within the root statocytes.
Recently, the tensegrity model also has been proposed to explain the role of the cytoskeleton during amyloplast sedimentation in root statocytes (Staehelin et al., 2000; Yoder et al., 2001). According to this model, the actin cytoskeleton forms a channeled network across the cytoplasm linking the stretch receptors at the plasma membrane. In this model, the amyloplasts are not physically attached to this cytosekeletal network. During the sedimentation process, the amyloplasts fall through the network and disrupt the connection, eventually causing the stretch receptors to be activated. When a cell is exposed to mechanical force such as gravity, the internal stress on the cytoskeleton is balanced out by the equal and opposite forces generated by microtubules, microfilaments, intermediate filaments, proteins, enzymes, and the transmembrane receptors (Ingber, 2003a). As a consequence, the ion channels are opened due to stress because they are linked to the cytoskeleton (Ingber, 2003b), and this opening of channels may ultimately end in a cellular response resulting in the differentiation or bending of the organ.
The change in amyloplast movement in statocytes of arg1 may be due to alteration of the actin cytoskeleton. Pharmacological studies have shown that cytoskeleton disruption in the statocytes of roots and shoots results in an enhancement of the gravitropic response in roots and hypocotyls (Hou et al., 2004; Yamamoto and Kiss, 2002; Palmieri and Kiss, 2005). In Arabidopsis hypocotyls, while the application of latrunculin B, an inhibitor of F-actin polymerization resulted in an increased curvature response, amyloplast movement was arrested (Palmieri and Kiss, 2005). Thus, this study suggests a role of amyloplast pressure on a sensitive surface (Volkmann and Sievers, 1979) instead of the plastid movement. In contrast, the results of our present study suggest that amyloplast movement per se in statocytes plays an important role in gravity perception. However, multiple mechanisms in the cell could be involved in gravity perception, thus allowing for both amyloplast movement and pressure to play a role in the process (Barlow, 1995; MacCleery and Kiss, 1999).
ARG1 plays a role in both perception and the response phases of gravitropism
Previous reports have shown that ARG1 is involved in auxin transport and the response phase of gravitropism (Sedbrook et al., 1999; Boonsirichai et al., 2003). The results of our study suggest that ARG1 plays a role in plastid movement in the statocytes as well and that this protein is involved in gravity perception. One possible scenario is that ARG1 interacts with the actin cytoskeleton to modulate gravity-dependent plastid movement. Taken together, our study supports a complex role for the actin cytoskeleton in the cellular mechanisms of gravitropism.
FOOTNOTES
1 The authors thank P. H. Masson for his critical review of the manuscript and M. Duley for technical advice. Financial support was provided by a grant from the National Aeronautics and Space Administration (NCC2-1200). 
2 Author for correspondence (e-mail: kissjz{at}muohio.edu)
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