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. 1998 Jul;117(3):893–900. doi: 10.1104/pp.117.3.893

Autonomic Straightening after Gravitropic Curvature of Cress Roots1

Bratislav Stanković 1,2, Dieter Volkmann 2, Fred David Sack 1,*
PMCID: PMC34943  PMID: 9662531

Abstract

Few studies have documented the response of gravitropically curved organs to a withdrawal of a constant gravitational stimulus. The effects of stimulus withdrawal on gravitropic curvature were studied by following individual roots of cress (Lepidium sativum L.) through reorientation and clinostat rotation. Roots turned to the horizontal curved down 62° and 88° after 1 and 5 h, respectively. Subsequent rotation on a clinostat for 6 h resulted in root straightening through a loss of gravitropic curvature in older regions and through new growth becoming aligned closer to the prestimulus vertical. However, these roots did not return completely to the prestimulus vertical, indicating the retention of some gravitropic response. Clinostat rotation shifted the mean root angle −36° closer to the prestimulus vertical, regardless of the duration of prior horizontal stimulation. Control roots (no horizontal stimulation) were slanted at various angles after clinostat rotation. These findings indicate that gravitropic curvature is not necessarily permanent, and that the root retains some commitment to its equilibrium orientation prior to gravitropic stimulation.

The reorientation of most plant organs results in gravitropic curvature that normally persists for the life of the organ. This curvature is due to differential growth that at some point becomes stabilized and long-lasting. However, before stabilization, the locus of gravitropic curvature actually migrates in some organs (Firn and Digby, 1979; MacDonald et al., 1983; Tarui and Iino, 1997; for review, see Stanković et al., 1998). Thus, some curved regions later straighten, and more basal regions that were straight later become curved. Although the net result is a curved organ, loss of gravitropic curvature (axis straightening) does occur distal to the final curve.

The local straightening described above occurs in organs that are kept stationary with a constant g stimulus. In contrast, straightening throughout the organ seems to occur when a g stimulus is withdrawn by placement in microgravity in spaceflight or by rotation of the plant on a clinostat on earth (for review, see Stanković et al., 1998). The loss of gravitropic curvature in space has been documented using oat coleoptiles and cress (Lepidium sativum L.) roots (Chapman et al., 1994; Volkmann and Tewinkel, 1996). Seedlings centrifuged in flight at 1g continued gravitropic curvature when removed from the centrifuge. Later, previously curved regions straightened in microgravity so that the organ approached the angle it was in prior to the 1g stimulus.

There are also relatively few descriptions of the straightening of gravitropically curved organs resulting from the use of a clinostat in ground-based studies. In some cases, straightening apparently only occurred at very slow speeds of rotation (0.008–0.016 rpm), and not at higher speeds (roots of Artemisia absinthium and cress; Larsen, 1953, 1957). In another report, loss of gravitropic curvature took place when roots were rotated at 2 and 4 rpm (Arabidopsis; Mirza et al., 1984). But Larsen's studies did not continually follow the same roots through time and none of these reports analyzed the regions of the root responsible for straightening. Other studies on the effects of clinostat rotation on cress roots (Hensel and Iversen, 1980; Hoson et al., 1997) did not address the presence and extent of straightening. Moreover, it cannot be assumed that because curved cress roots straighten in microgravity (Volkmann and Tewinkel, 1996) they will also do so on a clinostat, since oat coleoptiles lose gravitropic curvature in space but not on a clinostat (Chapman et al., 1994). Obviously, stimulus withdrawal in space and on a clinostat are qualitatively different, since clinostat rotation results in a continuously changing stimulation that is circumlateral (one axis of clinostat rotation) or omnilateral (three-dimensional clinostat; Hoson et al., 1997), whereas in microgravity, a g stimulus is essentially eliminated.

Relatively few data exist that document the response of curved organs to a withdrawal of a constant g stimulus. Further study of this response is valuable both in evaluating the stability of gravitropic curvature and in understanding how the orientation of new growth is coordinated with that of older regions. For example, for organ straightening to occur, curved regions must straighten and new growth must be coordinately aligned (Fig. 1E). Such alignment is only one of several possible fates, since in theory the growth that occurs in the absence of a constant g stimulus could be random or could reference persistent or past internal signal distributions (Fig. 1, A–D).

Figure 1.

Figure 1

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Theoretically possible outcomes of the direction of root growth after gravitropically curved roots are then rotated on a clinostat. In A to D, the root retains gravitropic curvature and only new growth (black segments) is affected. A, Return to original vertical. B, No change from previous direction. C, Persistence of an internal signal gradient established by a previous constant g stimulus. D, Random growth. E and F, Loss of gravitropic curvature (root straightening) on clinostat and roots either fully (E) or partially (F) return to prestimulus vertical.

To address these issues, the behavior of individual cress roots was followed through reorientation and subsequent rotation on a clinostat. We demonstrate that clinostat rotation results both in the loss of gravitropic curvature and in the coordinated alignment of new growth to produce mostly straight roots. However, these roots do not return completely to the prestimulus vertical (Fig. 1F), and the final angle between the root and the former vertical is positively related to the length of prior stimulation.

MATERIALS AND METHODS

Plant Material and Experimental Procedure

Seeds of garden cress (Lepidium sativum L.) were obtained from Chrysant (Bonn, Germany), allowed to imbibe in double-distilled water, and then germinated on filter paper in vertically positioned plastic Petri plates. After 24 h in darkness at 22 ± 1.5°C, roots were approximately 5 mm long. Dishes were then turned to the horizontal for 1 or 5 h in darkness and then, along with vertical controls, were placed on a clinostat (Fig. 2A). The custom-made clinostat was built with a 1 rpm synchronous instrument motor (model KS, Hurst Corp., Princeton, IN). Roots were rotated for 6 h either in an “axial” configuration (the long axis of the base of the root was parallel to the axis of clinostat rotation) or in a “somersault” configuration (root axis perpendicular to the axis of rotation).

Figure 2.

Figure 2

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Diagram of experiment and angle measurement. A, Vertically grown roots (24 h) were turned to the horizontal and then rotated on a clinostat in two different configurations (curved arrow, bottom center). The gravity vector is toward the bottom of the diagram. B and C, Method of angle measurement relative to the original vertical (prestimulus) reference line (0°). Tracings from gravitropically curved roots after 5 h of horizontal stimulation (B, gravity vector toward left) and then after 6 h of rotation on a clinostat (C). The boundary (arrowhead) between the hypocotyl (light shading) and the root base is distinguished by root hairs (fine lines). The seed coat (dark shading) is shown at the top. C, Decrease in the angle of the apical and middle segments indicates a loss of gravitropic curvature and root straightening. Bar in B = 0.5 cm.

Video Imaging and Data Analysis

Roots on the clinostat were continuously illuminated with dim-green light (intensity of approximately 0.9 μmol m−2 s−1 at root level) provided by an incandescent lamp filtered through two layers of a Roscolux filter (no. 1090, Rosco Laboratories, Port Chester, NY) with a peak transmission of 526 nm and a half-bandwidth of about 58 nm. This enabled visualization of root growth and behavior using a Hi8 videocamera (model CCD-V101, Sony, Tokyo, Japan). Images were archived at 1-h intervals using a videocassette recorder (model EV-5900, Sony) and were subsequently digitized using a computer equipped with a video capture card (Snappy Play, Inc., Rancho Cordova, CA). Images were stored and processed using imaging software (Adobe Photoshop 4.0).

To measure curvature, roots were divided into three segments (Fig. 2, B and C): the tipmost 2 mm, the next 4 mm (middle or subapical segment), and the entire remaining basal segment. The basal segment extended to the base of the hypocotyl, which could be distinguished from the root by the absence of root hairs on the hypocotyl and by the larger diameter and the lighter color of the root. Even though the basal segment varied in length from 2 to 7 mm (depending upon the overall length and age of the root), initial experiments indicated that it showed enough uniformity in the distribution of curvature that it could be quantified as a single segment. To test methods of delimiting root segments, root-straightening data were compared for the same sample of 10 roots divided either into three segments as above or into 2-mm segments throughout the length of each root. Since all trends were comparable using both methods for individual roots and for pooled data (data not shown), the simpler three-segment method was adopted. The angle measured was between the tangent of each of the three segments and the original vertical reference line designated as 0° (Fig. 2B).

RESULTS

Cress roots turned to the horizontal for 1 h curved down gravitropically at a mean of 62 ± 5° (± se). When such roots were subsequently placed on a clinostat and rotated for 6 h, some gravitropic curvature was lost and the roots mostly straightened (Fig. 3, A and C). This straightening on the clinostat occurred in part in regions of the root that previously had curved gravitropically (Fig. 3, A, C, and E). Loss of gravitropic curvature of the root was observed regardless of whether the direction of rotation of the clinostat was around the root axis (axial configuration, Fig. 3A) or perpendicular to the root axis (“somersault” configuration, Fig. 3C). Vertically grown (control) roots grew in a more or less straight direction on a clinostat, although frequently these roots slanted or curved spontaneously away from their original direction of growth (Fig. 3, B and D).

Figure 3.

Figure 3

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Images of the same roots through time showing the loss of gravitropic curvature (after 1 h of horizontal stimulation) during rotation on a clinostat (A, C, and E). Control roots were kept vertical prior to placement on a clinostat (B and D). The numbers indicate the time elapsed (hours) following placement on a clinostat. Each figure (A–D) shows a different sample of six roots with each root depicted three times. The positions of the roots are different in A and B versus C and D to reflect the orientation of clinostat rotation that was either in a “somersault” configuration (A and B) or in an axial configuration (C and D). The circular arrow at the right indicates the direction of rotation of the clinostat. The original gravity vector was toward the bottom of the figure for A, B, and E. Arrowheads indicate the transition zone between the root and the hypocotyl. Bar = 1 cm for A to D. E, Tracings from a single root kept horizontal for 1 h and then rotated on a clinostat for 6 h. The white and gray images show the root at the time labeled and at the previous time point, respectively. The horizontal line indicates the transition zone between the root and the hypocotyl. The double arrow (6 h) shows the length of the root at 0 h for a comparison.

The behavior of the three regions of the roots was approximated by measuring segment angles (Fig. 2, B and C) through time to determine the location, timing, and extent of straightening (Fig. 4). Many roots that were kept in a horizontal orientation for 1 h contained part of the zone of gravitropic curvature in their tips (distal 2 mm). The tip angle remained unchanged during the 1st h of rotation on the clinostat (Fig. 4, A and C). The tip angle subsequently decreased 25 to 30° over the next 5 h of clinostat rotation. This decrease resulted from the former zone of gravitropic curvature becoming located farther from the tip due to new root growth. Also, growth at the tip became oriented closer to the original vertical. The middle and basal segments continued curving toward the last constant gravity vector during the first 2 to 4 h of clinostat rotation, i.e. some gravitropic curvature continued to be expressed in these segments. By 5 to 6 h of rotation, the values for the angles of each of the three root segments converged, indicating a significant amount of root straightening. The same pattern and timing of root straightening occurred in both the axial and somersault configurations of root rotation (Fig. 4, A and C). In control roots the mean angles for all three segments were comparable throughout the period of clinostat rotation, indicating that on average these roots showed no preferred direction of root growth and/or that many roots were more or less straight. Thus, the straightening of gravitropically curved roots results in part from the loss of gravitropic curvature in older regions and in part from the angle of new root growth on the clinostat moving closer to the original vertical (prior to horizontal stimulation). These processes appear coordinated so that the angles of both regions become roughly aligned.

Figure 4.

Figure 4

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Angles of root segments through time showing the development of gravitropic curvature and subsequent straightening on a clinostat. Negative and positive values on abscissa indicate times for both horizontal and on clinostat, respectively. A and C, Roots horizontal for 1 h. B and D, Control (vertical) roots. All roots were rotated for 6 h either in a somersault (A and B) or an axial configuration (C and D). Mean angles (± se) for each segment (tip [○], middle [□], and base [▵]) were obtained from 60 to 80 plants for each treatment.

Although these roots mostly straightened, they were still slanted 25 ± 3° away from the original vertical (Fig. 4, A and C) in a direction that indicated the retention of some gravitropic reaction. However, this angle was reduced by 37° compared with the previous angle of gravitropic curvature (62° after 1 h in a horizontal orientation).

Roots rotated on the clinostat extended in length at the same rate, approximately 0.75 mm h−1, as that of horizontally and vertically grown stationary roots. Neither prior root orientation nor the configuration of rotation affected this growth rate. During the 6 h on a clinostat, the roots grew about 4.5 mm.

To determine whether an extended period of horizontal stimulation would preclude root straightening after withdrawal of the directional g stimulus, roots were horizontally stimulated for 5 h. The horizontal, stationary roots reached maximal gravitropic curvature within 2 h of reorientation from the vertical, and after 5 h of horizontal stimulation the mean curvature was 88 ± 3°. After these roots were rotated on a clinostat for 6 h, the majority lost gravitropic curvature and were essentially straight regardless of the direction of clinostat rotation (Fig. 5, A and C). A small fraction of roots lost no or only some gravitropic curvature and were still curved after clinostat rotation.

Figure 5.

Figure 5

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Images of roots on a clinostat as in Figure 3 except that roots in A and C were horizontal for 5 h before placement on the clinostat. A and C, Despite variability most roots exhibited partial loss of gravitropic curvature (roots marked with *) and root straightening after 6 h on the clinostat. B and D, Control roots mostly resembled those in Figure 3, B and D. Bar = 1 cm.

Measurement of the angles of subsections of roots that were horizontally stimulated for 5 h yielded results (Fig. 6, A and C) comparable to roots that were horizontal for 1 h. The tip segment started to move closer to the original vertical within 1 h of clinostat rotation. By 6 h, new root growth was oriented 20 to 30° away from the angle that the tip had occupied at the start of rotation (Fig. 6, A and C). Gravitropic curvature continued to be expressed at a rate of about 2 to 5° h−1 in the middle and basal regions during the first 3 to 4 h of clinostat rotation. The reciprocal loss of tip curvature and the increase in the angles of the middle and basal segments resulted in a convergence of all three angles, indicating an alignment or straightening of much of the root axis. Roots that were fully curved gravitropically (after 5 h of horizontal stimulation) straightened on average about 35° on a clinostat, essentially the same value obtained for roots stimulated for only 1 h. But since the 5-h roots were more curved to start with, they retained more of the graviresponse at the end of clinostat rotation; i.e. the mean angle of the entire root (also equal to the convergence angle of the three segments) was 53 ± 5° for roots stimulated for 5 h compared with 25° for roots that were horizontal for 1 h.

Figure 6.

Figure 6

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Angles of root segments as in Figure 4, except that roots were horizontal for 5 h before placement on the clinostat. n = 40 to 60 plants for each treatment. A and C, Note that angles converge at 50 to 60°, indicating the retention of more of a graviresponse than in roots horizontal for 1 h. Symbols are the same as those for Figure 4.

Control roots exhibited a range of responses to clinostat rotation, including curvature and slanting at various angles (Fig. 5, B and D). Some control roots rotated in a somersault configuration slanted slightly away from the hypocotyl hook (Figs. 5B and 6B), a direction corresponding to the loss of gravitropic curvature (Figs. 5A and 6A). But the degree of this slanting in controls was less than the loss of gravitropic curvature, and these controls exhibited much more variability (compare ses in Fig. 6, A and B). In all other controls, the final net angle of the root axis was zero.

To determine whether seed position affected root straightening, seeds were positioned above or below the hypocotyl root axis in horizontal seedlings. The position of the radicle can be determined in dry cress seeds (Volkmann et al., 1986). In all experiments the seeds were planted on the substrate so that the radicle emerged to the right of the seed (Fig. 2A). For all experiments except those shown in Figure 7, vertical roots were turned counterclockwise to the horizontal so that the cotyledons, the seed, and the hypocotyl hook were on the lower side of the hypocotyl-root axis (Fig. 2A). This resulted in both the hypocotyl and the gravitropically curved root forming a “C” that was a clockwise curve starting from the apex of the hook to the root tip (0 h in Figs. 3A and 5A). The curvature of the hypocotyl was maintained after root straightening on a clinostat.

Figure 7.

Figure 7

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Seed position does not affect root straightening. In contrast to previous figures, the seed and the hypocotyl hook were positioned on the upper side relative to the horizontal roots (A). Both root straightening and retention of some gravitropic reaction occurred after 7 h of clinostat rotation, as indicated by the slanting of most roots to the right (B), the direction of the gravity vector when roots were previously horizontal for 1 h. Bar = 1 cm.

In the experiments shown in Figure 7 vertical roots were turned clockwise to the horizontal so that the cotyledons, seed, and hook were on the upper side of the hypocotyl-root axis. In this case the curves in the hypocotyl (below the hook) and in the root were in opposite orientations so that the two formed an “S” (at 0 h). When these seedlings were rotated on a clinostat for 7 h, the roots straightened (Fig. 7), just as they did when the seeds were originally positioned below the root (Figs. 3 and 5). Thus, root straightening occurs regardless of the positions of the seed and the hypocotyl hook. The curve in the hypocotyl (basal to the hook) was always toward the side of the axis containing the seed regardless of orientation with respect to gravity, indicating that the hypocotyl of 1-d-old seedlings does not exhibit significant gravitropic curvature after 1 h of horizontal stimulation. Also, unlike the gravitropic curvature of the root, significant curvature of the hypocotyl was maintained throughout clinostat rotation.

DISCUSSION

This study documents the straightening of gravitropically curved roots following withdrawal of a constant g stimulus. Curved roots straighten on a clinostat through a combination of a loss of gravitropic curvature and the alignment of new growth closer to the prestimulus vertical.

Several previous reports exist of organ straightening after g-stimulus withdrawal (Larsen, 1953, 1957; Mirza et al., 1984; Chapman et al., 1994; Volkmann and Tewinkel, 1996; Tarui and Iino, 1997). But even in studies in which the same organs were analyzed through time, only the tip angle was measured, and the stages of straightening were not shown (Mirza et al., 1984; Chapman et al., 1994; Tarui and Iino, 1997). To our knowledge, our data provide the first visual depiction and multiregion analysis of the successive loss of gravitropic curvature in the same organs through time following stimulus withdrawal. These data also show that root straightening in cress can occur at clinostat speeds of 1 rpm, whereas Larsen (1953, 1957) only found straightening at much slower speeds.

This finding of root straightening shows that gravitropic curvature, at least complete curvature induced by 5 h of stimulation, can be partly or fully reversed, whereas in roots that are left stationary and that are not rotated on a clinostat, gravitropic curvature persists for the life of the organ. This reversibility of gravitropic curvature on a clinostat might result from active breakdown and wall reconditioning and/or from wall elasticity in the zone of curvature. This raises the question of when, if ever, curvature gets sufficiently plastic and rigid such that it becomes irreversible. Analyses of the responses of growing maize coleoptiles to applied tensile forces have shown that even apparent plastic deformations can actually be a type of reversible viscoelastic deformation or retarded elasticity (Hohl and Schopfer, 1992; Cosgrove, 1993). Further study of this phenomenon of loss of gravitropic curvature might prove valuable in identifying changes in the biomechanical properties of cell walls responsible for differential tropic growth.

In addition to the loss of gravitropic curvature in regions of the root formed before placement on the clinostat, root straightening also involves new growth on the clinostat. Possible explanations for this outcome are that in the absence of a constant g stimulus, that new growth follows and aligns with the straightening of older regions, or, conversely, that the loss of curvature results from coordination with new growth.

Root straightening cannot be due to the influence of hypocotyl position or of some automorphogenetic component (Masuda et al., 1994; Stanković et al., 1998), since it occurs regardless of whether the seed and hypocotyl were located above or below the horizontally stimulated root. Similarly, it is found regardless of whether the roots were rotated along their axis or at right angles to their axis.

The phenomenon of organ straightening following tropistic curvature has been referred to as “autotropism” (Pfeffer, 1906; Firn and Digby, 1979; Hart, 1990). The various usages of these terms have recently been critically reviewed (Stanković et al., 1998). Although the migration of curvature during a constant g stimulus has been termed “autotropism” (Firn and Digby, 1979; Hart, 1990; Myers et al., 1995; Tarui and Iino, 1997), it may be more appropriate to consider these growth adjustments to be part of the overall process of gravitropism rather than a separate “tropism,” autotropism that only occurs during and in response to gravitropism (Stanković et al., 1998). In contrast, the straightening that occurs after a withdrawal of a g stimulus is clearly not part of gravitropism and for historical reasons might still be called “autotropic straightening.” But as this straightening is not a bona fide tropism in the sense of a directional response of an organ to a current environmental vector, the term autonomic straightening might be more accurate.

Regardless of terminology, the findings that the root returns closer to the prestimulus vertical indicates that there is some sort of inherent, autonomic, or default tendency for disoriented organs to revert to a previous equilibrium orientation (Fig. 1, E and F). This behavior seems to reflect some persistent commitment to return root growth toward a previous alignment (before it was turned on its side).

At the same time, since the final angle is still below what was the horizontal (double arrow in Fig. 1F), some gravitropic reaction seems to have been retained, even though the roots are no longer curved. This apparent persistence of some gravitropic reaction might represent the limits of autonomic straightening. This possibility is supported by the finding that roots that were horizontally stimulated for 1 and 5 h both moved about 36° closer to the prestimulus vertical after clinostat rotation. Further study is required to determine whether roots with gravitropic curvatures smaller than 36° (before clinostat rotation) return completely to the prestimulus vertical. In any case, the total amount of autonomic straightening is not simply limited by properties of the zone of gravitropic curvature (e.g. wall elasticity), but is actively and coordinately regulated in several regions of the root.

ACKNOWLEDGMENTS

We would like to thank K. Aram for technical assistance and Michael Evans and several anonymous reviewers for their valuable comments on the manuscript.

Footnotes

1

This work was supported by grants from the National Aeronautics and Space Administration (grant no. NAG2-1023) to F.S. and by Deutsche Agentur für Raumfahrtangelegenheiten (Bonn, Germany, grant no. 50 9429) and MWF (Düsseldorf) to D.V.

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