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Physiology and Development |
2Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel; 3The Kennedy-Leigh Centre for Horticultural Research, Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot 76100, Israel
Received for publication October 15, 2002. Accepted for publication January 10, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Antirrhinum majus cut spikes • bending zone • calcium antagonists • cortex • epidermis cells • lower and upper flanks • relative growth rate • shrinkage
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Kaufman et al., 1995
; Cosgrove, 1997
). The gravitropic response of vegetative and inflorescence shoots was also studied in several cases (Kohji et al., 1979
; Halevy and Mayak, 1981
; Mueller et al., 1984
; Woltering, 1991
; Meicenheimer and Nackid, 1994
; Philosoph-Hadas et al., 1995
; Fukaki et al., 1996
, 1998
; Hejnowicz and Sievers, 1996
). Recently, the mechanism of bending of inflorescence shoots has become more of a focus, and it is being extensively investigated (Weise et al., 2000
; Morita et al., 2002
; Friedman et al., 2003
). In hypocotyls, coleoptiles, and grass pulvini, the upward bending resulted from differential growth of the upper and lower flanks (Digby and Firn, 1979
; Firn and Digby, 1980
; Dayanandan and Kaufman, 1984
; Salisbury, 1993
; Cosgrove, 1997
; Edelmann, 1997
). However, the growth pattern was rarely characterized in detail in gravistimulated mature stems and flowering shoots (Clifford and Oxlade, 1989
; Meicenheimer and Nackid, 1994
).
Studies of gravitropism-related differential growth usually emphasize the increase in growth occurring at the lower flank of the horizontally positioned organs (MacDonald et al., 1983
; Dayanandan and Kaufman, 1984
; Jaffe et al., 1985
; Berg et al., 1986
; Cosgrove, 1997
). However, several studies showed that the bending response is also associated with growth cessation and even shrinkage of the upper flank (Digby and Firn, 1979
; MacDonald et al., 1983
; Mueller et al., 1984
; Jaffe et al., 1985
; Berg et al., 1986
; Cosgrove, 1990
; Meicenheimer and Nackid, 1994
). Most of these studies were based on growth measurements of the upper and lower organ flanks in the bending zone during gravistimulation and were missing a detailed spatial and temporal analysis of cell dimensions in these sites. It is well accepted that both the epidermal and the cortical cells participate in vertical growth (Kutschera, 1992
; Peters and Tomos, 1996
; Hejnowicz, 1997
). However, the contribution of each of these cell layers to the bending response of gravistimulated organs was evaluated only by removing the peripheral cell layers (Firn and Digby, 1977
) and was not studied by measurements of cell dimensions. Such a characterization of the growth response during stem bending is an essential step towards elucidation of the complex multistep process of gravistimulation.
Cytoplasmic Ca2+ levels have been implicated as an important component of the gravitropic bending response (Salisbury, 1993
; Sinclair and Trewavas, 1997
; Plieth and Trewavas, 2002
). Accordingly, we have shown previously that various calcium antagonists, such as 10 mmol/L 1,2-bis(2-aminophenoxy) ethane-N,N,N',N'-tetraacetic acid (BAPTA), 20 mmol/L trans-1,2-cyclohexane dinitro-N,N,N',N'-tetraacetic acid (CDTA), trans-1,2-cyclohexane dinitro-N,N,N',N'-tetraacetic acid (EGTA), or LaCl3, significantly inhibited the gravitropic curvature of snapdragon spikes (Philosoph-Hadas et al., 1995
, 1996
). Because bending is a result of differential growth, these calcium antagonists may serve as useful tools for additional characterization of these growth processes in this system. Of the calcium antagonists assayed, only the calcium channel blocker, LaCl3, was shown to specifically inhibit gravity-induced growth, based on length measurements of the stem-bending zone (Friedman et al., 1998
). However, we have not yet examined the direct effect of LaCl3 or calcium chelators on the differential growth of the lower and upper stem flanks.
In the present study we have expanded our investigation on the model system of snapdragon spikes and have studied the differential growth processes of stems during gravistimulation. For this purpose we analyzed temporal growth of gravistimulated spikes in detail and examined at one time point how growth was modified in the presence of various calcium antagonists that inhibit bending. The growth analysis was accompanied by analysis of changes in epidermal and cortical cell dimensions in the upper and lower flanks of the stem-bending zone. Our results show that (a) the differential growth patterns in both the upper and lower flanks of horizontal spikes were completely and specifically abolished in the presence of the various calcium antagonists, further showing that differential growth is necessary for stem curvature; (b) the gravitropic bending of snapdragon spikes results from dynamic modifications of cell dimensions in the epidermis and cortex stem layers, leading to shrinkage of the upper flank and increased growth of the lower flank.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Spikes bearing 4–6 open florets were harvested and held vertically overnight with the stem cut ends in water to enable their straightening. Based on the degree of opening florets, the inflorescences were divided into three different zones, designated I to III, starting from the stem apex at 50-mm intervals (Fig. 1A). Zone II of vertical or horizontal stems was designated as the elongation or the bending zone, respectively. Open and partially open florets were removed only from zones II and III, resulting in bud stumps (see Fig. 1C). The closed buds were not removed from the top 50-mm apical region (zone I) (Fig. 1A, B) because they were in such close proximity to each other that their removal would have damaged the shoot. Therefore, detailed examination of growth at this zone was not possible. For growth measurements, zones II and III of the flowerless stems were marked into subdivisions at 5-mm intervals using a pen (Fig. 1B), and spikes were trimmed to a length of 30–35 cm from the apex. Each marked stem was then placed vertically in a test tube with double-distilled water (DDW) for 24 h to enable recovery from possible wound and touch stresses.
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, 1996
; Friedman et al., 1998
). After pulsing with the various chemicals, spikes were transferred to test tubes containing DDW.
Following the 20-h preincubation, the treated and untreated, flowerless, marked stems in the test tubes were either held vertically or placed horizontally for up to 12 h (Fig. 1B). Gravitropic stimulation was provided by tilting the test tubes horizontally as previously described (Friedman et al., 1998
). Marked shoots without florets were bent at the same rate as shoots with florets (data not shown). To monitor the kinetics of stem bending, the curvature angle of spikes was measured either directly with a protractor or from the stem photographs taken at the indicated intervals. Stem photographs were taken with a high-resolution video camera MSV 800 (Applitec, Rishon Leziyon, Israel), equipped with a 12.5–75-mm zoom lens, and further analyzed as detailed below for stem growth analysis. The curvature angle of nonbending stems at a horizontal position was defined as 0°, and this angle progressively increased as the shoot bent upwards. Each experiment was repeated at least three times with similar results, and data from representative, individual experiments are presented.
Stem growth analysis
The flowerless, marked spikes were photographed at the indicated intervals during gravistimulation or vertical orientation (Fig. 1B), using a high-resolution video camera MSV 800. The photographs were directly stored in the computer using a frame grabber (FlashPoint, Indianapolis, Indiana, USA) and were further analyzed with the SigmaScan 3 program (Jandel Scientific, SPSS, Chicago, Illinois, USA) to determine the growth increment of each marked 5-mm subsection comprising the stem zone (Fig. 1B). The actual sizes of the stem zones were determined using the 5-mm fixed division scale attached to each tube prior to stem growth measurements (Fig. 1B). This procedure allowed measurements of growth increment from the photographed stems with an accuracy to 0.7%. Flower bud stumps (see Fig. 1C) did not disrupt stem growth (data not shown). Growth was measured either on the two opposite flanks of vertical spikes or on the upper and the lower flanks of horizontal spikes.
Shoot growth was expressed either as a relative or a percentage of growth rate. Relative growth rate represented the growth increment of the whole zone II within a time unit relative to the size obtained in the previous measurement. This value was calculated from the cumulative relative growth values of the 5-mm subsections marked in this zone. Percentage relative growth represented the growth increment of zone II at each time point in relation to its original size at time zero (prior to horizontal or vertical placements). This percentage was calculated based on the cumulative relative growth values of its subsections.
Determination of cell dimensions
The epidermal and cortical cell sizes of vertical and horizontal spikes were determined in the middle of stem zone II. The epidermal peels used for cell size analysis were small (about 2 x 4 mm) and were sampled from a small section located between two flower stumps (Fig. 1C). To evaluate modifications in cell dimensions in horizontal shoots during bending, epidermal peels were first taken from vertical shoots to determine the initial size of cells (Fig. 1C). The same shoots were subsequently rotated by 90° around their axes (to avoid placing the shoots for gravistimulation on the site from which the epidermis was peeled) and tilted to a horizontal position for 12 h. Additional epidermal peels were then taken from the upper and lower flanks of the bending zone of the same shoot (Fig. 1C) after the shoot reached curvature angles of either 40° or 90°. Unlike in previous reports with hypocotyls in which the peripheral cell layers were removed (Firn and Digby, 1977
), the initial peeling of the small epidermal section prior to gravistimulation in snapdragon shoots did not affect the bending response (data not shown). This lack of effect is probably because the epidermis peels were very small and were not taken from the sites that comprised the upper or lower flanks of the gravistimulated shoot. To determine the cortical cell dimensions during gravistimulation, longitudinal sections were excised from the middle of zone II (Fig. 1C) of different vertical or horizontal stems (after it reached curvature angles of either 40° or 90°) using a cryomicrotome (Mectron, Saline, Missouri, USA).
All tissue preparations (epidermal and cortical) were fixed on glass slides for 2–5 h with 2.3% formaldehyde (m/v) in phosphate-buffered saline (PBS). Tissues were then rinsed twice with PBS, stained with 0.05% toluidine blue (m/v) (in PBS), and washed again twice with PBS. The stained tissue preparations were kept in 50% glycerol (v/v) at 4°C until monitored with a light microscope. Cortical cells were measured on cells in the fourth to sixth cell layers below the epidermal layer (see Fig. 5A). For epidermal cells, the length and the width (which are both parallel to the growth axis) were determined (see Fig. 4A). For cortical cells, the length (which is parallel to the growth axis) and height (which is perpendicular to the growth axis) were measured (see Fig. 5A).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, 1996
; Friedman et al., 1998
). During this period, untreated horizontal control shoots reached an angle of 54° ± 12°, while the treated shoots did not curve (data not shown). The results presented in Fig. 3 demonstrate that the various calcium antagonists reduced the relative growth of vertical shoots from 1.7% to 0.8–1.1%, but this reduction was statistically insignificant. On the other hand, in gravistimulated shoots, these antagonists decreased the relative growth of the lower flank by more than 75% and completely prevented the shrinkage of the upper stem flank. Consequently, the differential growth gradient obtained across the gravistimulated control stem was completely abolished, but the antagonist-treated shoots still grew (Fig. 3). These results further indicate that the bending inhibition by the calcium antagonists in snapdragon spikes was specific to the gravity-induced differential growth and that this process is necessary for curvature formation.
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Cell dimensions during gravistimulation also were analyzed in the cortical tissue (Fig. 5A). The results represent the average cell dimensions for 3–6 stems (Fig. 5), held either vertically or horizontally. The results depicted in Fig. 5B show that the length of cortical cells measured in vertical stems was 67.2 µm. Upon gravistimulation to an angle of 40°, the length of these cortical cells in the upper flank was reduced to 58.6 µm, while the length of cells in the lower flank was concomitantly increased to 79.7 µm. In parallel, cortical cell height in the upper flank decreased and in the lower flank it increased by about 12% each (Fig. 5C). These changes in cortical cell dimensions at an angle of 40° led to an average ratio of 1.39 ± 0.13 between cell length values of the lower and upper flanks (L/U ± SE) and to an L/U ± SE ratio of 1.32 ± 0.11 for cell height (Fig. 5). The corresponding L/U ± SE values for spikes curved at 90° (data not shown) were about 1.1 ± 0.01 for the cell length and 1.4 ± 0.16 for the cell height.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Philosoph-Hadas et al., 1995
). Growth of both vertical and horizontal shoots was analyzed to evaluate the alterations in growth patterns during gravistimulation and in the presence of curvature inhibitors.
The curvature of snapdragon spikes was characterized by shrinkage of the upper stem flank and increased growth of the lower stem flank (Figs. 2, 3). These results are in accordance with the idea that both halves of the gravistimulated shoot have independent graviresponses, as previously demonstrated in various seedlings and hypocotyls (Firn and Digby, 1977
, 1980
; Digby and Firn, 1979
; Edelmann, 2001
). The importance of this independent gravity-induced growth response of both stem flanks to the process of curvature formation was further demonstrated by our study with the calcium antagonists (Fig. 3), which were previously reported to inhibit stem curvature in snapdragon spikes (Philosoph-Hadas et al., 1996
; Friedman et al., 1998
). Our results clearly and directly show for the first time that all the examined calcium antagonists abolished this independent graviresponse in the upper and lower stem flanks (Fig. 3). Consequently, by inhibiting the increased growth of the lower flank and preventing the shrinkage of the upper flank, the calcium antagonists equalized the growth ability of both flanks, which became similar to that of vertical shoots. The calcium antagonists thus seem to inhibit bending not by halting growth processes, but rather by abolishing the specific independent gravity-induced growth pattern of the upper and lower stem flanks. These results provide additional support to the findings that the changes leading to differential stem growth are indeed necessary for curvature formation.
The shrinkage in our snapdragon system seems to result from a reduction in the relative growth rate of the upper flank of the bending zone, as compared to that of the elongation zone of vertical shoots (Fig. 2A). These changes were measured at the earliest only 3 h following gravistimulation. The reduction in relative growth of the upper flank was caused by shrinkage of both epidermal (Fig. 4B) and cortical (Fig. 5B) cells when stems reached an angle of 40°. Also, a decrease in the height of cortical cells at 40° was concomitantly observed (Fig. 5C). These changes were accompanied by a parallel widening of epidermal cells observed on the upper flank both at 40° (Fig. 4C) and 90° (Fig. 4E), followed by their increased length at 90°, mainly on the lower flank (Fig. 4D). Therefore, the dynamic changes in cell dimensions occurring during gravistimulation seem to include both alleviation of shrinkage and increased growth of epidermal and cortical cells at the lower flank, when stems reached an angle of 90°. It should be noted that a significant increase in growth of cortical cells on the lower flank was observed at 40° (Fig. 5) but not in the corresponding epidermal cells (Fig. 4B, C). This situation is possible because the epidermal layer can constrain the expansion of cortical cells (Firn and Digby, 1977
; Kutschera, 1992
), and this constraint is released upon tissue sectioning. Thus, the measurements of the cortical cells after tissue sectioning seem to reflect their real dimension without the epidermis constraint.
Shrinkage at the upper side of gravistimulated shoots has been observed in Xanthium strumarium (Mueller et al., 1984
; Sliwinski and Salisbury, 1984
), cucumber hypocotyls (Cosgrove, 1990
), and kalanchoe stems (Meicenheimer and Nackid, 1994
). In maize roots, growth cessation at the lower flank of the gravistimulated root was associated with a decrease in cell length (Ishikawa et al., 1991
; Balu
ka et al., 1996
). However, this shrinkage phenomenon has received little attention. In one system of cucumber hypocotyls, the shrinkage was suggested to have resulted from passive compression caused by the length increase in the lower flank (Cosgrove, 1990
). In other systems, such as oat coleoptiles (Shen-Miller and Masuda, 1973
) and stems of herbaceous and woody plants (Hejnowicz and Sievers, 1996
; Hejnowicz, 1997
), the passive shrinkage was suggested to be due to the release of tissue tension at the lower flank, which could happen without any obvious epidermal growth at this site. Perhaps the increased height of the cortical cells observed in the lower stem flank of snapdragon (Fig. 5C), which may reflect an increased height of the whole lower cortex, can assist in releasing the tissue tension. This release may occur by pushing the epidermal layer of the lower stem flank outwards.
Alternatively, the shrinkage at the upper stem flank may be a result of an active process of growth modification, as suggested also by Mueller et al. (1984)
for Xanthium stems. Indeed, our study of snapdragon spikes clearly shows that the shrinkage is accompanied by a widening of epidermal cells (Fig. 4) and changes in both length and height of cortical cells (Fig. 5). One possible explanation for this shrinkage and widening of the epidermal cells at the upper flank might be related to microtubule reorientation (Nick et al., 1990
). Microtubules in the epidermal layer of vertical shoots are organized in a perpendicular position to the plant axis, and after bending they become parallel to this axis only at the upper flank. A change in the microtubule orientation can alter cell wall deposition leading to cell widening. A change in orientation is supported by our observations that only the shrinkage of the upper flank of snapdragon shoots was inhibited by the microtubule depolymerizing agent, oryzalin (Friedman et al., 2003
). In addition, the possibility that part of the shrinkage of epidermal cells may stem from the peeling procedure cannot be excluded because the epidermal tissue has a tendency to shrink when it is peeled (Hejnowicz and Sievers, 1996
).
The role of the epidermis as the prime site of auxin action, and therefore, the site of growth, has been emphasized over the years (Kutschera, 1992
; Salisbury, 1993
; Peters and Tomos, 1996
). Nevertheless, several reports show that the inner tissues also play an important role in vertical growth (Kutschera and Briggs, 1987
; Kutschera et al., 1987
; Peters et al., 1992
), as well as in the gravitropic response (Salisbury, 1993
; Peters and Tomos, 1996
). Our results show that indeed the cortical cells, both at the lower and the upper stem flanks, responded to the gravitropic stimulation (Fig. 5). Moreover, the height and length of cortical cells in the lower flank increased (Fig. 5) before any apparent changes in epidermal cells were observed (Fig. 4). Since the endodermis was recently shown to be the site of signal perception in inflorescence stems (Fukaki et al., 1998
; Weise et al., 2000
; Morita et al., 2002
), it is possible that the signal is directly transmitted from the endodermis to the cortical cells, thereby changing their growth orientation. However, the mechanism involved in the increase in length and height of cortical cells and the possible participation of auxin in this process is not yet clear.
In summary, our results clearly show that the gravitropic bending of snapdragon spikes is associated with stem differential growth, which is specifically abolished by curvature inhibitors such as various calcium antagonists. In addition, we have shown that dynamic modifications in cell dimensions of both the epidermal and cortical cells in the upper and lower stem flanks are responsible for this differential growth patterns that leads to the upward bending response of shoots.
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FOOTNOTES |
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4 Author for reprint requests (vtsoniap{at}volcani.agri.gov.il
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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ka F. M. Hauskrecht P. W. Barlow A. Sievers 1996 Gravitropism of the primary root of maize: a complex pattern of differential cellular growth in the cortex independent of microtubule cytoskeleton. Planta 198: 310-318[ISI][Medline]Berg A. R. I. R. MacDonald J. W. Hart D. C. Gordon 1986 Relative elemental elongation rates in the etiolated hypocotyl of sunflower (Helianthus annus L.): a comparison of straight growth and gravitropic growth. Botanical Gazette 147: 373-382[CrossRef]
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