Journal of Experimental Botany, Vol. 53, No. 374, pp. 1627-1634,
July 1, 2002
© 2002 Oxford University Press
The gravitropic setpoint angle of dark-grown rye seedlings and the role of ethylene
Received 9 November 2001; Accepted 13 March 2002
1 Botanisches Institut der Universität Bonn, Abteilung Ökophysiologie der Pflanzen, Kirschallee 1, D-53115 Bonn, Germany
2 Institut für Angewandte Phsyik, Universität Bonn, Wegelerstr. 8, D-53115 Bonn, Germany
3 To whom correspondence should be addressed. Fax: +49 228 73 2677. E-mail: edelmann{at}uni-bonn.de
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Abstract |
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The orientation growth of coleoptiles of dark-grown seedlings of rye (Secale cereale L. cv. Marder II), when grown under various conditions, was analysed with respect to the gravivector (‘gravitropic setpoint angle’, GSA). Coleoptiles growing through moist vermiculite attain and maintain a GSA with an average of about 180°, i.e. a vertical orientation. Seedlings growing uncovered either on the surface of vermiculite or positionally fixed on filter paper attain and maintain a GSA of 140–150° (i.e. deviating from the vertical by an average of 30–40°). Changing the position of the embryo relative to the horizontally fixed seed kernel or of the angle of the seed with respect to gravity during germination (±40° relative to the horizontal) had no significant effect on the subsequent GSA of both covered and uncovered seedlings. The GSA of uncovered coleoptiles could be restored close to 180° by treatment of the seedlings with ethylene, either applied via ethephon or 1-aminocyclopropane-1-carboxylic acid (ACC) as well as by fruit-released ethylene. The results are discussed with respect to the mechanism of the regulation of gravitropic growth of grass seedlings.
Key words: Key words: Coleoptiles, ethylene, gravitropic setpoint angle, Secale cereale L.
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Introduction |
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Exact spatial positioning, as mediated via the regulation of the direction of organ growth, is vital for a plant to develop successfully, especially for germinating seedlings. By comparison with other exogenous factors such as light, temperature or nutritional conditions which affect the direction and velocity of growth of plant organs (Wilkins, 1965; Quail and Briggs, 1987; Nick and Schäfer, 1988a; Vitha et al., 2000; Ruppel et al., 2001), gravity exerts its effect constantly on each individual cell and any compound of plants in a uniform manner. There is no pattern or gradient across or within the plant or its cells; it is a persistent and unvarying vectorial force.
Traditionally, the capacity of plants to align their organs precisely with respect to the gravity vector is categorized into positive and negative orthogravitropic (parallel or antiparallel to gravity), plagiotropic (in a special angle relative to the gravivector), and diagravitropic forms of growth (in an angle of 90° relative to the gravivector), of which the last mentioned are commonly regarded as being the result of the adverse impact of positive and negative orthogravitropic growth (Haupt, 1977). However, a more recent, unifying terminology proposes that every gravitropically competent organ maintains under certain conditions a development-dependent angle with respect to gravity (the gravitropic setpoint angle, GSA) by a common gravitropic mechanism (Digby and Firn, 1995; Firn et al., 1999).
Classic and some of the most commonly studied organs in terms of their gravitropic behaviour are the grass seedling coleoptiles, which have been demonstrated to act as gravi-guiding systems (Edelmann, 1996). These organs are generally regarded as orthogravitropic (GSA = 180°, i.e. growing vertically upwards), and in a vast number of studies (for a recent reference see Chen et al., 1999, and literature cited therein) coleoptiles of intact seedlings have been shown to have a pronounced gravi-sensitivity and -responsivity once they deviate from the gravitropic equilibrium, i.e. from the vertical. As demonstrated by Pickard (1973) a few seconds in which these organs deviate from the plumb-line suffice to induce a response in the form of differential gravitropic growth. It was also demonstrated that deviations of only a few degrees from the vertical result in appropriate graviresponses. Apparently divergent from this view, Johnsson et al. (1993) observed that coleoptiles of Avena seedlings often deviated from the vertical by up to 6°, such deviations increasing with plant age. The finding that such deviation could be reduced by increasing longitudinally applied centripetal acceleration led to the proposal that the variation in coleoptile orientation was ‘g-related’, implying either a reduced gravisensitivity of some seedlings or an impaired processing of the gravisignal (Johnsson et al., 1993).
While studying the growth and development of rye seedlings, even greater deviations of coleoptiles from the vertical (up to 30°) were noted than had been described by Johnsson et al. Furthermore, the variation in coleoptile orientation differed from sowing to sowing; hence it was possible to investigate systematically the cause of this variation and to gain further understanding of the gravitropic behaviour of coleoptiles.
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Materials and methods |
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Plants
Seeds were sown in perspex trays of 20x20x9 cm (lengthxwidthxheight) on moist vermiculite or covered with a layer of moist vermiculite as indicated in the legends and germinated in the dark or under continuous light (approximately 35 µmol m–2 s–1; L 18W/19 daylight 5000 de Luxe, Osram, München, Germany) at 25 °C as described earlier (Edelmann and Köhler, 1995). When seedlings were grown on filter paper, where appropriate, some seeds were fixed with solvent-free glue (Pritt, Alleskleber, Henkel KgaA, Germany).
Measurements
The angle of the axis running between the basal region of the coleoptile and the very tip was estimated and expressed relative to the vertical (180°). Length measurements of the coleoptiles were carried out by placing the organs next to a ruler. For analysing gravitropic growth of horizontally gravistimulated isolated coleoptiles, 2.5 cm long segments (with intact tips) were cut from approximately 3.5 cm long coleoptiles and the primary leaves were removed. Subsequently, such segments were fixed on perspex blocks with ‘plastic-fermit’ (Installationskitt; Nissen and Volk, Hamburg, FRG) and placed in a horizontal position in chambers in water-saturated air. When ethylene was added it was released from separate solutions of ethephon in containers in the chamber or ethephon solution was added directly to the filter paper.
Ethylene measurement
Ethylene production was measured in real-time with a photoacoustic laser spectrometer consisting of a line-tunable CO2 laser and two resonant photoacoustic cells (Beßler et al., 1998). Caryopses were fixed on filter-paper and placed on Petri-dishes in a 2.0 l glass cuvette which received a constant flow of 33 ml min–1 air. Ambient air was drawn over a platinum catalyst at 450 °C prior to entering the cuvette to remove hydrocarbons. After passing through the cuvette, the air was pushed through a liquid-N2 cooling trap to remove CO2 and H2O before entering the photoacoustic cell in which ethylene concentrations were measured every 3 min (where applicable: emissions from treatment and control were measured simultaneously in the two cells). To identify and quantify ethylene unambiguously, measurements were taken at three different laser lines. The detection limit for this experiment was about 500 ng l–1, calibration was performed with certified gas samples of ethylene in N2 (Praxair, Biebesheim am Rhein, Germany).
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Results |
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As reported for roots and for coleoptiles of maize, respectively (Feldman, 1983; Perdue et al., 1988; Lu and Feldman, 1997), light enhances and standardizes the gravitropic growth response of these organs. This has been ascribed either to enhanced gravisensitivity and/or better transduction of the gravi-stimulus (Feldman and Briggs, 1987; Nick and Schäfer, 1988b). Similar effects can now be reported for rye coleoptiles. As demonstrated in Fig. 1 the coleoptiles of light-grown rye seedlings quickly attain a vertical orientation (GSA = 180°) which is maintained until the coleoptiles cease growth when the primary leaves break through the very tip region after about 3 d. By contrast, apart from an, in many cases, bow-shaped growth behaviour, coleoptiles of dark-grown rye coleoptiles showed a wide range of deviations from the vertical (Fig. 1) with the average GSA being 120–170° depending on the batch being studied. This heterogeneity of organ orientation was observed even when the sowings were standardized (with respect to the number of the seeds, the total volume of vermiculite per tray, and the amount of supplied water) and the average GSA of dark-grown rye coleoptiles was consistently much less than 180°. One plausible reason for the heterogeneity in early experiments was that the varying heights of the vermiculite layer covering the germinating seedlings influenced the GSA of the coleoptiles. Variations of the GSA of graviresponding roots depending on the medium in which they germinated were demonstrated earlier (Bennet-Clark et al., 1959). Therefore, grains were covered with defined different depths of vermiculite. By this, it was revealed that the GSA of the coleoptiles was indeed dependent on the depth of the layer of vermiculite (Table 1). Seedlings not covered with vermiculite showed the most pronounced scatter with an average GSA of 146°, but in some cases the GSA was as low as 120–130° and even lower. Seedlings grown in deep beds of vermiculite had a much higher GSA, i.e. they grew in a more or less vertical position. The difference in organ orientation was independent of seedling density, indicating that the pronounced organ deviations are not due to some mutual impediment or evasive movements of the germinating seedlings (data not shown).
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In order to demonstrate that the phenomenon was not due to reorientation of the seedlings during germination (e.g. induced by displacement of the seeds during root outgrowth), and also to standardize the germination procedure with respect to the positioning of the seeds, the gravitropic behaviour of coleoptiles growing from seeds fixed with glue to vertically moist filter paper was recorded. Such uncovered coleoptiles maintain their lower GSA throughout this time period (Fig. 2), whereas coleoptiles covered with vermiculite generally exhibit an increasingly vertical orientation. Since it could be argued that, in uncovered seedlings, the moist surface of the filter paper on which the seeds germinated may induce some positive hydrotropic growth, thereby contributing to the pronounced deflection from the vertical, seedlings were germinated on filter paper covered with a plastic foil except for a small area adjacent to the seeds. Such seedlings behaved identically to seedlings grown on uncovered filter paper and, hence, any possible effects of hydrotropism were eliminated.
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Studies were undertaken to determine the cause of the effect of vermiculite depth on the GSA of dark-grown coleoptiles. It was known that ethylene could influence the orientation of organs with respect to gravity, as shown by the effect of exogenous ethylene on the orientation of pea epicotyls (Neljubow, 1901). It seemed plausible that the gaseous environment around the coleoptiles could differ depending on the depth of vermiculite cover. It, therefore, appeared interesting to test the effect of ethylene on the GSA of dark-grown uncovered seedlings. For this, fixed seeds were germinated on filter papers soaked with differently concentrated solutions of ethephon, which is known to release ethylene upon hydrolysis (Agrawal et al., 2001), and the effect on the GSA was measured. This treatment had a concentration-dependent effect on elongation growth (Table 2; Moss et al., 1988). More interestingly, however, there was a strong effect on the GSA of the coleoptiles. Seedlings without added ethylene had a GSA of 147° and those with ethylene originating from 0.69 µM ethephon had a GSA of nearly 180°. With respect to the GSA therefore, exogenous ethylene mimics the effect of the vermiculite cover. A similar effect on the GSA of coleoptiles was observed when ethephon was supplied in separate Petri dishes to the seedlings germinating in closed chambers on water-soaked filter paper, indicating that the effect was mediated via ethylene released from the solutions into the gas phase due to hydrolysis. In addition, the GSA of dark-grown uncovered seedlings was affected in a similar manner when they germinated in plastic boxes together with slices of apples generally know to release ethephon (data not shown).
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Since an incubation concentration of 0.69 µM ethephon turned out as the most efficient with respect to its ethylene-mediated enhancing effect on gravitropic orientation of uncovered seedlings, it was decided to characterize this effect over a time period of 4 d. As demonstrated in Fig. 3, an original GSA of an average 146° existing within the very short coleoptiles is more or less maintained in water-incubated seedlings during the entire growth phase. Therefore, despite pronounced elongation growth occurring throughout the entire time period the angle of the uncovered, dark-grown coleoptiles is not changed. By comparison, seedlings germinating uncovered in solutions of ethephon are characterized by a continuously developing enhanced gravitropic growth, i.e. an increasingly vertical orientation.
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The pronounced organ deviation from the vertical of uncovered dark-grown seedlings was independent of positional conditions of the embryo relative to the kernel or of the angle of the kernel relative to the gravivector, respectively. As demonstrated in Fig. 4, the angle of the coleoptiles of uncovered seedlings was similar, irrespective of whether the embryo was positioned on top of the horizontally fixed kernel or on the side, i.e. in a median position. Even a shift of the germination plane by 40° in both directions relative to the longitudinal axes of the horizontally positioned kernels did not result in an appropriately changed positional angle. Independent of the positioning of the embryo relative to the kernel or of the germination plane seeds covered with vermiculite exhibited a nearly vertical orientation.
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To examine the effect of a precursor of ethylene, seeds were germinated on filter paper soaked with solutions of 1-aminocyclopropane-1-carboxylic acid (ACC) which is converted to ethylene by ACC-oxidase (Bleeker and Kende, 2000). As shown in Fig. 5, increasing concentrations of ACC up to 2 mM had an increasing ability to increase the GSA of dark-grown, uncovered coleoptiles; higher concentrations resulted in a less enhancing effect on gravitropic growth.
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In order to confirm that ACC and ethephon do result in enhanced ethylene synthesis and release, respectively, ethylene was measured in chambers containing seedlings either germinating in water, or in solutions of ethephon or ACC. For better resolution of the amount of released ethylene, this was performed with 50 seeds fixed on filter paper soaked with the appropriate solutions for germination and by measuring ethylene using the photoacoustic method (Beßler et al., 1998). By contrast with earlier approaches in which ethylene was analysed subsequent to a certain treatment (Philosoph-Hadas et al., 1996) this method allows a real time on-line measurement. As demonstrated in Fig. 6, seedlings germinating in water release a very small amount of ethylene for a brief period starting after about 10 h up to 30 h after the beginning of germination. By contrast, the amount of released ethylene was strongly enhanced in chambers in which seedlings germinated in ACC solution. Such seedlings released ethylene after about 6–7 h after the start of germination which gradually increased. In seedlings germinating in solutions of ACC, ethylene synthesis was enhanced in the light and was characterized by a more or less pronounced decreased release during the dark periods, similar to an earlier report (Beßler, 1998). This effect is even more obvious in chambers in which seedlings were germinated in solutions of ethephon, in which the amounts of released ethylene was highest. When ethephon was supplied, ethylene evolved more or less instantaneously to values of 100 ppb. Further ethylene release is strongly enhanced due to light up to values of 400 ppb. More or less instantly ethylene decreased at the onset of the dark phase which was again enhanced at the onset of the light phase.
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Since similar initial values were measured in chambers in which solutions of ethephon alone were placed (i.e. without seedlings), these measurements imply that the first instant increase in ethylene concentration is due to metabolism-independent hydrolysis, whereas the second increase seems due to metabolism-dependent and obviously light-enhanced processes. This metabolism-independent release of ethylene into the gas phase from solutions of ethephon, therefore, may explain the effect on the GSA under conditions without direct contact of the seedlings with the solution. The results demonstrate that the amount of released ethylene during the three different germination conditions correlate with the observed impact of this gas on the GSA (Table 2; Fig. 3).
To test the effect of ethylene synthesis inhibition on GSA, seeds were germinated on solutions of aminoethoxyvinylglycine (AVG), an inhibitor of the ACC-synthase, the activity of which has earlier been demonstrated to limit ethylene synthesis (Boller et al., 1979; Yu et al., 1979; Yang and Hoffman, 1984). By this, elongation growth of the coleoptiles was severely impaired, indicating that either ethylene plays some essential role in the mechanism of elongation growth or that processes indirectly affected exert such an effective influence. The orientation of such seedlings was more or less randomly distributed. As shown in Fig. 7, apart from exceptions, coleoptiles grew generally downwards, apparently pushing the glued seeds from the filter paper which was not observed in controls. This unusual behaviour generally resulted in overturned seedlings which, in some cases, led to an apparently normal growth. By contrast to the drastic reduction of coleoptile elongation, root elongation growth tended to be enhanced by this treatment, indicating either a very different sensitivity of root cells towards this inhibitor or a strongly differing relevance of ethylene with respect to cell elongation. With respect to organ orientation in roots, the inhibition of ethylene synthesis by AVG obviously changed the direction of growth upside down within the observed time period, indicating that under these conditions the gravi-signal was processed in an opposite manner to that in the controls. This effect is currently being investigated in detail.
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Discussion |
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It has been shown by the reported studies on rye that (1) coleoptiles, like many other organs, do not have a fixed GSA, (2) the GSA of a coleoptile can be greatly influenced by exposure to exogenous ethylene, and (3) the manipulation of ethylene homeostasis can influence the GSA of the coleoptiles.
The fact that the GSA of coleoptiles can be manipulated so easily by the conditions adopted during the growth of the seedlings may explain the lack of observations in the literature concerning the deviations of coleoptiles from the vertical. Experimenters with a preconceived idea that coleoptiles must be vertical at the start of any study of coleoptile gravitropism would have adopted conditions for growing their seedlings which produced vertical coleoptiles. Observations of wheat and maize coleoptiles suggest that rye is not atypical in joining the growing list of organs in which the GSA is a variable that can be influenced by environmental conditions.
The fact that ethylene can influence the GSA of rye coleoptiles is unsurprizing in the light of the observation of Neljubow (1901) that ethylene could influence the angle with respect to gravity of pea epicotyls. It is remarkable, however, that it has taken 100 years before one of the first reported effects of a plant hormone has been explored in more detail with respect to its effect on gravitropic growth. While a great many studies of the other aspects of the ‘triple response’ have been published in the century since Neljubow first reported it, there is only one other previous report that exposure to low ethylene concentrations caused plants (cotton) to adopt a prostrate habit (Hall et al., 1957). More studies were made of the ethylene-induced epinastic response of tomato petioles and it is possible that this response could involve an interaction with gravity because the effectiveness of ethylene depends on the orientation of the plant with respect to gravity (Crocker, 1932).
Why does ethylene cause a reduction in the GSA in pea epicotyls (sometimes labelled as impaired or even agravitropic growth), but causes an increase in the GSA (or a ‘better graviresponse’) of rye coleoptiles? The answer may lie in the differences between dicots and monocots in terms of the effects of ethylene on cell elongation. In dicots, ethylene causes a dramatic reduction in longitudinal expansion and an increase in radial expansion, but, in monocots, ethylene is less potent in inhibiting cell elongation. A comparison of the effects of ethylene on cell elongation in dicots and monocots showed that cell elongation in coleoptiles and mesocotyls of oat and maize seedlings was much less inhibited by the gas than the elongation of pea epicotyls. More importantly, ethylene-induced radial cell expansion was not evident in coleoptiles (Malloch and Osborne, 1976; HG Edelmann, G Gudi, F Kühnemann, unpublished observations). Indeed, although it is commonly stated that the ‘triple response’ in young seedlings is a characteristic ethylene response, it might more accurately be called a characteristic response of young dicot seedlings because there is little evidence that young monocot seedlings respond in a similar manner. Hence the dramatic reduction in the GSA of dicots may be related to a 90° shift in the axis of polarity of expansion, and the absence of ethylene-induced radial expansion in coleoptiles could explain why ethylene does not cause a reduction but an increase of the GSA in coleoptiles. Clearly the present study confirms the fact that monocots and dicots respond somewhat differently to ethylene with respect to its effect on gravitropic growth; yet it cannot, at least at this stage, explain those differences.
Light is known to influence the GSA of Tradescantia nodes, tomato hypocotyls and the roots of several species. The present study shows that light can increase the GSA of rye coleoptiles in a manner similar to applied ethylene. As demonstrated for Tillandsia and pea seedlings (Beßler et al., 1998; Goeschl et al., 1967), light induces the production of ethylene. As illustrated in Fig. 6, it was not possible to detect in water-incubated rye seedlings high amounts of released ethylene during this very early stage of seedling development. However, as illustrated in Fig. 6a, ethylene release seems generally to be enhanced during the light phases which decreases during the dark phases. This effect of light on ethylene release is more conspicuous when seedlings are grown either in solutions of ACC or ethephon. As demonstrated in Fig. 6b, dark phases are characterized by strongly inhibited ethylene release, whereas light phases are characterized by strongly enhanced ethylene release. It could therefore be speculated that the action of light on the GSA of the germinating seedlings is mediated via triggered ethylene synthesis.
Recently, surface-dependent alterations of the vector of root growth in Arabidopsis seedlings have been reported which is also modified by the mechanical resistance of the medium on or in between which they grow (Rutherford and Masson, 1996). In fact, with respect to the reported increased sensitivity of oat coleoptiles due to enhanced g conditions of up to 19.4 g (Johnsson et al., 1993) it is conceivable that this described effect may be due to an enhanced stress-induced synthesis of ethylene. Further studies are now needed to provide a better spatial and temporal analysis of the two processes in order to determine whether endogenous ethylene synthesis is used to regulate the GSA of some organs.
In dicots the story may be reversed, red light causes hook opening and ethylene causes hook closing in young dicot seedlings. The role of ethylene in the previously reported light-induced GSA changes awaits exploration.
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Acknowledgements |
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We thank Dr Richard Firn, University of York, GB, for helpful discussions and critical comments. This work was supported by the Fonds der Chemischen Industrie, which is gratefully acknowledged.
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References |
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