Journal of Experimental Botany, Vol. 53, No. 375, pp. 1825-1828,
August 1, 2002
© 2002 Oxford University Press
Ethylene perception generates gravicompetence in gravi-incompetent leaves of rye seedlings
Received 3 January 2002; Accepted 23 April 2002
Botanisches Institut der Universität Bonn, Abteilung Molekularbiologie, Kirschallee 1, D-53115 Bonn, Germany
1 Fax: +49 228 73 9004. E-mail: edelmann{at}uni-bonn.de
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Abstract |
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The elongating leaves of young rye seedlings do not show a gravitropic response when placed horizontally. However, after treatment with ethylene, either supplied exogenously via ethephon or by application of its precursor 1-aminocyclopropane-1-carboxylic acid (ACC), gravicompetence is seen. The inhibition of ethylene perception by 1-methylcyclopropene (MCP) prevents gravicompetence. Young rye leaves provide a useful model system in which to identify the components of the gravity sensing or response systems, the presence of which govern gravicompetence.
Key words: Key words: ACC, coleoptiles, ethephon, ethylene, gravicompetence, gravitropism, primary shoots, rye, Secale cereale.
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Introduction |
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One of the most obvious features of plant development, namely asymmetric growth that results from the gravitropic stimulation of an organ, is still enigmatic (Chen et al., 1999, and studies cited therein). Traditionally, the spatial (re)directioning of plant growth, either of individual organs or of entire plants, is considered to result from three principal sequential processes, namely the perception of the gravitropic stimulus, the transduction of a signal and the initiation of an asymmetric growth response (Audus, 1969). The growth rate changes that are initiated by the exposure of some cells to a particular gravity vector are thus the result of a signal transduction pathway. The factors that determine whether an organ will be showing a gravitropic response include whether it has been displaced sufficiently from its gravitropic equilibirium angle (Pickard, 1972) and whether it possesses all the elements of the signal transduction chain, i.e. whether it is gravicompetent. From a cybernetical point of view, plant organs which are characterized by pronounced elongation growth, yet do not respond gravitropically, either lack the capacity for graviperception or for processing or transduction of the perceived gravi-signal (Volkmann and Sievers, 1979). One such system is the primary leaf of germinating rye seedlings which shows pronounced elongation growth but lacks gravicompetence. During the early phase of seedling development, the coleoptile is gravicompetent but the enclosed leaf is not (Edelmann, 1996). Studies of the gravitropic response of the intact seedlings revealed that ethylene has a pronounced effect on the gravitropic setpoint angle (Firn and Digby, 1997) of the coleoptile (Edelmann et al., 2002). When studies were conducted on intact seedlings it was impossible to distinguish whether the effects of ethylene were caused by effects directly on the coleoptile or whether some effect was also the result of an effect on the enclosed primary leaf, even though this organ was found to lack gravicompetence when studied in the absence of the coleoptile. Surprisingly, it was found that ethylene generates gravicompetence in the primary shoots of rye. Although a number of studies have suggested that ethylene can influence gravitropism (Wheeler and Salisbury, 1980; Kaufman et al., 1985; Madlung et al., 1999), this is the first report of an ethylene involvement in the establishment of gravicompetence.
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Materials and methods |
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Seeds of rye (Secale cereale cv. Marder II) were germinated and grown in the dark at 25±2 °C in vermiculite for 2 d, giving seedlings with 1.5–2 cm coleoptiles and 1–1.5 cm primary leaves. To remove the coleoptile, its base was partially circumscribed with a sharp blade and the coleoptile was gently flexed about that point to cause a circumferential splitting off of the coleoptile, but not of the primary leaves. The coleoptile could then be removed by cautiously pulling it upwards between the thumb and the forefinger. Residual basal parts of the coleoptiles attached to the seed were removed with forceps (Edelmann, 1996). Such coleoptile-less seedlings were placed in the dark at 25 °C on moist filter paper and treated as indicated in the figures. Ethylene treatment was performed by application of solutions of EthephonTM or of its precursor 1-aminocyclopropane-1-carboxylic acid (ACC), as indicated in the figures. Methylcyclopropene (MCP) was applied by dissolving 5 mg in a total volume of 5 ml water in Petri dishes prior to closure of the incubation boxes.
The distribution of elongation in an organ was analysed by marking five similar (2 mm) sized zones on the organs with an ink pen and measuring the length of each zone at the times specified. For documentation purposes, photographs were taken at specific time points with a RICOH digital camera.
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Results and discussion |
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In rye seedlings, the patterns of elongation in the coleoptile and the primary leaf it encloses are very different. In the coleoptile, most elongation occurs in the upper half of the organ. In primary leaves the intercalary elongation growth of the basal region predominates. Because of this different pattern, the apical part of the leaf is pushed into the elongating coleoptile and the cells of the upper leaf show no change in length during the analysed period of 4 d (Fig. 1).
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When placed either in an inverse vertical position (Edelmann, 1996; Fig. 2) or in a horizontal position (or any other direction), the coleoptile-less primary shoots do not respond gravitropically. However, when the coleoptile-less seedlings are grown for very long periods (18–22 d), the primary leaves eventually become able to show a gravitropic response. This gaining of gravicompetence is dependent on the season of the year and also on the conditions of light (HG Edelmann and S Kramer, unpublished data).
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Ethylene has recently been demonstrated to influence the GSA of intact, dark-grown rye seedlings (Edelmann et al., 2002). In order to test whether this gaseous hormone also exerts any effect on the primary leaves of coleoptile-less seedlings with respect to their gravicompetence, ethylene released from solutions of EthephonTM was applied. The primary leaves of dark-grown seedlings treated at 25 °C with EthephonTM for 3 d showed a pronounced gravitropic response (Fig. 2b) which was not observed in water-incubated control seedlings, despite marked elongation growth evident in these controls (Fig. 2a). The region of gravitropic curvature corresponds with the profile of elongation of the gravi-insensitive primary leaves (Fig. 1). This gain in gravitropic competence could also be induced by the application of ACC (data not shown), a precursor of ethylene within the incubation solution (Bleeker and Kende, 2000).
When coleoptile-less seedlings were treated with methylcyclopropene (MCP), which in a number of studies has been shown to inhibit ethylene perception (Serek et al., 1994; Sisler and Serek, 1997; Müller et al., 2000) elongation growth is slightly inhibited and now and again the lamina of the primary leaves are more flattened compared to the rolled up habit of the control leaves. Most important, however, ethylene is no longer capable of generating gravicompetence in such seedlings (Fig. 2c).
Whether ethylene imparts a capacity or capability in the mechanisms of graviperception or in the components of signal transduction or response pathways cannot be established by the experiments reported. However, in contrast to the secondary role attributed to ethylene for the mechanism of gravitropic growth regulation in a broad number of studies, these results clearly demonstrate that ethylene perception must be an indispensable step in the mechanism of gravitropic growth regulation in primary shoots of rye.
With respect to the necessity of ethylene for gravitropic growth, the list of the reported effects of ethylene dates back to the observations of Neljubow (1901). Wright et al. (1978) measured increases in auxin followed by 3-fold increases in the evolution of ethylene in horizontally placed grass nodes (Echinochloa colonum) and therefore concluded ethylene to be symptomatic rather than causal. While Wheeler and Salisbury (1980), advocated ‘a role for ethylene’ in gravitropism, Harrison and Pickard (1986) demonstrated that ethylene is not a mediator for gravitropic growth in tomato. Lomax and coworkers (Madlung et al., 1999) attributed ethylene multiple roles in the gravitropic response of tomatoes while emphasizing that ethylene does not play a primary role. In fact, neither in reviews on gravitropism (Chen et al., 1999), nor on ethylene action (Bleeker and Kende, 2000) has any crucial role been attributed to ethylene in gravitropism. The present study suggests that the emphasis of previous work in seeking a primary role for ethylene as a causative agent in controlling differential elongation, may have been misplaced. The role of ethylene in gravitropism would seem to be more concerned with the gravicompetence (this study) and the establishment of the gravitropic setpoint angle (Edelmann et al., 2002).
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Conclusions |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionsReferences |
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The finding that exogenous ethylene generates gravicompetence in a gravi-incompetent system is novel. It implies that ethylene perception either constitutes a decisive part of the mechanism of graviperception or that it is a cardinal step within the transduction of the perceived gravi-signal. Within this newly introduced system, further physiological, biochemical and molecular characterization of the discovered effect will allow us to relate and narrow down at least part of the potential steps causally involved in gravitropic growth regulation also to ethylene-perception-dependent processes. In fact, it may represent a key finding shedding new light on the still unknown parts of the mechanism of gravitropic growth regulation.
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Acknowledgements |
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This work was supported by the Fonds der Chemischen Industrie, which is gratefully acknowledged. We also thank M Serek (University of Hannover, Germany) and Hans de Wild (University of Wageningen, Netherlands) for the supply of MCP.
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References |
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