Journal of Experimental Botany, Vol. 51, No. 344, pp. 579-586,
March 2000
© 2000 Oxford University Press
Auxin-dependent cell wall depositions in the epidermal periplasmic space of graviresponding nodes of Tradescantia fluminensis
Botanisches Institut der Universität Bonn, Abteilung Zellbiologie der Pflanzen, Venusbergweg 22, D-53115 Bonn, Germany
Received 1 June 1999; Accepted 8 October 1999
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Abstract |
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Differential growth of the nodal regions of graviresponding Tradescantia fluminensis (Wandering Jew) was analysed with special respect to the extension-restricting epidermal cells of the opposite growing and growth-inhibited organ flanks. Gravicurvature of horizontally gravistimulated isolated nodes depends on auxin (indolyl-3-acetic acid, IAA) and shows a node-specific profile in which the third node below the tip showed the greatest response. Exogenously supplied gibberellic acid induced no gravitropic growth. Vertically oriented isolated nodes supplied with exogenous IAA showed, on an electron microscopical level, conspicuous membrane invaginations with adjacent wall depositions restricted to the outer tangential epidermal cell walls. Their number was more than doubled by exogenously supplied Ca2+, which inhibited IAA-induced growth. No such changes could be detected in water-incubated segments or inner tissues of IAA-supplied segments. Gravistimulated differential growth of nodes of intact shoots and of nodal segments was characterized by changes similar to the ones induced by exogenous IAA, with greatly increased numbers of wall depositions within the epidermal cells of the growth-inhibited upper organ flank. Similar to the gravistimulated wall depositions, an asymmetric distribution pattern of Ca2+ was detected in the epidermal cell walls employing x-ray energy spectrum analysis (EDX). The results indicate that growth of nodes of Tradescantia fluminensis is regulated via IAA-induced secretion and subsequent infiltration of wall components enabling wall extension. The data support the hypothesis that temporary differential growth during gravicurvature of Tradescantia fluminensis is mediated by the antagonistic effect of Ca2+ -ions on the infiltration of IAA-induced wall-loosening components into the outer, extension-restricting epidermal walls thereby inhibiting growth.
Key words: Auxin, IAA, calcium redistribution, gravitropic growth, growth-associated depositions (GAD), osmiophilic particles (OPs), Tradescantia fluminensis L., wall-loosening.
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Introduction |
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Gravitropic growth of plant organs is mediated by temporary differences of growth rates between the opposite organ flanks (Firn and Digby, 1980
). In principle, differential growth could be mediated by various processes related to asymmetric changes in either synthesis, secretion or infiltration of both wall-loosening as well as wall-stiffening components. According to the Cholodny–Went hypothesis (Cholodny, 1928; Went, 1928), these changes are due to the gravistimulated lateral redistribution of IAA, with decreasing amounts of IAA in the upper flank and increasing amounts in the physiologically lower flank (Wilkins, 1979). In support of this hypothesis, lateral IAA redistribution in gravistimulated organs has been demonstrated in a number of studies (Wilkins, 1966; Iino, 1990). In several studies, however, it could be shown that during gravitropic growth no such lateral movement of IAA occurs (Bridges and Wilkins, 1973; Mertens and Weiler, 1983; Batten, 1982) or that the measured redistribution lags behind the tropic curvature (Firn and Digby, 1980). Therefore, at least in these cases, either other hormones or processes independent of IAA redistribution must be responsible for differential cell extension.
Earlier reports (Kutschera et al., 1987; Hoffmann-Benning et al., 1994; Edelmann et al., 1995) demonstrated that IAA-induced as well as gibberellic acid-induced elongation growth is characterized by the secretion-dependent occurrence of osmiophilic particles (OPs) specifically within the periplasmic space of the extension-restricting epidermis. Due to their strict growth-related occurrence it was speculated that they might be involved in hormone-induced cell wall-loosening and may represent visual images of secreted wall-loosening factors on their way into the walls (Edelmann et al., 1995). Recently, the relationship between elongation growth and their occurrence has also been demonstrated in epidermal cells of dicotyledon hypocotyls and epicotyls and also of roots. This indicates that their occurrence is not restricted to monocots and that they are not related to cuticle synthesis (Samajova et al., 1998).
Employing this epidermis-specific occurrence of periplasmic OPs as a probe for IAA-induced secretion, the distribution of these growth-related, presumably glycoproteinaceous particles (Hoffmann-Benning et al., 1994), has been analysed within the epidermal cells of the growing and growth-inhibited flank of graviresponding rye coleoptiles (Edelmann and Sievers, 1995). In contrast to what would be expected if there was a simple relationship between the periplasmic occurrence of these putative wall-loosening factors and elongation growth, under these horizontally gravistimulated conditions, the number of OPs was strongly increased in the growth-inhibited flank as compared to the lower flank in which the number of OPs was similar to vertical controls (Edelmann and Volkmann, 1996). As an hypothesis, it was therefore suggested that OPs do play a role in wall-loosening and that temporary growth inhibition of the epidermal cells of the upper flank is mediated by the inhibition of OPs to infiltrate into the walls, thereby causing a temporary standstill of extension growth of the upper flank (Edelmann and Sievers, 1995; Edelmann, 1997). In support of such an hypothesis was the finding that, in contrast to their periplasmic occurrence, the number of OPs was similar within the peripheral cytoplasm of the epidermal cells of both organ flanks (Edelmann and Volkmann, 1996). The result was interpreted in such a way that the asymmetries in OP numbers within the periplasmic space were due to changes other than secretion rates, but changes outside the membrane such as changes of the periplasmic milieu.
Similar to the asymmetric distribution pattern of periplasmic OPs, a strong increase of cell wall-bound Ca2+ within the outer epidermal cells of the growth-inhibited upper flank of graviresponding Avena coleoptiles has been described using the antimonate method (Slocum and Roux, 1983). These authors suggested that the temporary establishment of gravitropic growth may largely be a consequence of the antagonistic effect of Ca2+ on IAA-mediated cell wall-loosening and elongation growth within the upper organ flank.
Due to the coinciding asymmetric redistributions of both Ca2+ as well as of OPs it appeared conceivable, that the two phenomena may be causally related with respect to gravistimulated growth inhibition. In order to address this question, Tradescantia fluminensis was chosen as a model system since it is characterized by some distinct, from a methodological point of view, advantageous features: (i) gravitropic growth is characterized by a developmentally- and light-regulated gravitropic sign reversal (Myers et al., 1994); (ii) in contrast to coleoptiles, hypocotyls and epicotyls differential growth is restricted to the graviresponsive basal internode adjacent to the nodal plate (commonly labelled as ‘node’); (iii) different from grass nodes, extension growth of this internodal section is not restricted to gravistimulated growth.
The study was interested in whether this system is also characterized by (a) IAA-inducible OPs; (b) asymmetries of OPs during graviresponsive differential growth; and (c) asymmetries in wall-bound calcium during gravitropic growth.
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Materials and methods |
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Plant and culture conditions
Shoots of Tradescantia fluminensis Vell.
(Wandering Jew) were grown in the greenhouse (16–18 °C, 60% average air humidity). Young, nearly vertically grown shoots were cut below the 5th node (as counted from the tip), fixed in plastic caps filled with a volume of 15 ml Knop's solution and grown for 4 d in a light-chamber (approximately 35 µmol m-2 s-1; L18W/19 daylight 5000 de Luxe, Osram, München, FRG; 16/8 h light/dark) at 25±1 °C. Thereafter, they were placed for experimental periods up to 48 h in a dark-chamber at 25±1 °C with only temporary green safety light conditions (according to Mohr and Appuhn, 1963
). For gravistimulation vertically grown rooted cuttings and segments of shoots including the third node (‘isolated nodes’) were placed in a horizontal position. For testing the gravitropic growth response on hormones (or on the presence of intact leaves) the upper cut ends of isolated nodes were covered with lanolin paste which had previously been mixed with either distilled water (control), 10-5 M IAA, or 10-5 M GA, in a ratio of 2 : 1. Growth of intact shoots and of segments and the reorientation of the internodes was recorded by photography using a Nikon F 301 camera (Nikon, Japan) combined with a Nikon AF objective (2.8/100 mm, Nikon, Japan) in dim green safety light. The films used were Kodak Gold Ultra 400, (400 ASA) and Fujicolor Superia 400, (400 ASA).
The effect of IAA on growth as well as on wall-associated changes was tested in vertically oriented segments containing the third node. Each 10 segments were placed for 3 h in an aerated box filled with distilled water, or 10-5 M IAA or 10-5 M IAA together with 2x10-3 M CaCl2 (10 segments/200 ml).
Electron microscopy
Samples for transmission electron microscopy (TEM) were taken as 4–5 mm long segments from the two opposite flanks of the 3rd node 0 h, 3 h, 6 h, and 12 h after the onset of gravistimulation. Immediately after excision tissue samples were vacuum-infiltrated and fixed in 2% (v/v) glutaraldehyde in phosphate buffer (50 mM, pH 7,2) for 3 h. Thereafter the segments were washed in phosphate buffer, post-fixed for 2 h in 2% (w/v) aqueous OsO4, dehydrated in a graded acetone series and embedded in Spurr's epoxy medium (Spurr, 1969). Ultrathin transverse sections were cut with glass on a Reichert ultramicrotome OM U3 (Reichert, Vienna, Austria), mounted on copper grids, post-stained with 2% aqueous uranyl acetate for 20 min and examined in a Zeiss EM 10 electron microscope (Zeiss, Oberkochen, Federal Republic of Germany). Membrane-associated wall changes were analysed in at least three individual samples from each of which at least 10 cells were counted. The average values of each individual were combined to a mean value (±SE).
Electron dispersal X-ray (EDX) analysis
Epidermal strips were peeled of the upper and lower node flanks, fixed in 3% (v/v) glutaraldehyde, dehydrated in an increasing ethanol/water mixture, critical point- (CP) dried with carbon dioxide (Balzers CPD 020, Balzers, Wiesbaden, Germany), sputtered with gold and analysed at a 5000-fold magnification.
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Results |
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As shown in Fig. 1A
, light-grown shoots of Tradescantia fluminensis exhibit node-specific set point angles (Digby and Firn, 1995) which change in a developmentally regulated manner, thereby forming a ‘standing wave’ (Myers et al., 1994). Generally, the third node, as counted from the tip, showed the most pronounced curvature angle of an average 50–60° relative to the organ axes, which again decreased to a value of an average 10° as soon as it shifted into the fourth node position due to the formation of a new node at the shoot tip. Similar graviresponses as well as their development-dependent changes have been described previously (Digby and Firn, 1995).
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For kinetic characterization of the graviresponsivity of the different nodes following standardized horizontal gravistimulation, shoot cuttings (including five nodes as counted from the tip) were placed in such a way that all internodes were in a horizontal position by tilting them from their original postion by 90° perpendicular to the basal organ axes. Under these standardized conditions the profile of the degree of graviresponsivity of the nodes was similar to the profile of the node angles of the intact trailing shoots (Fig. 2
). Again the third node showed the fastest and eventually most pronounced gravitropic growth response. The angle of curvature continuously increased for a period of up to 48 h. As compared to this continuous increase the first and second node showed a temporarily increased gravicurvature which decreased again between 24 h and 48 h after the onset of gravistimulation. Due to this antagonistic response, an overall angle of the entire shoot internodes of roughly 90° was maintained. In contrast to grass nodes, gravisresponsive growth of nodes of Tradescantia is characterized by a pronounced length increase of the graviresponsive and the adjacent organ part subsequent to gravicurvature, contributing to an increase in internode length. As shown in Fig. 1B after 3 d, this effect is most pronounced in the most graviresponsive third node. On a cellular level gravitropic growth of the nodes was characterized by a pronounced length increase of the epidermal cells of the lower flank whereas the cells of the growth-inhibited upper flank maintained more or less their original lengths. As shown in Fig. 3, 60 h after the onset of gravistimulation the cells increased about 2–3-fold in length illustrating cell extension as the principal means for the length increase of the lower organ flank. In order to test whether gravitropic growth of Tradescantia fluminensis depends on IAA or on gibberellic acid, shoot segments consisting of nodes proximal to two internodal halves were gravistimulated in the dark in a horizontal position and their effect was analysed as supplied on the cut end surfaces dissolved in lanolin paste (Fig. 4). Similar to intact shoots, containing five nodes, gravitropic growth was more or less restricted to the first three nodes. No gravitropic growth was observed in the control, i.e. segments in which the lanolin paste was applied together with water (data not shown). Similar to water controls, segments supplied with gibberellic acid showed no gravitropic growth within 24 h. In contrast, a node-specific profile of graviresponsive growth was observed in segments which were supplied with IAA (Fig. 4A). Although not as pronounced, gravicurvature was also observed in segments without exogenous IAA-supply but with intact leaves, confirming earlier reported results (Schuhmacher, 1923). From these results it can be inferred that differential extension growth during gravicurvature of Tradescantia depends on IAA-induced wall-loosening.
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), 12 h (
), 24 h (
), and 48 h (
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As demonstrated in previous studies (Kutschera et al., 1987
; Hoffmann-Benning and Kende, 1992; Hoffmann-Benning et al., 1994; Edelmann et al., 1995), IAA- as well as gibberellin-induced elongation growth of coleoptiles—but also, as shown recently (Samajova et al., 1998), of hypocotyls and epicotyls of both sunflower and pea, respectively—is characterized by the IAA-induced occurrence of osmiophilic particles (OPs) within the outer periplasmic space of the epidermal cells. Therefore, whether similar putatively wall-loosening related structures could be detected in Tradescantia during IAA-induced elongation growth was tested by incubating segments in a vertical position in either distilled water or IAA-solution. Although not as osmiophilic as observed in other analysed systems (Edelmann and Volkmann, 1996; Samajova et al., 1998), similar structures could be detected in the periplasmic space of IAA-incubated segments which were associated with more or less pronounced membrane invaginations (Fig. 5). The strongly enhanced occurrence of these structures by IAA was restricted to the epidermis and it was possible to detect them only very rarely in epidermal cells of water-incubated segments (Table 1). Due to their strict epidermis-specific and growth-related occurrence, it is conceivable that the physiological significance of these structures may be analogous to the one ascribed to OPs. Therefore, this study was also interested in whether the distribution pattern of these structures was similar to the one observed in OPs during gravitropic growth of coleoptiles (Edelmann and Sievers, 1995). As illustrated (Table 2) the occurrence of these wall-associated structures was temporarily augmented in the epidermal cells of both the lower and upper flank of the graviresponding nodes. As compared to the lower flank, however, their numbers were strongly increased in the growth-inhibited upper flank. The increased and strongly asymmetric occurrence of OPs from 3–6 h after the onset of gravistimulation coincides with the phase of visible differential growth (data not shown) which is temporarily succeeded by symmetrical, undifferentiated elongation growth (compare Fig. 1B and Fig. 2).
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It was shown earlier (Slocum and Roux, 1983
) that gravicurvature of Avena coleoptiles is characterized by the accumulation of Ca2+ within the cell walls of the growth-inhibited upper flank. In order to elucidate whether the enhanced numbers of wall-associated structures within the periplasmic space of the growth-inhibited epidermal cells of graviresponding Tradescantia coincide with enhanced Ca2+ levels, its relative distribution within the outer epidermal cell walls of the opposite organ flanks was measured using the electron dispersal X-ray method (EDX). Although this method does not yield absolute but only relative amounts (Newbury, 1979), the measured results clearly show that a 2–3-fold increased amount of Ca2+ is located within the cell walls of the epidermal cells of the upper, growth-inhibited organ flank (Fig. 6).
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For testing whether there may be a causal relationship between the increased occurrence of IAA-induced wall-associated depositions and increased calcium levels within the apoplast, vertically oriented segments were incubated in distilled water and IAA-solution with and without CaCl2. Calcium has been demonstrated to inhibit growth in a number of studies (Virk and Cleland, 1988
). As shown in Table 1, in segments incubated without IAA infiltration of the walls in 10-3 M CaCl2 solutions had no significant effect on the number of periplasmic deposits. In contrast to this, Ca2+, in addition to its inhibiting effect on growth, caused a strong enhancing effect on the number of wall depositions in their periplasmic space of the epidermal cells of IAA-incubated nodal segments. However, no effect of Ca2+ could be measured on the extensibility of isolated, frozen/thawed walls of either nodes as measured with the creep test method (data not shown).
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Discussion |
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As demonstrated in this study, gravistimulated, differential growth of nodes of Tradescantia fluminensis depends on IAA, which is generally accepted to induce cell extension via the secretion of wall-loosening factors (Cleland, 1971
; Taiz, 1984). According to the Cholodny–Went hypothesis, differences in extension rates of opposite plant organs due to tropic stimulation are due to the lateral redistribution of IAA. In addition to, or as a possible alternative, temporary growth rate changes could, in principle, also be due to asymmetrically induced processes superimposed onto wall loosening such as asymmetries in phenolic cross-linking (Biggs and Fry, 1987) or to prevention of wall-loosening due to processes interfering with the sequence of IAA-mediated causal steps prior to wall changes. In fact, any step along the IAA-induced sequence of causal events, such as processing of wall-loosening factors within the cells, their secretion or their infiltration into the walls may be subject to asymmetric modifications leading to differential growth.
In favour of such scenarios, it has been shown in a number of studies, that graviresponding plant organs are characterized by changes in apparent IAA-sensitivities (Salisbury et al., 1988; Rorabaugh and Salisbury, 1989; Stinemetz, 1996) although interaction changes of IAA with its receptors (as implied by the expression sensibility) have not been demonstrated. In an attempt to identify asymmetries related to secretory processes, Carrington and Firn analysed the percentage volume of the cytoplasm occupied by various membrane fractions of the upper and lower epidermal cells of graviresponding cucumber hypocotyls (Carrington and Firn, 1983). However, similar to the results reported previously (Edelmann and Volkmann, 1996) for the distribution of epidermis-specific cytoplasmic osmiophilic particles (OPs), they did not detect any significant differences in vesicles, dictyosomes or rough endoplasmic reticulum, respectively.
In contrast to the conditions observed within the cytoplasm, the results of this and of earlier presented studies (Edelmann and Sievers, 1995; Edelmann and Volkmann, 1996) demonstrated pronounced asymmetries between the plasma membrane and the outer cell walls of the extension-restricting epidermal cells. Similar to the asymmetric distribution pattern of OPs observed in graviresponding coleoptiles, gravitropic growth of Tradescantia is characterized by enhanced numbers of wall depositions within the periplasmic space of the upper growth-inhibited epidermal cells of graviresponding nodes as compared to the growing epidermal cells of the temporarily growth-induced lower flank.
Analogous to periplasmic OPs in coleoptiles in Tradescantia, these structures are induced by IAA along with its inducing effect on extension growth (Table 1). Based on a linear correlation between the number of these secretion-dependent, IAA-induced wall depositions and extension growth, their distribution pattern between the opposite organ flanks during graviresponsive growth appears in contrast to their presumed wall-loosening role (Robinson, 1995).
However, a wall-loosening effect would be expected to depend on the infiltration of these factors into the wall matrix thereby inducing cell extension. In principle, therefore, an increase in the periplasmic occurrence of these presumptive wall-loosening factors would also be expected if they were inhibited, subsequent to their secretion, from infiltrating the walls. In such a case, despite their enhanced periplasmic numbers, growth would be inhibited due to the prevention of the wall-loosening within the wall matrix.
It has been demonstrated earlier, that Ca2+, which inhibits extension growth (Cleland and Rayle, 1978), accumulates within the cell walls of the epidermal cells of the growth-inhibited upper flank of graviresponding Avena coleoptiles (Slocum and Roux, 1983). In principle, therefore, asymmetrical inhibition of growth during gravicurvature could be mediated via a temporary inhibiting effect of Ca2+ on the infiltration of wall-loosening factors into the walls, without a direct inhibiting effect on the extensibility of isolated walls (Cleland and Rayle, 1978).
In support of such a causal role of different amounts of wall-bound Ca2+ during gravitropic growth, it was possible to demonstrate its relative increase also in the walls of the growth-inhibited flanks of graviresponding nodes of Tradescantia. Most importantly, it was possible to demonstrate the inhibiting effect of Ca2+ on IAA-induced growth (Table 1) to be accompanied by the very same effects as observed during differential growth of graviresponding nodes of Tradescantia (Table 2). On the one hand IAA-dependent extension growth of vertically incubated controls, as well as of the lower flanks of graviresponding nodes, is characterized by the occurrence of periplasmic wall deposits. On the other hand growth inhibition of the upper organ flank which is characterized by a 2–3-fold increase in wall calcium exhibits a strong increase in wall deposits similar to the effects observed during inhibition of IAA-induced growth due to exogenously supplied calcium. However, in water-incubated nodal segments, exogenously supplied calcium did not induce the occurrence of periplasmic wall deposits (Tables 1, 2; Fig. 6). Since it was not possible to demonstrate any effect of Ca2+ on the extensibility of tension-stressed isolated walls of epidermal strips of Tradescantia nodes (data not shown), the inhibiting effect on growth does not seem to be due to a direct interaction with wall polymers, but to its inhibiting effect on secretion-dependent wall-loosening processes.
Whether Ca2+ is redistributed from the lower to the upper organ flanks has not been analysed nor whether the asymmetric content originates from more localized translocations. Yet these present measurements clearly demonstrate an asymmetric distribution pattern within the graviresponding region as measured with EDX.
At present, it is only possible to speculate how this asymmetric Ca2+ pattern is brought about and where the wall calcium causing the asymmetric distribution within the region of differential growth comes from. As demonstrated in earlier studies, calcium is not homogeneously distributed within the walls of an organ but shows a distinct tissue-specific longitudinal as well as radial distribution pattern (Slocum and Roux, 1983; Bagshaw and Cleland, 1993a, b). Possibly, redistributions of wall calcium in either of these directions may play a crucial role. Interestingly, calcium-containing crystallites (presumably calcium-oxalate) were observed within the cells of the peripheral tissues as measured with the EDX method (data not shown); it is conceivable that they might have some relevance in this respect.
Apparent evidence against the involvement of wall-bound Ca2+ redistribution within the extension-restricting epidermal cells has been presented (Bagshaw and Cleland, 1993a, b). However, as indicated (Edelmann, 1997), their measurements using ‘epidermal peels’ which consisted of five to seven cell layers may not yield sufficiently detailed data. In fact, these measurements indicate that the Ca2+ asymmetries are restricted to the epidermal walls and cannot be detected in the peripheral mesophyl (data not shown).
Since it was possible to demonstrate that the frequency of IAA-inducible wall deposits is enhanced by increased levels of Ca2+which inhibits growth, it is conceivable, that both effects are causally related.
Interestingly, similar, yet more osmiophilic particles within the periplasmic space have been described previously (Heumann, 1983) in Chara internodal cells, the number of which was greatly enhanced when the cells had been preincubated in Ca2+-rich medium before fixation. Since Ca2+ inhibits growth it is conceivable that in this system, too, increased numbers of OPs as well as increased wall–Ca2+ may be causally related to growth inhibition.
According to these results, and in support of earlier presented models, a scenario of how the processes leading to temporary growth inhibition during gravitropic bending may consist of the inhibiting effect of temporarily increased calcium levels on the infiltration of IAA-induced secreted wall-loosening factors. Due to their elongation-related occurrence, it is possible that IAA-induced, secretion-dependent OPs as well as the IAA-induced less osmiophilic wall depositions in the epidermal walls of Tradescantia represent such wall-loosening factors. Such an interaction could also explain the inhibiting effect of calcium on growth without any effect on the extensibility of isolated walls as also reported previously (Cleland and Rayle, 1978; Virk and Cleland, 1990).
In conclusion, the dependence of gravicurvature on IAA, together with the measured increase of calcium in the growth-inhibited node flank as well as the demonstrated effect of calcium on growth and the occurrence of IAA-induced wall deposits strongly support the hypothesis, that gravicurvature of Tradescantia is mediated by temporarily increased Ca2+ levels within the upper epidermal walls, temporarily preventing IAA-induced wall-loosening due to the inhibition of wall-loosening factors to infiltrate the walls.
Such a mechanism would suffice for temporary differential growth even without lateral movement or asymmetric distribution of IAA, the absence of which, apart from grass nodes, has also been demonstrated in the nodes of related, graviresponding Zebrina pendula (Batten, 1982).
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Acknowledgments |
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We thank Hans Jürgen Ensikat (University of Bonn) for advice and assistance regarding the EDX analyses.
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Notes |
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1 To whom correspondence should be addressed: Fax: +49 228 2677. E-mail:edelmann{at}uni\|[hyphen]\|bonn.de
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References |
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