Journal of Experimental Botany, Vol. 54, No. 389, pp. 1899-1907,
August 1, 2003
© 2003 Oxford University Press
Relationship between endogenous indole-3-acetic acid and abscisic acid changes and bark recovery in Eucommia ulmoides Oliv. after girdling
Received 25 December 2002; Accepted 2 May 2003
1 Peking University, College of Life Sciences, Dept of Plant Molecular and Developmental Biology, Beijing 100871, PR China
2 Commissariat Général à l’Energie Atomique-CREN-K, BP 868, Kinshasa XI, Democratic Republic of the Congo
* To whom correspondence should be sent. Fax: +86 10 62751526. E-mail: ckm{at}pku.edu.cn
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Abstract |
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Eucommia ulmoides (Eucommiaceae), a traditional Chinese medicinal plant, is often subjected to severe manual peeling of its bark. If the girdled trunk is well protected from desiccation, new bark forms within 1 month. It has been proposed that phytohormones play a key role in this process. Research has been conducted to determine the distribution of endogenous indole-3-acetic acid (IAA) and abscisic acid (ABA) during the bark recovery, using high-performance liquid-chromatography (HPLC) and fluoro-immuno-localization techniques. Results showed that, from 2 d after girdling, the IAA content in the recovering bark (RB) increased markedly while that of ABA decreased. The opposite pattern was observed during progressive re-establishment of the tissues. Immuno-localization showed that most of the IAA was located in the RB tissue layers undergoing cell division, dedifferentiation and (re)differentiation, such as xylary rays, immature xylem, phellogen and cambial regions. This study also provides evidence that IAA and ABA are involved in the bark reconstitution.
Key words: Abscisic acid (ABA), auxin (IAA), bark recovery, cambial region, dedifferentiation, Eucommia ulmoides, girdling, HPLC, immuno-localization.
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Introduction |
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Most higher plants possess the ability to reconstitute their vascular tissues after relatively severe wounding. This phenomenon is due to the totipotency of plant cells when they are not highly differentiated. During the structural and functional regeneration of damaged parts, plant cells are first dedifferentiated and become meristematic before entering a second differentiation (Fukuda, 1997).
Phytohormones have been reported to play a key role in vascular tissue regeneration (Aloni, 1995; Cui et al., 1995; Wang and Cui, 1998), some acting as promoters and others as inhibitors. Among the plant growth regulators dynamically intervening in this mechanism, indole acetic acid (IAA), abscisic acid (ABA) and cytokinins are cited most often. Broadly, IAA promotes cell division, elongation and differentiation, whereas ABA regulates IAA biosynthesis and activity. Cytokinins increase the sensibility of cambial initials and derivatives to auxin, stimulating them to differentiate into xylem cells (Baum et al., 1991; Aloni, 1995).
Eucommia ulmoides Oliv. is a multipurpose tree indigenous to China. It is a living fossil plant and the only species in both its genus (Eucommia) and its family (Eucommiaceae). Among its numerous attributes, this plant species is widely used in Chinese Medicine (Feng et al., 1997). Thus, it is frequently subjected to radical peeling of its bark, which contains the bioactive substances used for treating some human diseases.
Depending on the severity of peeling, E. ulmoides can either survive by reconstituting the removed bark or die. Li et al. (1981) have established optimal conditions for recovery of lost tissue in E. ulmoides stems without application of exogenous phytohormones. They concluded that when E. ulmoides trunks are covered with a transparent plastic sheet on the girdled area, the trees are protected against desiccation and recover their bark within 40 d. In another study, these workers also described the anatomical changes that occurred during bark reconstitution (Li et al., 1982).
However, some questions still remain unanswered. (1) What are the spatial and temporal patterns of phytohormone distributions within E. ulmoides tissues at different stages of bark reconstitution? (2) Where do the phytohormones act in these tissues? (3) What is the correlation between the morphological changes and the localization patterns of the phytohormones in the reconstituting tissues? (4) If IAA and other phytohormones play an important role in this process, what is their likely source, since the tissues that could transport them from sites of synthesis to the wounded area have been peeled off?
This study addresses some of these questions by quantification and immuno-localization techniques. Amounts of endogenous IAA and ABA were measured and the IAA localized in E. ulmoides vascular tissues at different stages of bark recovery after girdling.
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Materials and methods |
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Plant material and sampling
Four 6-year-old E. ulmoides trees, growing at Shunyi Eucommia Forestry Station, Chinese Agricultural Ministry (Beijing, PR China), were girdled as previously described (Li et al., 1982) in the summer of 2001 (Fig. 1A, B). Samples were taken at 0, 1, 2, 4, 7, 14, 21, 28, 42, and 63 d after girdling. At each sampling, a portion of the exposed surface of the progressively regenerating bark was carefully scraped with a sterilized scalpel at a depth that included the immature xylem cell layers. As revealed by light microscopy, the layers harvested on day 0 contained radially expanded vessels undergoing secondary wall thickening. A second scraping comprised some layers of mature xylem cells. All sampled materials were immediately fixed in liquid N2 for at least 1 h, then stored at –70 °C. The same sampling procedure was carried out on the cambial region (immature xylem-cambium-immature phloem) and mature xylem of non-girdled trees, which served as controls.
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Another series of samples consisted of excisions from the peeled stems of small tissue blocks. These blocks were immediately pre-fixed in 1-(3-dimethylaminopropyl)-3-ethyl carbodiimide (EDC), as described by Ohmiya et al. (1990) and Moctezuma (1999), for at least 2 h. They were then cut into smaller cubes, degassed for 15 min under a vacuum pump and post-fixed in a mixture of 2% paraformaldehyde and 0.5% glutaraldehyde overnight, before storage in 70% alcohol.
IAA and ABA quantification
The scraped samples were finely ground in liquid N2. Phyto hormones were extracted in 5 ml of 65% acetone overnight at 4 °C and polyvinylpyrrolidone (PVP) was added as an antioxidant. After centrifugation (4000 tpm, 15 min), the supernatant was retained. The pellet was re-extracted with 3 ml of 65% acetone and recentrifuged as above. The supernatants were pooled. After evaporation under a gas N2 flow at 45 °C, the pH of the remaining water phase was adjusted to 3. IAA and ABA purification was performed with 3 ml of pure acetyl acetate and passage through a C18 column. The acetyl acetate was also evaporated under an N2 stream. The resulting dried precipitate was collected in 0.8 ml of 50% methanol, filtered through a 45 µl membrane and submitted to high-performance liquid-chromatography (HPLC) analysis. No internal standard was applied, but, using the elution technique of Nordström and Eliasson (1991), 76% and 80% recovery were found, respectively, for ABA and IAA in this extraction-purification procedure. Phytohormone analysis was conducted on an Agilent computer-assisted HP1100 (Agilent Technologies, CA, USA), equipped with a vacuum degasser, a quandary pump, an auto-sampler, thermostated column compartment and a diode array detector. A ZORBAX RX-C8 column (4.6 mm x 25 cm, 5 µm) and a detection wavelength of 280 nm were used. The mobile phase consisted of 50% methanol in double-distilled water supplemented with 1% acetic acid after filtration through a 0.45 µm membrane filter. A sample (50 µl) was automatically injected at a flow rate of 1 ml min–1. Quantification was obtained by comparing the peak areas with those of known amounts of IAA and ABA (Zhongshan Corporation Ltd, China).
IAA localization
Tissue blocks preserved in 70% alcohol were dehydrated in an alcohol series and embedded in paraffin wax. Sections (9–10 µm thick) were obtained using a rotary microtome and allowed to dry overnight at 37 °C. Paraffin was removed and sections rehydrated in pure xylene, a reversed alcohol series, and distilled water. Blocking solution (0.2 ml of 0.1% Tween-20, 1.5% glycine, and 5% BSA, in PBS pH 7.2) was applied to sections for 45 min. The indirect immunostaining procedure of Moctezuma (1999) was followed, modified in respect of antibodies applied, the incubation times and the fluorescence-labelling used. The primary antibody was a polyclonal anti-IAA raised against carboxyl-linked IAA in rabbits (China Agricultural University, Beijing, China). Cross-reactivity was measured by enzyme-linked immunosorbent assay (ELISA). Compounds tested for competition with immobilized IAA-BSA included a series of indole derivatives, tryptophol and DL-tryptophan; all showed less than 2% of the reactivity of indole-3-acetic acid. The secondary antibody was a Rhodamin Red-conjugated goat anti-rabbit (Zhongshan Corporation Ltd, Beijing, China).
The sections were incubated in a humid chamber for 3 h and 1.5 h, respectively, after application of the primary and secondary antibodies. Rhodamin Red fluorescence was allowed to develop for 1 h. After mounting in Mowiol 4.88 (1:5/Mowiol:PBS, w:v; pH 8.5), sections were observed and photographed under a confocal laser-scanning microscope (Bio-Rad MCR-1024).
To check the effectiveness of the immunolocalization technique and the efficiency of the primary antibody used, negative and positive controls were performed on sections of very young E. ulmoides twigs and included the following treatments; (1) omission of all antibodies or application of (2) only primary antibody, (3) only secondary antibody, and (4) primary antibody incubated overnight with IAA to saturate binding sites of the antibody. This last control was carried out to check the occurrence of cross-activity of the primary polyclonal antibody with other antigens on the sections.
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Results |
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IAA and ABA change pattern
HPLC standards and sample peaks: HPLC peaks obtained from standard and sample solutions are presented in Fig. 2. Retention times were 5.781 and 10.420 min for IAA and ABA, respectively. Although some impurities still persisted in the extracts, the IAA and ABA purification protocol sufficed for quantification of the two phytohormones; their HPLC peaks were clearly distinct (Fig. 2).
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IAA and ABA content: Girdled and ungirdled trees of E. ulmoides showed consistently different IAA and ABA contents (Fig. 3). From 2–28 d, the amount of IAA in the recovering bark (RB) of girdled plants was significantly higher (P <0.01) than that in the cambial region (CR) of control plants (Fig. 3A1). The opposite tendency was recorded in the mature xylem (MX) from 1–7 d and at 28 d, where the ungirdled trees exhibited higher IAA content (P <0.01) than the girdled ones (Fig. 3A2).
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However, the ABA content was higher (P <0.05) from 1–14 d in the RB of ungirdled than in the peeled trees (Fig. 3B1). This trend gradually changed from 28 d, when the ABA amount in the ringed trees increased significantly (P <0.05) in comparison with the controls. At 63 d, there was no difference in ABA content between the two treatments. In the MX (Fig. 3B2), although the ABA values in the girdled trees were generally higher than those in controls, statistical analysis showed a significant difference (P <0.05) only on days 1, 7, 14, and 28.
Figure 3 shows noticeable differences between the time-courses of the two phytohormones in the RB and MX of peeled E. ulmoides. The total content of IAA in the RB was higher (P <0.01) than that in the MX (Fig. 3A1, A2). During the first 2 d after bark ringing (0–1 d), no change in IAA could be detected in the RB (Fig. 3A1). At day 2, however, the IAA content had almost doubled. It decreased slightly at 4 d before rising to a peak (780.19 ng g–1 FW) at 14 d. Between 28 d and 63 d the amount remained almost constant. The overall IAA pattern in the MX of girdled trees after 4 d closely resembled that in the RB (Fig. 3A2).
In both tissues, however, the time-course of ABA differed from that of IAA (Fig. 3B). It was higher in the MX than in the RB up to 21 d (P <0.05), then significantly declined until the end of the experiment (63 d) (Fig. 3B2). In the RB, the ABA content reached 3693 and 3574 ng g–1 FW at day 0 and day 1, respectively, but fell markedly at day 2 (1755 ng g–1 FW), then slowly increased to a maximum (5880 ng g–1 FW) at day 42.
IAA localization
Controls: Under fluorescence microscopy, a strong IAA signal was visible in the CR of newly developed branches from ungirdled tree samples (Fig. 4E) in comparison with the controls (Fig. 4A–D). The very dispersed fluorescence in the control sections can be attributed to autofluorescence, which has previously been reported in the walls of suberized cells in higher plants (Brown and Lemon, 1995), or in Fig. 4D to unbound antibodies in the primary antibody-IAA mixture.
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IAA location in E. ulmoides tissues after girdling: The IAA signal profile varied markedly with time in the cross-sections of peeled E. ulmoides (Fig. 5A–I). Throughout the bark recovery process, IAA remained present in the immature xylem region. Tissue samples freshly harvested on the day of bark peeling (day 0) showed very little IAA, almost evenly distributed in both immature and mature xylem cells (Fig. 5A). At day 1, the IAA signal in the exposed immature xylem zone was clear, especially in the dilated xylem ray cells on the peeled surface (Fig. 5B). At day 2, a strong IAA signal appeared in both the xylary rays and the developing callus (Fig. 5C). At day 4 the IAA signal could be perceived in the growing callus layers which, by this time, were invading almost all the girdled trunk area (Fig. 5D).
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The callus cell layers remained unsuberized until phellogen formation, which had begun at day 7 (Fig. 5E). At this stage the IAA was mostly detected in the nascent phellogen and the dividing immature xylem cell areas. This IAA profile is clearer at day 14 (Fig. 5F), when phellogen formation was complete and cambium differentiation had begun. The Rhodamin staining intensity persisted in the developing CR and the phellogen at day 21 (Fig. 5G). This period coincided with the progressive production of phloem cell layers from the cambium already active at that time. By day 28 (Fig. 5H) and day 42 (Fig. 5I), the CR was fully recovered. Interestingly, the IAA signal intensity has gradually diminished during these two stages.
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Discussion |
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Girdling usually disorganizes the physiological communication between leaves (sites of synthesis of most plant products) and roots. To survive and recover from this trauma, the plant must rapidly re-establish communications. The bark recovery process includes a variety of anatomical, physiological and hormonal changes.
The objectives of this study were (1) to assess the amount of endogenous IAA and ABA and (2) to locate the IAA in the newly elaborated RB and the adjacent MX during recovery.
Girdled trees versus ungirdled trees
IAA and ABA changes differed markedly, in both RB or CR and MX, in girdled and ungirdled trees (Fig. 3). The IAA content in the RB of peeled plants was significantly higher than that in the CR of unpeeled plants (Fig. 3A1). The opposite trend was obtained in the MX (Fig. 3A2). Converse changes occurred in ABA amount. Compared to the ungirdled trees, the bark peeling stimulated an increase of IAA and a decrease of ABA accumulation of about 100% between 2 d and 28 d.
Different plant tissues might be expected to participate in the response to such a severe trauma. In fact, although the IAA content of MX in girdled trees was lower (<100 µg g–1 FW) than in the RB (>250 µg g–1 FW), this decrease might be interpreted as IAA transfer from other (neighbouring) tissues. The increase of ABA in MX throughout the bark reconstitution process might promote this transfer of IAA by excluding it from the MX. If ABA inhibits IAA production, this might explain why the statistical difference between IAA or ABA values in girdled and ungirdled trees diminished from 28–42 d, coinciding with the full re-establishment of the bark in general and the vascular cambium in particular.
IAA and bark formation after girdling
According to the anatomical findings of Li et al. (1981, 1982) and Cui (1992) on E. ulmoides and in Juglans regia, respectively, after girdling, bark recovery involves four main steps; (1) Callus initiation (0–4 d), (2) division and dedifferentiation of exposed immature xylem cells (7–14 d), (3) phellogen and cambium formation (14–21 d), and (4) cambial region establishment (>21 d). In this study, the accumulation (Fig. 3A1) and strong fluorescence signal (Fig. 5A–G) of IAA during the first three steps showed that bark recovery was IAA-dependent. In fact, cell division, differentiation, dedifferentiation, and transdifferentiation are known to be phytohormone-dependent (Aloni, 1980; Catesson, 1994; Fan et al., 1999; Lachaud et al., 1999; Ye, 2002).
This finding indicates that IAA induces both dedifferentiation and differentiation (two opposite processes) of xylem cells, the cell dedifferentiation requiring probably higher IAA content than the cell differentiation. Additionally, recent observations (J Cao, F Jiang, KN’K Mwange, KM Cui, unpublished data) have revealed that, around 7 d after girdling, few sieve elements could be found near the immature xylem cell layers. They possibly resulted from a transdifferentiation of some immature xylems cells. If this finding is confirmed by further investigations, IAA could also be involved in the transdifferentiation process, which could require less IAA level, as low intensity of Rhodamin Red staining was displayed outwards near the immature xylem cell layers (Fig. 5E). The IAA receptors and signal transduction channels involved in the three processes are probably different.
Results described in this paper show that IAA content decreased at advanced stages of bark recovery (Figs 3A1, 5G–H) and became low by 42 d (Fig. 5I). From then onwards, with the complete recovery of the vascular cambial tissue, the tree regained its normal physiological activity. The previously peeled surface of the tree was protected by the new periderm, beneath which all the distinctive tissue layers (phellogen, cambial region, etc.) were operating fully.
Relationship between IAA quantification and localization in the RB
Several previous studies have demonstrated changes of IAA levels in plants after girdling (Cui et al., 1999) and removal of xylem (Wang et al., 1999), with seasons (Sundberg et al., 1987, 1990, 1991), or in bud development (Neil-Emery et al., 1998). However, these studies did not define the location of the phytohormone in the tissues. In this paper, IAA distribution in recovering E. ulmoides tissues was ascertained for 2 months using the fluoro-immunostaining procedure, and quantitative data were obtained by HPLC. A clear relationship between IAA quantification (Fig. 3) and location (Fig. 5) was apparent. As a matter of fact, although the IAA content at day 1 remained low (Fig. 3A1), its signal in the exposed immature xylem (Fig. 5B) was stronger than at day 0 (Fig. 5A), showing mobilization of IAA in this tissue layer. The elevated amount of IAA at 2 d (Fig. 3A1) was mainly located in the xylary ray cells (extending deeply in the MX), in the immature xylem cells and the nascent callus (Fig. 5C). Also, the slight decrease of IAA (509 ng g–1 FW) at 4 d was mainly found in the immature xylem and the callus (Fig. 5D), which is still small at this stage of bark restoration. Furthermore, the IAA amount increase noted between 7 d and 21 d (Fig. 3A1) was mainly confined to the immature xylem and the callus where cell differentiation was imminent, such as cambial and phellogen regions (Fig. 5E–G). A relative decrease of the IAA signal was exhibited in the RB at 28 d and 42 d (Fig. 5H–I); most of the IAA was now in the new CR and phellogen, already functional at this step of bark recovery.
Do IAA and ABA interact during bark recovering?
Interactions between different signalling systems are common in living organisms. In plants, hormones seldom act as unique controllers of a physiological or biochemical event; rather, a network of interacting factors is involved, some of which may be synergistic and others antagonistic (see reviews by Fukuda, 1996; Ross et al., 2002; Ye, 2002).
It was notable that, in this study, the IAA and ABA content changes from 0–63 d were opposite in both RB and MX. Such mirror-image behaviour of IAA and ABA has been noted previously (Wijayanti et al., 1995; Peres et al., 1997; Kojima et al., 1999). This study agreed that ABA and IAA interact in recovering bark.
Sources of IAA and ABA during the process of bark recovering
In plants, IAA and ABA are usually synthesized in apical buds, young leaves or growing tissues and in dormant buds, mature leaves, fruits or seeds (Raven et al., 1992; Cutler and Krochko, 1999; Sauter et al., 2001). IAA polar movement in plant shoots and roots has only been observed to about 7.5 mm h–1 (Epstein and Ludwig-Müller, 1993) or 1 cm h–1 (Moore et al., 1995). The trees used in this study were 6-years-old. The girdled areas (Fig. 1B) on the trunks were wide (1.2 m long) and distant from sites of IAA and ABA biosynthesis. No exogenous IAA or ABA was applied during the experiment. Therefore, the IAA and ABA (Figs 3, 5) in the girdled part were endogenous, but their source was uncertain.
Plant hormone biosynthesis is not yet fully elucidated. For instance, several pathways have been implicated in IAA biosynthesis (Normanly et al., 1993). Bartel (1997) and Bartel et al. (2001) observed that plants produce free IAA by both de novo synthesis (tryptophan-dependent or tryptophan-independent pathways) and IAA-conjugate hydrolysis.
In this study, the quantified and immuno-localized IAA in E. ulmoides RB was presumably released from conjugated IAA. The trees were girdled in late June (summer) when physiological activity had reached a plateau. Much of the IAA synthesized during late spring and early summer had been stored as conjugates. The trunk bark peeling probably induced the recovery of IAA from these conjugates, as suggested by Cui et al. (2000).
Both in vitro (Feung et al., 1977; Hangarter and Good, 1981) and in vivo (Bialek et al., 1983; Bialek and Cohen, 1992) investigations established that (1) IAA conjugates are slow-release sources of free IAA in plants tissues, and (2) tissue activity is directly related to the amount of free IAA obtained by their hydrolysis. IAA-conjugates hydrolyzing enzymes have been detected in a number of plants (Helmlinger et al., 1987; Jakubowska et al., 1993; Ludwig-Müller et al., 1996).
The rate of hydrolysis of ester- and amide-conjugates of IAA has been investigated mainly in relation to plant growth (see review by Cohen and Bandurski, 1982), but not to plant recovery after girdling. As the hydrolysis rates of IAA-conjugates differ (Baldi et al., 1989), a systematic screening of the IAA-conjugates present in E. ulmoides needs to be undertaken and their hydrolysis rates determined.
Less is known about ABA. However, the antagonism between IAA and ABA in plant tissues suggests that the fate of ABA in plant wound recovery follows the opposite pattern to IAA. It is probable that during E. ulmoides bark recovery, ABA removal (conjugation or degradation) accelerates to amplify the expression of IAA required for cell division, dedifferentiation and differentiation.
The progressive decrease of IAA content observed after the complete formation of the bark in the girdled trees (at 28 d) (Fig. 3A1), is concomitant with the increase of ABA (Fig. 3B). With the progressive reactivation of vascular tissues, ABA might be transported from leaves to the recovered bark through the usual (non polar) transport mechanism. Both IAA-decrease and ABA-increase movements are probably necessary to re-establish hormonal homeostasis in the trunk recuperating from the wounding stress.
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Acknowledgements |
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This paper was supported by the State Key Basic Research and Development Plan of China (G19999 [GenBank] 016002) and the National Natural Science Foundation of China (30170056, 30070614). The authors also thank the Governments of China and Democratic Republic of the Congo for the scholarship awarded to Mr KN’K Mwange.
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