JXB Advance Access originally published online on October 9, 2006
Journal of Experimental Botany 2006 57(14):3857-3867; doi:10.1093/jxb/erl150
RESEARCH PAPER |
ABP1 expression regulated by IAA and ABA is associated with the cambium periodicity in Eucommia ulmoides Oliv.
College of Life Sciences, Peking University, Beijing 100871, China
¶ To whom correspondence should be addressed. E-mail: ckm{at}pku.edu.cn
Received 3 April 2006; Accepted 7 August 2006
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Abstract |
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A cDNA clone of Eucommia ulmoides Oliv. encoding auxin binding protein 1 (ABP1), one of the putative receptors of auxin, was isolated, and the seasonal expression of ABP1 in relation to IAA and ABA annual variation was investigated by different technical approaches including RT-PCR, real-time PCR, northern blotting, western blotting, and immunolocalization. In the cambial region, ABP1 expression at both the protein and the mRNA level was found to be high, low, and remarkably scarce in the active, quiescent, and resting stages, respectively, during cambium periodicity. The signal abundance of ABP1 follows the opposite pattern to ABA accumulation and correlates with auxin responsiveness of the cambial tissues, suggesting a role for ABP1 in mediating auxin-dependent regulation of cambial activation in the activity–dormancy cycle. This paper attempts to explain why IAA would ‘boost’ the reactivation of a quiescent cambium, and not that of a resting cambium. Results also show that ABP1 expression is improved by IAA, while inhibited by ABA.
Key words: ABA, ABP1, dormancy, Eucommia ulmoides, IAA, quiescence, rest
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Introduction |
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In the northern temperate zone, the vascular cambium of woody plants displays a cyclical pattern of activity and dormancy, with two distinctive phases in dormancy: quiescence and rest (Catesson, 1994). According to the definition of quiescence proposed by Little and Bonga (1974), investigations on cambial dormancy in the Eucommia ulmoides tree have shown that the rest phase is inserted between two quiescence phases (quiescence-1 and quiescence-2) (Luo et al., 1995; Cui and Luo, 1996; Mwange et al., 2003). Additional studies, conducted on the cambial periodicity of this tree, have largely covered and elucidated in detail the changes affecting vascular tissue structure, total proteins, specific enzymes (such as peroxidases and esterase isosymes), some polysaccharides, and phytohormones (Luo et al., 1995; Hou et al., 2004). However, an understanding of the molecular variations occurring in cambial tissues of higher plants during their annual development, especially in the dormancy period, is still needed. Research works by Schrader et al. (2004) and Espinosa-Ruiz et al. (2004) are, to date, among the most relevant on the subject.
The plant hormone indole-3-acetic acid (IAA) is an endogenous auxin involved in all aspects of vascular differentiation (Aloni, 2001). It acts as a morphogenetic signal, forming polar concentration gradients along the plant from the free-IAA-producing hydathodes to the root tips and inducing polar patterns of increasing vessel diameter and decreasing vessel density from leaves to roots (Aloni, 2004; Aloni et al., 2006). In the vascular tissues of trees, the IAA flows mainly via the cambium and its radial distribution may control xylem patterning (Uggla et al., 1996, 1998). The mechanism of the IAA signal transduction pathway has been extensively investigated. Receptors play a key role in the perception of the hormonal signal, qualitatively and quantitatively determining the competence of cells and tissues toward various hormone classes (Romanov, 2002). Recently, the simultaneous discovery by Kepinski and Leyser (2005) and Dharmasiri et al. (2005), that the transport inhibitor response 1 (TIR1) is an auxin receptor mediating rapid Aux/IAA protein degradation and consequent changes in the expression of auxin-regulated genes, unveils some aspects of the mystery of the signal transduction cascade from auxin to gene expression. Nevertheless, there still exist several aspects in plant auxin perception, which need deeper investigation for a better understanding. For instance, in the cambial region, plant auxin-induced growth involves cell division, enlargement, and differentiation (into xylem inwards and phloem outwards), and exogenous IAA would ‘boost’ the reactivation of a quiescent cambium, and not that of a resting cambium, the mechanisms of these processes are still open questions.
A remarkable research effort has been concentrated on auxin-binding protein 1 (ABP1). ABP1 has for some time been considered the best candidate auxin receptor (Timpte, 2001; Napier et al., 2002), given some receptor function characteristics shown by this protein. However, the role of ABP1 in auxin signalling still remains undetermined. ABP1 was originally purified from maize (Löbler and Klämbt, 1985a). Since then, its genomic or cDNA clones have been isolated from a range of plants, such as maize (Tillman et al., 1989; Hesse et al., 1989; Shimomura et al., 1986), Arabidopsis (Palme et al., 1992; Shimomura et al., 1993), tobacco (Leblanc et al., 1997; Watanabe and Shimomura, 1998), strawberry (Lazarus and MacDonald, 1996), red pepper (Choi, 1996), and sunflower (Thomas et al., 2003). Sequences have shown a high level of residue conservation throughout the mature protein amongst all higher plant ABP1s. ABP1 sequences have little homology to other protein sequences in the databases (Hesse et al., 1989), rendering simple its immunological detection with antibodies raised against it (Löbler and Klämbt, 1985b; Shimomura et al., 1986; Napier et al., 1988; Bronsema et al., 1998). Recent studies have demonstrated that ABP1 is highly involved in the perception of auxin in various responses such as protoplast swelling (Steffens et al., 2001), auxin-dependent electrical responses (Leblanc et al., 1999; Bauly et al., 2000), auxin-dependent cell expansion (Jones et al., 1998), or cell elongation and division during embryogenesis (Chen et al., 2001). Comprehensive investigations on ABP1 have mainly been conducted on herbs, such as maize and Arabidopsis, with relatively few on woody species. Although various aspects of ABP1 have been approached, the temporal and spatial expression of the ABP1 gene at the cellular level has not been well characterized.
A recent study conducted by Mwange et al. (2005) highlights seasonal changes in the concentration and distribution of endogenous abscisic acid (ABA) and indole-3- acetic acid (IAA) in the vascular tissues of Eucommia ulmoides. IAA and ABA contents were found to be higher, respectively, in the active and dormant periods and an application of exogenous ABA to quiescent E. ulmoides branches, in a water-culture system, inhibited the external IAA action on cambial reactivation. Such apparent phytohormone integration needs to be elucidated for a better comprehension of plant growth and development. Thus, molecular studies establishing relationships between hormones and the substances mediating their signal transduction (such as receptors or carriers) in plants are urgently required.
This paper aims at monitoring the ABP1 cDNA annual expression in the cambial region of E. ulmoides and establishing its relationship with the opposite seasonal patterns of ABA–IAA observed in this vascular tissue. Its possible function in the periodicity of cambial activity is also discussed.
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Materials and methods |
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Plant material and sampling
Eucommia ulmoides Oliv. trees (about 20 years old, 15 m tall, and 25–30 cm in diameter at 1.3 m above the ground level) were selected in a natural stand of Peking University campus (Beijing, China). The experiment was conducted for 1 year, thus including all the four (temperate) seasons and the related cambium activity phases as identified previously on this tree species (Luo et al., 1995; Mwange et al., 2003): active (7 April; 25 June), Quiescence-1 (14 October), rest (18 November) and Quiescence-2 (7 February; 20 January).
Samples (0.5–1 g) for mRNA isolation and protein extraction were harvested from 2-year-old twigs on the trees and consisted of cell layers carefully scraped with a scalpel from the exposed surface of xylem after bark peeling. As revealed by light microscopy observation, the scraped material mainly included immature xylem cell layers and some cambial cells. In June, during the cambial active phase, two samples were taken in the same way from mature xylem (beneath immature xylem) and phloem (in the peeled bark). This sampling was done to study the gene expression pattern across the cambial region. All the sampled materials were immediately fixed in liquid N2 for more than 1 h, before their preservation at –70 °C for further analyses.
ABP1 gene analysis
Samples at each harvesting time were pulverized in liquid nitrogen using a mortar and pestle. Total RNA was extracted with TRISOL Reagent (Life Technologies, Frederick, MD) according to the manufacturer's protocol, resuspended in 50 µl DEPC (diethylpyrocarbonate)-treated distilled H2O, and stored at –70 °C until needed. The full-length ABP1 cDNA was generated from total RNA of the cambium region tissue by RT-PCR and RACE. For Southern hybridization analysis, the cDNA probes were labelled using the random-primed DNA labelling kit (TaKaRa Biotech, Dalian, China) with 32P-dCTP according to the manufacturer's protocol. Genomic DNA was isolated from the active cambial tissues (harvested in June) using the SDS method (Edwards et al., 1991).
To study the pattern of ABP1 gene expression, cDNA probes for northern hybridization analysis were labelled using the random-primed DNA labelling kit (TaKaRa Biotech, Dalian, China) with 32P-dCTP according to the manufacturer's protocol. An aliquote of 20 µg of total RNA isolated from the cambium region was separated by electrophoresis on 1.2% (w/v) agarose gels containing 1x MOPS, 2.2 mol l–1 formaldehyde, blotted onto Biodyne B Membrane (Gelman), and fixed by UV cross-linker (UV stratalinker 2400, Stratagene, USA). After prehybridization at 65 °C for 30 min in 1% BSA, 1 mmol l–1 EDTA, 0.5 mol l–1 sodium phosphate (pH 7.2), and 7% SDS, the membrane was hybridized with the same solution containing the 32P-labelled DNA probe previously made for Southern blotting. Hybridization was carried out for 16 h at 65 °C, with the blots washed at high stringency (0.1x SSC and 0.1% SDS) at 65 °C and finally exposed to an X-ray film at –70 °C for 48 h. Equal reactivity and amount of RNA in all samples were verified by hybridization with 32P-labelled Eu-18S rRNA.
ABP1 gene expression was also determined by RT-PCR using the QUANTUM 18S RNA internal standard kit (Ambion, Austin, TX, USA) following the manufacturer's recommendations. Total RNA 5 µg was reverse-transcribed into cDNA as described above and subsequently diluted for RT-PCR. Using newly designed specific 5' primer A-P4 (5'-GTACTAAAGGGCAGTGCC-3') and 3' primer A-P5 (5'-GGAGGAGGTCAGAGCTC-3'), a fragment of 317 bp in length was amplified. Cycle numbers for standard PCR amplification were chosen to stay below saturation (25 cycles). The PCR bands were separated on 1.5% agarose gels and visualized by ethidium bromide staining.
For quantitative real-time RT-PCR analysis, cDNAs were synthesized from 5 µg of total RNA as described above. Quantitative RT-PCR was performed with 2x SYBR Green Master Mix (ABI, Warrington, UK) and analysed in the ABI Prism 7000 real-time PCR detection system (Applied Biosystem Instruments, USA), according to the manufacturer's instructions. Primers 5'-GTGGTACTAAAGGGCAGTG-3' and 5'-CTCGTATATAAACACTTTGAC-3' (harbouring 211 bp ABP1, intron spanned) were adopted to quantify ABP1 expression levels. Each quantitative PCR experiment, starting from total RNA isolation, was conducted in triplicate.
In situ hybridization analysis of E. ulmoides ABP1 mRNA in active 1- and 2-year-old branches was conducted using the DIG Nucleic Acid Detection Kit (Roche, Germany). Progression of the colour reaction was terminated by washing the slides for 5 min in water, followed by an air-drying in the dark at room temperature. Slides were then covered with cover-slips for microscopy observation using a Permount (Fisher Scientific) as a mounting medium without counter-staining.
Western blot analysis
For protein extraction, samples were thoroughly ground in liquid N2 in a prechilled mortar. The resulting powder was suspended in extraction buffer (0.5 mol l–1 TRIS–HCl, pH 6.8, 5% 2-mercaptoethanol, 10% glycerol, 2.5% SDS, and a trace of bromophenol blue). After centrifugation (12 000 g, 15 min at 4 °C), the supernatant was collected as the protein extract. This extract (25 µl) was electrophoretically separated on 12% SDS gels, transferred to nitrocellulose (Hybond ECL, Amersham Pharmacia Biotech), and blocked with 5% non-fat dry milk (NFDM) in TRIS-buffered saline supplemented with 0.5% Tween 20 (TTBS). After discarding the blocking solution in distilled water, the nitrocellulose membrane was incubated under gentle shaking for 1 h at 37 °C in the primary antibody diluted in TBS (1:1000) at 37 °C. The primary antibody was a polyclonal rabbit anti mz-ERabp1, kindly provided by Dr RM Napier (Warwick HRI, UK). After several washes, blots were incubated with horseradish peroxidase (HRP)-conjugated anti-rabbit IgG (1:5000 dilution in TBS, Amersham Pharmacia Biotech). HRP signal was detected using an enhanced chemiluminescence (ECL; Pierce SuperSignal) and X-ray film.
ABP1 immunofluorescence localization
For ABP1 immunofluorescence localization, E. ulmoides stem tissues were fixed with 4% paraformaldehyde in 0.1 M phosphate buffer (pH 7.2) for 16 h, dehydrated in an ethanol series, infiltrated with a xylene/Paraplast mixture and embedded in Paraplast. Transverse 10 µm thick sections were cut on a Leica microtome (Jung RM 2035), mounted on poly-L-lysine-coated slides and dried overnight at 37 °C. Paraplast removal from, and rehydration of, sections were done in pure xylene and a reversed alcohol series, respectively. Sections were rinsed in freshly prepared 15 mM NaBH4 and 0.1 M NH4Cl in PBS (both for 5 min) to quench aldehydes and blocked with 1% bovine serum albumin (BSA) in PBS for 30 min. The immunostaining procedure and chemicals used were previously described by Mwange et al. (2005), with differences only in the types of antibodies utilized. The ABP1 antibody was diluted to 1:150 in PBS. The secondary antibody was a Rhodamine-conjugated goat anti-rabbit antibody (Zhongshan Co., Beijing, China). To test possible non-specific labelling, controls included the replacement of rabbit ABP1 antibodies with either preimmune rabbit serum or PBS.
For ABP1 localization at the cellular level, the immunogold labelling was carried out according to Bronsema et al. (1998) with minor modifications. Nickel grids were incubated floating in immunolabelling solutions. Antibodies were diluted in PBS supplemented with 0.1% BSA. The primary antibody (dilution 1:50, v/v) was a rabbit anti-ABP1 antibody. The secondary antibody (dilution 1:60, v/v) was a goat antirabbit antibody conjugated with 10 nm gold particles (Sigma). Grids were finally visualized and photographed under a JEM 100 CX TEM. Controls were carried out as in the LM trial.
Water culture and exogenous ABA and IAA treatment
To test the effect of ABA and IAA on ABP1 expression in E. ulmoides, 1-year-old active (A) and resting (R) branches were harvested from the trees, respectively, in June and December. Resting branches were firstly divided into two groups. Upon harvest from the tree, active and first group resting branches were directly treated as described below. The second group of resting branches was first wrapped in black plastic bags, then kept at 4 °C for 2 weeks before receiving the same treatments. Following a bud removal, branch treatments included the application of IAA and ABA separately or together. Another treatment consisted of ABA application to budded branches. A set of only budded and lanolin-treated branches served as controls. Branches were cultured in tap water. A water-culture system was set up in a growth chamber with a 16 h photoperiod, light of 12 000 lux, temperatures of 24/17 °C (day/night), and a relative humidity of 75±7%. Wherever applied, 10 µM ABA were added to the water in 150 ml glass bottles and IAA in lanolin (1 mg IAA g–1 lanolin) was spread over the excised tops of the branches according to Luo et al. (1995) and Cui and Luo (1996). The application of exogenous ABA and IAA was performed weekly and the removal of branches bottom in contact with the water every 4 d. After a 3-week water culture, the cambial tissue was collected for ABA and IAA quantification by GC-MS (Edlund et al., 1995) and for ABP1 expression investigation by RT-PCR as above.
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cDNAs encoding ABP1 in E. ulmoides
cDNA clones of ABP1 from the active cambial region of Eucommia ulmoides have been isolated (Eu, Genbank accession number AY509875). The cloned ABP1 cDNA was found to be highly similar to other ABP1 proteins described from other plants (Fig. 1). Southern hybridization analysis of E. ulmoides genomic DNA with a 32P-labelled ABP1 cDNA probe detected a single band of similar intensity between 4 kb and 15 kb in length (Fig. 2), suggesting the existence of only one gene encoding the ABP1 protein in the E. ulmoides genome.
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DNA/HindIII and EcoRI).Seasonal expression pattern of ABP1 at a transcriptional level
Both northern hybridization (Fig. 3A) and RT-PCR (Fig. 3B) assays revealed that the ABP1 transcripts were strongly expressed in the active (A), weakly in the quiescent (Q1 and Q2) and almost undetectable in the resting (R) phases. Also, during the active phase, the cambial region displayed laterally a more consistent ABP1 signal compared with the phloem (P) and xylem (X) tissues. The relative ABP1 expression revealed by real-time PCR (Fig. 3C) followed the same pattern as shown by the northern hybridization and RT-PCR assays above. ABP1 was highly observed in active time.
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In situ hybridization results indicate that, with the antisense probe, an intense signal developed in the cambial zone and ray cells (Fig. 4C, E, G), whereas almost no signal was seen on control sections (Fig. 4A, B), only weak signals were observed in the mature cortex, mature phloem, and mature xylem due to the background (Fig. 4D, F).
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Seasonal expression pattern of ABP1 at the protein level
The accumulation of ABP1 mRNA in the E. ulmoides cambial region is reflected by the detection through western blotting of a 22 kDa protein corresponding to the ABP1 band (Fig. 5). This band was intensely detected in tissue extracts collected in the active period and slightly in the quiescent (Q1 and Q2) stages. It was not visualized in the resting (R) cambial tissues.
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Immunofluorescent labelling (Fig. 6) also showed a different distribution of ABP1 in the active-dormant cambial region of E. ulmoides. ABP1 accumulated to very high levels during the growing season (Fig. 6D) and quiescent (Fig. 6E, G) periods. The lowest ABP1 appearance was recorded in the resting phase (Fig. 6F). Cambial and radial enlarging cells were more fluorescence-stained, revealing a prominent presence of ABP1 in these areas. Mature xylem and phloem exhibited a weak ABP1-related fluorescence gradient, especially in the active phase (Fig. 6D).
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At the cellular level, transmission electron microscopy (TEM) revealed that the cambial cells close to the phloem and xylem sides were all labelled in a similar pattern (Fig. 7A, B). The most intense ABP1 signal was observed in the endoplasmic reticulum (ER) and the Golgi apparatus, while vacuoles and cell walls remained unlabelled. The cytoplasm, including the plasma membrane region, was regularly labelled in all tissues at low density. Nuclear labelling was present, but somewhat reduced.
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Effect of exogenous IAA and ABA on ABP1 expression
PCR analysis of ABP1 mRNA isolated from water-cultured branches harvested in the active period (Fig. 8) displayed an ABP1 band in samples from branches treated with IAA (T2) and in those where buds were not removed (T5). ABP1 expression was clearly decreased in branches treated with only ABA (T1), ABA with IAA (T3), and ABA with buds (T4). Furthermore, ABP1 was weakly expressed in samples from branches freshly collected in the resting period (Fig. 9A), even after the application of exogenous IAA only (T3). However, samples from branches incubated at 4 °C for 2 weeks prior to exogenous hormone treatment (Fig. 9B), exhibited an ABP1 expression-related band when treated with either IAA (T3) or both IAA and ABA (T6). Budded (T1) and lanolin-treated (T2) controls as well as ABA-treated branches with (T5) and without buds (T4) did not show the ABP1 signal. GC-MS quantification of IAA (Fig. 10A) and ABA (Fig. 10B) showed high concentrations of ABA compared with that of IAA in resting branches (T0). A 2-week treatment (W2) of branches at 4 °C prior to water culture induced an ABA decrease (>2/3) in the branches (T0, T1) compared with the untreated branches (W0). The maintenance of buds (Fig. 7A, T1) as well as the application of exogenous IAA (Fig. 9B, T3) or ABA (Fig. 9B, T4) alone to branches has increased the amount of IAA or ABA, especially in the 2-week 4 °C-treated branches (W2).
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Discussion |
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ABP1 mediates IAA signal during cambial cyclical activity in E. ulmoides
ABP1 has been considered as a possible auxin receptor, specifically mediating its control of cell growth (Hertel et al., 1972; Jones, 1994; Venis, 1995; Jones et al., 1998). Although this ABP1 receptor role has been greatly criticized (Tian et al., 1995; Napier et al., 2002), it is nowadays hypothesized that, given the complexity of auxin transport, metabolism and signalling in plants, these hormones could be assigned several receptors. In this aspect, ABP1 is increasingly thought to act as an auxin receptor for some responses such as change in ion transport at the plasma membrane level (Leblanc et al., 1999). It may interact through a ‘docking protein’ in the plasma membrane, as it has no obvious transmembrane domain (Barbier-Brygoo et al., 1991).
If ABP1 mediates cell growth, it should be present in the cambium during active growth. This idea was tested using different approaches and it was found that the ABP1 signal in the cambial region was high, low, and very scarce during the active, quiescent, and resting phases, respectively. The seasonal ABP1 expression is closely correlated to the annual IAA distribution previously highlighted by Mwange et al. (2005) in the cambial zone of the same tree, suggesting an evident qualitative and quantitative relationship between the two hormones during the annual activity cycle of E. ulmoides. None of the previous studies on ABP1 (transcript or protein level) has mentioned this ABP1 characteristic during a tree vascular development.
This positive correlation between ABP1 and IAA noticed in the E. ulmoides cambial region could easily be explained by their complementary roles in mediating the induction of cambial cell division and elongation/expansion. Bauly et al. (2000) found that the modulation of ABP1 expression level is sufficient to generate a marked change in auxin responsiveness. Recently, Thomas et al. (2003) have also observed that a high ABP1 expression level correlated with a high cellular sensitivity to auxin. The cell elongation and division processes, occurring in the active phase, are consistent with high IAA content (Mwange et al., 2005) and ABP1 appearance (this study) found in the E. ulmoides cambial region at that phase. The reduction and absence of cell division activity observed, respectively, in the quiescence and rest stages, could, in large part, be due to the substantial reduction of both IAA concentration and ABP1.
ABP1 expression is influenced by IAA-ABA interaction during cambial activity in E. ulmoides
An opposite change in annual concentration pattern of IAA and ABA has recently been observed (Mwange et al., 2005). The seasonal ABP1 expression pattern found in this study follows that of IAA, thus evolving oppositely to that of ABA. To test a possible negative regulatory effect of ABA on ABP1 expression, a series of experiments involving the application of exogenous ABA and IAA to E. ulmoides branches were conducted using a water-culture system. Results broadly showed that ABP1 expression significantly increased with exogenous application of IAA to branches, and that treatment with ABA was always correlated with no or low expression of ABP1. Moreover, in resting vascular tissues, ABA concentration was high and ABP1 expression could not be detected, even after exogenous IAA application (Fig. 9A). Finally, after resting branches have been incubated at 4 °C for a period (±15 d), sufficient to drastically reduce ABA levels, the cambium could be ‘reboosted’ by exogenous IAA application (Fig. 9B, T0-T1) and ABP1 could be detected again (Fig. 9B, T3). These data suggest that ABA may negatively regulate ABP1 and explains why ABP1 accumulated during the active period in the growing cambial region, but was absent during dormancy when ABA content was high. In quiescent vascular tissues, the ABA concentration is not high enough to prevent the ABP1 expression and the application of exogenous IAA can consequently enable the cambium reactivity (Mwange et al., 2005). Low temperature induces ABP1 expression whereas ABA reduces this expression, suggesting an interaction between auxin and ABA signalling pathways in activity–dormancy cycle. It is likely that, in the rest stage, high levels of ABA block ABP1 expression, thus inhibiting the IAA-induced response in the cambial region. This idea is consistent with the observation that the cambium of fully resting branches cannot be reactivated, even after the application of exogenous IAA and improvement of plant growing conditions (temperature, light, moisture, ...) (Catesson, 1994; Mwange et al., 2003). In the absence of the ABP1, exogenous IAA application could not act to reactivate the cambial cells, indicating that ABP1 is an essential link in the global IAA signalling pathway.
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The present study describes the seasonal changes of ABP1, a ‘putative’ auxin receptor required for plant cell elongation/expansion and division, in the cambial region of E. ulmoides. ABP1 expression at both protein and mRNA level is high in the active period, reduced during the quiescence, and almost non-existent in the resting stage, showing the opposite pattern to ABA changes previously detected in the E. ulmoides cambial region. Abundance of ABP1 expression correlates positively with IAA and negatively with ABA responsiveness in the cambial tissues, suggesting a role for ABP1 in mediating the regulation of cambial activation in the activity–dormancy cycle. The data suggest a possible inhibitory effect of ABA on ABP1 during dormancy. The extreme reduction of ABP1 during the rest stage diminishes IAA responsiveness in the cambial cells, leading to a non-reactivation of the cambium in a resting tree.
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Acknowledgements |
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This study was supported by the National Natural Science Foundation of China (30471367, 30530620). Special thanks are addressed to Professor Dr RM Napier (Warwick HRI, UK) for providing the ABP1 antibody and for his suggestions and to Dr Elizabeth Schultz (University of Lethbridge, Canada) for her critical reading of the manuscript. Thanks also to the anonymous reviewers for their constructive comments on an earlier version of this paper. The authors greatly appreciate the scholarship awarded to Dr KN Mwange by the Chinese and Congolese (RD Congo) Governments.
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Footnotes |
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* These authors contributed equally to this work.
Present address: Department of Biological Sciences, University of Lethbridge, Lethbridge, AB, Canada T1K 3M4.
Present address: Yuncheng University, Yuncheng, Shanxi Province, China.
$ Present address: Commissariat Général à l'Energie Atomique/CREN-K, B.P. 868, Kinshasa XI, R. D. Congo.
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