Journal of Experimental Botany, Vol. 53, No. 371, pp. 1047-1054,
May 2002
© 2002 Oxford University Press
Original Papers |
Distinct nuclear organization, DNA methylation pattern and cytokinin distribution mark juvenile, juvenile-like and adult vegetative apical meristems in peach (Prunus persica (L.) Batsch)
1Dipartimento di Ecologia, Università della Calabria, I-87030 Arcavacata di Rende, (CS), Italy
2Istituto di Biochimica ed Ecofisiologia Vegetali, CNR, Via Salaria, Km 29,300, I-00016, Monterotondo Scalo, Roma, Italy
3Istituto di Mutagenesi e Differenziamento, CNR, Area della Ricerca, Via di S. Cataldo, I-56100 Pisa, Italy
4Laboratory for Plant Biochemistry and Physiology, Department of Biology, University of Antwerp, B-2610 Antwerp, Belgium
Received 6 August 2001; Accepted 2 January 2002
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Abstract |
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Chromatin organization, nuclear DNA methylation and endogenous zeatin localization were investigated in shoot apical meristems (SAM) during juvenile and adult phases of peach (Prunus persica (L.) Batsch). The aim was to examine the extent to which these parameters could discriminate the juvenile and adult SAMs. Seedlings (juvenile, cannot flower), basal shoots (called juvenile-like, because they exhibit juvenile macroscopic traits) and apical shoots (competent to form flowers) of adult plants were chosen. Nuclear chromatin exhibited chromocentres that were peripherally distributed in SAMs of juvenile and juvenile-like shoots, but were diffusely spread in those of adult shoots. These patterns coincided with a peripheral labelling of DNA methylation in juvenile and juvenile-like meristem nuclei versus a diffuse labelling pattern in adult meristem nuclei. During vegetative growth (from March to June), the level of nuclear DNA methylation was higher in adult meristems than in juvenile and juvenile-like ones. The immunolocalization of zeatin in juvenile SAM was in the subapical region, but adult meristems exhibited a widespread localization or a signal confined within the boundaries of the central zone. The extent to which the acquisition of a strongly zonated pattern of these parameters as markers of floral competence in adult SAMs is discussed.
Key words: DNA methylation, peach, Prunus persica, shoot apical meristem, vegetative phases, zeatin.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In higher plants, the shoot apical meristem (SAM) represents the site at which organs are initiated and the growth pattern of the aerial plant body is established (Medford, 1992; Lyndon, 1994; Clark, 1997). Developmental transitions from juvenile to either vegetative or reproductive adult phases involve changes in the pattern of cellular differentiation and organ formation and are strictly regulated by genes in the SAM (Poethig, 1990; Evans and Barton, 1997; Meyerowitz, 1997; Lenhard and Laux, 1999). The molecular and genetic bases of SAM fates have been widely investigated and several genes related to the switch to reproductive phases have been characterized (Martinez-Zapater et al., 1994; Weigel, 1995; Amasino, 1996; Koornneef et al., 1998; Levy and Dean, 1998). Selective patterns of gene expression are associated with the SAM's capacity to initiate leaf primordia during vegetative growth (Jackson et al., 1994; Clark, 1997; Evans and Barton, 1997; Kerstetter and Hake, 1997; Meyerowitz, 1997; Mayer et al., 1998; Fletcher et al., 1999; Schoof et al., 2000). Nevertheless, the specific genetic programmes which distinguish developmental competence in juvenile and adult vegetative meristems have yet to be fully understood. This is an important transition because, whilst adult meristem are competent to flower, juvenile ones are not.
Clearly, substantial progress has been made in mapping the molecular landscape of SAMs in Arabidopsis (Bowman and Eshed, 2000; Doerner, 2000; Fletcher and Meyerowitz, 2000). However, comparatively little is known about the molecular basis of developmental phase change in woody plants. As a beginning to this work, a rigorous cytological study of SAMs in Prunus persica (L.) Batsch (peach) has been undertaken. This species was chosen, not only for its economic importance, but also because of the interesting differences in heteroblasty between juvenile and adult plants which, ultimately, must be strongly related to the activity of the SAM in these plants.
DNA methylation changes lead to qualitative alterations in both gene expression and chromatin structure (Amasino et al., 1990; Lewis and Bird, 1992) and are also involved in gene regulation during developmental phases (Burn et al., 1993; Mazzuca et al., 1995; Finnegan, 1996; Richards, 1997; Finnegan et al., 1998). There is interest in the extent of DNA methylation and structural changes in chromatin that occur in the mature, relative to the juvenile, SAM of peach. Consequently, the organization of nuclear chromatin and the immunolocalization of 5-methyl-cytidine at both the light and electronic microscope levels were investigated.
The natural cytokinin, zeatin, promotes vegetative shoot formation (Meeks-Wagner et al., 1989) and is also involved in developmental phase changes (Bernier et al., 1993; Estruch et al., 1993; Mok, 1994; Dewitte et al., 1999). To test whether the level and localization of cytokinins differ in SAMs that exhibit different developmental competence, zeatin was immunolocalized in peach SAMs in order to characterize juvenile and adult SAMs further.
To compare juvenile and adult phases, terminal vegetative buds of shoots borne on (i) one-year old plants and (ii) mature fruiting plants were chosen. Basal shoots, which originate from adventitious buds of adult plants (Crabbé, 1987), were also analysed because their overall morphology closely resembles important features of juvenile plants.
Hence, the aim of the work reported here was to determine whether specific cytological and hormonal changes could be used as markers of the juvenile–adult transition of peach SAMs. This work is regarded as an important prelude to examining this phase change at the molecular level.
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Materials and methods |
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Plant material
An open pollinator, OP16, Prunus persica (L.) Batsch cv. chiripa was chosen for this study. Seeds from OP16 (peach has 95% autogamy) were germinated in vivo and in vitro. To achieve genetically homogeneous material, clones were obtained by in vitro apex propagation, rooted, soil planted, and transferred to growth chambers (Lauri et al., 1999; Shatnawi et al., 1999). Two months later, in vitro plants, regenerated from one line, were transferred into the greenhouse and thereafter moved to the open field. One-year-old plants (both clones and seedlings), unable to flower, were considered as the juvenile phase. The material mentioned was kindly provided by Dr C Damiano from the Institute for Fruit Tree Culture of MIPA, Rome.
All the analyses were carried out on the terminal vegetative buds of (i) juvenile, (ii) adult and (iii) adult basal shoots (these are referred to as ‘juvenile-like’). Vegetative buds were sampled monthly starting from the vegetative burst (March) until the end of summer growth (June). Adult and juvenile-like shoots were excised from the mother plant OP16, whereas juvenile shoots were derived from the juvenile clones; moreover, the juvenile-like shoots were picked from adult plants taking care to select those fully exposed to light. Juvenile, juvenile-like and adult shoots having the same internode number were collected. Stem length differed since the growth rate of juvenile and juvenile-like shoots was higher than adult shoots.
Chromatin structural organization
Excised apices (5 for each sample) were fixed in 3% gluteraldehyde in 0.1 M cacodylate buffer (pH 6.9) overnight at 4 °C and post-fixed for 2 h in 15% osmium tetroxide in the same buffer and at the same temperature. Specimens were dehydrated in a graded series of ethyl alcohol and propylene oxide solutions and embedded in araldite. Staining with uranyl acetate was carried out while dehydrating with 75% alcohol. Ultrathin sections (0.06 µm) were cut with a Leica Ultracut UCT, stained with lead citrate and observed with a transmission electron microscope (Zeiss EM900) operating at 50 kV.
Qualitative fluorescence
For RNA localization, acridine orange staining was used. Excised apices (n=5 for each sample) were fixed in 4% paraformaldehyde in 1xPBS pH 7.0 and incubated for 24 h at 4 °C. After dehydration through an alcohol series, the material was wax-embedded and longitudinally sectioned (8 µm) using a Leica 2155 microtome. The slides were dewaxed, rehydrated and stained with acridine orange solution for 15 min (stock acridine orange 0.1% in the ratio 1/9 in Walpole's buffer at pH 4.2) and washed with Walpole's buffer (0.2 M HCl, 0.3 M sodium acetate). Other excised apices (n=5 for each sample) were fixed in absolute ethanol:glacial acetic acid (3:1, v/v). After dehydration, the material was embedded in Technovit resin and longitudinally sectioned (4 µm), using a Leica 2155 microtome. Slides were stained with the fluorochrome, chromomycin A3 (CMA, Sigma, St Louis, MO, USA), at a final concentration of 0.5 mg ml-1 in McIlvaine buffer (pH 7.2) in the dark for 50 min. The slides were examined using a Leica DMRB epifluorescent microscope equipped with a 50 W mercury lamp. A Leica excitation filter (BP 450–490 nm) plus a barrier filter (LP 515 nm), and an excitation filter (BP 436 nm) plus a barrier filter (LP 470 nm) were used for acridine orange and CMA staining, respectively.
5-methylcytidine-immunocytolabelling
Preparation and specificity testing of the monoclonal antibody directed against 5-methylcytidine (5-mC) were carried out as described previously (Podestà et al., 1993). Excised buds (10 for each sample) were fixed in absolute ethanol:glacial acetic acid (3:1 v/v). After drying, the material was embedded in Immuno-bedTm2 (Polysciences Inc., Warrington, PA, USA) resin and longitudinally sectioned at 3 µm using a Reichert Ultracut microtome. Nuclear DNA denaturation and incubation with the primary antibody anti-5-mC (1:200 in 0.1 M PBS, 1% BSA, 0.1% Tween 20) were performed as described earlier (Bitonti et al., 1996). Thereafter, slides were exposed to goat anti-mouse gold conjugated antibody, subjected to silver-enhancement of gold signal and then stained in basic fuchsin (1%). Controls were: (1) replacement of the first monoclonal antibody with somatostatine antibody; (2) primary antibody dilution; and (3) omission of DNA denaturation. Observations were made with a Leica DMRB microscope and the number of SAM-labelled cells was determined by scoring all the serial sections. The fraction of labelled area per nucleus was expressed as a percentage and estimated using a Leica Q500/W image-analyser equipped with a CCD camera. The number of silver grains in areas equal and adjacent to labelled nuclei was extremely low (
2). Statistical differences were evaluated by the Student's t-test.
Pre-embedding immunolocalization of zeatin (Z)
The localization of Z was performed in the SAM of juvenile and adult buds at the onset of cell proliferation in March. Preparation and specificity testing of rabbit antiserum against Z were performed as described earlier (Dewitte et al., 1999). For pre-embedding immunolocalization, excised buds (10 for each sample) were fixed in 0.5% (v/v) gluteraldehyde and 3% (w/v) paraformaldehyde mixture in PBS (135 mM NaCl, 2.7 mM KCl, 1.5 mM KH2PO4, 8 mM K2HPO4, pH 7.2). Thick sections (18–20 µm) were cut with a Leica VT1000E vibratome. The sections were preincubated (3 times, 10 min each) in blocking buffer (0.1% v/v fish gelatin, 0.5% w/v BSA, 1% v/v normal goat serum, 20 mM glycine, and PBS) and then in a 0.07% saponin solution in PBS for 20 min. Afterwards, sections were incubated with primary antibody in a dilution of 1:200 in blocking buffer at 4 °C overnight, followed by 1 h at room temperature. After three washes (10 min each), the secondary antibody was diluted (1:100) in blocking buffer. The secondary antibodies were goat anti-rabbit IgG either conjugated with alkaline phosphatase (Boehringer–Mannheim) or colloidal gold-linked for light microscopy. The detection of alkaline phosphatase-conjugated antibodies and colloidal gold-linked secondary antibodies were performed as previously described (Dewitte et al., 1999). Controls were: (1) omission of the primary antibody; (2) inhibition of immunoresponse by preincubating the antibodies with an excess of Z before adding to the slides. Samples were mounted in a PBS and glycerine mixture (1:1 v/v) and immediately observed with a Leica photomicroscope in order to avoid oxidation of the tetrazolium salt (Boehringer–Mannheim).
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Results |
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The peach system
This study focused on the vegetative terminal meristem of (a) shoots borne on young plants (juvenile) and (b) basal and apical shoots borne on mature fruiting plants. Basal shoots originated from adventitious buds at the collar of adult plants and were referred to as juvenile-like shoots because their morphology resembled features of juvenile plants. In fact, they were characterized by a pronounced vegetative vigour and originated leaves which were lanceolate, less green (likely due to a minor chlorophyll content) and with a smaller average surface area compared with leaves borne on adult apical shoots (Fig. 1A
, B, C). The shoots from each source exhibited different photosynthetic capability and differences in starch, sucrose and sorbitol levels (A. Battistelli, personal communication). Moreover, basal (juvenile-like) shoots did not exhibit floral buds for at least two years after their formation and they maintained a high rooting potential when cuttings were performed. Such characteristics were, once again, very similar to those of juvenile plants.
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SAM zonation and chromatin structural organization
In longitudinal sections, juvenile and juvenile-like SAMs exhibited the same dome-shaped morphology (Fig. 2A, B). In addition, in the adult SAM (Fig. 2C) the nuclei of the central zone appear to be stained more; the greater intensity of staining in the adult SAM is a function of a greater chromatin condensation compared with the juvenile and juvenile-like SAMs (Fig. 2A, B). Hence, a clear CZ could be identified in adult SAMs (Fig. 2C), but not in juvenile or juvenile like SAMs.
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The clear zonation occurring in adult compared with juvenile SAMs was also observed when a stain specific for total RNA was applied. In fact, in juvenile (Fig. 2D
) and juvenile-like (Fig. 2E) shoots, cytoplasmic orange staining was observed in all the cells of the apical dome, whereas staining was very reduced in the CZ of adult SAMs (Fig. 2F).
Under both the light (Fig. 3A–C) and electron microscope (Fig. 3D–F), nuclei from all three sources revealed an articulate structure: diffuse nuclei with prominent dense chromatin areas (chromocentres). When GC-sequence-specific fluorochrome was applied, chromocentres were visualized as bright yellow areas set against a green background (Fig. 3A–C). However, only in cells from the juvenile (Fig. 2A, D) and juvenile-like (Fig. 2B, E) SAMs were rings of chromocentres observed on the circumference of the nuclei. By contrast, in adult meristems they were spread across the entire nucleus and this is particularly well-demonstrated in Fig. 2C and F.
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A specific pattern of 5-methylcytidine immunolabelling distinguishes adult from juvenile and juvenile-like SAMs
Changes in DNA methylation regulate or occur during developmental phase changes in higher plants, prompting the need to consider methylation changes in this study's system at the cellular level. Juvenile, juvenile-like and adult shoots were sampled from April to June and incubated with the antibody anti-5-methylcytidine. Several reaction controls were carried out (data not shown) and are described in the Materials and methods. During the whole period adult SAMs showed a significantly greater frequency (P<0.01) of labelled cells and a larger fraction (P<0.05) of labelled area per nucleus than juvenile SAMs (Table 1). In addition, two distinct patterns of methylation were observed consisting of either a peripheral or a diffused distribution of nuclear labelling, respectively. The apical meristems of both juvenile and juvenile-like shoots (Fig. 3G, H) exhibited a higher frequency of nuclei with a peripheral pattern (50±5% and 45±3%, respectively) than the adult apices (Fig. 3J, 24±3%). Hence, the labelling pattern in the adult SAM was not only stronger, but was distributed all over the nucleus compared with nuclei in the juvenile and juvenile-like SAMs.
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Differential patterns of zeatin localization in adult compared with juvenile and juvenile-like SAMs
Immunolocalization of Z was performed on the SAM of juvenile, juvenile-like and adult shoots (Fig. 4A, D) in early March, just at the onset of cell proliferation. In juvenile SAMs the major accumulation of Z occurred in the subapical region, which corresponds to the zone of incipient internode and in the leaf marginal meristem (Fig. 4A). There was a degree of heterogeneity of zeatin localization in the SAMs of adult plants (Fig. 4C, D). This was reflected in either a spreading of zeatin on the whole SAM (Fig. 4C) or in a more intensive signal in the CZ, in leaf primordia and sub-apical region in others (Fig. 4D). In the SAM of basal shoots (Fig. 4B), the signal seems rather restricted to the SAM and the proliferating cells of the leaf primordia while the differentiating cells of the young internodes are not reactive (Fig. 4B). No signal was detected in the controls (Fig. 4E, F).
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Discussion |
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The data show that SAM zonation is much more prominent in adult meristems than either of the juvenile meristem types at each sampling time. This is consistent with the hypothesis that zonation of the SAM into distinct CZ to the PZ is a feature of well-defined vegetative SAMs (Nougarède, 1967). Notably, founder cells in the CZ exhibit low rates of division to mantain a population of indeterminate cells and to replace those that have been incorporated into leaf primordia. Conversely, the frequent cell divisions in the PZ lead to the formation of leaf primordia (Nougarède, 1967; Medford, 1992; Lyndon, 1994; Clark, 1997). The strong zonation found in the adult SAMs may reflect the strong expression of vegetative meristem specific genes (Fleming et al., 1993; Nishimura et al., 1999).
At the cytological level, a different chromatin organization distinguished the three meristem types. The SAM of adult shoots exhibited a lower frequency of nuclei with a peripheral distribution of chromocentres than both juvenile and juvenile-like shoots. Moreover, these data were consistent with a strong zonation in the SAM of adult compared with juvenile and juvenile-like shoots. These findings lead to an hypothesis that there is a tight relationship between SAM cytological features and specific phenotypic traits of the generated shoot. Note that the transition of the SAM from the juvenile to the adult state parallels a change from a peripheral to a more diffuse distribution of chromocentres. Perhaps, change at the level of chromatin organization predisposes the expression of the genes which confers adult character to the SAM.
In situ localization of 5-methylcytidine, resulted in a higher number of labelled nuclei and a higher level of labelling per nucleus in adult meristems compared with juvenile and juvenile-like SAMs. This finding implies a greater hypermethylation of specific chromatin domains, such as the highly GpC-rich sequences, in adult meristems than in juvenile ones. In Arabidopsis, plants transformed with antisense MET1 exhibited delayed flowering, leaf heterophylly and flowers that lacked carpels (Finnegan, 1996; Richards, 1997; Finnegan et al., 1998). Hence, the level of methylation can have pronounced effects on development. Peach SAM types also showed a differential pattern of nuclear DNA methylation. A peripheral pattern was prevalent in juvenile meristem nuclei, whereas diffuse labelling was predominant in adult meristem nuclei. These patterns coincided with the different structural organization of chromatin (peripheral versus diffuse chromocentre distribution mentioned above). DNA methylation has been demonstrated to be crucial in terms of both chromatin condensation and gene expression (Amasino et al., 1990; Lewis and Bird, 1992) as well as in maintaining epigenetic changes (Henikoff and Matzke, 1997; Jacobsen and Meyerowitz, 1997).
Juvenile, juvenile-like and adult meristems of peach exhibit distinctly different patterns of zeatin localization which could reflect a possible cytokinin redistribution in the SAM, either in relation to the different stages of leaf initiation or to the distinct leaf shape at each developmental phase. In fact, a pivotal role has been assigned to cytokinins in controlling plant morphogenesis (Mok, 1994; Kende and Zeevart, 1997; Dewitte et al., 1999; Frugis et al., 1999). Nevertheless, both gibberellic acid and cytokinins are involved in the juvenile or adult leaf phenotype (Engelke et al., 1973) and, in aquatic plants, the shape of floating and submerged leaves seems much more regulated by ABA (Young and Horton, 1985). Hence, it may be taken into account that the cytokinins alone cannot be the only determinant for heterophylly.
More interestingly, the main differences in zeatin distribution were seen in the central zone of adult SAMs. Indeed, a faint signal was detected in the CZ of juvenile SAMs, but a strong reaction occurred in the CZ of adult SAMs. Since a role for cell signalling in a co-ordinated pattern of growth and organ formation has been hypothesized (Clark, 1997; McLean et al., 1997; Rinne and van der Schoot, 1998; van der Schoot and Rinne, 1999; Fletcher and Meyerowitz, 2000), zeatin might be involved in the signal transduction chain leading to a specific pattern of gene expression which underlies the distinct organogenetic fates. In this context, the presence of zeatin in adult SAMs in the zone of ‘founder cells’ could be an important prerequisite for floral competence of adult SAMs.
In conclusion, in adult SAMs a strong zonation of chromatin condensation, DNA methylation and distribution of zeatin was observed, features that were not shared by juvenile and juvenile-like meristems. These strong zonating patterns in adult SAMs may be cellular markers of changes in gene expression that confer shoot identity. This is an hypothesis that can now be tested experimentally.
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Acknowledgements |
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We thank Dr Damiano Carmine (Institute for Fruit Tree Culture of MIPA, Rome) for providing plant material. We also thank Mr Enrico Perrotta for technical assistance in electronic microscopy. This work was supported by grants from MIPA, piano Nazionale Biotecnologie Vegetali.
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Footnotes |
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5 To whom correspondence should be addressed. Fax: +39 0984 492964. E-mail: b.bitonti{at}unical.it
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