JXB Advance Access originally published online on November 26, 2007
Journal of Experimental Botany 2007 58(15-16):4027-4035; doi:10.1093/jxb/erm259
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© 2007 The Author(s).
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RESEARCH PAPER |
Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction
Departamento de Botânica, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 893, 4150-181 Porto, Portugal
* To whom correspondence should be addressed. E-mail: scoimbra{at}fc.up.pt
Received 1 August 2007; Revised 27 September 2007 Accepted 28 September 2007
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Abstract |
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Some of the most important changes that occur in plants during sexual reproduction involve the transition from a sporophytic to a gametophytic type of development. In this paper, these changes were evaluated for Arabidopsis thaliana. The results obtained clearly show differences in the pattern of distribution of specific arabinogalactan protein (AGP) sugar epitopes, during anther and ovule development. AGPs are hydroxyproline-rich glycoproteins that are massively glycosylated and ubiquitous in plants. The molecular mechanism of action of AGPs is still unknown, mainly due to the difficulties posed by the complex saccharide chains. However, the complex structure of the sugar fraction of AGPs makes them a potential source of signalling molecules. The selective labelling obtained with AGP mAbs JIM8, JIM13, MAC207, and LM2, during Arabidopsis pollen and pistil development, suggests that some AGPs can work as markers for gametophytic cell differentiation. Specific labelling of the first gametophytic cells in the pistil, the strong labelling of the secretory cells of the embryo sac, the synergid cells, and the labelling of the integument micropylar cells, apparently outlining the pollen tube pathway into its final target, the embryo sac, have all been shown. In the anthers, the specific labelling of gametophytic cells, and of the male gametes that travel along the pollen tube, may indicate AGP epitopes acting as signals for the pollen tube to reach its final destiny. The specific labelling of cells destined to go into programmed cell death is also discussed.
Key words: Arabidopsis, arabinogalactan proteins, immunolocalization, monoclonal antibodies, gametic cells
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Introduction |
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Plant sexual reproduction depends on the formation of male and female gametes that are produced by the haploid generation. In the ovule of Arabidopsis thaliana, usually a single megasporocyte undergoes meiosis and produces four haploid megaspores. Following the programmed cell death (PCD) of three of the four megaspores, the functional remaining megaspore divides mitotically to give rise to the embryo sac. The developmental pattern of the female gametophyte exhibited by Arabidopsis is referred to as the polygonum type which is present in 70% of all angiosperms. This female gametophyte is a seven-cell eight-nucleate structure, with a very specific and defined organization of its cells, two synergid cells and the egg cell at the micropylar end, three antipodal cells at the calazal end, and two polar nuclei which eventually fuse, localized in the central cell (Drews and Yadegari, 2002). The female gametophyte or embryo sac develops coordinately with the sporophytic tissues of the ovule, providing an ideal system to study its involvement in cellular communication and the role of cell lineage and position in cell specification and differentiation.
In the anther, several microsporocytes give rise by meiosis to tetrads of haploid microspores, each of which will develop into a pollen grain. The first mitosis of the microspore is asymmetric and originates a large and transcriptionally active vegetative cell, and a small generative cell with condensed chromatin that will divide again and originate the two male gametes (Tanaka, 1997).
Although the general pattern of development that leads to gamete formation is clear, little is known about the molecular mechanisms that regulate the transition from a sporophytic type of development to a specific gametophytic programme. The result of this programme is to achieve the process known as double fertilization. This includes the germination of the pollen grain into the pollen tube and the extremely efficient way through which this structure finds its target cells in the embryo sac.
All the steps of this complex process are seemingly dependent on an intricate network of signalling events, largely undefined, and likely to involve molecules of different kinds (Preuss, 2002). Glycosylated proteins, such as arabinogalactan proteins (AGPs), prevail in many stigma exudates, style transmitting tissues, and pollen itself, and are believed to provide recognition signals and directional guidance for the pollen tube (Wu et al., 2001). AGPs are hydroxyproline-rich glycoprotein that are massively glycosylated, ubiquitous in plants, and particularly abundant in cell walls, plasma membranes, and extracellular secretions (Showalter, 2001).
Subsequent to the full sequencing of the Arabidopsis genome, 47 genes with characteristics typical of AGPs were identified (Schultz et al., 2000, 2002; Gaspar et al., 2001) and classified into four subclasses based on the properties of the polypeptide core. ‘Classical’ AGPs include an N-terminal signal peptide that is removed from the mature protein, a central domain rich in Pro/Hyp, and a C-terminal hydrophobic domain containing a glycosylphosphatidylinositol (GPI)-anchor signal sequence. Other AGP subclasses are those with Lys-rich domains, the arabinogalactan peptides with short protein backbones, and the fasciclin-like AGPs with fasciclin domains (Schultz et al., 2002; Johnson et al., 2003).
It is believed that most, if not all, AGPs are anchored to the plasma membrane by the GPI anchor (Schultz et al., 2000). AGPs could then be released to the cell wall by cleavage of the GPI anchor by a specific phospholipase in response to cellular signals (Knox, 2006).
Some authors say that after performing their functions, AGPs can be interiorized, transported by means of multivesicular bodies, and degraded in the vacuole. This process of biosynthesis and degradation would be important for the cells to react rapidly to any kind of extracellular changes (Kreuger and Van Holst, 1996; Samaj et al., 2000). Recently, Lamport et al. (2006) proposed a model for the dynamic flux of AGPs, in which the GPI anchor would be cleaved, allowing AGPs to go from the plasma membrane to the periplasmic space, from here to the cell wall, and finally to the extracellular space. The authors speculate that AGPs have the ability to work as cell wall plasticizers, enlarging the pectin matrix, allowing the extension of the wall, and, with this, cell expansion.
AGPs can be localized in tissues and cells through the use of specific monoclonal antibodies (mAbs) that bind to structurally complex carbohydrate epitopes typical of these proteoglycans (Knox, 1997). AGP-specific mAbs have been instrumental in revealing the development dynamics of the AGP glycan moiety and represent a diagnostic tool for AGPs. Accumulated information, obtained by the extensive use of anti-AGP mAbs by the scientific community, shows that AGPs are finely regulated and differentially expressed during plant development, namely during sexual plant reproduction.
Evidence implicating AGPs in sexual plant reproduction has been obtained for several plant species, namely Actinidia deliciosa, Amaranthus hypochondriacus, and Catharanthus roseus (Coimbra and Salema, 1997; Coimbra and Duarte, 2003). In the present work, the aim was to provide a dynamic map of AGP epitope distribution in Arabidopsis reproductive tissues, with the available collection of anti-AGP mAbs, and thus to contribute to the understanding of the role of AGPs in the establishment of the gametophytic lineages, in both the male and female organs of the flower. This work was also envisaged as a means of complementing genetic and expression studies that have been performed, namely for AGP18 (Acosta-Garcia and Vielle-Calzada, 2004), and AGP6 and AGP11 (Pereira et al., 2006). In the present research, labelling specific to the gametophytic cells in the pistil, labelling of the integument micropylar cells, and the micropylar nucellus have been shown, apparently outlining the pollen tube pathway into its final target, the embryo sac. In the anthers, the specific labelling of gametophytic cells and of cells destined to go into PCD is also discussed.
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Materials and methods |
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Plant material
Plants of Arabidopsis thaliana (L.) Heynh., ecotype Columbia (from The European Arabidopsis Stock Center, NASC), were grown in individual pots in sterilized soil, within a growth cabinet (Fitoclima 13000E), under a 16 h photoperiod, at 21 °C, with 60% relative humidity, and a light intensity of 90–130 µmol m–2 s–1. Plants were watered twice a week. The flowers were collected at different stages of pistil and anther development, according to the stages of early flower development set by Smyth et al. (1990), starting at stage 8, when locules appear in stamens, up to stage 13, when buds open and anthesis occurs.
Pollen tube germination and growth
Dehiscent anthers were carefully dipped onto the surface of Petri dishes containing solidified germination medium (Fan et al., 2001), covered with small square pieces (
1 cm2) of Visking dialysis membrane (molecular weight cut-off value 12 000–14 000 Da). The membranes were pre-treated by boiling for 10 min in 10 mM EDTA (ethylenediaminetetraacetic acid) and then for another 10 min in distilled water, after which the membranes were stored at 4 °C in distilled water until use. Pollen was germinated and grown overnight in the dark at 23 °C.
Monoclonal antibodies
A collection of mAbs directed against glycosyl moieties specific to AGPs was provided by Prof. Paul Knox from the Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, UK. The mAbs used were JIM8 (Pennell et al., 1991), JIM13 (Knox et al., 1991), MAC207 (Pennell et al., 1989), and LM2 (Smallwood et al., 1996). The secondary antibody was fluorescein isothiocyanate (FITC)-conjugated anti-rat IgG (F-1763; Sigma).
Light microscopy and immunolocalization of AGPs
Pistils and anthers were fixed in 2% paraformaldehyde and 2.5% glutaraldehyde in phosphate buffer (0.025 M, pH 7, with one micro drop of Tween 80), placed under vacuum for 1 h and then at 4 °C overnight.
After dehydration in a graded ethanol series, the material was embedded in LR White. Thick sections (0.5 µm) were obtained with a Leica Reichart Supernova microtome, placed on glass slides, circled with a Pap pen, and treated as follows: 5 min in phosphate-buffered saline (PBS), pH 7.4, containing 5% BSA (blocking solution), followed by incubation with primary antibody (diluted 1:5 in blocking solution), overnight and at 4 °C. After washing with PBS, the sections were incubated with secondary antibody (diluted 1:100 in blocking solution) for 3 h in the dark, and then finally washed with PBS followed by distilled water. Slides were further stained with calcofluor white (fluorescent brightener; Sigma) and mounted with Vectashield (Vector Laboratories, Petersborough, UK). Membranes with pollen tubes were placed in microscope glass slides and also circled with the lipophilic pen. Pollen tubes were fixed for 1 h with Histochoice fixative MB (Amresco) and treated as for the thick sections. Bright field and fluorescence observations were performed on a Zeiss Axio Imager Z1 inverted epifluorescence microscope (objectives were Plan Apochromatic 63x/1.40 or Plan Neofluor 20x/0.50, and filters were 365/445 nm for calcofluor and 470/525 nm for fluorescein stain). Images were captured with an Axiocam MR in automatic exposure mode, and processed with Axiovision 4.4 software.
Control experiments, performed omitting the incubation with the primary antibody (incubation with blocking solution only), demonstrated no unspecific staining. Confidence in specific antibody binding was reinforced by the different patterns of labelling obtained with the different mAbs used.
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Results |
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AGPs have been implicated in sexual plant reproduction of a few plant species. However, a detailed map of AGP sugar epitopes in different flower parts and at different stages of development has not been obtained for the genetic model plant Arabidopsis. Given the vast knowledge of the Arabidopsis genome and gene expression, information on the presence in time and space of a particular type of gene product may become extremely useful to the broad understanding of Arabidopsis biology.
Immunolocalization of AGPs in anthers of Arabidopsis during microsporogenesis
In Arabidopsis, at the pre-meiotic stage of microsporogenesis, the five wall layers of the anthers are well differentiated; the microsporocytes have thin cell walls and are successively surrounded by the tapetum, median layer, endothecium, and epidermis. Epitopes recognized by mAbs JIM8 and JIM13 were detected with great intensity in the median layer and less so in the tapetum cells and microsporocytes (Fig. 1A). At the beginning of meiosis, the labelling obtained with mAbs JIM8 and JIM13 was selective for the tapetal cells and microsporocytes, and was noticeable in the wall that surrounds these microsporocytes (Fig. 1B). This wall separates the microsporocytes that are dedifferentiating, and it is at this moment that callose deposition begins.
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Following meiosis and cytokinesis, the four haploid microspores are arranged in tetrads encased by a thick wall, which is the initial wall of the microsporocytes that is greatly reinforced by further callose deposition. The initial wall of the microsporocytes, the cytoplasm of the microspores, and the tapetal cells were still labelled at this stage of development (Fig. 1C). Results obtained with mAbs MAC207 and LM2 did not show any defined pattern of binding, labelling throughout and in all stages of microsporogenesis (data not shown).
Immunolocalization of AGPs in Arabidopsis microgametogenesis
After the degeneration of the callose wall that surrounds the tetrads, the angular-shaped microspores are released. AGP epitopes recognized by mAbs JIM8 and JIM13 were detected in tapetal cells and also in the endothecium, which develops at this stage. These two mAbs reacted strongly with epitopes present in the cytoplasm and outer surface of the microspores (Fig. 1D). At the stage of bicellular pollen, after the first pollen mitosis, when the generative cell occupies a central position inside the vegetative cell, the labelling of the generative cell wall and/or plasma membrane was strong and remarkably specific (Fig. 1E). The same type of labelling was maintained in the two male gametes, after the second pollen mitosis (Fig. 1F). At these two last stages of pollen development, the tapetal cells were no longer labelled by JIM8 and JIM13, but the endothecium wall and respective thickenings were. As for microsporogenesis, the fluorescence signal observed with mAbs MAC207 and LM2 during all stages of microgametogenesis did not produce a defined pattern of binding (Fig. 2C, D). The specific labelling of male gametes with mAbs JIM8 and JIM13 was retained after pollination (Fig. 2A) and, at least in pollen germinated in vitro, also during pollen tube growth (Fig. 2B).
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Immunolocalization of AGPs in Arabidopsis pistil tissues
The stigma of Arabidopsis thaliana is composed of bulbous epidermal cells called stigma papillae. The stigma where the pollen grains first make contact has a fundamental role in its germination. In this work, utilizing the four mAbs, there was no labelling of the papillae cells during any stages of flower development (Fig. 2A).
The style of Arabidopsis is solid, composed of cells involved in secretion. The present results have shown a specific labelling of the central transmitting tissue of the style and also of the tracheary elements present all over the ovary with mAbs JIM8 and JIM13 (Fig. 3A).
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Immunolocalization of AGPs during macrosporogenesis and macrogametogenesis
At the beginning of ovule development, the nucellus is centrally located inside the two emerging integuments. When sections of Arabidopsis ovules were treated with mAbs JIM8 or JIM13, the specific labelling of the entire megaspore surface was striking. This labelling was specific to the first cell with a haploid constitution, marking the beginning of the gametophytic generation (Fig. 3B).
As the ovule continued to develop, the labelling with the same two mAbs was observed in the embryo sac wall, and was particularly intense in the synergid cells and in their filiform apparatus (Fig. 3C, D). At this more advanced stage of development, the labelling obtained with JIM8 and JIM13 extended to the inner integument, the cell layer that defines the micropyle, and thus the pollen tube pathway into the embryo sac (Fig. 3E). The labelling obtained with mAbs MAC207 and LM2 was again found to be extensive and scattered throughout most cell types, during both macrosporogenesis and macrogametogenesis, although excluded from the embryo sac (Fig. 2E, F).
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Discussion |
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The results obtained in this work clearly show differences in the pattern of distribution of specific AGP sugar epitopes during Arabidopsis anther and ovule development. These differences are apparent both in sporophytic and in gametophytic tissues, and it has become evident that AGP-specific epitopes can work as markers for certain cell or tissue types, in very precise stages of sporogenesis and gametogenesis.
Earlier studies have shown that AGP genes are expressed in Arabidopsis pollen grains and pollen tubes and also that AGPs are present along the Arabidopsis pollen tube cell surface and tip region, which is different from that reported by Lennon and Lord (2000). Also it has been shown that only a subset of AGP genes is expressed in pollen tubes, with a prevalence for Agp6 and Agp11, suggesting a specific and defined role for some AGPs in Arabidopsis sexual reproduction (Pereira et al., 2006). Other recent results (Acosta-Garcia and Vielle-Calzada, 2004) indicate that Agp18 is essential for the establishment of the female gametophytic phase, also in Arabidopsis.
In the present work, mAbs MAC207 and LM2 showed similar binding patterns, both defining extended cell populations in different tissues, as opposed to JIM8 and JIM13 which seemed to define single tissues or single cell types. Similar observations with these antibodies have also been reported by Pennell et al. (1991) for oilseed rape flowers. In this study, the labelling obtained with JIM8 and JIM13 was always identical.
AGPs in microsporogenesis
In the pre-meiotic stage of microsporogenesis the epitopes recognized by the mAbs JIM8 and JIM13 are specifically and intensely localized in the median layer of the anther. Later in development, at the beginning of meiosis, the same mAbs JIM8 and JIM13 produced lessintense labelling in the median layer, but it was now stronger in the tapetum cells and microsporocytes. The selective labelling of the microsporocyte walls is quite important at this stage of development; microsporocytes have dense cytoplasm and a thin pectocellulosic cell wall. During prophase, microsporocytes start a dedifferentiation which is probably related to the transition from sporophytic gene expression to a type of gametophytic gene expression. This transition relates to the change from a diploid to a haploid generation. As soon as prophase starts, the callose deposition also starts, resulting in thick callose walls surrounding the microsporocytes. It has already been assumed that this callose wall can be the trigger to start the gametophytic type of development (McCormick, 1993). This physical isolation is important to activate such dramatic changes in development. Following meiosis and cytokinesis of the four haploid microspores, individual tetrads are completely encased by a thick wall. Within the callose wall, a microspore-produced cell wall, the primexine, is present. It is curious to notice that the first separation wall produced in microsporocytes is still present at this stage and still labelled by mAbs JIM8 and JIM13. This labelling pattern may be related to the signals that must be generated for the efficient release of callase, by the tapetum cells, or a type of developmental time specificity related to the gametophytic development.
The presence of AGPs in the tapetum clearly shows that this tissue synthesizes and secretes these molecules. The interaction of the sporophytic tapetal cells, and the gametophytic differentiation of meiocytes into microspores, are present in the synchronism of callase release from the tapetum endoplasmic reticulum, as well as from the sporopolenine precursors released into the anther locule. AGPs are strong candidates for cell differentiation signals at this stage of development. It may also be important to associate the presence of AGPs with tissues that are set to undergo PCD. It has already been shown that the tapetum cells, during their degeneration process, show morphological features characteristic of PCD (Papini et al., 1999). Recently, it was reported that the expression of AtBI-1, which suppresses Bax-induced cell death in the tapetum at the tetrad stage, inhibits tapetum degeneration and, subsequently, results in pollen abortion, while activation of AtBI-1 at later stages of development does not (Kawanabe et al., 2006). These results clearly showed that PCD signals start at the tetrad stage of pollen development and are essential for microsporogenesis. In the present study, it could also be observed that the stage at which PCD occurs is associated with the stronger presence of AGPs recognized by mAbs JIM8 and JIM13. Other instances in which phenomena of PCD are of prime importance have already been reported also to involve AGPs, namely in vascular cells (Schindler et al., 1995; Motose et al., 2004), in cell suspension cultures (Gao and Showalter, 1999), and in somatic embryogenesis (McCabe et al., 1997).
AGPs in microgametogenesis
The ultrastructural description of microspores just released from tetrads shows high exocitic activity in tapetum cells and the elaboration of the intine wall by microspores (Owen and Makaroff, 1995). The labelling with mAbs JIM8 and JIM13 is also strong in tapetum cells, in the cytoplasm, and the outer surface of the microspores, which is the site where the intine wall will be built, indicating some association of this important developmental stage with AGP synthesis.
During pollen development, the vegetative cell cytoplasm shows strong metabolic alterations related to asymmetric cell division, one of the most striking events of cell differentiation occurring during the plant life cycle. One mitosis will give rise to two completely different cells in size, function, and gene activity. JIM8 and JIM13 specifically label the generative and gametic cells, but not the gametophytic cell. This labelling may function as a molecular marker for cell development and may also be related to the signals necessary to direct the pollen tube to the embryo sac. Moreover, after the second pollen mitosis, the two resulting sperm cells that are inside the pollen grain or inside the pollen tube are still strongly labelled by these two mAbs. Specific labelling of the generative cell was also reported for oilseed rape (Pennell et al., 1991), Nicotiana tabacum (Li et al., 1995), and Brassica campestris male gametes (Southworth and Kwiatkowski, 1996). JIM8 and JIM13 do not label the pollen tube wall, which instead is labelled by MAC207 and LM2 (Pereira et al., 2006). These two mAbs are probably related to epitopes in structural AGPs present in several types of plant cell walls.
AGPS in pistil tissues
At all stages of ovule development the stigmatic papillae were not labelled by any of the mAbs used in this work, but the central region of the stigma, in continuity with the stylar transmitting tissue, was labelled by mAbs JIM8 and JIM13. In Arabidopsis plants, the stigma is dry and the style is solid, with the transmitting tissue in its central zone. Different studies have shown the presence of AGPs in the style of several plant species, mainly Nicotiana alata (Wu et al., 2001), N. tabacum (Cheung et al., 1995; Wu et al., 1995, 2001), Lilium longiflorum (Jauh and Lord, 1996), and Amaranthus hypochondriacus and Actinidia deliciosa (Coimbra and Duarte, 2003). These results suggest a role for AGPs along the pollen tube pathway, possibly as a biochemical support and/or giving directional clues for the pollen tube to reach its target. Supporting evidence for a chemo-attracting role for AGPs arose from the work of Cheung et al. (1995) and Wu et al. (1995) in which the TTS proteins of N. tabacum showed a glycosylation gradient towards the direction of growth of the pollen tube, and were deglycosylated by pollen tubes during their growth, suggesting that these proteins may contribute to the creation of a gradient responsible for the guidance of the pollen tubes.
The Arabidopsis ovary is a cylinder with a central septum and four rows of approximately 40–45 ovules (Sessions and Zambryski, 1995). All along the development of the ovary there is specific labelling with JIM8 and JIM13 in all xylem conducting cells, which is probably associated with the well-documented role of AGPs in the differentiation and PCD of all xylem tracheary elements (Motose et al., 2004).
AGPs in macrosporogenesis and macrogametogenesis
The results obtained for the early stages of ovule development were quite interesting, with JIM8 and JIM13 specifically and intensely labelling the gametophytic cells only. In the very young ovules, the intense labelling of the macrospores resulting from meiosis was remarkable. With these two antibodies no other cell types were labelled, which means that these AGPs are probably acting as gametic determinants, involved in the transition from a sporophytic to a gametophytic generation.
The last stage of pollen tube growth is the arrival at the ovule, and it is at that moment that, most of the time, there is an abrupt change in growth direction, the tube turning by >90° in order to reach the micropyle of the ovule. At this stage, pollen tubes certainly detect orientation signals released by the ovules and essential for the attraction (Palanivelu and Preuss, 2006). In Torrenia fournieri it was shown, by laser ablation of individual cells of the embryo sac, that the synergid cells are responsible for pollen tube attraction, one synergid cell being sufficient for the attraction to be effective (Higashiyama et al., 2001). However, Higashiyama et al. (2001) did not identify the biochemical nature of this attractor. In the present work, the strong and specific labelling with JIM8 and JIM13 of the embryo sac wall and of the synergid cells, especially their filiform apparatus, is quite indicative of a role related to the secretions by these cells, through the micropyle. The Golgi-derived vesicles in synergid cells of oilseed rape were also labelled by JIM8 (Pennell et al., 1991). The labelling of the integument lining the micropyle suggests that AGP molecules, or sugar residues released by AGP molecules, may be related to the attraction phenomena of the pollen tube growth into the embryo sac. This type of labelling was also shown for N. tabacum (Qin and Zhao, 2006), A. hypochondriacus (Coimbra and Salema, 1997), and A. deliciosa (Coimbra and Duarte, 2003).
The molecular mechanism of action of AGPs is still unknown, mainly due to the difficulties posed by the complex glycoproteins. However, the complex structure of the sugar fraction of AGPs makes them a potential source of small signalling molecules, such as biologically active oligosaccharides.
Results presented in this work may be important not only from a development point of view but also because they may lay the foundation for characterizing the expression of individual AGP genes in each of the developmental stages considered.
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