Journal of Experimental Botany, Vol. 53, No. 373, pp. 1429-1436,
June 2002
© 2002 Oxford University Press
Original Papers |
4-Fucosyltransferase is regulated during flower development: increases in activity are targeted to pollen maturation and pollen tube elongation
Glycobiologie et Biotechnologie EA3176, Institut des Sciences de la Vie et de la Santé, Université de Limoges, 123 avenue Albert Thomas, 87060 Limoges Cedex, France
Received 22 November 2001; Accepted 11 February 2002
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
4-Fucosylation represents a final step of protein N- glycosylation. 4-fucosylated N-glycans are thought to be involved in cell-to-cell communication and recognition in primates and plants. Nevertheless, in the plant life cycle, the function of 4-fucosylation remains largely unknown. To gain an insight into the role of 4-fucosylation during development, the study focused on tobacco flowers. It is shown that an increase in (1,4)fucosyltransferase (Fuc-T) activity is only observed during anther development, whereas it remains at a constant but low level (around 20 pmol Fuc h-1 mg-1 protein) in the gynoecium and perianth. At least a 4-fold higher activity is detected in mature pollen grains. These data suggest that (1,4)Fuc-T activity is regulated during anther development. Furthermore, (1,4)Fuc-T activity could be required during pollen tube elongation where the activity level peaks at 350 pmol h-1 mg-1 protein. Based on enzyme profile and cycloheximide effects on pollen germination and activity, it is hypothesized that the gene encoding 4-Fuc-T could be regulated late during pollen development. A potential role of 4- fucosylation during pollen tube elongation is also discussed. Key words: Elongation, fucosylation, pollen, tobacco.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
In both plant and mammalian cells, N-glycosylation is involved in protein maturation. Processing of N-linked glycans occurs along the secretory pathway from the endoplasmic reticulum through the Golgi apparatus. N- glycans seem to be involved in the correct folding of polypeptides, stability and transport to their proper destination (Hammond and Helenius, 1995
).
Arabidopsis mutants deficient in correct N-glycosylation patterns and, therefore, lacking complex N-glycans are mostly embryo lethal, unable to develop normally or fail to breed (von Schaewen et al., 1993; Boisson et al., 2001; Lukowitz et al., 2001). Also, N-glycans might also be involved in programmed cell death (Lindholm et al., 2000). Another critical aspect of plant N-glycans is their potential involvement in allergenic immune responses in mammals when complex carbohydrate structures are localized on pollen grains or in foodstuffs (Garcia-Casado et al., 1996; Wilson et al., 2001).
In plants and mammals, fucosyltransferases (Fuc-T) are a specific group among the large Golgi-resident glycosyltransferase families. They are mainly involved in the maturation of complex type N-glycans. Plant Fuc-T catalyse the transfer of fucose from GDP-fucose to GlcNAc in (1,3)-, (1,4)-linkages (Staudacher et al., 1999). Xyloglucan 2-Fuc-T exist in plants and catalyse transfer of fucose to galactose in xyloglucans which are involved in the polysaccharide–cellulose network of primary cell walls (Faik et al., 2000). The Lewisa motif is synthesized by transfer of galactose and fucose residues by ß3-galactosyltransferase and 4-fucosyltransferase onto GlcNAc residues of terminal lactosamine, respect ively. The Lewisa motif synthesized by the 4-Fuc-T has been found in unrelated species across the plant kingdom. Nevertheless, ambiguity about the presence of Lewisa still remains for the Cruciferae family, where the Lewisa motif was not detected in Arabidopsis plants, but was characterized in papaya fruit (Fitchette et al., 1999; Wilson et al., 2001). In animals, this motif seems to be exclusively present in primates (Blancher and Socha, 1997). In humans, Lewisa structures are involved in blood group determinism and in cell-to-cell interactions (Staudacher et al., 1999). In plants, 4-fucosylation may be involved in cell-to-cell communication and/or recognition (Fitchette-Lainé et al., 1997; Melo et al., 1997). Several immunolocalization studies revealed that this glycotope was associated with extracellular soluble or membrane bound-glycoproteins, but these glycoproteins were not fully characterized (Fitchette et al., 1999). Therefore, Lewisa-containing glycans could be considered as markers of protein transport (Fitchette et al., 1999). However, all these studies were mainly performed on cell suspension cultures or root tips and not during a specific plant developmental programme.
In flowering plants, pollen development represents a good model to study cell communication and signalling as well as cell elongation. Two categories of genes encoding pollen-specific proteins have been described according to their expression patterns during pollen development. Early genes are only expressed during microsporogenesis and might encode structural proteins (Mascarenhas, 1990, 1993). Late genes are expressed after microspore first mitosis during pollen maturation and pollen tube elongation. The regulation of late genes suggests that pollen late proteins might be key components involved in pollen germination and/or during pollen tube elongation (Mascarenhas, 1990, 1993). So far, several pollen late proteins are potentially N-glycosylated (Rogers et al., 1992; Tebbutt et al., 1994; Ogawa et al., 1996; Witting et al., 2000). Moreover, glycosylation seems to play a key role during pollen tube growth. An inhibitor of glycosylation, tunicamycin, which blocks the connection of glycan chains to peptides, inhibited pollen tube growth, suggesting an involvement of N-glycosylated proteins in the elongation process (Capkova et al., 1997). Only one N- glycoprotein Cry j I from japanese cedar (Cryptomeria japonica) pollen is 4-fucosylated (Ogawa et al., 1996). This protein has a pectate lyase enzyme activity and could be involved in cell wall elaboration during germination and pollen tube growth (Taniguchi et al., 1995).
4-Fucosylation could be involved in male gametophyte development, which represents a particular aspect of plant reproductive development. It could also contribute to biological activity and/or the correct targeting of proteins.
In order to define the role(s) of 4-fucosylation during reproductive development, (1,4)Fuc-T activity was analysed during tobacco flower development. It was shown that (1,4)Fuc-T activity is developmentally regulated with peaks of activity, firstly, during pollen maturation and, secondly, during pollen tube elongation. 4-Fucosylation could be involved in male gametophyte development which represents a particular aspect of plant reproductive development.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material
Tobacco (Nicotiana tabacum L. var Xanthi) plants were grown in a greenhouse at 25 °C with a 16 h photoperiod. Microspores and pollen grains were observed under light microscopy. Their developmental stages were chosen on morphological criteria such as diameter. Diameter measurement was performed using Adobe PhotoShop 5 software from pictures.
In vivo pollen tube growth assay
A 46 mm unopened flower was used for hand-pollination experiments. Its anthers were cut off and 48 h later the emasculated flower was fully opened and hand-pollinated on its exudating stigma. Pollen grains germinate on the stigma and pollen tubes elongate firstly into the stigma and thus, into the style.
In vitro pollen tube growth
Anthers were isolated from flowers at anthesis and pollen grains were collected. Pollen grains germination occured in liquid germination medium (3 mM HBO3, 1.7 mM Ca(NO3)2, 10% sucrose, pH 6.6), in darkness at 25 °C. Cycloheximide was purchased from Sigma (St Louis, MO).
Protein extraction
Plant tissues were ground in liquid nitrogen. The resulting powder was placed into an extraction buffer (20 mM MES, 0.1% Triton X100, 15% glycerol), vigorously vortexed and centrifuged at 12 000 g for 3 min.
Anthers were wounded in order to release microspores or pollen grains which were transferred to the extraction buffer described above. Homogenates were vortexed vigorously followed by several rounds of freezing in liquid nitrogen and then centrifuged at 4 °C at 12 000 g for 2 min.
The protein content of supernatants was determined using the Bio-Rad reagent (Bio-Rad, Hercules, CA) and BSA as a standard (Bradford, 1976). The same protein supernatants were used for in vitro enzymatic assay of (1,4)fucosyltransferase and dot blot analyses.
Pollen protein extraction was prepared as described previously (Capkova et al., 1994). Pollen grains were homogenized in 50 mM TRIS-HCl pH 6.8, 10% sucrose and 1% (v/v) mercaptoethanol buffer. The soluble cytosolic proteins were obtained by centrifugation at 13 000 g for 15 min at 4 °C. Wall and membrane-bound proteins were extracted from the pellet with the previous buffer supplemented with 1% SDS. Extraction of pollen coat proteins was performed as described earlier using diethyl ether as the organic solvent (Yih Bih et al., 1999).
In vitro enzymatic assay of 4-fucosyltransferase
Activity was performed on crude extracts for 2 h at 37 °C in a 60 µl volume reaction containing 25 mM sodium cacodylate (pH 6.5), 5 mM ATP, 20 mM MnCl2, 10 mM -L-fucose, 3 µM GDP [14C]-fucose (310 mCi mmol-1; Amersham Pharmacia Biotech, UK), 0.1 mM type I N-acetyl-lactosamine acceptor, and 15 µg protein. In crude plant extracts, only type I acceptor reveals (1,4)Fuc-T activity (Faik et al., 2000). The reaction was stopped by adding 3 ml water and the mixture was then filtered on a hydrophobic Sep-Pak C18 cartridge (Waters Millipore, Bedford, MA) that retains the acceptor (either fucosylated or not). Free GDP [14C]-fucose was washed off with 10 ml of water. The acceptor was eluted with 5 ml of ethanol, collected into scintillation vials and the fucosylated reaction product was quantified after addition of 2 vols of Biodegradable Counting Scintillant (Amersham Pharmacia Biotech, UK) by a liquid scintillation beta counter (Liquid scintillation analyser, Tri- Carb-2100TR, Packard).
Presence of Lewisa motifs by dot blot analysis
The blots were performed by using a chemiluminescence blotting substrate (POD) system according to the manufacturer's instructions (Boeringher Mannheim). Proteins were deposited onto a nitrocellulose membrane (Hybond-C extra membrane, Amersham, UK). After blocking in 1% blocking solution (v/v) containing (50 mM TRIS base, pH 7.5, 150 mM NaCl) TRIS-buffered saline TBS solution for 2 h at room temperature, the membrane was incubated with rabbit primary anti-sycamore laccase Lewisa antibody (generous gift from Dr L Faye, Mont St Aignan, France) in a 1 : 2000 dilution for 1 h at room temperature. It was then washed twice into TBS buffer containing 0.1% Tween 20 followed by two washes into 0.5% blocking solution (v/v). The membrane was incubated with a 1 : 1000 dilution secondary antibody conjugated with horseradish peroxidase (Dako, Denmark) and thoroughly washed in TBS buffer containing 0.1% Tween 20. The immunoreactive proteins were revealed by a chemiluminescence reaction. The membrane was then exposed to X-ray films (Biomax Film, Kodak) for different exposure times. Human saliva was used as a positive control and bovine proteins as the negative control (Yazawa and Furukawa, 1980; Oulmouden et al., 1997).
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
(1,4)Fuc-T activity is detected at a low level in tobacco flowers(1,4)Fuc-T activity was determined in sepals, petals, stamens, and pistils taken at three stages of flower development based on bud length (Fig. 1). A relatively constant basal (1,4)Fuc-T activity (approximately 20 pmol Fuc h-1 mg-1 protein) was detected in sepals, petals and non-pollinated pistils isolated from very young flower buds to opened flowers (Fig. 1). Therefore, in growing tissues, 4-fucosyltransferase seems to function as a housekeeping enzyme involved in N-glycoproteins maturation and in primary metabolism. Nevertheless, a 3- fold increase in (1,4)Fuc-T activity was observed in stamens at anthesis (Fig. 1).
|
(1,4)Fuc-T activity specifically increases in anthers
Five successive stages based on flower bud length are described: stage A (11–20 mm), stage B (22–39 mm), stage C (43–45 mm), stage D (46 mm), and stage E (46 mm). By contrast to stage D, stage E corresponds to the fully opened flower. In order to define these particular stages precisely, anthers and pistils were also weighed fresh and measured. These criteria were also confirmed by morphological data described previously (Koltunow et al., 1990). These stages correspond to cellular events occurring during male and female sporophyte and gametophyte development (Koltunow et al., 1990; De Martinis and Mariani, 1999). (1,4)Fuc-T activity was thus more accurately followed during anthers and pistils development (Fig. 2A, B).
|
In anthers, a weak
(1,4)Fuc-T activity was detected at stage A (approximately 15 pmol Fuc h-1 mg-1 protein). Two significative increases in (1,4)Fuc-T activity were measured during anther development (Fig. 2A
). The first activity burst between stages A and B was concomitant with an increase in anther weight. It corresponded to the degradation of connective tissue in the stomium region and the beginning of microgametogenesis. The second burst was observed between stages C and D (around 90 pmol Fuc h-1 mg-1 protein) (Fig. 2A). After stage D, the loss of anther weight was linked to its dehiscence (Fig. 2A). For stages D and E, a basal activity was measured in anthers empty of pollen grains (approximately 20 pmol Fuc h-1 mg-1 protein).
During ovule development (stages A–C) and megagametogenesis (stage D), a basal (1,4)Fuc-T activity was detected (approximately 15 pmol Fuc h-1 mg-1 protein) while pistil continuously gained in weight (Fig. 2B). By contrast to the results shown in Fig. 1, in fully opened flowers, a 3-fold increase in activity was measured in the pollinated pistil (Fig. 2B).
Regarding the high activity detected at stage E in both anthers and pollinated pistils, it is suggested that (1,4)Fuc-T activity is mainly associated with pollen development.
(1,4)Fuc-T activity specifically increases during late pollen maturation
Isolated microspores, pollen grains and the corresponding sporophytic tissues were isolated from stages A to E. A basal (1,4)Fuc-T activity was detected in free microspores (Table 1). Activity clearly increased in binucleate microspores and reached a maximal level in mature pollen grains (approximately 120 pmol Fuc h-1 mg-1 protein) (Table 1).
|
In order to correlate this high activity to the presence of Lewisa motifs in pollen proteins, dot blot analyses from free and binucleate microspores and mature pollen grains were performed (Fig. 3A
). Increased amounts of Lewisa motifs were detected from free microspores to mature pollen grains (Fig. 3A). Since the same protein amounts were loaded, it can be concluded that the appearance of Lewisa structures was clearly correlated with the increase in (1,4)Fuc-T activity during pollen development.
|
In addition, a dot blot analysis was performed on different fractions of pollen proteins in order to localize Lewisa epitopes on mature pollen grains (Fig. 3B
). Although Lewisa motifs were found in the cytosol, higher amounts of this motif were detected in the pollen coat, wall and membranes suggesting a role for 4-fucosylated proteins during the establishment of these structures.
A specific increase in (1,4)Fuc-T activity is observed during pollen germination and pollen tube elongation
In vivo germination pollen assays were performed on hand-pollinated stigmas. (1,4)Fuc-T activity was then followed in non-pollinated or hand-pollinated stigmas. A relatively constant and basal activity was always detected in non-pollinated stigmas and styles (Fig. 4). By contrast, a significative increase in activity was observed in these tissues after pollination (3-fold after 2 h and 5-fold after 5 h) (Fig. 4). Both results strongly suggest that an increase in (1,4)Fuc-T activity is linked to germination events and pollen tube elongation.
|
To assess pollen tube growth directly, in vitro germination assays were performed. Consequently, a time-course of in vitro pollen tube growth was performed and
(1,4)Fuc-T activity was measured at the different points. While (1,4)Fuc-T activity remained relatively constant in germinating pollen grains between 0 h and 5 h culture, a 3-fold increase in activity was found in a 12 h culture (Table 2). The activity remained at this high level even after 20 h culture (Table 2). This last result suggests that higher amounts of 4-fucosylated N-glycoproteins are likely to be synthesized during pollen tube elongation. This hypothesis was tested by immunodetection of Lewisa motifs on the same amount of proteins from mature pollen grains and pollen tubes from a 12 h and 20 h culture, respectively. The dot blot analysis revealed an increase in the Lewisa motif amounts from 0 to 20 h (Fig. 5). Both high levels of (1,4)Fuc-T activity and Lewisa structures are well correlated and suggest that 4- fucosylated proteins are required in pollen tube elongation.
|
|
Increase in (1,4)Fuc-T activity is due to protein neosynthesis during pollen tube elongation
To test whether the 3-fold increase in (1,4)Fuc-T activity (346 pmol Fuc h-1 mg-1 protein) was due to newly synthesized enzymes during pollen tube elongation, an in vitro pollen grains germination assay was performed in the presence of 150 µM cycloheximide (Chx) (Table 2). At this concentration, Chx is an inhibitor of de novo protein synthesis (Riou-Khamlichi et al., 2000). In order to check the Chx effect, percentages of germination and pollen tube elongation were determined after 5 h and 12 h treatment. 83% of pollen grains germinated after 5 h Chx treatment and only 8% of pollen grains presenting a normal pollen tube length, was detected after 12 h Chx treatment (Table 2). It is concluded that 150 µM Chx has no effect on pollen germination but strongly inhibits pollen tube elongation. This result was also in agreement with previous work (Mascarenhas, 1993).
Between 0 h and 5 h of Chx treatment, (1,4)Fuc-T activity remained constant around 110 pmol h-1 mg-1 protein similar to the level determined in untreated pollen grains (Table 2). This result suggests that this enzyme may have a low turnover or is stable as described for late specific pollen proteins (Ylstra and McCormick, 1999). By contrast, a very low increase in activity was observed on 12 h Chx-treated pollen grains (around 171 pmol h-1 mg-1 protein) (Table 2). This low increase could be due to the presence of the 8% of well-elongated pollen tubes (Table 2). Furthermore, an increase in the amount of Lewisa motifs was not observed within 12 h of Chx- treated pollen tubes (Fig. 5). In the presence of Chx, no additional amount of Lewisa is found, strongly suggesting an inhibition of the de novo synthesis of 4- fucosyltransferase. It is concluded that, during pollen tube elongation, a new pool of 4-Fuc-T enzyme is required.
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
In plants, Lewisa harbouring N-glycans were associated with extracellular soluble or membrane-bound glycoproteins (Fitchette et al., 1999
; Bakker et al., 2001). For the first time the variations of (1,4)Fuc-T activity during tobacco flower development have been investigated. It is postulated that this activity during pollen development and pollen tube elongation could reflect the localization of 4-fucosylated substrates and, therefore, their potential involvement in the male reproductive process. A positive correlation between an increase in the amount of Lewisa motifs and an increase in (1,4)Fuc-T activity during pollen maturation and pollen tube elongation is shown.
(1,4)Fuc-T could be a housekeeping enzyme
Cellular events such as division, elongation or expansion occur in the corolla and reproductive tissues during flower development. (1,4)Fuc-T activity always remained detec table at a constitutive and basal level in the perianth, non- pollinated pistils and empty anthers. This suggests that (1,4)Fuc-T activity is basically required during tobacco flower growth and is implicated in N- glyco protein maturation and in primary metabolism. Thus, it might be suspected that 4-Fuc-T simply acts as a housekeeping enzyme as described for another glycosyltransferase (Wenderoth and von Schaewen, 2000).
Strikingly, peaks of (1,4)Fuc-T activity were only associated with male gametophyte development whereas no significant variations were detected in the female gametophyte. These data suggest that (1,4)Fuc-T could be considered as a housekeeping enzyme during ovule development. Nevertheless, further immunolocalizations are necessary to confirm the presence or absence of specific Lewisa containing N-glycoproteins in the pistil.
(1,4)Fuc-T activity is up-regulated during microgametogenesis
A 2-fold increase in (1,4)Fuc-T activity was detected in binucleate microspores and also during late pollen grain maturation suggesting a role for 4-Fuc-T during microgametogenesis. The crucial event after mitosis I corresponds to the beginning of intine elaboration (McCormick, 1993). A pollen grain has two cell walls: an inner layer, intine, which is largely composed of pectocellulose and an outer network, exine, which is rich in sporopollenin and covered with tryphine (Lord, 2000). The tapetum plays a determinant role in exine deposition whereas the microspore itself controls intine production. It is suggested that these increases in 4-Fuc-T activity, generated by maturing pollen grains, could be linked to intine elaboration and maturation.
A specific and high (1,4)Fuc-T activity seems to be required during pollen tube elongation
During germination, intine is destabilized implying invagination and pollen tube emergence at pectin-rich aperture. After 5 h of pollen germination, (1,4)Fuc-T activity increases by about 3-fold strongly suggesting that new 4-fucosylated proteins are needed during pollen tube expansion. It is proposed that (1,4)Fuc-T activity might be up-regulated on demand and that N- glycoproteins harbouring such complex carbohydrates could play an essential role from germination to whole pollen tube elongation. Indeed, complex glycans are probably involved in such a developmental process because the Arabidopsis thaliana cgl homozygous mutant which lacks complex glycans is male sterile (Von Schaewen et al., 1993). Taken together, these data and those reported in previous studies support the idea that the pollen grain represent a unique developmental and highly specialized structure in which essential functions could be mediated by glycoproteins with complex N- glycans. Furthermore, N-glycoproteins involved in cell wall elaboration are essential for tobacco pollen tube growth (Capkova et al., 1997).
Gene encoding 4-Fuc-T might potentially belongs to the pollen late genes family
Proteins encoded by late genes seem to play an important role during pollen maturation and/or pollen tube elongation because mature pollen grains store large amounts of these proteins and mRNAs in readiness for pollen germination (Mascarenhas, 1990, 1993).
At least, a 4-fold increase in (1,4)Fuc-T activity was measured in mature pollen grains compared to that detected in free microspores. Moreover, in non-germinating quiescent pollen grains taken 72 h after anthesis, (1,4)Fuc-T activity was still high and similar to that detected in mature pollen grains at anthesis (data not shown). Thus, this high level of activity could be linked to a pre-existing pool of enzyme which might accumulate during late pollen development. An additional 3-fold increase in activity was observed in well-elongated pollen tubes after 12 h culture. Before 12 h culture, this new peak was not detected, but (1,4)Fuc-T activity level remained as important and constant as in mature pollen grains. Furthermore, a similar situation was also observed in cycloheximide-treated germinating pollen grains. Taken together, all these results are in favour of an accumulation of an active enzyme form during late pollen maturation ready to be used during germination and pollen tube elongation.
Cycloheximide treatment of germinating pollen grains suggests that the important increase in (1,4)Fuc-T activity was linked to de novo synthesized enzymes from a pool of mRNAs used between 5 h and 12 h culture. According to published literature and to this study's different results, which strongly suggest the existence of two pools of active enzyme and mRNAs in pollen grains, the gene encoding 4-Fuc-T might belong to the late pollen gene family. Therefore, it is suspected that 4- fucosylated proteins could also be regulated as late pollen proteins.
Most proteins encoded by late genes are involved in pectin metabolism during pollen intine and pollen tube cell wall elaboration. Furthermore, these proteins are often N-glycosylated (Tebbut et al., 1994; Ogawa et al., 1996; Witting et al., 2000). Cry j I allergenic protein from japanese cedar is 4-fucosylated and has a pectate lyase enzyme activity (Taniguchi et al., 1995; Ogawa et al., 1996). Two tobacco late pollen pectate lyases g10 and Nt59 are potentially N-glycosylated (Rogers et al., 1992; Kulikauskas and McCormick, 1997). As g10 deduced polypetide sequence is highly similar to Cry j I, but not to Nt59 (data not shown), further work is necessary to determine the involvement of the g10 enzyme during tobacco pollen development and, subsequently, its putative glycosylation profile.
In the plant kingdom, the functions of Lewisa-containing N-glycoproteins remain largely unknown. This study's results implicate, for the first time, (1,4)Fuc-T activity during pollen development and it might be relevant to an involvement of complex N- glycans in this process. Moreover, 4-Fuc-T is the first N-glycosyltransferase shown to be involved in a fundamental aspect of plant development. Further investigations should help to characterize and localize 4-fucosylated candidates in order to understand their function during pollen development and pollen tube elongation.
|
Acknowledgments |
|---|
We thank Dr Loïc Faye and Michel Carlué for their critical reading of the manuscript, Pascal Guillaume for his technical assistance. This work was performed within the French ‘GT-rec’ network and supported in part by grants MENRT (ACC SV No 9514111) and CNRS (PCV program). Caroline Joly was supported by a PDZR fellowship.
|
Notes |
|---|
1 To whom correspondence should be addressed. Fax: +33 555 457 653. E-mail: catherine.riou{at}unilim.fr
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bakker H, Bardor M, Molthoff JW, Gomord V, Elbers I, Stevens LH, Jordi W, Lommen A, Faye L, Lerouge P, Bosch D. 2001. Galactose-extended glycans of antibodies produced by transgenic plants. Proceeding of the National Academy of Sciences, USA 98, 2899–2904.
Blancher A, Socha WW. 1997. The ABO, Hh and Lewis blood group in humans and non-human primates. In: Blancher A, Klein, Socha WW, eds. Molecular biology and evolution of blood group and MHC antigens in primates. Berlin, Heidelberg: Springer-Verlag, 30–92.
Boisson M, Gomord V, Audran C, Berger N, Dubreucq B, Granier F, Lerouge P, Faye L, Caboche M, Lepiniec L. 2001. Arabidopsis glucosidase I mutants reveal a critical role of N- glycan trimming in seed development. The EMBO Journal 20, 1010–1019.[Web of Science][Medline]
Bradford MM. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.[Web of Science][Medline]
Capkova V, Zbrozek J, Tupy J. 1994. Protein synthesis in tobacco pollen tubes: preferential synthesis of cell-wall 69 kDa and 66 kDa glycoproteins. Sexual Plant Reproduction 7, 57–66.
Capkova V, Fidlerova A, van Amstel T, Croes AF, Mata C, Schrauwen JAM, Wullems GJ, Tupy J. 1997. Role of N- glycosylation of 66 and 69 kDa glycoproteins in wall formation during pollen tube growth in vitro. European Journal of Cell Biology 72, 282–285.[Medline]
De Martinis D, Mariani C. 1999. Silencing gene expression of the ethylene-forming enzyme results in a reversible inhibition of ovule development in transgenic tobacco plants. The Plant Cell 11, 1061–1071.
Faik A, Bar-Peled M, DeRocher AE, Zeng W, Perrin RM, Wilkerson C, Raikhel NV, Keegstra K. 2000. Biochemical characterization and molecular cloning of an - 1,2- fucosyltransferase that catalyses the last step of cell wall xyloglucan biosynthesis in pea. Journal of Biological Chemistry 275, 15082–15089.
Fitchette AC, Cabanes-Mancheteau M, Marvin L, Martin B, Satiat-Jeunemaitre B, Gomord V, Crooks K, Lerouge P, Faye L, Hawes C. 1999. Biosynthesis and immunolocalization of Lewis a-containing N-glycans in the plant cell. Plant Physiology 121, 333–343.
Fitchette-Lainé AC, Gomord V, Cabanes M, Michalski J-C, Saint Macary M, Foucher B, Cavelier B, Hawes C, Lerouge P, Faye L. 1997. N-glycans harboring the Lewis a epitopes are expressed at the surface of plant cells. The Plant Journal 12, 1411–1417.[Web of Science][Medline]
Garcia-Casado G, Sanchez-Monge R, Chrispeels MJ, Armentia A, Salcedo G, Gomez L. 1996. Role of complex asparagine-linked glycans in the allergenicity of plant glycoproteins. Glycobiology 6, 471–477.
Hammond C, Helenius A. 1995. Quality control in the secretory pathway. Current Opinion in Cell Biology 7, 523–529.[Web of Science][Medline]
Koltunow AM, Truettner J, Cox KH, Wallroth M, Goldberg RB. 1990. Different temporal and spatial gene expression patterns occur during anther development. The Plant Cell 2, 1201–1224.
Kulikauskas R, McCormick S. 1997. Identification of the tobacco and Arabidopsis homologues of the pollen-expressed LAT59 gene of tomato. Plant Molecular Biology 34, 809–814.[Web of Science][Medline]
Lindholm P, Kuittinen T, Sorri O, Guo D, Merits A, Tormakangas K, Runeberg-Roos P. 2000. Glycosylation of phytepsin and expression of dad1, dad2 and ost1 during onset of cell death in germinating barley scutella. Mechanisms of Development 93, 169–173.[Web of Science][Medline]
Lord E. 2000. Adhesion and cell movement during pollination: chercher la femme. Trends in Plant Science 5, 368–373.[Web of Science][Medline]
Lukowitz W, Nickle TC, Meinke DW, Last RL, Conklin PL, Somerville CR. 2001. Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point a requirement of N-linked glycosylation for cellulose biosy nthesis. Proceeding of the National Academy of Sciences, USA 98, 2262–2267.
Mascarenhas JP. 1990. Gene activity during pollen development. Annual Review of Plant Physiology and Plant Molecular Biology 41, 317–338.[Web of Science]
Mascarenhas JP. 1993. Molecular mechanisms of pollen tube growth and differentiation. The Plant Cell 5, 1303–1314.
McCormick S. 1993. Male gametophyte development. The Plant Cell 5, 1265–1275.
Melo NS, Nimtz M, Conradt HS, Fevereiro PS, Costa J. 1997. Identification of the human Lewis a carbohydrate motif in a secretory peroxidase from a plant cell suspension culture (Vaccinium myrtillus L.). FEBS Letters 415, 186–191.[Web of Science][Medline]
Ogawa H, Hijikata A, Amano M, Kojima K, Fukushima H, Ishizuka I, Kurihara Y, Matsumoto I. 1996. Structures and contribution to the antigenicity of oligosaccharides of Japanese cedar (Cryptomeria japonica) pollen allergen Cry j I: relationship between the structures and the antigenic epitopes of plant N-linked complex-type glycans. Glycoconjugate Journal 13, 555–566.[Web of Science][Medline]
Oulmouden A, Wierinckx A, Petit JM, Costache M, Palcic MM, Mollicone R, Oriol R, Julien R. 1997. Molecular cloning and expression of a bovine alpha(1,3)-fucosyltransferase gene homologous to a putative ancestor gene of the human FUT3- FUT5-FUT6 cluster. Journal of Biological Chemistry 272, 8764–8773.
Riou-Khamlichi C, Menges M, Healy SJ, Murray JAH. 2000. Sugar control of the plant cell cycle: differential regulation of the Arabidopsis D-type gene cyclin expression. Molecular Cell Biology 20, 4513–4521.
Rogers HJ, Harvey A, Lonsdale DM. 1992. Isolation and characterization of the tobacco gene with homology to pectate lyase which is specifically expressed during microsporogenesis. Plant Molecular Biology 20, 493–502.[Web of Science][Medline]
Staudacher E, Altmann F, Wilson IBH, März L. 1999. Fucose in N-glycans: from plant to man. Biochimica et Biophysica Acta 1473, 216–236.[Medline]
Tebbutt SJ, Rogers HJ, Lonsdale DM. 1994. Characterization of a tobacco gene encoding a pollen-specific polygalacturonase. Plant Molecular Biology 25, 283–297.[Web of Science][Medline]
Taniguchi Y, Ono A, Sawatani M, Nanba M, Kohno K, Usui M, Kurimoto M, Matuhasi T. 1995. Cry j I, a major allergen of japanese cedar pollen, has a pectate lyase enzyme activity. Allergen 50, 90–93.
von Schaewen A, Sturm A, O'Neill J, Chrispeels MJ. 1993. Isolation of a mutant Arabidopsis plant that lacks N-acetylglucosaminyltransferase I and is unable to synthesize Golgi-modified complex N-linked glycans. Plant Physiology 102, 1109–1118.[Abstract]
Wenderoth I, von Schaewen A. 2000. Isolation and characterization of plant N-acetylglucosaminyltransferase I (GntI) cDNA sequences. Functional analyses in the Arabidopsis cgl mutant and in the antisense plants. Plant Physiology 123, 1097–1108.
Wilson IBH, Zeleny R, Kolarich D, Staudacher E, Stroop CJM, Kamerling JP, Altmann F. 2001. Analysis of Asn-linked glycans from vegetable foodstuffs: widespread occurrence of Lewisa, core 1,3-linked fucose and xylose substitutions. Glycobiology 11, 261–274.
Witting FRA, Knuiman B, Derksen J, Capkova V, Twell D, Schrauwen JAM, Wullems GJ. 2000. The pollen-specific gene Ntp303 encodes a 69 kDa glycoprotein associated with the vegetative membranes and the cell wall. Sexual Plant Reproduction 12, 276–284.
Yazawa S, Furukawa K. 1980. alpha-L-Fucosyltransferases related to biosynthesis of blood group substances in human saliva. Journal of Immumogenetic 7, 137–148.
Yih Bih F, Wu SSH, Ratnayake C, Walling LL, Nothnagel EA, Huang AHC. 1999. The predominant on the surface of maize pollen is an endoxylanase synthesized by a tapetum mRNA with a long 5' leader. Journal of Biological Chemistry 274, 22884–22984.
Ysltra B, McCormick S. 1999. Analysis of mRNA stabilities during pollen development and in BY2 cells. The Plant Journal 20, 101–108.[Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  B. Ma, J. L. Simala-Grant, and D. E. Taylor Fucosylation in prokaryotes and eukaryotes Glycobiology, December 1, 2006; 16(12): 158R - 184R. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||