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Clemente, H.S.;  Jamet, E. N-glycoproteins in Plant Cell Walls. Encyclopedia. Available online: https://encyclopedia.pub/entry/38025 (accessed on 21 June 2024).
Clemente HS,  Jamet E. N-glycoproteins in Plant Cell Walls. Encyclopedia. Available at: https://encyclopedia.pub/entry/38025. Accessed June 21, 2024.
Clemente, Hélène San, Elisabeth Jamet. "N-glycoproteins in Plant Cell Walls" Encyclopedia, https://encyclopedia.pub/entry/38025 (accessed June 21, 2024).
Clemente, H.S., & Jamet, E. (2022, December 05). N-glycoproteins in Plant Cell Walls. In Encyclopedia. https://encyclopedia.pub/entry/38025
Clemente, Hélène San and Elisabeth Jamet. "N-glycoproteins in Plant Cell Walls." Encyclopedia. Web. 05 December, 2022.
N-glycoproteins in Plant Cell Walls
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Cell walls are an extracellular compartment specific to plant cells, which is not found in animal cells. Their composition varies between cell types, plant species, and physiological states. They are composed of a great diversity of polymers, e.g., polysaccharides, proteins, and lignins. Cell wall proteins (CWPs) are major players involved in the plasticity of cell walls which support cell growth and differentiation, as well as adaptation to environmental changes. In order to reach the extracellular space, CWPs are transported through the secretory pathway where they may undergo post-translational modifications, including N-glycosylations on the Asn residues in specific motifs (Asn-X-Ser/Thr-X, with X≠Pro).

cell wall cell wall protein Concanavalin A affinity chromatography glycopeptides

1. Introduction

Glycosylations are major post-translational modifications (PTMs) observed in plant cell wall proteins (CWPs), and they occur in the secretory pathway. There are of three types: N-glycosylation, O-glycosylation, and glypiation. N-glycosylation consists of the grafting of an oligosaccharide onto a particular amino acid, asparagine (Asn), in the context of a specific motif, Asn-X-Ser/Thr-X (with X≠Pro). Since it is short (only four amino acids), this motif is classified among the motifs with a high probability of occurrence. It means that the chance to find it in protein sequences is high even if the protein does not travel through the secretion pathway where N-glycans are synthesized and grafted. O-glycosylation occurs on the hydroxyl groups of Ser and hydroxyproline (Hyp) residues located in particular amino acid motifs, especially in the structural proteins of the hydroxyproline-rich glycoprotein families (HRGPs) [1][2][3][4][5]. Glypiation consists of the addition of a glycosylphosphatidylinositol (GPI) being anchored at the C-terminus of proteins and allows the anchoring of proteins at the external side of the plasma membrane. All these PTMs are crucial for the structure and the function of CWPs.
In plants, there are various types of N-glycans [7]. The biosynthesis of N-glycans has already been extensively reviewed (see for example, [7][8][9][10][11][12]), and it will not be described in detail here. Briefly, the N-glycosylation process starts in the endoplasmic reticulum (ER) by the co-translational transfer of an oligosaccharide precursor of the high-mannose type, Glc(3)Man(9)GlcNAc(2) (Figure 1), onto the Asn residues of the N-glycosylation motifs of proteins. Then, these N-glycans undergo several maturation steps consisting of the removal and the subsequent addition of sugar residues in the ER and the Golgi apparatus by glycosidases and glycosyl transferases, respectively; this gives rise to complex N-glycans with Lewis epitopes. The presence of a core α(1,3)-Fuc and a β(1,2)-Xyl is specific to plant N-glycans, compared to mammal N-glycans [7]. Overall, different types of N-glycans are generated from complex N-glycans, such as hybrid and paucimannose N-glycans (Figure 1).
Figure 1. Some examples of N-glycan structures grafted onto Asn-X-Ser/Thr motifs (with X≠Pro) of plant N-glycoproteins. They all share a core Man3GlcNAc2 structure. The core structure is substituted by two to six Man residues in high-mannose N-glycans. Complex N-glycans comprise a β-1,2-linked Xyl, an α-1,3-linked Fuc residue, and/or one or two β-1,2-linked GlcNAc residues bound to the core. Hybrid N-glycans share common features with high-mannose and complex N-glycans. Paucimannose N-glycans do not exhibit terminal GlcNAc residues. Some complex N-glycans also comprise one out of the two terminal α-1,4-Fuc and β-1,3-Gal residues which form Lewis a epitopes.
The structure of N-glycans has evolved in the green lineage [8][9]. In green algae, other types of N-glycans have been found. In the microalgae Chlorella vulgaris, N-glycans are mostly of the high mannose/oligomannose-type, and they are O-methylated at their non-reducing termini [13]. In the Chlamydomonas rheinardtii green alga, the main N-glycans are of three types: oligomannose N-glycans represent about 70% of the N-glycan population, and complex N-glycans with one or two pentose residues account for 14.1 and 16.6%, respectively [14]. In Penium margaritaceum, a charophycean green alga assumed to be sister to land plants, the same N-glycans as those of flowering plants are found [15]. In the bryophyte Marchantia polymorpha, preliminary results indicate the presence of complex N-glycans with two pentose residues (H Kolkas et al., unpublished results). In the moss Physcomitrella patens, the same types of N-glycans as in flowering plants have been characterized [16]. These results suggest that the whole machinery of N-glycosylation has been established very early in the green lineage and conserved along the evolution.
The importance of N-glycosylation has been stressed by the study of N-glycosylation mutants. The severity of their phenotypes depends on which step of N-glycan biosynthesis is impaired. The more severe phenotypes are observed when the mutation affects the early steps of N-glycan biosynthesis in the ER, especially the biosynthesis of lipid-linked oligosaccharide (LLO) precursors or the multi-subunit oligosaccharyl transferase (OST) complex. Some mutations can be lethal (for reviews, see [11][17]). At later stages of N-glycan biosynthesis, mutations can affect post-seedling development, as in the Oryza sativa N-acetylglucosaminyltransferase 1 (gnt1) mutant, but still allow callus development [18]. The gnt1 mutant is impaired with the addition of the β(1,2)-linked GlcNAc to the core Man(5)GlcNac(2) which is a prerequisite for the synthesis of complex and hybrid N-glycans. On the contrary, when the mutation affects a late stage of N-glycan biosynthesis, such as the grafting of α(1,3)-Fuc of β(1,2)-Xyl by the core xylosyl transferase (XYLT) or fucosyl transferases (FUT11 and FUT12) in A. thaliana, no developmental phenotype has been observed [19].

2. An Overview of the Present N-glycoproteomics Studies

A selection of articles devoted to N-glycoproteomics is presented in Table 1. Several plants have been studied: Marchantia polymorpha [20] as an early divergent plant; Zea mays [21], Triticum aestivum [22] and Brachypodium distachyon [23] as monocot plants; and Fagopyrum tataricum [24], Solanum lycopersicum [25][26][27], Gossypium hirsutum [28], Camellia sinensis [29], Arabidopsis thaliana [30][31][32][33][34][35] and Brassica oleracea [36] as dicot plants. N-glycoproteomes have been described in different organs: whole thalli corresponding to the haploid gametophytic stage of M. polymorpha [20]; seedlings [37]; aerial organs for flowering plants, such as actively growing hypocotyls of etiolated seedlings [31]; leaves [21][22][29][33]; stems [30][33]; inflorescences [35]; fruit pericarp [25][26][27]; and seeds [24][28]. The N-glycoproteome of the xylem sap of B. oleracea has also been analyzed, and looks very similar to a cell wall proteome [36]. Additionally, in a few studies, the N-glycans released by PNGase A, which cleaves N-glycans regardless of the presence of Xyl of Fuc residues, have been analyzed [38][39].
Table 1. A selection of N-glycoproteomes.
The sizes of these N-glycoproteomes are variable, ranging from 62 to 912 identified proteins (Table 1). The final extract which is enriched in N-glycoproteins after lectin affinity chromatography or HILIC contains proteins traveling through the whole secretion pathway from the ER to the Golgi apparatus, including plasma membrane, vacuolar and extracellular proteins. Most of them (from 84% to 100%, Table 1) exhibit the canonical N-glycosylation site (Asn-X-Ser/Thr-X, with X≠Pro) (PS00001, https://prosite.expasy.org/) (accessed on 22 September 2022). Some of them contain the canonical C-terminal motif for retention in the ER.
As mentioned above, combining the predictions of sub-cellular localization and functional domains using several bioinformatic programs allows the inference of the cell wall localization of the identified proteins. The percentage of proteins assumed to be CWPs in these N-glycoproteomes varies from 55.6 to 98.7% (Table 1). The study of N-glycoproteomes, thus, appears as a means to increase the coverage of cell wall proteomes (Figure 2). To illustrate this point, three examples can be mentioned where the same plant material was used to prepare a cell wall proteome from purified cell walls and a N-glycoproteome: the thalli of M. polymorpha [20], the etiolated hypocotyls of A. thaliana [31][40], and the leaves of C. sinensis [29]. In the same way, the xylem sap proteome of B. oleracea was complemented with a N-glycoproteome [36]. These data could be complemented with transcriptomic data for example, but the superimposition of transcriptomic data and cell wall proteomic data has proven to be difficult because of the complexity of the regulation of gene expression at post-transcriptomic levels [41].
Figure 2. Comparison between cell wall proteomes (red) and N-glycoproteomes (green) characterized from the same plant material. In each case, the overall coverage of the cell wall proteome increases by combining the two approaches.

3. The Heterogeneity of Plant N-glycans

All the N-glycans studied are grafted on an Asn amino acid residue, but their monosaccharide composition is variable. In Ma et al. [37], 161 possible structures have been collected in a library to allow the identification of N-glycopeptides and N-glycans in A. thaliana seedlings using MS.
The diversity of N-glycans grafted on a given protein is well-illustrated in the case of the A. thaliana α-xylosidase (AtXYL1, At1g68560) belonging to the glycoside hydrolase family 31 [42]. Eight N-glycosylation sites could be predicted using the Prosite motif (PS00001) on AtXYL1. Among them, five were experimentally found to be occupied [33], and there is no information about the others. Altogether, 19 different N-glycans have been identified in AtXYL1 and 196 N-glycan occurrences have been observed (Figure 3). These N-glycans belong to five classes of N-glycans: A single high mannose glycan is found, as well as one complex N-glycan with a Lewis a epitope. Otherwise, all the identified N-glycans are of the complex-, hybrid-, or paucimannose-type. Major N-glycans could be identified in each class: HexNAc(4)Hex(3)Fuc(1)Pent(1) for complex-type (46 occurrences), HexNAc(3)Hex(3)Pent(1) and HexNAc(3)Hex(3)Fuc(1)Pent(1) for hybrid-type (20 and 31 occurrences, respectively), and HexNAc(2)Hex(3)Fuc(1)Pent(1) for paucimannose-type (46 occurrences).
Figure 3. Diversity of N-glycans on a given protein. This figure uses the MS experimental results related to the At1g68560 protein identified in the A. thaliana rosettes N-glycoproteome described in [33]. At1g68560 exhibits eight predicted N-glycosylation sites, out of which five are shown to be occupied by N-glycans. Nineteen different N-glycans are found, including a single high mannose-type (light blue), a 53 complex-type (dark blue), a 59 hybrid-type (red), an 82 paucimannose-type (green), and a single complex-type with a Lewis a epitope.
In addition, a given N-glycosylation motif can be occupied by different types of N-glycans, and this feature has been called microheterogeneity [33]. Figure 4 illustrates this microheterogenity in the case of the At1g68560 protein. Each of the glycosites can be occupied by a great diversity of N-glycans as illustrated in Figure 4A,B. In each case, three types of N-glycans are always found: hybrid-, complex-, and paucimannose-type. Moreover, for a given glycosite, a major form of each N-glycan type is identified. Figure 4C illustrates this point for one of the glycosites: HexNAc(4)Hex(3)Fuc(1)Pent(1) for complex-type; HexNAc(3)Hex(3)Fuc(1)Pent(1) for hybrid-type; and HexNAc(2)Hex(3)Fuc(1)Pent(1) for paucimannose type. In addition to this particular study, this microheterogeneity has been observed for a tomato recombinant protein called XEGIP (xyloglucan-specific endoglucanases inhibitor) produced in Nicotiana benthamiana leaves, with a collection of high mannose N-glycans (HexNAc(2)(Hex(4-9)) being grafted onto four different N-glycosites [25].
Figure 4. Microheterogeneity of N-glycosylation. This figure uses the MS experimental results related to the At1g68560 protein identified in the A. thaliana rosettes N-glycoproteome described in [33]. (A). Types of N-glycans. Each N-glycan type is associated with a symbol. (B). Description of the eight predicted N-glycopeptides in the amino acid sequence of At1g68560. The Asn (N) residue of the underlined consensus N-glycosylation site (PS00001) is in pink, and the tryptic Lys (K) and Arg (R) recognition sites in light blue. In each case, the consensus N-glycosylation motif is underlined. N-glycans have been found for six out of them. (C). Distribution of the different types of N-glycans in one of the glycopeptides, as indicated by an arrow in B. The green area corresponds to the major N-glycan type in each case, whereas the blue area corresponds to the other types of N-glycans: the high mannose-type is represented once by HexNAc(2)Hex(9) (diamond); the major complex-type is HexNAc(4)Hex(3)Fuc(1)Pent(1) (star); the major hybrid-type is HexNAc(3)Hex(3)Fuc(1)Pent(1) (circle); and the major paucimannose-type is HexNAc(2)Hex(3)Fuc(1)Pent(1) (square).
Different hypotheses have been proposed to explain this heterogeneity. Since glycosylated proteins travel through the secretion pathway and undergo different steps of N-glycan maturation in the ER and the Golgi apparatus [43], they could exhibit different forms of a given N-glycan in different cell compartments. In A. thaliana, a correlation was found between the predicted sub-cellular localization of the N-glycoproteins and their N-glycans [33]. For example, high mannose N-glycans were found to be predominant in proteins predicted to be localized in the ER, whereas extracellular proteins were found to carry complex, hybrid, and paucimannose N-glycan types. Besides, complex N-glycans could be degraded by exoglycosidases in the vacuole or in the extracellular compartment [8]. Paucimannose N-glycans could be partly degraded by β-N-acetylhexosaminidases (HEXO2 and HEXO3) located at the plasma membrane [44] and/or they could be sequentially degraded by bacterial enzymes, such as those of Xanthomonas campestris or Capnocytophaga canimorsus [45][46]. It was also shown that stress, such as a cold treatment of A. thaliana seedlings, could lead to the degradation of high mannose N-glycans of proteins located in the ER [37], and that the amount of some glycopeptides was regulated upon de-etiolation of maize seedling leaves [47].
N-glycosylation can be regulated at different levels. In T. aestivum seedling leaves, the four following motifs were found to be present in plasma membrane-associated proteins and their frequency was found to be modified upon drought stress: Asn-X-Thr (51.2%), Asn-X-Ser (40.0%), Asn-X-Thr-Ala (4.6%), and Ala-Asn-X-Thr (4.2%) with X≠Pro [22]. In Z. mays seedling leaves, two motifs were found: Asn-X-Thr (58%) and Asn-X-Ser (42%) [21]. Ala and Leu were over-represented in the vicinity of both of them. Slightly different proportions of these canonical motifs were found in B. distachyon seedling leaves, with 64% of Asn-X-Thr and 36% of Asn-X-Ser [23]. The higher abundance of N-glycosylated Asn-X-Thr compared to Asn-X-Ser has been attributed to a higher affinity for the oligosaccharide transferase (OST) [48]. It has also been shown that the amino acid at the X position, as well as the one following the Asn-X-Ser/Thr motif, are important for effective N-glycosylation [49][50].

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