Exploring the Role of Cell Wall-Related Genes and Polysaccharides during Plant Development

Abstract

The majority of organs in plants are not established until after germination, when pluripotent stem cells in the growing apices give rise to daughter cells that proliferate and subsequently differentiate into new tissues and organ primordia. This remarkable capacity is not only restricted to the meristem, since maturing cells in many organs can also rapidly alter their identity depending on the cues they receive. One general feature of plant cell differentiation is a change in cell wall composition at the cell surface. Historically, this has been viewed as a downstream response to primary cues controlling differentiation, but a closer inspection of the wall suggests that it may play a much more active role. Specific polymers within the wall can act as substrates for modifications that impact receptor binding, signal mobility, and cell flexibility. Therefore, far from being a static barrier, the cell wall and its constituent polysaccharides can dictate signal transmission and perception, and directly contribute to a cell's capacity to differentiate. In this review, we re-visit the role of plant cell wall-related genes and polysaccharides during various stages of development, with a particular focus on how changes in cell wall machinery accompany the exit of cells from the stem cell niche.

Keywords: cell wall; development; differentiation; glycosyl hydrolase; glycosyltransferase; polysaccharide; root meristem; shoot meristem.

Figure 1

Detection of different cell wall components in distinct tissues of Arabidopsis thaliana, Hordeum vulgare (barley), Oryza sativa (rice), Cicer arietinum (chickpea), Vitis vinifera (grape), Nicotiana benthamiana (tobacco), and Triticum aestivum (bread wheat). The tissue origin of each section is indicated at the bottom left of each panel. The antibody or stain is indicated at the top left of each panel. Labelling of polymers was achieved through the use of diverse antibodies including BG1 (1,3;1,4-β-glucan), JIM13 (arabinogalactan proteins, AGP), LM19 (homogalacturonan, HG), LM20 (methylesterified homogalacturonan, meHG), callose (1,3-β-glucan), LM15 (mannan), LM6 (arabinan), LM11 (arabinoxylan), and CBM3a (cellulose), or stains such as aniline blue (1,3-β-glucan) and Calcofluor White (β-glycan), or UV autofluorescence. Differential contrast (DIC) microscopy was used to image the barley root tip and is shown as a reference for the adjoining immunolabelled sample. Images were generated for this review, but further details can be found in previous studies [23,29,30,31,32]. Scale bar dimensions are shown in µm.

Figure 2

Cell wall components that contribute to growth, development, and differentiation. The model shows polymers superimposed on a TEM image of a leaf cell wall, including 1,3;1,4-β-glucan (MLG), cellulose, xyloglucan (XG), mannan, callose, and pectin. Enzymes that contribute to the biosynthesis or modification of these components are shown. The spatial separation of polymers is only shown for schematic purposes. Biosynthetic enzymes are shown in blue, hydrolytic enzymes are shown in purple, receptors are shown in orange, mobile transcription factors are shown in white, pectin methylesterase (PME) is shown in green, and arabinogalactan protein (AGPs) in pink. Deposition and hydrolysis of callose at the neck of plasmodesmata (PD) can alter the size exclusion limit (SEL) of the PD, hence limiting the mobility of intercellular signaling molecules such as transcription factors (e.g., WUSCHEL [59], SHORT ROOT [60], and KNOTTED [61]), microRNAs (miRNAs [60,62]), and short interfering RNAs (siRNAs [63,64]). Hydrolysis of callose by GH17 enzymes leads to the release of stimulatory oligosaccharides (OS) from the glucan backbone in fungi, but it remains unclear if similar OS contribute to growth and development in plants. By contrast, release of oligogalacturonides (OG) from pectin by polygalacturonase (PG) has been implicated in plant development through antagonistic effects on auxin pathways. The small circles on XG indicate galactosyl residues present due to the activity of XLT2 (xyloglucan galactosyltransferase). GT8 family enzymes contribute to the biosynthesis of pectin, which is usually synthesized in a methylesterified form (e.g., methylesterified homogalacturonan; meHG). Removal of methylesters (red hexagons) through the activity of PME can lead to calcium binding and subsequent cross-linking of pectin polysaccharides, which influences wall stiffness. GT, glycosyltransferase, XXT, xylosyltransferase, MTH, mannan transglycosylase/hydrolase, XTH, xyloglucan transglycosylase/hydrolase, CslF, cellulose synthase-like F, CslA, cellulose synthase-like A, GH, glycosyl hydrolase, WAK, wall-associated kinase, ERU, ERULUS receptor-like kinase.

Figure 3

Analysis of cell wall-related gene expression during differentiation of stem cells in the root and shoot meristem of Arabidopsis thaliana. The upper panels in (a,b) show schematic representations of the root and shoot apical meristem [120]. (a) In the root meristem, initial cells (stem cells) directly adjoining the QC enter differentiation pathways as they divide away from the niche (shown by arrows for columella and lateral root cap). V, vasculature, Vi, vascular initial, QC, quiescent centre, E, endodermis, C, cortex, CEi, cortex/endodermis initials, Epi, epidermal initials, Ep, epidermis, LRi, lateral root cap initial, LRC, lateral root cap, Ci, columella initial, Co, columella. (b) In the shoot meristem, the organizing center (OC) functions via WUSCHEL (WUS) to maintain the stem cells (SC) in an undifferentiated state. The stem cells express the signal peptide CLAVATA3 (CLV3). Divisions of the stem cells provide daughters that enter differentiation pathways at the flanks of the meristem and become organ primordia (OP), which is marked by expression of genes such as FILAMENTOUS FLOWER (FIL). The second row of panels highlights gene families encoding CAZy carbohydrate-related enzymes [42] that are enriched in each meristem cell type according to FACS-mediated sorting and transcriptional profiling [118,119]. The genes are superimposed on sections of root and shoot meristem tissues. Family names in bold indicate that multiple members from the same family were up-regulated in the QC or OC (depending on the meristem) relative to both of the other cell types. GH, glycosyl hydrolase, GT, glycosyltransferase, PL, pectate lyase, AGP, arabinogalactan protein, EXP, expansin, CE, carbohydrate esterase, FLA, fasciclin-like arabinogalactan protein. See Table 1 for putative functions of enzyme families. The third row of panels shows expression patterns of selected CAZy family members in the different meristem cell types. Several of the individual genes reflect the behavior of the entire family. For example, At1g02360 is up-regulated in the columella and LRC relative to the OC, and this is a pattern shown for many GH19 family members. However, other genes such as At3g47400, At3g10720, and At4g02130 show unique patterns compared to other members of their families. The reason why multiple family members are recruited into some cell-type preferential expression pathways, while in others only individual members are expressed, remains to be elucidated.