Sweet Modifications Modulate Plant Development

Abstract

Plant development represents a continuous process in which the plant undergoes morphological, (epi)genetic and metabolic changes. Starting from pollination, seed maturation and germination, the plant continues to grow and develops specialized organs to survive, thrive and generate offspring. The development of plants and the interplay with its environment are highly linked to glycosylation of proteins and lipids as well as metabolism and signaling of sugars. Although the involvement of these protein modifications and sugars is well-studied, there is still a long road ahead to profoundly comprehend their nature, significance, importance for plant development and the interplay with stress responses. This review, approached from the plants' perspective, aims to focus on some key findings highlighting the importance of glycosylation and sugar signaling for plant development.

Keywords: glycolipids; glycoproteins; glycosylation; plant development; signaling; sugars.

Figure 1

Graphical representation of the most important plant organs. The plant in this figure is generic and does not necessarily represent tomato. For each organ, the most significant phenotypical traits when glycosylation enzymes are knocked-out, knocked-down or over-expressed are highlighted. In the flowering parts, defects in glycosylation cause abnormal development of anthers and pistils, pollen tube germination and elongation, and defective gametogenesis which often leads to sterility. At the level of the fruit, glycosylation enzymes are important for fruit ripening and softening. Seeds show aberrant seed morphology, seed set, (embryo) lethality and cell wall defects when the expression of one or more glycosylation enzymes is disturbed. Vegetative tissues such as the leaves and the roots also experience morphological changes due to aberrant protein glycosylation. This figure was created with BioRender.com.

Figure 2

Overview of the most important glycosylated structures in the plant cell. N-glycan synthesis initiates in the endoplasmic reticulum, after which the glycan is added onto a polypeptide. Well-folded proteins are then guided towards the Golgi apparatus through vesicular transport, where the glycan structure is modified. After glycan maturation in the Golgi, glycoproteins are transported towards the vacuole, plasma membrane, cell wall or secreted. O-glycosylation occurs mainly in the Golgi apparatus. The O-GlcNAc modification takes place in the nucleus and cytoplasm. This figure was created with BioRender.com.

Figure 3

Graphical representation of a generic flower and phenotypes caused by impaired activity of glycosylation enzymes or glycoproteins. Disturbances cause phenotypes in both male and female gametes, anthers, pollen and pollen sacs, pollen germination and pollen tube elongation. Abbreviations: APTG1 (ABNORMAL POLLEN TUBE GUIDANCE1), EVN (EVAN), FucT (α-1,3-fucosyltransferase), GFAT1 (glutamine:fructose-6-phosphate amidotransferase), GlcNAc.UT (GlcNAc-phosphate UDP-transferase), HAP6 (HAPLESS6), MTR1 (MICROSPORE AND TAPETUM REGULATOR1), OFT (O-fucosyltransferase), PELP (Pistil-Specific Extensin-Like Proteins), SCR (S-locus Cysteine Rich), SRK (S-locus Receptor Kinase), TTSO (Transmitting Tissue Specific O-glycoprotein), TUN (TURAN), USP (UDP-sugar pyrophosphorylase). This figure was created with BioRender.com.

Figure 4

Graphical representation of the glycosylation-related enzymes and their role in fruit ripening and seed development and germination. For fruits, specific glycan-degrading enzymes and CAZymes are important for ripening and softening. Defects in glycosylation enzymes cause aberrant seed morphologies, cell wall shortcomings, embryonal defects, (embryo)lethality and reduced seed set. For the germinating seed, disturbed glycosylation enzymes will postpone germination, reduce germination capacity or will yield unviable seeds. Additionally, the glycosylation state of endosperm glycoproteins will cause certain developmental phenotypes. Abbreviations: ACINUS (Apoptotic Chromatin condensation Inducer in the Nucleus), AGPs (arabinogalactan proteins), α-MAN (α-mannosidase), β-NAHase (β-N-acetylhexosaminidase), CAZymes (carbohydrate-active enzymes), CYT1 (GTP:α-D-mannose-1-phosphate guanylyltransferase), DER1 (DEGRADATION IN THE ENDOPLASMIC RETICULUM1), DGL1 (DEFECTIVE IN GLYCOSYLATION1), DPMS1 (dolichol phosphate mannose synthase complex 1), ENGase (endo-N-acetyl-β-D-glucosaminidase), FucT (α-1,3-fucosyltransferase), GALT (galactosyltransferase), GCSI (α-glucosidase I), GCSII (α-glucosidase II), GlcNAc.UT (GlcNAc-phosphate UDP-transferase), GnT1 (N-acetylglucosaminyltransferase I), KNF (KNOPF), LEW3 (Leaf Wilting 3), MN1 (Miniature1), MNS1 (mannosidase I), PNGase (peptide-N4-(N-acetyl-β-D-glucosaminyl) asparagine amidase), RCN11 (Reduced Culm Number 11), RSW1 (RADIALLY SWOLLEN1), SEC (SECRET AGENT), SPY (SPINDLY), XTH (xyloglucan endotransglycosylase/hydrolase). This figure was created with BioRender.com.

Figure 5

Graphical representation of the glycosylation-related enzymes and their role in leaf development, trichome morphology and root (hair) development. Both abnormal N-glycosylation and O-glycosylation result in changes of phenotype and morphology. Abbreviations: ALG10 (α-1,2-glucosyltransferase 10), BZ1 (Brittle stem and Zebra Leaf 1), DGL1 (DEFECTIVE IN GLYCSOYLATION1), ExAD (extensin arabinose deficient transferase), FUCTc (α1,4-fucosyltransferase), GALT (β1,3-galactosyl-transferase), GLCAT (β-glucuronosyltransferases), GnT1 (N-acetylglucosaminyltransferase I), HPAT1-2 (Hyp O-arabinosyltransferases 1 and 2), HPGT (Hydroxyproline O-galactosyltransferase), Hyp-O-GALT (hydroxyproline-O-β-galactosyltransferase), MANII (α-mannosidase II), MNS (α-mannosidase I), MOGS (mannosyloligosaccharide glucosidase), OST3/6 (oligosaccharyltransferase subunit 3/6), P4H (prolyl 4-hydroxylase), PSL (premature senescence leaf), RAY1 (REDUCED ARABINOSE YARIV1), RRA (REDUCED RESIDUAL ARABINOSE), SEC (SECRET AGENT), SGT (serine O-α-galactosyltransferase), SPY (SPINDLY), STT3a (STAUROSPORIN AND TEMPERATURE SENSITIVE3A), XEG113 (Xylo-endoglucanase113). This figure was created with BioRender.com.

Figure 6

Scheme illustrating the links between sugar metabolism/signaling and glycosylation and the trade-off between growth and stress responses. The figure illustrates the effect of sugar metabolism and signaling during unstressed conditions and stressed conditions in terms of sugar availability. Under non-stressed conditions, photosynthesis provides sugars to be used in metabolism and directly in glycosylation reactions. Sugar availability stimulates Target of Rapamycin (TOR), promoting growth and development and inhibiting stress responses. Sugar availability can also directly influence glycosylation by serving as the substrates, for instance through O-GlcNAc transferases (OGTs). Invertases (INVs) are key components, specifically in sink tissue, to convert sucrose to metabolizable hexoses. Under these conditions, Snf1-related protein kinase 1 (SnRK1) is inhibited by trehalose-6-phosphate (T6P). When exposed to severe stresses, photosynthesis is hampered, resulting in sugar deprivation, reflected through T6P levels (mirror sucrose levels). Low T6P results in an active SnRK1, inhibiting growth and possibly also glycosylation by regulating OGTs as is the case in animals. Active SnRK1 also promotes stress responses. It is important to note that mild abiotic stresses result in temporal leaf sweetening which can also potentially stimulate SnRK1 and/or stress responses. During sugar deprivation, TOR is typically inactive. Apart from sugar signaling pathways, limited sugar availability can also directly hamper glycosylation due to limited substrate availability and low energy levels. It is unclear whether a sugar sensor exists that translates sugar availability to glycosylation reactions in plants; however, candidates include OGTs themselves or SnRK1, since this appears to be the case in animals. In animals, AMP-activate protein kinase (AMPK), the homolog of SnRK1, and OGTs co-regulate one another to alter their activities and localization. It is important to note that glycosylation will never be completely inhibited even under severe stresses, as a low level of glycosylation is also important during these conditions. Arrows with arrow heads indicate stimulatory effects whereas arrows with blunt ends indicate inhibitory effects. Solid lines are known effects and dashed lines predicted effects. Grey arrows indicate an inactive pathway under a specific condition. This figure was created with BioRender.com.