Dataset Information

Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice.

ABSTRACT: Golgi-localized nucleotide sugar transporters (NSTs) are considered essential for the biosynthesis of wall polysaccharides and glycoproteins based on their characteristic transport of a large number of nucleotide sugars to the Golgi lumen. The lack of NST mutants in plants has prevented evaluation of this hypothesis in plants. A previously undescribed Golgi NST mutant, brittle culm14 (bc14), displays reduced mechanical strength caused by decreased cellulose content and altered wall structure, and exhibits abnormalities in plant development. Map-based cloning revealed that all of the observed mutant phenotypes result from a missense mutation in a putative NST gene, Oryza sativa Nucleotide Sugar Transporter1 (OsNST1). OsNST1 was identified as a Golgi-localized transporter by analysis of a fluorescence-tagged OsNST1 expressed in rice protoplast cells and demonstration of UDP-glucose transport activity via uptake assays in yeast. Compositional sugar analyses in total and fractionated wall residues of wild-type and bc14 culms showed a deficiency in the synthesis of glucoconjugated polysaccharides in bc14, indicating that OsNST1 supplies the glucosyl substrate for the formation of matrix polysaccharides, and thereby modulates cellulose biosynthesis. OsNST1 is ubiquitously expressed, with high expression in mechanical tissues. The inferior mechanical strength and abnormal development of bc14 plants suggest that OsNST1 has pleiotropic effects on cell wall biosynthesis and plant growth. Identification of OsNST1 has improved our understanding of how cell wall polysaccharide synthesis is regulated by Golgi NSTs in plants.

SUBMITTER: Zhang B

PROVIDER: S-EPMC3064376 | biostudies-literature | 2011 Mar

REPOSITORIES: biostudies-literature

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Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice.

Zhang Baocai B Liu Xiangling X Qian Qian Q Liu Lifeng L Dong Guojun G Xiong Guangyan G Zeng Dali D Zhou Yihua Y

Proceedings of the National Academy of Sciences of the United States of America 20110307 12

Golgi-localized nucleotide sugar transporters (NSTs) are considered essential for the biosynthesis of wall polysaccharides and glycoproteins based on their characteristic transport of a large number of nucleotide sugars to the Golgi lumen. The lack of NST mutants in plants has prevented evaluation of this hypothesis in plants. A previously undescribed Golgi NST mutant, brittle culm14 (bc14), displays reduced mechanical strength caused by decreased cellulose content and altered wall structure, an ...[more]

PMID: 21383162

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Project description:Photosynthesis is the final determinator for crop yield. To gain insight into genes controlling photosynthetic capacity, we selected from our large T-DNA mutant population a rice stunted growth mutant with decreased carbon assimilate and yield production named photoassimilate defective1 (phd1). Molecular and biochemical analyses revealed that PHD1 encodes a novel chloroplast-localized UDP-glucose epimerase (UGE), which is conserved in the plant kingdom. The chloroplast localization of PHD1 was confirmed by immunoblots, immunocytochemistry, and UGE activity in isolated chloroplasts, which was approximately 50% lower in the phd1-1 mutant than in the wild type. In addition, the amounts of UDP-glucose and UDP-galactose substrates in chloroplasts were significantly higher and lower, respectively, indicating that PHD1 was responsible for a major part of UGE activity in plastids. The relative amount of monogalactosyldiacylglycerol (MGDG), a major chloroplast membrane galactolipid, was decreased in the mutant, while the digalactosyldiacylglycerol (DGDG) amount was not significantly altered, suggesting that PHD1 participates mainly in UDP-galactose supply for MGDG biosynthesis in chloroplasts. The phd1 mutant showed decreased chlorophyll content, photosynthetic activity, and altered chloroplast ultrastructure, suggesting that a correct amount of galactoglycerolipids and the ratio of glycolipids versus phospholipids are necessary for proper chloroplast function. Downregulated expression of starch biosynthesis genes and upregulated expression of sucrose cleavage genes might be a result of reduced photosynthetic activity and account for the decreased starch and sucrose levels seen in phd1 leaves. PHD1 overexpression increased photosynthetic efficiency, biomass, and grain production, suggesting that PHD1 plays an important role in supplying sufficient galactolipids to thylakoid membranes for proper chloroplast biogenesis and photosynthetic activity. These findings will be useful for improving crop yields and for bioenergy crop engineering.

Project description:Nucleotide-diphospho-sugars (NDP-sugars) are the building blocks of diverse polysaccharides and glycoconjugates in all organisms. In plants, 11 families of NDP-sugar interconversion enzymes (NSEs) have been identified, each of which interconverts one NDP-sugar to another. While the functions of these enzyme families have been characterized in various plants, very little is known about their evolution and origin. Our phylogenetic analyses indicate that all the 11 plant NSE families are distantly related and most of them originated from different progenitor genes, which have already diverged in ancient prokaryotes. For instance, all NSE families are found in the lower land plant mosses and most of them are also found in aquatic algae, implicating that they have already evolved to be capable of synthesizing all the 11 different NDP-sugars. Particularly interesting is that the evolution of RHM (UDP-L-rhamnose synthase) manifests the fusion of genes of three enzymatic activities in early eukaryotes in a rather intriguing manner. The plant NRS/ER (nucleotide-rhamnose synthase/epimerase-reductase), on the other hand, evolved much later from the ancient plant RHMs through losing the N-terminal domain. Based on these findings, an evolutionary model is proposed to explain the origin and evolution of different NSE families. For instance, the UGlcAE (UDP-D-glucuronic acid 4-epimerase) family is suggested to have evolved from some chlamydial bacteria. Our data also show considerably higher sequence diversity among NSE-like genes in modern prokaryotes, consistent with the higher sugar diversity found in prokaryotes. All the NSE families are widely found in plants and algae containing carbohydrate-rich cell walls, while sporadically found in animals, fungi and other eukaryotes, which do not have or have cell walls with distinct compositions. Results of this study were shown to be highly useful for identifying unknown genes for further experimental characterization to determine their functions in the synthesis of diverse glycosylated molecules.

Dataset Information

Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice.

Publications

Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice.

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