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91.
Yanbin Yin Huiling Chen Michael G. Hahn Debra Mohnen Ying Xu 《Plant physiology》2010,153(4):1729-1746
Carbohydrate-active enzyme glycosyltransferase family 8 (GT8) includes the plant galacturonosyltransferase1-related gene family of proven and putative α-galacturonosyltransferase (GAUT) and GAUT-like (GATL) genes. We computationally identified and investigated this family in 15 fully sequenced plant and green algal genomes and in the National Center for Biotechnology Information nonredundant protein database to determine the phylogenetic relatedness of the GAUTs and GATLs to other GT8 family members. The GT8 proteins fall into three well-delineated major classes. In addition to GAUTs and GATLs, known or predicted to be involved in plant cell wall biosynthesis, class I also includes a lower plant-specific GAUT and GATL-related (GATR) subfamily, two metazoan subfamilies, and proteins from other eukaryotes and cyanobacteria. Class II includes galactinol synthases and plant glycogenin-like starch initiation proteins that are not known to be directly involved in cell wall synthesis, as well as proteins from fungi, metazoans, viruses, and bacteria. Class III consists almost entirely of bacterial proteins that are lipooligo/polysaccharide α-galactosyltransferases and α-glucosyltransferases. Sequence motifs conserved across all GT8 subfamilies and those specific to plant cell wall-related GT8 subfamilies were identified and mapped onto a predicted GAUT1 protein structure. The tertiary structure prediction identified sequence motifs likely to represent key amino acids involved in catalysis, substrate binding, protein-protein interactions, and structural elements required for GAUT1 function. The results show that the GAUTs, GATLs, and GATRs have a different evolutionary origin than other plant GT8 genes, were likely acquired from an ancient cyanobacterium (Synechococcus) progenitor, and separate into unique subclades that may indicate functional specialization.Plant cell walls are composed of three principal types of polysaccharides: cellulose, hemicellulose, and pectin. Studying the biosynthesis and degradation of these biopolymers is important because cell walls have multiple roles in plants, including providing structural support to cells and defense against pathogens, serving as cell-specific developmental and differentiation markers, and mediating or facilitating cell-cell communication. In addition to their important roles within plants, cell walls also have many economic uses in human and animal nutrition and as sources of natural textile fibers, paper and wood products, and components of fine chemicals and medicinal products. The study of the biosynthesis and biodegradation of plant cell walls has become even more significant because cell walls are the major components of biomass (Mohnen et al., 2008), which is the most promising renewable source for the production of biofuels and biomaterials (Ragauskas et al., 2006; Pauly and Keegstra, 2008). Analyses of fully sequenced plant genomes have revealed that they encode hundreds or even thousands of carbohydrate-active enzymes (CAZy; Henrissat et al., 2001; Yokoyama and Nishitani, 2004; Geisler-Lee et al., 2006). Most of these CAZy enzymes (Cantarel et al., 2009) are glycosyltransferases (GTs) or glycoside hydrolases, which are key players in plant cell wall biosynthesis and modification (Cosgrove, 2005).The CAZy database is classified into 290 protein families (www.cazy.org; release of September 2008), of which 92 are GT families (Cantarel et al., 2009). A number of the GT families have been previously characterized to be involved in plant cell wall biosynthesis. For example, the GT2 family is known to include cellulose synthases and some hemicellulose backbone synthases (Lerouxel et al., 2006), such as mannan synthases (Dhugga et al., 2004; Liepman et al., 2005), putative xyloglucan synthases (Cocuron et al., 2007), and mixed linkage glucan synthases (Burton et al., 2006). With respect to the synthesis of xylan, a type of hemicellulose, four Arabidopsis (Arabidopsis thaliana) proteins from the GT43 family, irregular xylem 9 (IRX9), IRX14, IRX9-L, and IRX14-L, and two proteins from the GT47 family, IRX10 and IRX10-L, are candidates (York and O''Neill, 2008) for glucuronoxylan backbone synthases (Brown et al., 2007, 2009; Lee et al., 2007a; Peña et al., 2007; Wu et al., 2009). In addition, three proteins have been implicated in the synthesis of an oligosaccharide thought to act either as a primer or terminator in xylan synthesis (Peña et al., 2007): two from the GT8 family (IRX8/GAUT12 [Persson et al., 2007] and PARVUS/GATL1 [Brown et al., 2007; Lee et al., 2007b]) and one from the GT47 family (FRA8/IRX7 [Zhong et al., 2005]).The GT families involved in the biosynthesis of pectins have been relatively less studied until recently. In 2006, a gene in CAZy family GT8 was shown to encode a functional homogalacturonan α-galacturonosyltransferase, GAUT1 (Sterling et al., 2006). GAUT1 belongs to a 25-member gene family in Arabidopsis, the GAUT1-related gene family, that includes two distinct but closely related families, the galacturonosyltransferase (GAUT) genes and the galacturonosyltransferase-like (GATL) genes (Sterling et al., 2006). Another GAUT gene, GAUT8/QUA1, has been suggested to be involved in pectin and/or xylan synthesis, based on the phenotypes of plant lines carrying mutations in this gene (Bouton et al., 2002; Orfila et al., 2005). It has further been suggested that multiple members of the GT8 family are galacturonosyltransferases involved in pectin and/or xylan biosynthesis (Mohnen, 2008; Caffall and Mohnen, 2009; Caffall et al., 2009).Aside from the 25 GAUT and GATL genes, Arabidopsis has 16 other family GT8 genes, according to the CAZy database, which do not seem to have the conserved sequence motifs found in GAUTs and GATLs: HxxGxxKPW and GLG (Sterling et al., 2006). Eight of these 16 genes are annotated as galactinol synthase (GolS) by The Arabidopsis Information Resource (TAIR; www.arabidopsis.org), and three of these AtGolS enzymes have been implicated in the synthesis of raffinose family oligosaccharides that are associated with stress tolerance (Taji et al., 2002). The other eight Arabidopsis GT8 genes are annotated as plant glycogenin-like starch initiation proteins (PGSIPs) in TAIR. PGSIPs have been proposed to be involved in the synthesis of primers necessary for starch biosynthesis (Chatterjee et al., 2005). Hence, the GT8 family is a protein family consisting of enzymes with very distinct proven and proposed functions. Indeed, a suggestion has been made to split the GT8 family into two groups (Sterling et al., 2006), namely, the cell wall biosynthesis-related genes (GAUTs and GATLs) and the non-cell wall synthesis-related genes (GolSs and PGSIPs).We are interested in further defining the functions of the GAUT and GATL proteins in plants, in particular their role(s) in plant cell wall synthesis. The apparent disparate functions of the GT8 family (i.e. the GAUTs and GATLs as proven and putative plant cell wall polysaccharide biosynthetic α-galacturonosyltransferases, the eukaryotic GolSs as α-galactosyltransferases that synthesize the first step in the synthesis of the oligosaccharides stachyose and raffinose, the putative PGSIPs, and the large bacterial GT8 family of diverse α-glucosyltransferases and α-galactosyltransferases involved in lipopolysaccharide and lipooligosaccharide synthesis) indicate that the GT8 family members are involved in several unique types of glycoconjugate and glycan biosynthetic processes (Yin et al., 2010). This observation led us to ask whether any of the GT8 family members are sufficiently closely related to GAUT and GATL genes to be informative regarding GAUT or GATL biosynthetic function(s) and/or mechanism(s).To investigate the relatedness of the members of the GT8 gene family, we carried out a detailed phylogenetic analysis of the entire GT8 family in 15 completely sequenced plant and green algal genomes (Abbreviation Clade Species Genome Published Downloaded from mpc Green algae Micromonas pusilla CCMP1545 Worden et al. (2009) JGI version 2.0 mpr Green algae Micromonas strain RCC299 Worden et al. (2009) JGI version 2.0 ol Green algae Ostreococcus lucimarinus Palenik et al. (2007) JGI version 1.0 ot Green algae Ostreococcus tauri Derelle et al. (2006) JGI version 1.0 cr Green algae Chlamydomonas reinhardtii Merchant et al. (2007) JGI version 3.0 vc Green algae Volvox carteri f. nagariensis No JGI version 1.0 pp Moss Physcomitrella patens ssp. patens Rensing et al. (2008) JGI version 1.1 sm Spike moss Selaginella moellendorffii No JGI version 1.0 pt Dicot Populus trichocarpa Tuskan et al. (2006) JGI version 1.1 at Dicot Arabidopsis thaliana Arabidopsis Genome Initiative (2000) TAIR version 9.0 vv Dicot Vitis vinifera Jaillon et al. (2007) http://www.genoscope.cns.fr/ gm Dicot Glycine max Schmutz et al. (2010) JGI version 1.0 os Monocot Oryza sativa Goff et al. (2002); Yu et al. (2002) TIGR version 6.1 sb Monocot Sorghum bicolor Paterson et al. (2009) JGI version 1.0 bd Monocot Brachypodium distachyon Vogel et al. (2010) JGI version 1.0