A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex

Journal of Biological Chemistry - Tập 293 - Trang 19047-19063 - 2018
Robert A. Amos1,2, Sivakumar Pattathil1, Jeong-Yeh Yang1, Melani A. Atmodjo1,2, Breeanna R. Urbanowicz1, Kelley W. Moremen1,2, Debra Mohnen1,2
1Complex Carbohydrate Research Center and University of Georgia, Athens, Georgia 30602
2The Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia, 30602

Tài liệu tham khảo

Atmodjo, 2013, Evolving views of pectin biosynthesis, Annu. Rev. Plant Biol, 64, 747, 10.1146/annurev-arplant-042811-105534 Tan, 2013, An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein, Plant Cell, 25, 270, 10.1105/tpc.112.107334 Cosgrove, 2016, Catalysts of plant cell wall loosening, F1000Res, 5, 10.12688/f1000research.7180.1 Voxeur, 2016, Cell wall integrity signaling in plants: “To grow or not to grow that's the question”, Glycobiology, 26, 950, 10.1093/glycob/cww029 Dick-Pérez, 2011, Structure and interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR, Biochemistry, 50, 989, 10.1021/bi101795q Wang, 2012, Pectin-cellulose interactions in the Arabidopsis primary cell wall from two-dimensional magic-angle-spinning solid-state nuclear magnetic resonance, Biochemistry, 51, 9846, 10.1021/bi3015532 Wang, 2016, Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls, J. Exp. Bot, 67, 503, 10.1093/jxb/erv416 Lionetti, 2010, Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion, Proc. Natl. Acad. Sci. U.S.A, 107, 616, 10.1073/pnas.0907549107 Chung, 2014, Deletion of a gene cluster encoding pectin degrading enzymes in Caldicellulosiruptor bescii reveals an important role for pectin in plant biomass recalcitrance, Biotechnol. Biofuels, 7, 147, 10.1186/s13068-014-0147-1 Biswal, 2018, Working towards recalcitrance mechanisms: increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase12 (GAUT12) causes increased recalcitrance and decreased growth in Populus, Biotechnol. Biofuels, 11, 9, 10.1186/s13068-017-1002-y Biswal, 2015, Downregulation of GAUT12 in Populus deltoides by RNA silencing results in reduced recalcitrance, increased growth and reduced xylan and pectin in a woody biofuel feedstock, Biotechnol. Biofuels, 8, 41, 10.1186/s13068-015-0218-y Biswal, 2018, Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis, Nat. Biotechnol, 36, 249, 10.1038/nbt.4067 Lombard, 2014, The carbohydrate-active enzymes database (CAZy) in 2013, Nucleic Acids Res, 42, D490, 10.1093/nar/gkt1178 Sterling, 2006, Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase, Proc. Natl. Acad. Sci. U.S.A, 103, 5236, 10.1073/pnas.0600120103 Atmodjo, 2011, Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex, Proc. Natl. Acad. Sci. U.S.A, 108, 20225, 10.1073/pnas.1112816108 Petersen, 2009, Assay and heterologous expression in Pichia pastoris of plant cell wall type-II membrane anchored glycosyltransferases, Glycoconj. J, 26, 1235, 10.1007/s10719-009-9242-0 Culbertson, 2015, The glycosyltransferases involved in synthesis of plant cell wall polysaccharides: present and future, JSM Enzymol. Protein Sci, 1 Wu, 2010, Functional identification of two nonredundant Arabidopsis α(1,2)fucosyltransferases specific to arabinogalactan proteins, J. Biol. Chem, 285, 13638, 10.1074/jbc.M110.102715 Geshi, 2013, A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in Arabidopsis, Plant J, 76, 128 Liwanag, 2012, Pectin biosynthesis: GALS1 in Arabidopsis thaliana is a β-1,4-galactan β-1,4-galactosyltransferase, Plant Cell, 24, 5024, 10.1105/tpc.112.106625 Chiniquy, 2012, XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan, Proc. Natl. Acad. Sci. U.S.A, 109, 17117, 10.1073/pnas.1202079109 Knoch, 2013, A β-glucuronosyltransferase from Arabidopsis thaliana involved in biosynthesis of type II arabinogalactan has a role in cell elongation during seedling growth, Plant J, 76, 1016, 10.1111/tpj.12353 Basu, 2013, Functional identification of a hydroxyproline-o-galactosyltransferase specific for arabinogalactan protein biosynthesis in Arabidopsis, J. Biol. Chem, 288, 10132, 10.1074/jbc.M112.432609 Urbanowicz, 2014, Two Arabidopsis proteins synthesize acetylated xylan in vitro, Plant J, 80, 197, 10.1111/tpj.12643 Urbanowicz, 2017, Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism, Plant J, 91, 931, 10.1111/tpj.13628 Meng, 2013, Enzymatic basis for N-glycan sialylation: structure of rat α2,6-sialyltransferase (ST6GAL1) reveals conserved and unique features for glycan sialylation, J. Biol. Chem, 288, 34680, 10.1074/jbc.M113.519041 Praissman, 2014, B4GAT1 is the priming enzyme for the LARGE-dependent functional glycosylation of α-dystroglycan, eLife, 3, 10.7554/eLife.03943 Praissman, 2016, The functional O-mannose glycan on α-dystroglycan contains a phospho-ribitol primed for matriglycan addition, eLife, 5, 10.7554/eLife.14473 Subedi, 2015, High yield expression of recombinant human proteins with the transient transfection of HEK293 cells in suspension, J. Vis. Exp, 10.3791/53568 Halmo, 2017, Protein O-linked mannose β-1,4-N-acetylglucosaminyl-transferase 2 (POMGNT2) is a gatekeeper enzyme for functional glycosylation of α-dystroglycan, J. Biol. Chem, 292, 2101, 10.1074/jbc.M116.764712 Sheikh, 2017, Rapid screening of sugar-nucleotide donor specificities of putative glycosyltransferases, Glycobiology, 27, 206, 10.1093/glycob/cww114 Moremen, 2018, Expression system for structural and functional studies of human glycosylation enzymes, Nat. Chem. Biol, 14, 156, 10.1038/nchembio.2539 Kellokumpu, 2016, Glycosyltransferase complexes in eukaryotes: long-known, prevalent but still unrecognized, Cell Mol. Life Sci, 73, 305, 10.1007/s00018-015-2066-0 Oikawa, 2013, Golgi-localized enzyme complexes for plant cell wall biosynthesis, Trends Plant Sci, 18, 49, 10.1016/j.tplants.2012.07.002 Zeng, 2016, Asparagus IRX9, IRX10, and IRX14A are components of an active xylan backbone synthase complex that forms in the Golgi apparatus, Plant Physiol, 171, 93, 10.1104/pp.15.01919 Jiang, 2016, Composition, assembly, and trafficking of a wheat xylan synthase complex, Plant Physiol, 170, 1999, 10.1104/pp.15.01777 Yasui, 2009, In vitro synthesis of polygalacturonic acid, 167 Akita, 2002, Successive glycosyltransfer activity and enzymatic characterization of pectic polygalacturonate 4-α-galacturonosyltransferase solubilized from pollen tubes of Petunia axillaris using pyridylaminated oligogalacturonates as substrates, Plant Physiol, 130, 374, 10.1104/pp.005587 Doong, 1998, Solubilization and characterization of a galacturonosyltransferase that synthesizes the pectic polysaccharide homogalacturonan, Plant J, 13, 363, 10.1046/j.1365-313X.1998.00042.x Ishii, 2002, A sensitive and rapid bioassay of homogalacturonan synthase using 2-aminobenzamide-labeled oligogalacturonides, Plant Cell Physiol, 43, 1386, 10.1093/pcp/pcf150 Scheller, 1999, Pectin biosynthesis: a solubilized α1,4-galacturonosyltransferase from tobacco catalyzes the transfer of galacturonic acid from UDP-galacturonic acid onto the non-reducing end of homogalacturonan, Planta, 207, 512, 10.1007/s004250050511 Persson, 2001, Crystal structure of the retaining galactosyltransferase LgtC from Neisseria meningitidis in complex with donor and acceptor sugar analogs, Nat. Struct. Biol, 8, 166, 10.1038/84168 Gibbons, 2002, Crystal structure of the autocatalytic initiator of glycogen biosynthesis, glycogenin, J. Mol. Biol, 319, 463, 10.1016/S0022-2836(02)00305-4 Cornish-Bowden, 2012, 210 Piszkiewicz, 1977, 97 Chaikuad, 2011, Conformational plasticity of glycogenin and its maltosaccharide substrate during glycogen biogenesis, Proc. Natl. Acad. Sci. U.S.A, 108, 21028, 10.1073/pnas.1113921108 Ly, 2002, Mechanistic studies of a retaining α-galactosyltransferase from Neisseria meningitidis, Biochemistry, 41, 5075, 10.1021/bi012031s Doong, 1995, Cell-free synthesis of pectin (identification and partial characterization of polygalacturonate 4-α-galacturonosyltransferase and its products from membrane preparations of tobacco cell-suspension cultures), Plant Physiol, 109, 141, 10.1104/pp.109.1.141 Keys, 2014, Engineering the product profile of a polysialyltransferase, Nat. Chem. Biol, 10, 437, 10.1038/nchembio.1501 Levengood, 2011, Monitoring processivity and length control of a carbohydrate polymerase, J Am. Chem. Soc, 133, 12758, 10.1021/ja204448t Mort, 1991, Problems encountered during the extraction, purification, and chromatography of pectic fragments, and some solutions to them, Carbohydr. Res, 215, 219, 10.1016/0008-6215(91)84022-7 Pattathil, 2010, A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies, Plant Physiol, 153, 514, 10.1104/pp.109.151985 Bloom, 2001, Polymerase processivity: measurement and mechanisms, 1 Fiebig, 2018, Efficient solid-phase synthesis of meningococcal capsular oligosaccharides enables simple and fast chemoenzymatic vaccine production, J. Biol. Chem, 293, 953, 10.1074/jbc.RA117.000488 Bambara, 1995, Methods of analyzing processivity, Methods Enzymol, 262, 270, 10.1016/0076-6879(95)62023-0 Nardone, 1986, Differences in the kinetic properties of BamHI endonuclease and methylase with linear DNA substrates, J. Biol. Chem, 261, 12128, 10.1016/S0021-9258(18)67212-6 Yin, 2010, Evolution and function of the plant cell wall synthesis-related glycosyltransferase family 8, Plant Physiol, 153, 1729, 10.1104/pp.110.154229 Culbertson, 2016, Enzymatic activity of xyloglucan xylosyltransferase 5, Plant Physiol, 171, 1893, 10.1104/pp.16.00361 Dilokpimol, 2014, Galactosyltransferases from Arabidopsis thaliana in the biosynthesis of type II arabinogalactan: molecular interaction enhances enzyme activity, BMC Plant Biol, 14, 90, 10.1186/1471-2229-14-90 Basu, 2015, A small multigene hydroxyproline-O-galactosyltransferase family functions in arabinogalactan-protein glycosylation, growth and development in Arabidopsis, BMC Plant Biol, 15, 295, 10.1186/s12870-015-0670-7 Rennie, 2012, Three members of the Arabidopsis glycosyltransferase family 8 are xylan glucuronosyltransferases, Plant Physiol, 159, 1408, 10.1104/pp.112.200964 Lee, 2012, Arabidopsis GUX proteins are glucuronyltransferases responsible for the addition of glucuronic acid side chains onto xylan, Plant Cell Physiol, 53, 1204, 10.1093/pcp/pcs064 Vuttipongchaikij, 2012, Arabidopsis GT34 family contains five xyloglucan α-1,6-xylosyltransferases, New Phytol, 195, 585, 10.1111/j.1469-8137.2012.04196.x Ogawa-Ohnishi, 2015, Identification of three potent hydroxyproline O-galactosyltransferases in Arabidopsis, Plant J, 81, 736, 10.1111/tpj.12764 Laursen, 2018, Bifunctional glycosyltransferases catalyze both extension and termination of pectic galactan oligosaccharides, Plant J, 94, 340, 10.1111/tpj.13860 Raga-Carbajal, 2016, Size product modulation by enzyme concentration reveals two distinct levan elongation mechanisms in Bacillus subtilis levansucrase, Glycobiology, 26, 377, 10.1093/glycob/cwv112 Forsee, 2006, Role of the carbohydrate binding site of the Streptococcus pneumoniae capsular polysaccharide type 3 synthase in the transition from oligosaccharide to polysaccharide synthesis, J. Biol. Chem, 281, 6283, 10.1074/jbc.M511124200 Morgan, 2013, Crystallographic snapshot of cellulose synthesis and membrane translocation, Nature, 493, 181, 10.1038/nature11744 Breyer, 2001, A structural basis for processivity, Protein Sci, 10, 1699, 10.1110/ps.10301 Davis, 2010, Arabidopsis mannan synthase CSLA9 and glucan synthase CSLC4 have opposite orientations in the Golgi membrane, Plant J, 64, 1028, 10.1111/j.1365-313X.2010.04392.x Pauly, 2016, Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan, Annu. Rev. Plant Biol, 67, 235, 10.1146/annurev-arplant-043015-112222 Vionnet, 2007, Successive glycosyltransfer of sialic acid by Escherichia coli K92 polysialyltransferase in elongation of oligosialic acceptors, Glycobiology, 17, 735, 10.1093/glycob/cwm032 Chavaroche, 2010, In vitro synthesis of heparosan using recombinant Pasteurella multocida heparosan synthase PmHS2, Appl. Microbiol. Biotechnol, 85, 1881, 10.1007/s00253-009-2214-2 DeAngelis, 2002, Identification and molecular cloning of a heparosan synthase from Pasteurella multocida type D, J. Biol. Chem, 277, 7209, 10.1074/jbc.M112130200 Fiebig, 2014, Functional expression of the capsule polymerase of Neisseria meningitidis serogroup X: a new perspective for vaccine development, Glycobiology, 24, 150, 10.1093/glycob/cwt102 Fiebig, 2014, Molecular cloning and functional characterization of components of the capsule biosynthesis complex of Neisseria meningitidis serogroup A: toward in vitro vaccine production, J. Biol. Chem, 289, 19395, 10.1074/jbc.M114.575142 Litschko, 2015, The capsule polymerase CslB of Neisseria meningitidis serogroup L catalyzes the synthesis of a complex trimeric repeating unit comprising glycosidic and phosphodiester linkages, J. Biol. Chem, 290, 24355, 10.1074/jbc.M115.678094 Weigel, 2015, Hyaluronan synthase assembles chitin oligomers with -GlcNAc(α1→)UDP at the reducing end, Glycobiology, 25, 632, 10.1093/glycob/cwv006 Weigel, 2017, Hyaluronan synthase assembles hyaluronan on a [GlcNAc(β1,4)]n-GlcNAc(α1→)UDP primer and hyaluronan retains this residual chitin oligomer as a cap at the nonreducing end, Glycobiology, 27, 536 Liljebjelke, 1995, Enzymatic synthesis and purification of uridine diphosphate [14C]galacturonic acid: a substrate for pectin biosynthesis, Anal. Biochem, 225, 296, 10.1006/abio.1995.1158 Laemmli, 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680, 10.1038/227680a0 Sterling, 2005, Development of a filter assay for measuring homogalacturonan: α-(1,4)-galacturonosyltransferase activity, Anal. Biochem, 343, 231, 10.1016/j.ab.2005.05.037 Jacobs, 2001, Enhancement of the quality of MALDI mass spectra of highly acidic oligosaccharides by using a nafion-coated probe, Anal. Chem, 73, 405, 10.1021/ac001222i Pattathil, 2012, Immunological approaches to plant cell wall and biomass characterization: glycome profiling, Methods Mol. Biol, 908, 61 Benen, 1999, Kinetic characterization of Aspergillus niger N400 endopolygalacturonases I, II and C, Eur. J. Biochem, 259, 577, 10.1046/j.1432-1327.1999.00080.x