Subcellular coordination of plant cell wall synthesis

Organelles of the plant cell cooperate to synthesize and secrete a strong yet flexible polysaccharide-based extracellular matrix: wall. Cell wall composition varies among species, across types within plant, different regions single wall, in response intrinsic or extrinsic signals. This diversity makeup is underpinned by common cellular mechanisms for production. Cellulose synthase complexes function at plasma membrane deposit their product into Matrix polysaccharides are synthesized multitude glycosyltransferases hundreds mobile Golgi stacks, an extensive set vesicle trafficking proteins govern secretion In this review, we discuss subcellular locations which synthesis occurs, review molecular that control biosynthesis, examine how these regulated perturbations maintain homeostasis. The matrix cells provides mechanical support counter osmotically driven turgor pressure. main load-bearing element walls cellulose, embedded mixture hemicelluloses, pectins, (Anderson Kieber, 2020Anderson C.T. Kieber J.J. Dynamic construction, perception, remodeling walls.Annu. Rev. Plant Biol. 2020; 71: 39-69Crossref PubMed Scopus (15) Google Scholar). requires coordination multiple organelles, primarily endomembrane system. Cellulose, homopolymer ?-1,4-linked glucose, made cellulose (CESA) (CSCs) membrane. (hemicelluloses pectins) (GTs) apparatus, glycoprotein processing occurs endoplasmic reticulum (ER) apparatus. Furthermore, coordinated biosynthesis context unique features cells: potential grow large sizes, prominent central vacuoles, cortical microtubule cytoskeleton periphery, bodies traveling around actin-myosin-dependent fashion. confine shapes, reflect developmental state (Figure 1). illustrated spherical shape when experimentally removed 1A), contrast variety shapes defined (Figures 1B–1F). also play important functional roles. For example, highly interdigitated leaf epidermal distribute forces during tissue growth (Sapala et al., 2018Sapala A. Runions Routier-Kierzkowska A.-L. Das Gupta M. Hong L. Hofhuis H. Verger S. Mosca G. Li C.-B. Hay al.Why plants make puzzle cells, emerges.eLife. 2018; 7e32794Crossref (67) Scholar), heavily reinforced stem xylem resist extreme negative pressure water-conducting (Roumeli 2020Roumeli E. Ginsberg McDonald R. Spigolon Hendrickx Ohtani Demura T. Ravichandran Daraio C. Structure biomechanics vessel transdifferentiation Arabidopsis thaliana.Plants. 9: 1715Crossref (0) Scholar) 1D 1F). Despite examples distinct key physiological roles, responsible producing remarkably similar from one type another. As differentiate, new layers sequentially deposited. Following mitosis, precisely positioned cytokinesis (Livanos Müller, 2019Livanos P. Müller Division plane establishment cytokinesis.Annu. 2019; 70: 239-267Crossref (18) Primary as laid down joined adjacent pectin-rich middle lamella 1E relatively extensible rich pectins (Anderson, 2016Anderson ‘We be jammin’: update on pectin dynamics.J. Exp. Bot. 2016; 67: 495-502Crossref certain hemicelluloses (e.g., xyloglucan dicot plants, such thaliana) (Scheller Ulvskov, 2010Scheller H.V. Ulvskov Hemicelluloses.Annu. 2010; 61: 263-289Crossref (1444) Scholar; Cosgrove, 2014Cosgrove D.J. Re-constructing our models primary assembly.Curr Opin 2014; 22: 122-131Crossref (211) extensibility due many non-covalent interactions between cross-linking acidic via Ca2+) capacity modify covalent polysaccharide (Zhang 2016Zhang Zheng Y. Cosgrove Spatial organization microfibrils imaged multichannel atomic force microscopy.Plant J. 85: 179-192Crossref (111) Secondary generally deposited specialized after expansion has ceased 1C 1E). These thickened body up vascular conducts water nutrients throughout plant. glucuronoxylans plants) fortified with lignin, covalently cross-linked polymer formed phenylalanine derivatives called monolignols (Meents 2018Meents M.J. Watanabe Samuels A.L. biology secondary biosynthesis.Ann. 121: 1107-1125Crossref (57) both rely biosynthetic mechanisms, including production CSCs (Paredez 2006Paredez A.R. Somerville C.R. Ehrhardt D.W. Visualization demonstrates association microtubules.Science. 2006; 312: 1491-1495Crossref (836) 2018Watanabe Schneider Barkwill Gonzales-Vigil Hill J.L. Persson Mansfield S.D. display dynamic behaviors transdifferentiation.Proc. Natl. Acad. Sci. USA. 115: E6366-E6374Crossref Staehelin, 1992Zhang G.F. Staehelin L.A. Functional compartmentation apparatus immunocytochemical analysis high-pressure frozen- freeze-substituted sycamore maple suspension culture cells.Plant Physiol. 1992; 99: 1070-1083Crossref controlled targeting secretory vesicles (Žárský 2013Žárský V. Kulich I. Fendrych Pe?enková Exocyst functions pathways.Curr. Opin. 2013; 16: 726-733Crossref 2). Using produce diverse materials depending state. addition changes cues, biotic abiotic modification structure, composition, environmental cues can referred homeostasis transcriptional level, through post-translational enzymes, polymers. signaling stimuli trigger modifications (Vaahtera 2019Vaahtera Schulz Hamann integrity maintenance development interaction environment.Nat. Plants. 5: 924-932Crossref (34) Rui Dinneny, 2020Rui Dinneny J.R. A integrity: surveillance under stress.New Phytol. 225: 1428-1439Crossref (30) pathogens elicit local deposition site pathogen attack surface (Chowdhury 2014Chowdhury Henderson Schweizer Burton R.A. Fincher G.B. Little Differential accumulation callose, arabinoxylan nonpenetrated versus penetrated papillae leaves barley infected Blumeria graminis f. sp. hordei.New 204: 650-660Crossref correlated disease resistance (Molina 2021Molina Miedes Bacete Rodríguez Mélida Denancé N. Sánchez-Vallet Rivière M.-P. López Freydier al.Arabidopsis determines specificity fitness.Proc. 2021; 118 (e2010243118)Crossref (1) Abiotic factors may affect (Wang 2016Wang McFarlane H.E. impact synthesis.J. 543-552Crossref (58) Scholar); salt stress dramatically short term, intricate exist recover sustained (Endler 2015Endler Kesten Zhang Ivakov Froehlich Funke mechanism stress.Cell. 2015; 162: 1353-1364Abstract Full Text PDF Feng 2018Feng W. Kita D. Peaucelle Cartwright H.N. Doan Duan Q. Liu M.C. Maman Steinhorst Schmitz-Thom al.The FERONIA receptor kinase maintains cell-wall Ca2+ signaling.Curr. 28: 666-675.e5Abstract (160) perturbations. Although bulk membrane, ER plays several roles facilitating proper protein folding, complex assembly, glycosylation initiation, transport Golgi. N-glycosylation essential affects trafficking/retention enzymatic activity, well protein-protein (Strasser, 2016Strasser glycosylation.Glycobiology. 26: 926-939Crossref (173) initiated ER, N-glycans further modified GTs Proteomic approaches have demonstrated N-glycosylated (Zeng 2018Zeng Ford K.L. Bacic Heazlewood N-linked glycan micro-heterogeneity glycoproteins Arabidopsis.Mol. Cell. Proteomics. 17: 413-421Abstract carrying mutations glucosidases had lower amounts radially swollen roots, defects (Burn 2002Burn J.E. Hurley U.A. Birch R.J. Arioli Cork Williamson R.E. cellulose-deficient mutant rsw3 defective gene encoding putative glucosidase II, enzyme quality control.Plant 2002; 32: 949-960Crossref (105) Gillmor 2002Gillmor C.S. Poindexter Lorieau Palcic M.M. ?-glucosidase I required morphogenesis Arabidopsis.J. 156: 1003-1013Crossref (136) Many proteins, e.g., arabinogalactan O-glycosylated hydroxyproline residues (Seifert, 2020Seifert G.J. On II O-glycosylation regulating fate proteins.Front. 11: 563735Crossref (2) enzymes first committed steps localized (Velasquez 2011Velasquez S.M. Ricardi Dorosz J.G. Fernandez P.V. Nadra A.D. Pol-Fachin Egelund Gille Harholt Ciancia al.O-glycosylated root hair growth.Science. 2011; 332: 1401-1403Crossref (178) Basu 2015Basu Wang Ma DeBrosse Poirier Emch K. Soukup Tian Showalter A.M. Two galactosyltransferases, GALT5 GALT2, arabinogalactan-protein glycosylation, Arabidopsis.PLoS One. 10e0125624Crossref (33) Mutations affecting proline hydroxylation result reduced elongation swelling implying role and/or assembly. components lignin monomers soluble cytoplasmic ER-associated cytochrome P450s then exported (Gou 2018Gou Ran X. Martin C.J. scaffold lingin P450 enzymes.Nat. 4: 299-310Crossref Secreted oxidative laccases peroxidases, activate precursors radicals randomly couple form polymer. Laccases peroxidases where specific domains, thick corners/middle (Schuetz 2014Schuetz Benske Smith Tobimatsu Ralph Ellis B. direct lignification discrete domains protoxylem.Plant 166: 798-807Crossref (107) Hoffmann 2020Hoffmann Betz Schuetz co-localize lignified development.Plant 184: 806-822Crossref glycoproteins, they presumably processed secreted precise contain numerous, independent, stacks travel cytoplasm actin filaments (Boevink 1998Boevink Oparka Santa Cruz S.S. Betteridge Hawes Stacks tracks: traffics actin/ER network.Plant 1998; 15: 441-447Crossref (674) share similarities animal Golgi, cis-to-trans polar distribution cargo, lipids, pH gradient cisternae (Davis 2016aDavis Wilkop T.E. Drakakaki apparatus.in: Dashek W.V. Miglani G.S. Cells Their Organelles. John Wiley & Sons, 2016: 61-87Crossref critical it location polysaccharides, assembly/trafficking CSCs. Co-localization epitopes same stack all cooperatively contribute Young 2008Young Hahn M.G. Western T.L. Haughn G.W. Analysis seed coat polarized mucilage.Plant 2008; 20: 1623-1638Crossref (86) 2017Wang Chen Goldbeck Chung Kang B.H. class derived trans-Golgi mediates xylogalacturonan border cell.Plant 2017; 92: 596-610Crossref (17) Meents 2019Meents Motani Organization xylan biosynthesis.Plant 181: 527-546Crossref (5) Each therefore expected carry full complement resident synthesis. Nucleotide sugar transporters translocate activated cytosol lumen (Rautengarten 2014Rautengarten Ebert Moreno Temple Herter Link Doñas-Cofré Saéz-Aguayo Blanco F. bifunctional UDP-rhamnose/UDP-galactose transporter family Arabidopsis.Proc. 111: 11563-11568Crossref (23) type-I type-II use substrates backbone add side chains, respectively, Anderson, Additional Golgi-resident methylation acetylation). mammalian steady-state localization recycling COPI vesicles, hypothesized (Gimeno-Ferrer 2017Gimeno-Ferrer Pastor-Cantizano Bernat-Silvestre Selvi-Martínez Vera-Sirera Gao Perez-Amador M.A. Jiang Aniento Marcote ?2-COP involved early traffic growth.J. 68: 391-401PubMed although evidence currently lacking. polymers numerous monosaccharides linkages thus require GTs. There two non-mutually exclusive hypotheses organized apparatus: sequential model complex-mediated model. predicts sub-compartments, thereby separating reactions. interact together catalyze reactions multi-enzyme complex. Clarifying whether cisternae, combination implications understanding GT retention more generally, will inform partitioning biochemical eukaryotic organelles. Prior must added stepwise manner 3A), analogous O- progress cis-, medial-, trans-cisternae (Saint-Jore-Dupas 2006Saint-Jore-Dupas Nebenführ Boulaflous Follet-Gueye M.L. Plasson Driouich Faye Gomord N-glycan employ spatial arrangement along pathway.Plant 18: 3182-3200Crossref (150) could explain mostly transmission electron microscopy (TEM) images, unmodified homogalacturonan cis- medial-cisternae methylesterified later medial- Localization fluorescently tagged hemicellulose xylosylation found cis-cisternae, galactosylation medial-cisternae, final fucosylation (Chevalier 2010Chevalier Bernard Ramdani Lamour Bardor Lerouge Subcompartment chain xyloglucan-synthesizing tobacco suspension-cultured 64: 977-989Crossref 3B). However, transient, heterologous overexpression study complicates interpretation, given cause artifacts. Recently, free-flow electrophoresis was used separate compartments cultures (Parsons 2019Parsons H.T. Stevens T.J. Vidal-Melgosa Griss Lawrence Butler Sousa M.M.L. Salemi Willats W.G.T. al.Separating cis trans reveals underlying properties cisternal localization.Plant 31: 2010-2034Crossref glycomic analyses fractions, supported TEM immunolocalization super-resolution structured illumination microscopy, differential cargo stacks. were supplying additional 3). model, studies documented GTs, prompting hypothesis function. instance, GAUT1 GAUT7, necessary (Atmodjo 2011Atmodjo Sakuragi Zhu Burrell A.J. Mohanty Atwood J.A. Orlando Scheller Mohnen Galacturonosyltransferase (GAUT)1 GAUT7 core homogalacturonan: galacturonosyltransferase complex.Proc. 108: 20225-20230Crossref methyltransferases oligosaccharyltransferases, co-immunoprecipitated GAUT1:GAUT7 complex, suggesting facilitate Similarly, appears dependent upon formation, simultaneous co-expression genes IRX9, IRX10, IRX14A asparagus 2016Zeng Lampugnani E.R. Picard Song Wu Farion I.M. Zhao Doblin M.S. Asparagus active forms apparatus.Plant 171: 93-109Crossref (39) increase efficiency reactions, since yeast most efficient co-expressed (Cocuron 2007Cocuron J.C. Lerouxel O. Alonso A.P. Liepman A.H. Keegstra Raikhel Wilkerson C.G. synthase-like C encodes ?-1,4 glucan synthase.Proc. 2007; 104: 8550-8555Crossref Bimolecular fluorescence complementation (BiFC) pull-down assays provided synthases (CSLCs), xylosyltransferases (XXTs), galactosyltransferases (MUR3 XLT2), fucosyltransferases (FUTs) physically associate vivo (Chou 2015Chou Y.H. Pogorelko Z.T. Zabotina O.A. Protein-protein formation Golgi-localized multiprotein complexes.Plant 56: 255-267Crossref Lund 2015Lund C.H. Bromley Stenbæk Rasmussen reversible Renilla luciferase assay rapid identification existence network apparatus.J. 66: 85-97Crossref (20) Such would allow decorations cisterna 3B 3C). quick shuttling growing molecule shield aggregation insoluble undecorated (Cavalier Keegstra, 2006Cavalier D.M. xylosyl cellohexaose.J. Chem. 281: 34197-34207Abstract (83) interact, complete not because co-incubation XXT2 XXT5 did significantly xylosyltransferase activity i