Cellulose synthase complex organization and cellulose microfibril structure

Cellulose consists of linear chains of β-1,4-linked glucose units, which are synthesized by the cellulose synthase complex (CSC). In plants, these chains associate in an ordered manner to form the cellulose microfibrils. Both the CSC and the local environment in which the individual chains coalesce to form the cellulose microfibril determine the structure and the unique physical properties of the microfibril. There are several recent reviews that cover many aspects of cellulose biosynthesis, which include trafficking of the complex to the plasma membrane and the relationship between the movement of the CSC and the underlying cortical microtubules (Bringmann et al. 2012 Trends Plant Sci. 17 , 666–674 ( doi:10.1016/j.tplants.2012.06.003 ); Kumar & Turner 2015 Phytochemistry 112 , 91–99 ( doi:10.1016/j.phytochem.2014.07.009 ); Schneider et al. 2016 Curr. Opin. Plant Biol. 34 , 9–16 ( doi:10.1016/j.pbi.2016.07.007 )). In this review, we will focus on recent advances in cellulose biosynthesis in plants, with an emphasis on our current understanding of the structure of individual catalytic subunits together with the local membrane environment where cellulose synthesis occurs. We will attempt to relate this information to our current knowledge of the structure of the cellulose microfibril and propose a model in which variations in the structure of the CSC have important implications for the structure of the cellulose microfibril produced. This article is part of a discussion meeting issue ‘New horizons for cellulose nanotechnology’.

Download Full-text

Characterization of Cellulose Synthesis in Plant Cells

The Scientific World JOURNAL ◽

10.1155/2016/8641373 ◽

2016 ◽

Vol 2016 ◽

pp. 1-8 ◽

Cited By ~ 18

Author(s):

Samaneh Sadat Maleki ◽

Kourosh Mohammadi ◽

Kong-shu Ji

Keyword(s):

Plant Cell Wall ◽

Current Knowledge ◽

Cellulose Synthase ◽

Cellulose Microfibrils ◽

Cellulose Synthesis ◽

Forest Trees ◽

Cellulose Biosynthesis ◽

Wood Production ◽

Cellulose Synthase Complex

Cellulose is the most significant structural component of plant cell wall. Cellulose, polysaccharide containing repeated unbranchedβ(1-4) D-glucose units, is synthesized at the plasma membrane by the cellulose synthase complex (CSC) from bacteria to plants. The CSC is involved in biosynthesis of cellulose microfibrils containing 18 cellulose synthase (CesA) proteins. Macrofibrils can be formed with side by side arrangement of microfibrils. In addition, beside CesA, various proteins like the KORRIGAN, sucrose synthase, cytoskeletal components, and COBRA-like proteins have been involved in cellulose biosynthesis. Understanding the mechanisms of cellulose biosynthesis is of great importance not only for improving wood production in economically important forest trees to mankind but also for plant development. This review article covers the current knowledge about the cellulose biosynthesis-related gene family.

Download Full-text

BRASSINOSTEROID INSENSITIVE2 negatively regulates cellulose synthesis in Arabidopsis by phosphorylating cellulose synthase 1

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1615005114 ◽

2017 ◽

Vol 114 (13) ◽

pp. 3533-3538 ◽

Cited By ~ 36

Author(s):

Clara Sánchez-Rodríguez ◽

KassaDee Ketelaar ◽

Rene Schneider ◽

Jose A. Villalobos ◽

Chris R. Somerville ◽

...

Keyword(s):

Phosphorylation Site ◽

Point Mutations ◽

Cellulose Synthase ◽

Negative Regulator ◽

Primary Cell Wall ◽

Cellulose Synthesis ◽

Cellulose Biosynthesis ◽

Plant Growth And Development ◽

Cellulose Synthase Complex ◽

A Subunit

The deposition of cellulose is a defining aspect of plant growth and development, but regulation of this process is poorly understood. Here, we demonstrate that the protein kinase BRASSINOSTEROID INSENSITIVE2 (BIN2), a key negative regulator of brassinosteroid (BR) signaling, can phosphorylate Arabidopsis cellulose synthase A1 (CESA1), a subunit of the primary cell wall cellulose synthase complex, and thereby negatively regulate cellulose biosynthesis. Accordingly, point mutations of the BIN2-mediated CESA1 phosphorylation site abolished BIN2-dependent regulation of cellulose synthase activity. Hence, we have uncovered a mechanism for how BR signaling can modulate cellulose synthesis in plants.

Download Full-text

Analysis of a cellulose synthase catalytic subunit from the oomycete pathogen of crops Phytophthora capsici

Cellulose ◽

10.1007/s10570-020-03362-9 ◽

2020 ◽

Vol 27 (15) ◽

pp. 8551-8565

Author(s):

Zhili Pang ◽

Lauren S. McKee ◽

Vaibhav Srivastava ◽

Stefan Klinter ◽

Sara M. Díaz-Moreno ◽

...

Keyword(s):

Cell Wall ◽

Biochemical Characterization ◽

Phytophthora Capsici ◽

Cellulose Synthase ◽

Economic Losses ◽

Cellulose Synthesis ◽

Major Reaction Product ◽

Major Reaction ◽

Oomycete Pathogen ◽

The Individual

Abstract Phytophthora capsici Leonian is an important oomycete pathogen of crop vegetables, causing significant economic losses each year. Its cell wall, rich in cellulose, is vital for cellular integrity and for interactions with the host organisms. Predicted cellulose synthase (CesA) proteins are expected to catalyze the polymerization of cellulose, but this has not been biochemically demonstrated in an oomycete. Here, we present the properties of the four newly identified CesA proteins from P. capsici and compare their domain organization with that of CesAs from other lineages. Using a newly constructed glucosyltransferase-deficient variant of Saccharomyces cerevisiae with low residual background activity, we have achieved successful heterologous expression and biochemical characterization of a CesA protein from P. capsici (PcCesA1). Our results demonstrate that the individual PcCesA1 enzyme produces cellobiose as the major reaction product. Co-immunoprecipitation studies and activity assays revealed that several PcCesA proteins interact together to form a complex whose multiproteic nature is most likely required for cellulose microfibril formation. In addition to providing important insights into cellulose synthesis in the oomycetes, our data may assist the longer term identification of cell wall biosynthesis inhibitors to control infection by pathogenic oomycetes.

Download Full-text

Cellulose biosynthesis in higher plants

Acta Societatis Botanicorum Poloniae ◽

10.5586/asbp.1996.003 ◽

2014 ◽

Vol 65 (1-2) ◽

pp. 17-24 ◽

Cited By ~ 1

Author(s):

Krystyna Kudlicka ◽

R. M. Brown, Jr

Keyword(s):

Higher Plants ◽

Regulatory Protein ◽

Cellulose Synthase ◽

Cell Disruption ◽

Cellulose Synthesis ◽

Higher Plant ◽

Cellulose Synthase Complex ◽

Enzyme Complexes

Knowledge of the control and regulation of cellulose synthesis is fundamental to an understanding of plant development since cellulose is the primary structural component of plant cell walls. In vivo, the polymerization step requires a coordinated transport of substrates across membranes and relies on delicate orientations of the membrane-associated synthase complexes. Little is known about the properties of the enzyme complexes, and many questions about the biosynthesis of cell wall components at the cell surface still remain unanswered. Attempts to purify cellulose synthase from higher plants have not been successful because of the liability of enzymes upon isolation and lack of reliable in vitro assays. Membrane preparations from higher plant cells incorporate UDP-glucose into a glucan polymer, but this invariably turns out to be predominantly β -1,3-linked rather than β -1,4-linked glucans. Various hypotheses have been advanced to explain this phenomenon. One idea is that callose and cellulose-synthase systems are the same, but cell disruption activates callose synthesis preferentially. A second concept suggests that a regulatory protein as a part of the cellulose-synthase complex is rapidly degraded upon cell disruption. With new methods of enzyme isolation and analysis of the in vitro product, recent advances have been made in the isolation of an active synthase from the plasma membrane whereby cellulose synthase was separated from callose synthase.

Download Full-text

Trafficking of the cellulose synthase complex in developing xylem vessels

Biochemical Society Transactions ◽

10.1042/bst0380755 ◽

2010 ◽

Vol 38 (3) ◽

pp. 755-760 ◽

Cited By ~ 16

Author(s):

Raymond Wightman ◽

Simon Turner

Keyword(s):

Plasma Membrane ◽

Secondary Wall ◽

Cellulose Microfibril ◽

Cellulose Synthase ◽

Cellulosic Biomass ◽

Cell Cortex ◽

Wall Formation ◽

Cellulose Synthase Complex ◽

Secondary Wall Formation

The potential for using cellulosic biomass as a source of fuel has renewed interest into how the large cellulose synthase complex deposits cellulose within the woody secondary walls of plants. This complex sits within the plasma membrane where it synthesizes numerous glucan chains which bond together to form the strong cellulose microfibril. The maintenance and guidance of the complex at the plasma membrane and its delivery to sites of secondary wall formation require the involvement of the cytoskeleton. In the present paper, we discuss the dynamics of the complex at the cell cortex and what is known about its assembly and trafficking.

Download Full-text

Investigation of Bacterial Cellulose Biosynthesis Mechanism in Gluconoacetobacter hansenii

ISRN Microbiology ◽

10.1155/2014/836083 ◽

2014 ◽

Vol 2014 ◽

pp. 1-7 ◽

Cited By ~ 3

Author(s):

Bhavna V. Mohite ◽

Satish V. Patil

Keyword(s):

Bacterial Cellulose ◽

Congo Red ◽

Gel Electrophoresis ◽

Membrane Fraction ◽

Cellulose Synthase ◽

Free Enzyme ◽

Cellulose Synthesis ◽

Cellulose Biosynthesis ◽

Native Gel

The present study explores the mechanism of cellulose biosynthesis in Gluconoacetobacter hansenii. The cellulose synthase enzyme was purified as membrane fraction and solubilized by treatment with 0.1% digitonin. The enzyme was separated by native-gel electrophoresis and β-D-glucan analysis was carried out using in vitro gel assay. The cellulose synthase has glycoprotein nature and composed two polypeptide subunits of 93 KDa and 85 KDa. The confirmation of β-1,4-glucan (cellulose) was performed in whole and hydrolyzed monomeric sugar form. Tinopal and Congo red were used for cellulose detection on the gel. Thus the in vitro cellulose synthesis assay with cell free enzyme fraction was attempted to improve the understanding of cellulose biosynthesis.

Download Full-text

Cellulose-Synthesizing Machinery in Bacteria

10.21203/rs.3.rs-633140/v1 ◽

2021 ◽

Author(s):

Kenji Tajima ◽

Tomoya Imai ◽

Toshifumi Yui ◽

Min Yao ◽

Inder Saxena

Keyword(s):

Protein Complexes ◽

Bacterial Species ◽

Model Organism ◽

Cellulose Fibers ◽

Cellulose Synthase ◽

Acetic Acid Bacterium ◽

Cellulose Microfibrils ◽

Cellulose Biosynthesis ◽

Terminal Complexes ◽

Glucan Chain

Abstract Cellulose is produced by all plants and a number of other organisms, including bacteria. The most representative cellulose-producing bacterial species is Gluconacetobacter xylinus (G. xylinus), an acetic acid bacterium. Cellulose produced by G. xylinus, commonly referred to as bacterial cellulose (BC), has exceptional physicochemical properties resulting in its use in a variety of applications. All cellulose-producing organisms that synthesize cellulose microfibrils have membrane-localized protein complexes (also called terminal complexes or TCs) that contain the enzyme cellulose synthase and other proteins. The bacterium G. xylinus is a prolific cellulose producer and a model organism for studies on cellulose biosynthesis. The widths of cellulose fibers produced by Gluconacetobacter are 50‒100 nm, suggesting that cellulose-synthesizing complexes are nanomachines spinning a nanofiber. At least four different proteins (BcsA, BcsB, BcsC, and BcsD) are included in TC from Gluconacetobacter, and the proposed function of each is as follows: BcsA, synthesis of a glucan chain through glycosyl transfer from UDP-glucose; BcsB, complexes with BcsA for cellulose synthase activity; BcsC, formation of a pore in the outer membrane through which a glucan chain is extruded; BcsD, regulates aggregation of glucan chains through four tunnel-like structures. In this review, we discuss structures and functions of these four and a few other proteins that have a role in cellulose biosynthesis in bacteria.

Download Full-text

THE SHAPE OF THE TIPS OF GROWING BACTERIAL CELLULOSE MICROFIBRILS AND ITS RELATION TO THE MECHANISM OF CELLULOSE BIOSYNTHESIS

Canadian Journal of Microbiology ◽

10.1139/m64-097 ◽

1964 ◽

Vol 10 (5) ◽

pp. 763-767 ◽

Cited By ~ 8

Author(s):

J. Ross Colvin ◽

D. T. Dennis

Keyword(s):

Bacterial Cellulose ◽

Cellulose Microfibril ◽

Cellulose Microfibrils ◽

Longitudinal Growth ◽

High Polymer ◽

Cellulose Biosynthesis

Single growing bacterial cellulose microfibrils show blunt tips in contrast to observations reported from earlier studies. The hypothesis of crystallization of the cellulose microfibril from a soluble, intermediate high polymer is not consistent with the observed shape of the tips but longitudinal growth of the microfibril from activated single residues of glucose is in agreement with this morphology.

Download Full-text

Cellulose synthase-like D (CSLD) proteins move in the plasma membrane and their targeting to cell tips, but not cell plates, depends on the actin cytoskeleton

10.1101/2021.08.19.457018 ◽

2021 ◽

Author(s):

Shu-Zon Wu ◽

Arielle M. Chaves ◽

Rongrong Li ◽

Magdalena Bezanilla ◽

Alison W. Roberts

Keyword(s):

Plasma Membrane ◽

Cell Division ◽

Live Cell Imaging ◽

Cell Imaging ◽

Tip Growth ◽

Cellulose Synthase ◽

Live Cell ◽

Cellulose Microfibrils ◽

Apical Plasma Membrane ◽

Cellulose Synthesis

Cellulose Synthase-Like D (CSLD) proteins are implicated in cell wall remodeling during tip growth and cell division in plants, and are known to generate β-1,4-glucan. It is unknown whether they form complexes and move in the plasma membrane like members of the Cellulose Synthase (CESA) family. We used the genetically tractable moss Physcomitrium patens, which has a filamentous protonemal stage that undergoes both tip growth and cell division and is amenable to high resolution live cell imaging, to investigate CSLD function and intracellular trafficking. CSLD2 and CSLD6 are highly expressed in gametophores and are redundantly required for gametophore cellular patterning. Live cell imaging revealed that CSLD6 is also expressed in protonemata where it moves in the plasma membrane and localizes to cell plates and cell tips. Notably, delivery to the apical plasma membrane, but not the cell plate, depends on actin. By comparing the behavior of endogenously tagged CSLD6 and CESA10, we discovered that CSLD6 movements in the plasma membrane were significantly faster, shorter in duration and less linear than CESA10 movements and were insensitive to the cellulose synthesis inhibitor isoxaben. These data suggest that CSLD6 and CESA10 function within different structures and may thus produce structurally distinct cellulose microfibrils.

Download Full-text

Inhibition of cell expansion enhances cortical microtubule stability in the root apex of Arabidopsis thaliana

Journal of Biological Research-Thessaloniki ◽

10.1186/s40709-021-00143-8 ◽

2021 ◽

Vol 28 (1) ◽

Author(s):

Veronica Giourieva ◽

Emmanuel Panteris

Keyword(s):

Arabidopsis Thaliana ◽

Cell Wall ◽

Cell Expansion ◽

Cortical Microtubule ◽

Root Apex ◽

Cellulose Synthase ◽

Cellulose Biosynthesis ◽

Cortical Microtubules ◽

Wild Type ◽

Microtubule Stability

Abstract Background Cortical microtubules regulate cell expansion by determining cellulose microfibril orientation in the root apex of Arabidopsis thaliana. While the regulation of cell wall properties by cortical microtubules is well studied, the data on the influence of cell wall to cortical microtubule organization and stability remain scarce. Studies on cellulose biosynthesis mutants revealed that cortical microtubules depend on Cellulose Synthase A (CESA) function and/or cell expansion. Furthermore, it has been reported that cortical microtubules in cellulose-deficient mutants are hypersensitive to oryzalin. In this work, the persistence of cortical microtubules against anti-microtubule treatment was thoroughly studied in the roots of several cesa mutants, namely thanatos, mre1, any1, prc1-1 and rsw1, and the Cellulose Synthase Interacting 1 protein (csi1) mutant pom2-4. In addition, various treatments with drugs affecting cell expansion were performed on wild-type roots. Whole mount tubulin immunolabeling was applied in the above roots and observations were performed by confocal microscopy. Results Cortical microtubules in all mutants showed statistically significant increased persistence against anti-microtubule drugs, compared to those of the wild-type. Furthermore, to examine if the enhanced stability of cortical microtubules was due to reduced cellulose biosynthesis or to suppression of cell expansion, treatments of wild-type roots with 2,6-dichlorobenzonitrile (DCB) and Congo red were performed. After these treatments, cortical microtubules appeared more resistant to oryzalin, than in the control. Conclusions According to these findings, it may be concluded that inhibition of cell expansion, irrespective of the cause, results in increased microtubule stability in A. thaliana root. In addition, cell expansion does not only rely on cortical microtubule orientation but also plays a regulatory role in microtubule dynamics, as well. Various hypotheses may explain the increased cortical microtubule stability under decreased cell expansion such as the role of cell wall sensors and the presence of less dynamic cortical microtubules.

Download Full-text