Exploiting CELLULOSE SYNTHASE (CESA) Class Specificity to Probe Cellulose Microfibril Biosynthesis

Kumar, Manoj; Mishra, Laxmi S.; Carr, P.D.; Pilling, Michael J.; Gardner, Peter; Mansfield, Shawn D.; Turner, Simon R.

doi:10.1104/pp.18.00263

Cited by 35 publications

(37 citation statements)

References 50 publications

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“…For proteomics, Arabidopsis Col0 seed was grown for 7 days on plates followed by a further 4 weeks on soil as previously described 46 . The material collected was composed of inflorescence stem (after removing flowers, siliques and leaves and the basal 1cm), siliques (at various developmental stages), meristem (apical 1 cm of stem tip including unopened flowers) and rosette leaves.…”

Section: Methodsmentioning

confidence: 99%

An atlas of Arabidopsis protein S-Acylation reveals its widespread role in plant cell organisation of and function

Kumar

Carr

Turner

2020

Preprint

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6S-acylation is the addition of a fatty acid to a cysteine residue of a protein. While this modification 7 may profoundly alter protein behaviour, its effects on the function of plant proteins remains poorly 8 characterised, largely as a result to the lack of basic information regarding which proteins are S-9 acylated and where in the proteins the modification occurs. In order to address this gap in our 10 knowledge, we have performed a comprehensive analysis of plant protein S-acylation from 6 separate 11 tissues. In our highest confidence group, we identified 5185 cysteines modified by S-acylation, which 12 were located in 4891 unique peptides from 2643 different proteins. This represents around 9% of the 13 entire Arabidopsis proteome and suggests an important role for S-acylation in many essential cellular 14 functions including trafficking, signalling and metabolism. To illustrate the potential of this dataset, 15we focus on cellulose synthesis and confirm for the first time the S-acylation of all proteins known to 16 be involved in cellulose synthesis and trafficking of the cellulose synthase complex. In the secondary 17 cell walls, cellulose synthesis requires three different catalytic subunits (CESA4, CESA7 and CESA8) that 18 all exhibit striking sequence similarity. While all three proteins have been widely predicted to possess 19 a RING-type zinc finger at their N-terminus, for CESA4 and CESA8, we find evidence for S-acylation of 20 cysteines in this region that is incompatible with any role in coordinating metal ions. We show that 21 while CESA7 may possess a RING type domain, the same region of CESA4 and CESA8 appear to have 22 evolved a very different structure. Together, the data suggests this study represents an atlas of S-23 acylation in Arabidopsis that will facilitate the broader study of this elusive post-translational 24 modification in plants as well as demonstrates the importance of undertaking further work in this 25 area. 26 15 . This work required the use of systematic mutagenesis, which for a protein with 26 cysteines, is a 59 laborious approach and does not guarantee the identification of S-acylation sites. While the limited 60 knowledge of acylation sites has hampered studies on the role of S-acylation in the function of plant 61 proteins, analysis of the individual Arabidopsis PATs has implicated S-acylation in a variety of processes 62 including root hair formation, cell death, ROS production and branching, cell expansion and division, 63 gametogenesis and salt tolerance 2,[12][13][14]16 . So while our understanding of both the extent and function 64 of S-acylation of individual plant proteins remains limited, the available data indicates S-acylation is 65 important for many aspects of plant cell function. 66

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Section: Methodsmentioning

confidence: 99%

An atlas of Arabidopsis protein S-Acylation reveals its widespread role in plant cell organisation of and function

Kumar

Carr

Turner

2020

Preprint

Self Cite

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“…Quantitative immunoblotting analysis demonstrated that the three Arabidopsis secondary wall CESAs had an equimolar stoichiometry, and computational modeling of CESAs showed that a six‐fold assembly of CESA trimers had the best fit with the cellulose synthase rosette morphology (Hill et al ., ; Nixon et al ., ). However, the catalytic activity and hence the contribution to the overall rate of cellulose synthesis of each CESA in the rosette complexes may differ, as indicated by complementation analysis of Arabidopsis secondary wall CESAs (Kumar et al ., ).…”

Section: Cellulose Biosynthesismentioning

confidence: 97%

Secondary cell wall biosynthesis

2018

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Contents Summary1703I.Introduction1703II.Cellulose biosynthesis1705III.Xylan biosynthesis1709IV.Glucomannan biosynthesis1713V.Lignin biosynthesis1714VI.Concluding remarks1717Acknowledgements1717References1717 Summary Secondary walls are synthesized in specialized cells, such as tracheary elements and fibers, and their remarkable strength and rigidity provide strong mechanical support to the cells and the plant body. The main components of secondary walls are cellulose, xylan, glucomannan and lignin. Biochemical, molecular and genetic studies have led to the discovery of most of the genes involved in the biosynthesis of secondary wall components. Cellulose is synthesized by cellulose synthase complexes in the plasma membrane and the recent success of in vitro synthesis of cellulose microfibrils by a single recombinant cellulose synthase isoform reconstituted into proteoliposomes opens new doors to further investigate the structure and functions of cellulose synthase complexes. Most genes involved in the glycosyl backbone synthesis, glycosyl substitutions and acetylation of xylan and glucomannan have been genetically characterized and the biochemical properties of some of their encoded enzymes have been investigated. The genes and their encoded enzymes participating in monolignol biosynthesis and modification have been extensively studied both genetically and biochemically. A full understanding of how secondary wall components are synthesized will ultimately enable us to produce plants with custom‐designed secondary wall composition tailored to diverse applications.

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“…While MFA in SCWs is particularly relevant during wood formation in tree species, much of our current knowledge still relies on experimental model organisms and systems. Arabidopsis mutants with aberrant SCW patterning, for example, feature changes in MFA [48] and differential composition of the CSC results in alterations in cellulose microfibril polymerisation [49,50]. Even though CSC plays the same role in synthesising cellulose both in primary and secondary walls, variations in the composition and structure of CSCs appears to impart structural variations in cellulose microfibrils [49].…”

Section: Cellulose Properties and The Cscmentioning

confidence: 99%

The Cytoskeleton and Its Role in Determining Cellulose Microfibril Angle in Secondary Cell Walls of Woody Tree Species

Tobias

Spokevicius

McFarlane

et al. 2020

Plants

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Recent advances in our understanding of the molecular control of secondary cell wall (SCW) formation have shed light on molecular mechanisms that underpin domestication traits related to wood formation. One such trait is the cellulose microfibril angle (MFA), an important wood quality determinant that varies along tree developmental phases and in response to gravitational stimulus. The cytoskeleton, mainly composed of microtubules and actin filaments, collectively contribute to plant growth and development by participating in several cellular processes, including cellulose deposition. Studies in Arabidopsis have significantly aided our understanding of the roles of microtubules in xylem cell development during which correct SCW deposition and patterning are essential to provide structural support and allow for water transport. In contrast, studies relating to SCW formation in xylary elements performed in woody trees remain elusive. In combination, the data reviewed here suggest that the cytoskeleton plays important roles in determining the exact sites of cellulose deposition, overall SCW patterning and more specifically, the alignment and orientation of cellulose microfibrils. By relating the reviewed evidence to the process of wood formation, we present a model of microtubule participation in determining MFA in woody trees forming reaction wood (RW).

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Exploiting CELLULOSE SYNTHASE (CESA) Class Specificity to Probe Cellulose Microfibril Biosynthesis

Cited by 35 publications

References 50 publications

An atlas of Arabidopsis protein S-Acylation reveals its widespread role in plant cell organisation of and function

An atlas of Arabidopsis protein S-Acylation reveals its widespread role in plant cell organisation of and function

Secondary cell wall biosynthesis

The Cytoskeleton and Its Role in Determining Cellulose Microfibril Angle in Secondary Cell Walls of Woody Tree Species

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