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Structure/function relationships in the rosette cellulose synthesis complex illuminated by an evolutionary perspective

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Abstract

Cellulose microfibrils are a key component of plant cell walls, which in turn compose most of our renewable biomaterials. Consequently, there is considerable interest in understanding how cellulose microfibrils are made in living cells by the plant cellulose synthesis complex (CSC). This remarkable multi-subunit complex contains cellulose synthase (CESA) proteins, and it is often called a rosette due to its six-lobed shape. Each CSC moves within the plasma membrane as it spins a strong cellulose microfibril in its wake. To accomplish this biological manufacturing process, the CESAs harvest an activated sugar substrate from the cytoplasm for use in the polymerization of glucan chains. An elongating glucan is simultaneously translocated across the plasma membrane by each CESA, where the group of chains emanating from one CSC co-crystallizes into a cellulose microfibril that becomes part of the assembling cell wall. Here we review major advances in understanding CESA and CSC structure/function relationships since 2013, when ground-breaking insights about the structure of cellulose synthases in bacteria and plants were published. We additionally discuss: (a) the relationship of CSC substructure to the size of the fundamental cellulose fibril; (b) an evolutionary perspective on the driving force behind the existence of hetero-oligomeric CSCs that currently appear to dominate in land plants; and (c) how cellulose properties may be regulated by CESA and CSC activity. We also pose major questions that still remain in this rapidly changing and exciting research field.

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Abbreviations

BcsA:

Cellulose synthase in bacteria

BcsB:

Non-catalytic partner protein for BscA

CSC:

Cellulose synthesis complex

CESA:

Cellulose synthase in plants

CNE:

Constructive neutral evolution

CSR:

Class-specific region of CESA

DP:

Degree of polymerization

FF-TEM:

Freeze fracture transmission electron microscopy

P-CR:

Plant-conserved region of CESA

PCW:

Primary cell wall

PCW CSC:

Primary cell wall cellulose synthesis complex

SCW:

Secondary cell wall

SCW CSC:

Secondary cell wall cellulose synthesis complex

SSNMR:

Solid-state nuclear magnetic resonance

TMH:

Transmembrane helix

UDP-glucose:

Uridine diphosphate-alpha-d-glucose

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Acknowledgments

Under the Creative Commons License (http://creativecommons.org/licenses/by/4.0/), the graphical abstract includes a low resolution subset of the images originally published by the authors and their coworkers in Fig. 2 of Scientific Reports (Nixon et al. 2016). The writing of this review was supported by the US Department of Energy, Office of Science, Basic Energy Sciences as part of The Center for LignoCellulose Structure and Formation, an Energy Frontier Research Center under Award # DE-SC0001090.

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Correspondence to Candace H. Haigler.

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Haigler, C.H., Roberts, A.W. Structure/function relationships in the rosette cellulose synthesis complex illuminated by an evolutionary perspective. Cellulose 26, 227–247 (2019). https://doi.org/10.1007/s10570-018-2157-9

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  • DOI: https://doi.org/10.1007/s10570-018-2157-9

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