Structure of cellulose microfibrils in primary cell walls from collenchymas

LH Thomas, V. Trevor Forsyth, A Sturcova, CJ Kennedy, RP May, CM Altaner, DC Apperley, Timothy Wess, MC Jarvis

Research output: Contribution to journalArticle

167 Citations (Scopus)

Abstract

In the primary walls of growing plant cells, the glucose polymer cellulose is assembled into long microfibrils a few nanometers in diameter. The rigidity and orientation of these microfibrils control cell expansion; therefore, cellulose synthesis is a key factor in the growth and morphogenesis of plants. Celery (Apium graveolens) collenchyma is a useful model system for the study of primary wall microfibril structure because its microfibrils are oriented with unusual uniformity, facilitating spectroscopic and diffraction experiments. Using a combination of x-ray and neutron scattering methods with vibrational and nuclear magnetic resonance spectroscopy, we show that celery collenchyma microfibrils were 2.9 to 3.0 nm in mean diameter, with a most probable structure containing 24 chains in cross section, arranged in eight hydrogen-bonded sheets of three chains, with extensive disorder in lateral packing, conformation, and hydrogen bonding. A similar 18-chain structure, and 24-chain structures of different shape, fitted the data less well. Conformational disorder was largely restricted to the surface chains, but disorder in chain packing was not. That is, in position and orientation, the surface chains conformed to the disordered lattice constituting the core of each microfibril. There was evidence that adjacent microfibrils were noncovalently aggregated together over part of their length, suggesting that the need to disrupt these aggregates might be a constraining factor in growth and in the hydrolysis of cellulose for biofuel production.
Original languageEnglish
Pages (from-to)465-476
Number of pages12
JournalPlant Physiology
Volume161
Issue number1
DOIs
Publication statusPublished - Jan 2013

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Microfibrils
collenchyma
Cellulose
Cell Wall
cellulose
celery
cell walls
Apium graveolens
growth factors
hydrogen bonding
cell aggregates
biofuels
hydrogen
morphogenesis
nuclear magnetic resonance spectroscopy
polymers
X-radiation
hydrolysis
Intercellular Signaling Peptides and Proteins
cells

Cite this

Thomas, LH., Forsyth, V. T., Sturcova, A., Kennedy, CJ., May, RP., Altaner, CM., ... Jarvis, MC. (2013). Structure of cellulose microfibrils in primary cell walls from collenchymas. Plant Physiology, 161(1), 465-476. https://doi.org/10.1104/pp.112.206359
Thomas, LH ; Forsyth, V. Trevor ; Sturcova, A ; Kennedy, CJ ; May, RP ; Altaner, CM ; Apperley, DC ; Wess, Timothy ; Jarvis, MC. / Structure of cellulose microfibrils in primary cell walls from collenchymas. In: Plant Physiology. 2013 ; Vol. 161, No. 1. pp. 465-476.
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Thomas, LH, Forsyth, VT, Sturcova, A, Kennedy, CJ, May, RP, Altaner, CM, Apperley, DC, Wess, T & Jarvis, MC 2013, 'Structure of cellulose microfibrils in primary cell walls from collenchymas', Plant Physiology, vol. 161, no. 1, pp. 465-476. https://doi.org/10.1104/pp.112.206359

Structure of cellulose microfibrils in primary cell walls from collenchymas. / Thomas, LH; Forsyth, V. Trevor; Sturcova, A; Kennedy, CJ; May, RP; Altaner, CM; Apperley, DC; Wess, Timothy; Jarvis, MC.

In: Plant Physiology, Vol. 161, No. 1, 01.2013, p. 465-476.

Research output: Contribution to journalArticle

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AU - Forsyth, V. Trevor

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AU - Apperley, DC

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AU - Jarvis, MC

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N2 - In the primary walls of growing plant cells, the glucose polymer cellulose is assembled into long microfibrils a few nanometers in diameter. The rigidity and orientation of these microfibrils control cell expansion; therefore, cellulose synthesis is a key factor in the growth and morphogenesis of plants. Celery (Apium graveolens) collenchyma is a useful model system for the study of primary wall microfibril structure because its microfibrils are oriented with unusual uniformity, facilitating spectroscopic and diffraction experiments. Using a combination of x-ray and neutron scattering methods with vibrational and nuclear magnetic resonance spectroscopy, we show that celery collenchyma microfibrils were 2.9 to 3.0 nm in mean diameter, with a most probable structure containing 24 chains in cross section, arranged in eight hydrogen-bonded sheets of three chains, with extensive disorder in lateral packing, conformation, and hydrogen bonding. A similar 18-chain structure, and 24-chain structures of different shape, fitted the data less well. Conformational disorder was largely restricted to the surface chains, but disorder in chain packing was not. That is, in position and orientation, the surface chains conformed to the disordered lattice constituting the core of each microfibril. There was evidence that adjacent microfibrils were noncovalently aggregated together over part of their length, suggesting that the need to disrupt these aggregates might be a constraining factor in growth and in the hydrolysis of cellulose for biofuel production.

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Thomas LH, Forsyth VT, Sturcova A, Kennedy CJ, May RP, Altaner CM et al. Structure of cellulose microfibrils in primary cell walls from collenchymas. Plant Physiology. 2013 Jan;161(1):465-476. https://doi.org/10.1104/pp.112.206359