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.
Highlights
In the primary walls of growing plant cells, the glucose polymer cellulose is assembled into long microfibrils a few nanometers in diameter
The stiffness of the cell wall is greatest in the direction of the cellulose microfibrils, where growth is directional and the predominant microfibril orientation is usually transverse to the growth direction (Green, 1999; MacKinnon et al, 2006; Szymanski and Cosgrove, 2009)
When collagen or cellulose microfibrils of fixed diameter are packed in arrays with some degree of regularity, small-angle diffraction of x-rays or neutrons (Bragg scattering) from the microfibrils themselves can be observed (Hulmes et al, 1995; Fernandes et al, 2011)
Summary
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; cellulose synthesis is a key factor in the growth and morphogenesis of plants. Growth and form in plants are controlled by the precisely oriented expansion of the walls of individual cells. Primary wall cellulose was thought to have a unique crystal structure called cellulose IV1 (Dinand et al, 1996), but NMR evidence suggests the presence of forms similar to the better characterized cellulose Ia and Ib crystalline forms together with large quantities of less ordered cellulose (Wickholm et al, 1998; Sturcová et al, 2004; Wada et al, 2004). In certain other mutant lines, the crystallinity of the microfibrils appears to be affected (Fujita et al, 2011; Harris et al, 2012; Sánchez-Rodríguez et al, 2012)
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