Abstract
Plants use rigid cellulose together with non-cellulosic matrix polymers to build cell walls. Cellulose microfibrils comprise linear β(1,4)-glucan chains packed through inter- and intra-chain hydrogen-bonding networks and van der Waals forces. Due to its small size, the number of glucan chains and their arrangement in a microfibril remains elusive. Here we used atomic force microscopy (AFM) to directly image primary cell walls (PCWs) and secondary cell walls (SCWs) from fresh tissues of maize (Zea mays) under near-native conditions. By analyzing cellulose structure in different types of cell walls, we were able to measure the individual microfibrils in elongated PCWs at the sub-nanometer scale. The dimension of the microfibril was measured at 3.68 ± 0.13 nm in width and 2.25 ± 0.10 nm in height. By superimposing multiple AFM height profiles of these microfibrils, the overlay area representing the cross-section was estimated at 5.6 ± 0.4 nm2, which fitted well to an 18-chain model packed as six sheets with 234432 conformation. Interestingly we found in PCW, all these individual microfibrils could be traced back to a bundle in larger imaging area, suggesting cellulose are synthesized as large bundles in PCWs, and then split during cell expansion or elongation. In SCWs where cell growth has ceased we observed nearly-parallel twined or individual microfibrils that appeared to be embedded separately in the matrix polymers without the splitting effect, indicating different mechanisms of cellulose biosynthesis in PCW and SCW. The sub-nanometer structure of the microfibril presented here was measured exclusively from elongated PCWs, further study is required to verify if it represents the inherent structure synthesized by the cellulose synthase complex in PCWs and SCWs.
Highlights
Plant growth and development relies on the regulation of cell wall biogenesis
By exploring the high quality atomic force microscopy (AFM) images, we found only in the case of a microfibril that run across the top of another microfibril (Figure 5A), provided a relative firm base locally to allow highly stable data acquisition, which could be found in the surface of elongated primary cell walls (PCWs)
Considering the facts that a mixture of bundles in variable sizes and individual microfibrils co-exists in different layers of any given cell wall, and the amount of matrix components may affect the crystalline features of cellulose (Martinez-Sanz et al, 2017), the diffraction data measured from ensemble averaging of these mixed cellulose structures may not represent the fundamental structure of the microfibril
Summary
Plant growth and development relies on the regulation of cell wall biogenesis. As the main skeletal component, cellulose forms interwoven microfibril networks to constitute the multilayer (lamellae) architecture observed for plant cell walls (Somerville et al, 2004). During cell growth and development, the biosynthesis and dynamic arrangement of the cellulose microfibrils play a key role in maintaining the mechanical properties and physiological functions of the cell walls (Cosgrove, 2016; Zhang et al, 2017, 2019). Cellulose has relatively simple chemistry that comprises a number of Direct Imaging Plant Cellulose Microfibril linear homopolymeric chains of β(1,4)-D-glucosyl residues packed through intra- and inter-chain hydrogen bonding networks and van der Waals forces to form para-crystalline microfibrils. The cellulose microfibril has a small cross-sectional dimension (2–3 nm), in which the number of chains and how they pack into a microfibril is unknown
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