Direct Measurement of Plant Cellulose Microfibril and Bundles in Native Cell Walls
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 th...
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doaj-5fd5c60c47bd4733988c5c19729296932020-11-25T02:54:16ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-04-011110.3389/fpls.2020.00479521339Direct Measurement of Plant Cellulose Microfibril and Bundles in Native Cell WallsBo Song0Shuai Zhao1Shuai Zhao2Shuai Zhao3Wei Shen4Wei Shen5Cynthia Collings6Cynthia Collings7Shi-You Ding8Shi-You Ding9Department of Plant Biology, Michigan State University, East Lansing, MI, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, MI, United StatesGreat Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United StatesState Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, College of Life Science and Technology, Guangxi University, Nanning, ChinaDepartment of Plant Biology, Michigan State University, East Lansing, MI, United StatesGreat Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, MI, United StatesGreat Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, MI, United StatesGreat Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United StatesPlants 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.https://www.frontiersin.org/article/10.3389/fpls.2020.00479/fullcellulose microfibrilatomic force microscopydirect imagingprimary cell wallsecondary cell wallcellulose synthesis |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Bo Song Shuai Zhao Shuai Zhao Shuai Zhao Wei Shen Wei Shen Cynthia Collings Cynthia Collings Shi-You Ding Shi-You Ding |
spellingShingle |
Bo Song Shuai Zhao Shuai Zhao Shuai Zhao Wei Shen Wei Shen Cynthia Collings Cynthia Collings Shi-You Ding Shi-You Ding Direct Measurement of Plant Cellulose Microfibril and Bundles in Native Cell Walls Frontiers in Plant Science cellulose microfibril atomic force microscopy direct imaging primary cell wall secondary cell wall cellulose synthesis |
author_facet |
Bo Song Shuai Zhao Shuai Zhao Shuai Zhao Wei Shen Wei Shen Cynthia Collings Cynthia Collings Shi-You Ding Shi-You Ding |
author_sort |
Bo Song |
title |
Direct Measurement of Plant Cellulose Microfibril and Bundles in Native Cell Walls |
title_short |
Direct Measurement of Plant Cellulose Microfibril and Bundles in Native Cell Walls |
title_full |
Direct Measurement of Plant Cellulose Microfibril and Bundles in Native Cell Walls |
title_fullStr |
Direct Measurement of Plant Cellulose Microfibril and Bundles in Native Cell Walls |
title_full_unstemmed |
Direct Measurement of Plant Cellulose Microfibril and Bundles in Native Cell Walls |
title_sort |
direct measurement of plant cellulose microfibril and bundles in native cell walls |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Plant Science |
issn |
1664-462X |
publishDate |
2020-04-01 |
description |
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. |
topic |
cellulose microfibril atomic force microscopy direct imaging primary cell wall secondary cell wall cellulose synthesis |
url |
https://www.frontiersin.org/article/10.3389/fpls.2020.00479/full |
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