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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Main Authors: Bo Song, Shuai Zhao, Wei Shen, Cynthia Collings, Shi-You Ding
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.00479/full
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spelling 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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