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      Heterogeneity and Glycan Masking of Cell Wall Microstructures in the Stems of Miscanthus x giganteus, and Its Parents M. sinensis and M. sacchariflorus

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          Abstract

          Plant cell walls, being repositories of fixed carbon, are important sources of biomass and renewable energy. Miscanthus species are fast growing grasses with a high biomass yield and they have been identified as potential bioenergy crops. Miscanthus x giganteus is the sterile hybrid between M. sinensis and M. sacchariflorus, with a faster and taller growth than its parents. In this study, the occurrence of cell wall polysaccharides in stems of Miscanthus species has been determined using fluorescence imaging with sets of cell wall directed monoclonal antibodies. Heteroxylan and mixed linkage-glucan (MLG) epitopes are abundant in stem cell walls of Miscanthus species, but their distributions are different in relation to the interfascicular parenchyma and these epitopes also display different developmental dynamics. Detection of pectic homogalacturonan (HG) epitopes was often restricted to intercellular spaces of parenchyma regions and, notably, the high methyl ester LM20 HG epitope was specifically abundant in the pith parenchyma cell walls of M. x giganteus. Some cell wall probes cannot access their target glycan epitopes because of masking by other polysaccharides. In the case of Miscanthus stems, masking of xyloglucan by heteroxylan and masking of pectic galactan by heteroxylan and MLG was detected in certain cell wall regions. Knowledge of tissue level heterogeneity of polysaccharide distributions and molecular architectures in Miscanthus cell wall structures will be important for both understanding growth mechanisms and also for the development of potential strategies for the efficient deconstruction of Miscanthus biomass.

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          Most cited references28

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          Hemicelluloses.

          Hemicelluloses are polysaccharides in plant cell walls that have beta-(1-->4)-linked backbones with an equatorial configuration. Hemicelluloses include xyloglucans, xylans, mannans and glucomannans, and beta-(1-->3,1-->4)-glucans. These types of hemicelluloses are present in the cell walls of all terrestrial plants, except for beta-(1-->3,1-->4)-glucans, which are restricted to Poales and a few other groups. The detailed structure of the hemicelluloses and their abundance vary widely between different species and cell types. The most important biological role of hemicelluloses is their contribution to strengthening the cell wall by interaction with cellulose and, in some walls, with lignin. These features are discussed in relation to widely accepted models of the primary wall. Hemicelluloses are synthesized by glycosyltransferases located in the Golgi membranes. Many glycosyltransferases needed for biosynthesis of xyloglucans and mannans are known. In contrast, the biosynthesis of xylans and beta-(1-->3,1-->4)-glucans remains very elusive, and recent studies have led to more questions than answers.
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            Cellulose synthesis in higher plants.

            Cellulose microfibrils play essential roles in the organization of plant cell walls, thereby allowing a growth habit based on turgor. The fibrils are made by 30 nm diameter plasma membrane complexes composed of approximately 36 subunits representing at least three types of related CESA proteins. The complexes assemble in the Golgi, where they are inactive, and move to the plasma membrane, where they become activated. The complexes move through the plasma membrane during cellulose synthesis in directions that coincide with the orientation of microtubules. Recent, simultaneous, live-cell imaging of cellulose synthase and microtubules indicates that the microtubules exert a direct influence on the orientation of cellulose deposition. Genetic studies in Arabidopsis have identified a number of genes that contribute to the overall process of cellulose synthesis, but the role of these proteins is not yet known.
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              Heterogeneity in the chemistry, structure and function of plant cell walls.

              Higher plants resist the forces of gravity and powerful lateral forces through the cumulative strength of the walls that surround individual cells. These walls consist mainly of cellulose, noncellulosic polysaccharides and lignin, in proportions that depend upon the specific functions of the cell and its stage of development. Spatially and temporally controlled heterogeneity in the physicochemical properties of wall polysaccharides is observed at the tissue and individual cell levels, and emerging in situ technologies are providing evidence that this heterogeneity also occurs across a single cell wall. We consider the origins of cell wall heterogeneity and identify contributing factors that are inherent in the molecular mechanisms of polysaccharide biosynthesis and are crucial for the changing biological functions of the wall during growth and development. We propose several key questions to be addressed in cell wall biology, together with an alternative two-phase model for the assembly of noncellulosic polysaccharides in plants.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                29 November 2013
                : 8
                : 11
                : e82114
                Affiliations
                [1 ]Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, United Kingdom
                [2 ]Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Plas Gogerddan, Aberystwyth, United Kingdom
                Nanjing Agricultural University, China
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JX MB JPK. Performed the experiments: JX. Analyzed the data: JX MB JPK. Contributed reagents/materials/analysis tools: JX MB JPK. Wrote the manuscript: JX MB JPK.

                Article
                PONE-D-13-26312
                10.1371/journal.pone.0082114
                3843723
                24312403
                77cb984d-6653-46ae-89bb-4fa0bbf6ed6a
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 24 June 2013
                : 16 October 2013
                Funding
                The authors acknowledge financial support from the China Scholarship Council/University of Leeds to JX. MB was supported by the Biotechnology and Biological Sciences Research Council (BBSRC) Institute Strategic Programme Grant BBS/E/W/00003134. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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