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      Overproduction of native endo-β-1,4-glucanases leads to largely enhanced biomass saccharification and bioethanol production by specific modification of cellulose features in transgenic rice

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          Abstract

          Background

          Genetic modification of plant cell walls has been implemented to reduce lignocellulosic recalcitrance for biofuel production. Plant glycoside hydrolase family 9 (GH9) comprises endo-β-1,4-glucanase in plants. Few studies have examined the roles of GH9 in cell wall modification. In this study, we independently overexpressed two genes from GH9B subclasses ( OsGH9B1 and OsGH9B3) and examined cell wall features and biomass saccharification in transgenic rice plants.

          Results

          Compared with the wild type (WT, Nipponbare), the OsGH9B1 and OsGH9B3 transgenic rice plants, respectively, contained much higher OsGH9B1 and OsGH9B3 protein levels and both proteins were observed in situ with nonspecific distribution in the plant cells. The transgenic lines exhibited significantly increased cellulase activity in vitro than the WT. The OsGH9B1 and OsGH9B3 transgenic plants showed a slight alteration in three wall polymer compositions (cellulose, hemicelluloses, and lignin), in their stem mechanical strength and biomass yield, but were significantly decreased in the cellulose degree of polymerization (DP) and lignocellulose crystalline index (CrI) by 21–22%. Notably, the crude cellulose substrates of the transgenic lines were more efficiently digested by cellobiohydrolase (CBHI) than those of the WT, indicating the significantly increased amounts of reducing ends of β-1,4-glucans in cellulose microfibrils. Finally, the engineered lines generated high sugar yields after mild alkali pretreatments and subsequent enzymatic hydrolysis, resulting in the high bioethanol yields obtained at 22.5% of dry matter.

          Conclusions

          Overproduction of OsGH9B1/B3 enzymes should have specific activity in the postmodification of cellulose microfibrils. The increased reducing ends of β-1,4-glucan chains for reduced cellulose DP and CrI positively affected biomass enzymatic saccharification. Our results demonstrate a potential strategy for genetic modification of cellulose microfibrils in bioenergy crops.

          Electronic supplementary material

          The online version of this article (10.1186/s13068-018-1351-1) contains supplementary material, which is available to authorized users.

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          Most cited references53

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          Toward an aggregated understanding of enzymatic hydrolysis of cellulose: noncomplexed cellulase systems.

          Information pertaining to enzymatic hydrolysis of cellulose by noncomplexed cellulase enzyme systems is reviewed with a particular emphasis on development of aggregated understanding incorporating substrate features in addition to concentration and multiple cellulase components. Topics considered include properties of cellulose, adsorption, cellulose hydrolysis, and quantitative models. A classification scheme is proposed for quantitative models for enzymatic hydrolysis of cellulose based on the number of solubilizing activities and substrate state variables included. We suggest that it is timely to revisit and reinvigorate functional modeling of cellulose hydrolysis, and that this would be highly beneficial if not necessary in order to bring to bear the large volume of information available on cellulase components on the primary applications that motivate interest in the subject. 2004 Wiley Periodicals, Inc.
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            Lignin valorization through integrated biological funneling and chemical catalysis.

            Lignin is an energy-dense, heterogeneous polymer comprised of phenylpropanoid monomers used by plants for structure, water transport, and defense, and it is the second most abundant biopolymer on Earth after cellulose. In production of fuels and chemicals from biomass, lignin is typically underused as a feedstock and burned for process heat because its inherent heterogeneity and recalcitrance make it difficult to selectively valorize. In nature, however, some organisms have evolved metabolic pathways that enable the utilization of lignin-derived aromatic molecules as carbon sources. Aromatic catabolism typically occurs via upper pathways that act as a "biological funnel" to convert heterogeneous substrates to central intermediates, such as protocatechuate or catechol. These intermediates undergo ring cleavage and are further converted via the β-ketoadipate pathway to central carbon metabolism. Here, we use a natural aromatic-catabolizing organism, Pseudomonas putida KT2440, to demonstrate that these aromatic metabolic pathways can be used to convert both aromatic model compounds and heterogeneous, lignin-enriched streams derived from pilot-scale biomass pretreatment into medium chain-length polyhydroxyalkanoates (mcl-PHAs). mcl-PHAs were then isolated from the cells and demonstrated to be similar in physicochemical properties to conventional carbohydrate-derived mcl-PHAs, which have applications as bioplastics. In a further demonstration of their utility, mcl-PHAs were catalytically converted to both chemical precursors and fuel-range hydrocarbons. Overall, this work demonstrates that the use of aromatic catabolic pathways enables an approach to valorize lignin by overcoming its inherent heterogeneity to produce fuels, chemicals, and materials.
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              How biotech can transform biofuels.

              For cellulosic ethanol to become a reality, biotechnological solutions should focus on optimizing the conversion of biomass to sugars.
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                Author and article information

                Contributors
                hjfjiayoua@yeah.net
                xiatao@mail.hzau.edu.cn
                lighua@imu.edu.cn
                libusher@sina.com
                ly_8904@126.com
                wyt@mail.hzau.edu.cn
                wym_quiet@yeah.net
                2295853034@qq.com
                xiegsh@mail.hzau.edu.cn
                fwbai@dlut.edu.cn
                lpeng@mail.hzau.edu.cn
                +86 27 87281765 , lqwang@mail.hzau.edu.cn , http://bbrc.hzau.edu.cn
                Journal
                Biotechnol Biofuels
                Biotechnol Biofuels
                Biotechnology for Biofuels
                BioMed Central (London )
                1754-6834
                9 January 2019
                9 January 2019
                2019
                : 12
                : 11
                Affiliations
                [1 ]ISNI 0000 0004 1790 4137, GRID grid.35155.37, Biomass and Bioenergy Research Centre, College of Plant Science and Technology, College of Life Science and Technology, , Huazhong Agricultural University, ; Wuhan, 430070 China
                [2 ]ISNI 0000 0004 1761 0411, GRID grid.411643.5, State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, School of Life Sciences, , Inner Mongolia University, ; Hohhot, 010070 China
                [3 ]ISNI 0000 0004 1781 4780, GRID grid.488491.8, College of Bioengineering, , Jingchu University of Technology, ; Jingmen, 448000 China
                [4 ]ISNI 0000 0004 0368 8293, GRID grid.16821.3c, State Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, , Shanghai Jiao Tong University, ; Shanghai, 200240 China
                [5 ]ISNI 0000 0001 2254 5798, GRID grid.256609.e, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, College of Agriculture, , Guangxi University, ; Nanning, 530004 China
                Article
                1351
                10.1186/s13068-018-1351-1
                6325865
                30636971
                e787fe85-acdc-45d0-b64f-14bbb8aebe07
                © The Author(s) 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 30 July 2018
                : 29 December 2018
                Funding
                Funded by: National Science Foundation of China
                Award ID: 31670296
                Award ID: 31571721
                Award ID: 31171524
                Award ID: 31771775
                Award Recipient :
                Funded by: National 111 Project
                Award ID: B08032
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Biotechnology
                endo-β-1,4-glucanases,transgenic rice,gh9b,cellulose modification,biomass saccharification,bioethanol production,chemical pretreatment

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