CEF3 is involved in membrane trafficking and essential for secondary cell wall biosynthesis and its mutation enhanced biomass enzymatic saccharification in rice

Abstract Background As one of the most important staple food crops, rice produces large of agronomic biomass residues that contain lots of secondary cell walls (SCWs). Membrane trafficking plays key roles in SCWs biosynthesis, but information association membrane trafficking and SCWs formation in pl...

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Main Authors: Hongrui Jiang, Yan Ren, Junyao Guo, Huijie Yang, Xiaotong Zhu, Wenhao Li, Liangzhi Tao, Yue Zhan, Qi Wang, Yuejin Wu, Binmei Liu, Yafeng Ye
Format: Article
Language:English
Published: BMC 2022-10-01
Series:Biotechnology for Biofuels and Bioproducts
Subjects:
Online Access:https://doi.org/10.1186/s13068-022-02205-y
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author Hongrui Jiang
Yan Ren
Junyao Guo
Huijie Yang
Xiaotong Zhu
Wenhao Li
Liangzhi Tao
Yue Zhan
Qi Wang
Yuejin Wu
Binmei Liu
Yafeng Ye
author_facet Hongrui Jiang
Yan Ren
Junyao Guo
Huijie Yang
Xiaotong Zhu
Wenhao Li
Liangzhi Tao
Yue Zhan
Qi Wang
Yuejin Wu
Binmei Liu
Yafeng Ye
author_sort Hongrui Jiang
collection DOAJ
description Abstract Background As one of the most important staple food crops, rice produces large of agronomic biomass residues that contain lots of secondary cell walls (SCWs). Membrane trafficking plays key roles in SCWs biosynthesis, but information association membrane trafficking and SCWs formation in plants is limited. Results In this study, we report the function characterization of a rice mutant, c ulm e asily f ragile 3 (cef3), that exhibits growth retardation and fragile culm phenotype with significantly altered cell wall composition and reduced secondary wall thickness. Map-based cloning revealed that CEF3 encodes a homologous protein of Arabidopsis STOMATAL CYTOKINESIS DEFECTIVE2 (SCD2). The saccharification assays revealed that CEF3 mutation can improve biomass enzymatic saccharification. Expression pattern analysis indicated that CEF3 is ubiquitously expressed in many organs at different developmental stages. Subcellular localization revealed that CEF3 is a Golgi-localized protein. The FM4-64 uptake assay revealed CEF3 is involved in endocytosis. Furthermore, mutation of CEF3 not only affected cellulose synthesis-related genes expression, but also altered the abundance of cellulose synthase catalytic subunit 9 (OsCESA9) in the PM and in the endomembrane systems. Conclusions This study has demonstrated that CEF3 participates in the membrane trafficking that is essential for normal cellulose and other polysaccharides biosynthesis of the secondary cell wall, thereby manipulation of CEF3 could alter cellulose content and enhance biomass enzymatic saccharification in rice plants. Therefore, the study of the function of CEF3 can provide a strategy for genetic modification of SCWs in bioenergy crops.
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spelling doaj.art-4e2d41b9a0e942728d8088fd8d62fcd32022-12-22T02:23:49ZengBMCBiotechnology for Biofuels and Bioproducts2731-36542022-10-0115111310.1186/s13068-022-02205-yCEF3 is involved in membrane trafficking and essential for secondary cell wall biosynthesis and its mutation enhanced biomass enzymatic saccharification in riceHongrui Jiang0Yan Ren1Junyao Guo2Huijie Yang3Xiaotong Zhu4Wenhao Li5Liangzhi Tao6Yue Zhan7Qi Wang8Yuejin Wu9Binmei Liu10Yafeng Ye11Key Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesKey Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of SciencesAbstract Background As one of the most important staple food crops, rice produces large of agronomic biomass residues that contain lots of secondary cell walls (SCWs). Membrane trafficking plays key roles in SCWs biosynthesis, but information association membrane trafficking and SCWs formation in plants is limited. Results In this study, we report the function characterization of a rice mutant, c ulm e asily f ragile 3 (cef3), that exhibits growth retardation and fragile culm phenotype with significantly altered cell wall composition and reduced secondary wall thickness. Map-based cloning revealed that CEF3 encodes a homologous protein of Arabidopsis STOMATAL CYTOKINESIS DEFECTIVE2 (SCD2). The saccharification assays revealed that CEF3 mutation can improve biomass enzymatic saccharification. Expression pattern analysis indicated that CEF3 is ubiquitously expressed in many organs at different developmental stages. Subcellular localization revealed that CEF3 is a Golgi-localized protein. The FM4-64 uptake assay revealed CEF3 is involved in endocytosis. Furthermore, mutation of CEF3 not only affected cellulose synthesis-related genes expression, but also altered the abundance of cellulose synthase catalytic subunit 9 (OsCESA9) in the PM and in the endomembrane systems. Conclusions This study has demonstrated that CEF3 participates in the membrane trafficking that is essential for normal cellulose and other polysaccharides biosynthesis of the secondary cell wall, thereby manipulation of CEF3 could alter cellulose content and enhance biomass enzymatic saccharification in rice plants. Therefore, the study of the function of CEF3 can provide a strategy for genetic modification of SCWs in bioenergy crops.https://doi.org/10.1186/s13068-022-02205-ySecondary cell wall (SCW)RiceCellulose biosynthesisBiomassSaccharificationmembrane trafficking
spellingShingle Hongrui Jiang
Yan Ren
Junyao Guo
Huijie Yang
Xiaotong Zhu
Wenhao Li
Liangzhi Tao
Yue Zhan
Qi Wang
Yuejin Wu
Binmei Liu
Yafeng Ye
CEF3 is involved in membrane trafficking and essential for secondary cell wall biosynthesis and its mutation enhanced biomass enzymatic saccharification in rice
Biotechnology for Biofuels and Bioproducts
Secondary cell wall (SCW)
Rice
Cellulose biosynthesis
Biomass
Saccharification
membrane trafficking
title CEF3 is involved in membrane trafficking and essential for secondary cell wall biosynthesis and its mutation enhanced biomass enzymatic saccharification in rice
title_full CEF3 is involved in membrane trafficking and essential for secondary cell wall biosynthesis and its mutation enhanced biomass enzymatic saccharification in rice
title_fullStr CEF3 is involved in membrane trafficking and essential for secondary cell wall biosynthesis and its mutation enhanced biomass enzymatic saccharification in rice
title_full_unstemmed CEF3 is involved in membrane trafficking and essential for secondary cell wall biosynthesis and its mutation enhanced biomass enzymatic saccharification in rice
title_short CEF3 is involved in membrane trafficking and essential for secondary cell wall biosynthesis and its mutation enhanced biomass enzymatic saccharification in rice
title_sort cef3 is involved in membrane trafficking and essential for secondary cell wall biosynthesis and its mutation enhanced biomass enzymatic saccharification in rice
topic Secondary cell wall (SCW)
Rice
Cellulose biosynthesis
Biomass
Saccharification
membrane trafficking
url https://doi.org/10.1186/s13068-022-02205-y
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