Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis[OPEN]

被引:95
作者
Du, Juan [1 ]
Kirui, Alex [2 ]
Huang, Shixin [3 ,4 ]
Wang, Lianglei [1 ]
Barnes, William J. [3 ,5 ,8 ]
Kiemle, Sarah N. [3 ,5 ,9 ]
Zheng, Yunzhen [3 ]
Rui, Yue [5 ,10 ]
Ruan, Mei [1 ]
Qi, Shiqian [6 ,7 ]
Kim, Seong H. [3 ,4 ]
Wang, Tuo [2 ]
Cosgrove, Daniel J. [3 ,5 ]
Anderson, Charles T. [3 ,5 ]
Xiao, Chaowen [1 ]
机构
[1] Sichuan Univ, Coll Life Sci, Minist Educ, Key Lab Bioresource & Ecoenvironm, Chengdu 610064, Peoples R China
[2] Louisiana State Univ, Dept Chem, Baton Rouge, LA 70803 USA
[3] Penn State Univ, Ctr Lignocellulose Struct & Format, University Pk, PA 16802 USA
[4] Penn State Univ, Dept Chem Engn, University Pk, PA 16802 USA
[5] Penn State Univ, Dept Biol, University Pk, PA 16802 USA
[6] Sichuan Univ, West China Hosp, State Key Lab Biotherapy, Dept Urol, Chengdu 610041, Peoples R China
[7] Natl Collaborat Innovat Ctr, Chengdu 610041, Peoples R China
[8] Univ Georgia, Complex Carbohydrate Res Ctr, Athens, GA 30602 USA
[9] Mt Holyoke Coll, Ctr Sci, S Hadley, MA 01075 USA
[10] Stanford Univ, Dept Biol, Stanford, CA 94305 USA
基金
中国博士后科学基金;
关键词
PRIMARY-CELL WALL; MICROTUBULE-ASSOCIATED PROTEINS; RECEPTOR-LIKE KINASES; ARABIDOPSIS-THALIANA; PUTATIVE METHYLTRANSFERASE; HOMOGALACTURONAN METHYLTRANSFERASE; POLYSACCHARIDE INTERACTIONS; CORTICAL MICROTUBULES; S-ADENOSYLMETHIONINE; SPECTRAL FEATURES;
D O I
10.1105/tpc.20.00252
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Pectins are abundant in the cell walls of dicotyledonous plants, but how they interact with other wall polymers and influence wall integrity and cell growth has remained mysterious. Here, we verified that QUASIMODO2 (QUA2) is a pectin methyltransferase and determined that QUA2 is required for normal pectin biosynthesis. To gain further insight into how pectin affects wall assembly and integrity maintenance, we investigated cellulose biosynthesis, cellulose organization, cortical microtubules, and wall integrity signaling in two mutant alleles of Arabidopsis (Arabidopsis thaliana) QUA2, qua2 and tsd2. In both mutants, crystalline cellulose content is reduced, cellulose synthase particles move more slowly, and cellulose organization is aberrant. NMR analysis shows higher mobility of cellulose and matrix polysaccharides in the mutants. Microtubules in mutant hypocotyls have aberrant organization and depolymerize more readily upon treatment with oryzalin or external force. The expression of genes related to wall integrity, wall biosynthesis, and microtubule stability is dysregulated in both mutants. These data provide insights into how homogalacturonan is methylesterified upon its synthesis, the mechanisms by which pectin functionally interacts with cellulose, and how these interactions are translated into intracellular regulation to maintain the structural integrity of the cell wall during plant growth and development. Physical and functional interactions between pectin and cellulose are required for normal wall assembly and plant growth, as revealed in analyses of mutants for a pectin methyltransferase.
引用
收藏
页码:3576 / 3597
页数:22
相关论文
共 107 条
[1]   The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division [J].
Ambrose, J. Christian ;
Shoji, Tsubasa ;
Kotzer, Amanda M. ;
Pighin, Jamie A. ;
Wasteneys, Geoffrey O. .
PLANT CELL, 2007, 19 (09) :2763-2775
[2]   A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex [J].
Amos, Robert A. ;
Pattathil, Sivakumar ;
Yang, Jeong-Yeh ;
Atmodjo, Melani A. ;
Urbanowicz, Breeanna R. ;
Moremen, Kelley W. ;
Mohnen, Debra .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2018, 293 (49) :19047-19063
[3]   Evolving Views of Pectin Biosynthesis [J].
Atmodjo, Melani A. ;
Hao, Zhangying ;
Mohnen, Debra .
ANNUAL REVIEW OF PLANT BIOLOGY, VOL 64, 2013, 64 :747-+
[4]   Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan: galacturonosyltransferase complex [J].
Atmodjo, Melani A. ;
Sakuragi, Yumiko ;
Zhu, Xiang ;
Burrell, Amy J. ;
Mohanty, Sushree S. ;
Atwood, James A., III ;
Orlando, Ron ;
Scheller, Henrik V. ;
Mohnen, Debra .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2011, 108 (50) :20225-20230
[5]   Quantification of crystalline cellulose in lignocellulosic biomass using sum frequency generation (SFG) vibration spectroscopy and comparison with other analytical methods [J].
Barnette, Anna L. ;
Lee, Christopher ;
Bradley, Laura C. ;
Schreiner, Edward P. ;
Park, Yong Bum ;
Shin, Heenae ;
Cosgrove, Daniel J. ;
Park, Sunkyu ;
Kim, Seong H. .
CARBOHYDRATE POLYMERS, 2012, 89 (03) :802-809
[6]   PECTINS AS MEDIATORS OF WALL POROSITY IN SOYBEAN CELLS [J].
BARONEPEL, O ;
GHARYAL, PK ;
SCHINDLER, M .
PLANTA, 1988, 175 (03) :389-395
[7]   Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis [J].
Baskin, TI ;
Beemster, GTS ;
Judy-March, JE ;
Marga, F .
PLANT PHYSIOLOGY, 2004, 135 (04) :2279-2290
[8]   Pectin Biosynthesis Is Critical for Cell Wall Integrity and Immunity in Arabidopsis thaliana [J].
Bethke, Gerit ;
Thao, Amanda ;
Xiong, Guangyan ;
Li, Baohua ;
Soltis, Nicole E. ;
Hatsugai, Noriyuki ;
Hillmer, Rachel A. ;
Katagiri, Fumiaki ;
Kliebenstein, Daniel J. ;
Pauly, Markus ;
Glazebrook, Jane .
PLANT CELL, 2016, 28 (02) :537-556
[9]   Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis [J].
Biswal, Ajaya K. ;
Atmodjo, Melani A. ;
Li, Mi ;
Baxter, Holly L. ;
Yoo, Chang Geun ;
Pu, Yunqiao ;
Lee, Yi-Ching ;
Mazarei, Mitra ;
Black, Ian M. ;
Zhang, Ji-Yi ;
Ramanna, Hema ;
Bray, Adam L. ;
King, Zachary R. ;
LaFayette, Peter R. ;
Pattathil, Sivakumar ;
Donohoe, Bryon S. ;
Mohanty, Sushree S. ;
Ryno, David ;
Yee, Kelsey ;
Thompson, Olivia A. ;
Rodriguez, Miguel, Jr. ;
Dumitrache, Alexandru ;
Natzke, Jace ;
Winkeler, Kim ;
Collins, Cassandra ;
Yang, Xiaohan ;
Tan, Li ;
Sykes, Robert W. ;
Gjersing, Erica L. ;
Ziebell, Angela ;
Turner, Geoffrey B. ;
Decker, Stephen R. ;
Hahn, Michael G. ;
Davison, Brian H. ;
Udvardi, Michael K. ;
Mielenz, Jonathan R. ;
Davis, Mark F. ;
Nelson, Richard S. ;
Parrott, Wayne A. ;
Ragauskas, Arthur J. ;
Stewart, C. Neal, Jr. ;
Mohnen, Debra .
NATURE BIOTECHNOLOGY, 2018, 36 (03) :249-+
[10]   Differential innate immune signalling via Ca2+ sensor protein kinases [J].
Boudsocq, Marie ;
Willmann, Matthew R. ;
McCormack, Matthew ;
Lee, Horim ;
Shan, Libo ;
He, Ping ;
Bush, Jenifer ;
Cheng, Shu-Hua ;
Sheen, Jen .
NATURE, 2010, 464 (7287) :418-U116