Mutations of Arabidopsis TBL32 and TBL33 affect xylan acetylation and secondary wall deposition
Abstract
Xylan is a major acetylated polymer in plant lignocellulosic biomass and it can be monoand di-acetylated at O-2 and O-3 as well as mono-acetylated at O-3 of xylosyl residues that is substituted with glucuronic acid (GlcA) at O-2. Based on the finding that ESK1, an Arabidopsis thaliana DUF231 protein, specifically mediates xylan 2-O- and 3-O-monoacetylation, we previously proposed that different acetyltransferase activities are required for regiospecific acetyl substitutions of xylan. Here, we demonstrate the functional roles of TBL32 and TBL33, two ESK1 close homologs, in acetyl substitutions of xylan. Simultaneous mutations of TBL32 and TBL33 resulted in a significant reduction in xylan acetyl content and endoxylanase digestion of the mutant xylan released GlcA-substituted xylooligomers without acetyl groups. Structural analysis of xylan revealed that the tbl32 tbl33 mutant had a nearly complete loss of 3-O-acetylated, 2-O-GlcA-substituted xylosyl residues. A reduction in 3-Omonoacetylated and 2,3-di-O-acetylated xylosyl residues was also observed. Simultaneous mutations of TBL32, TBL33 and ESK1 resulted in a severe reduction in xylan acetyl level down to 15% of that of the wild type, and concomitantly, severely collapsed vessels and stunted plant growth. In particular, the S2 layer of secondary walls in xylem vessels of tbl33 esk1 and tbl32 tbl33 esk1more »
- Authors:
-
- Univ. of Georgia, Athens, GA (United States)
- Chinese Academy of Sciences (China)
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1311573
- Grant/Contract Number:
- FG02-03ER15415
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; acetylation; Arabidopsis thaliana; xylem; substitution mutation; flowering plants; plant growth and development; nuclear magnetic resonance; polymers
Citation Formats
Yuan, Youxi, Teng, Quincy, Zhong, Ruiqin, Haghighat, Marziyeh, Richardson, Elizabeth A., Ye, Zheng -Hua, and Zhang, Jin -Song. Mutations of Arabidopsis TBL32 and TBL33 affect xylan acetylation and secondary wall deposition. United States: N. p., 2016.
Web. doi:10.1371/journal.pone.0146460.
Yuan, Youxi, Teng, Quincy, Zhong, Ruiqin, Haghighat, Marziyeh, Richardson, Elizabeth A., Ye, Zheng -Hua, & Zhang, Jin -Song. Mutations of Arabidopsis TBL32 and TBL33 affect xylan acetylation and secondary wall deposition. United States. https://doi.org/10.1371/journal.pone.0146460
Yuan, Youxi, Teng, Quincy, Zhong, Ruiqin, Haghighat, Marziyeh, Richardson, Elizabeth A., Ye, Zheng -Hua, and Zhang, Jin -Song. Fri .
"Mutations of Arabidopsis TBL32 and TBL33 affect xylan acetylation and secondary wall deposition". United States. https://doi.org/10.1371/journal.pone.0146460. https://www.osti.gov/servlets/purl/1311573.
@article{osti_1311573,
title = {Mutations of Arabidopsis TBL32 and TBL33 affect xylan acetylation and secondary wall deposition},
author = {Yuan, Youxi and Teng, Quincy and Zhong, Ruiqin and Haghighat, Marziyeh and Richardson, Elizabeth A. and Ye, Zheng -Hua and Zhang, Jin -Song},
abstractNote = {Xylan is a major acetylated polymer in plant lignocellulosic biomass and it can be monoand di-acetylated at O-2 and O-3 as well as mono-acetylated at O-3 of xylosyl residues that is substituted with glucuronic acid (GlcA) at O-2. Based on the finding that ESK1, an Arabidopsis thaliana DUF231 protein, specifically mediates xylan 2-O- and 3-O-monoacetylation, we previously proposed that different acetyltransferase activities are required for regiospecific acetyl substitutions of xylan. Here, we demonstrate the functional roles of TBL32 and TBL33, two ESK1 close homologs, in acetyl substitutions of xylan. Simultaneous mutations of TBL32 and TBL33 resulted in a significant reduction in xylan acetyl content and endoxylanase digestion of the mutant xylan released GlcA-substituted xylooligomers without acetyl groups. Structural analysis of xylan revealed that the tbl32 tbl33 mutant had a nearly complete loss of 3-O-acetylated, 2-O-GlcA-substituted xylosyl residues. A reduction in 3-Omonoacetylated and 2,3-di-O-acetylated xylosyl residues was also observed. Simultaneous mutations of TBL32, TBL33 and ESK1 resulted in a severe reduction in xylan acetyl level down to 15% of that of the wild type, and concomitantly, severely collapsed vessels and stunted plant growth. In particular, the S2 layer of secondary walls in xylem vessels of tbl33 esk1 and tbl32 tbl33 esk1 exhibited an altered structure, indicating abnormal assembly of secondary wall polymers. Furthermore, these results demonstrate that TBL32 and TBL33 play an important role in xylan acetylation and normal deposition of secondary walls.},
doi = {10.1371/journal.pone.0146460},
journal = {PLoS ONE},
number = 1,
volume = 11,
place = {United States},
year = {Fri Jan 08 00:00:00 EST 2016},
month = {Fri Jan 08 00:00:00 EST 2016}
}
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Xylan in the Middle: Understanding Xylan Biosynthesis and Its Metabolic Dependencies Toward Improving Wood Fiber for Industrial Processing
journal, February 2019
- Wierzbicki, Martin P.; Maloney, Victoria; Mizrachi, Eshchar
- Frontiers in Plant Science, Vol. 10