Investigating Biochemical and Developmental Dependencies of Lignification with a Click-Compatible Monolignol Analog in Arabidopsis thaliana Stems
Abstract
Lignin is a key structural component of plant cell walls that provides rigidity, strength, and resistance against microbial attacks. This hydrophobic polymer also serves a crucial role in water transport. Despite its abundance and essential functions, several aspects of lignin biosynthesis and deposition remain cryptic. Lignin precursors are known to be synthesized in the cytoplasm by complex biosynthetic pathways, after which they are transported to the apoplastic space, where they are polymerized via free radical coupling reactions into polymeric lignin. However, the lignin deposition process and the factors controlling it are unclear. In this study, the biochemical and developmental dependencies of lignification were investigated using a click-compatible monolignol analog, 3-O-propargylcaffeyl alcohol (3-OPC), which can incorporate into both in vitro polymerized lignin and Arabidopsis thaliana tissues. Fluorescence labeling of 3-OPC using click chemistry followed by confocal fluorescence microscopy enabled the detection and imaging of 3-OPC incorporation patterns. These patterns were consistent with endogenous lignification observed in different developmental stages of Arabidopsis stems. However, the concentration of supplied monolignols influenced where lignification occurred at the subcellular level, with low concentrations being deposited in cell corners and middle lamellae and high concentrations also being deposited in secondary walls. Experimental inhibition of multiple lignificationmore »
- Authors:
-
- The Pennsylvania State Univ., University Park, PA (United States)
- The Pennsylvania State Univ., University Park, PA (United States); The Pennsylvania State Univ., Altoona, PA (United States)
- Publication Date:
- Research Org.:
- Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1388043
- Grant/Contract Number:
- SC0001090
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Volume: 7; Related Information: CLSF partners with Pennsylvania State University (lead); North Carolina State University; University of Rhode Island; Virginia Tech University; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; biofuels (including algae and biomass); bio-inspired; membrane; carbon sequestration; materials and chemistry by design; synthesis (self-assembly)
Citation Formats
Pandey, Jyotsna L., Kiemle, Sarah N., Richard, Tom L., Zhu, Yimin, Cosgrove, Daniel J., and Anderson, Charles T. Investigating Biochemical and Developmental Dependencies of Lignification with a Click-Compatible Monolignol Analog in Arabidopsis thaliana Stems. United States: N. p., 2016.
Web. doi:10.3389/fpls.2016.01309.
Pandey, Jyotsna L., Kiemle, Sarah N., Richard, Tom L., Zhu, Yimin, Cosgrove, Daniel J., & Anderson, Charles T. Investigating Biochemical and Developmental Dependencies of Lignification with a Click-Compatible Monolignol Analog in Arabidopsis thaliana Stems. United States. https://doi.org/10.3389/fpls.2016.01309
Pandey, Jyotsna L., Kiemle, Sarah N., Richard, Tom L., Zhu, Yimin, Cosgrove, Daniel J., and Anderson, Charles T. Wed .
"Investigating Biochemical and Developmental Dependencies of Lignification with a Click-Compatible Monolignol Analog in Arabidopsis thaliana Stems". United States. https://doi.org/10.3389/fpls.2016.01309. https://www.osti.gov/servlets/purl/1388043.
@article{osti_1388043,
title = {Investigating Biochemical and Developmental Dependencies of Lignification with a Click-Compatible Monolignol Analog in Arabidopsis thaliana Stems},
author = {Pandey, Jyotsna L. and Kiemle, Sarah N. and Richard, Tom L. and Zhu, Yimin and Cosgrove, Daniel J. and Anderson, Charles T.},
abstractNote = {Lignin is a key structural component of plant cell walls that provides rigidity, strength, and resistance against microbial attacks. This hydrophobic polymer also serves a crucial role in water transport. Despite its abundance and essential functions, several aspects of lignin biosynthesis and deposition remain cryptic. Lignin precursors are known to be synthesized in the cytoplasm by complex biosynthetic pathways, after which they are transported to the apoplastic space, where they are polymerized via free radical coupling reactions into polymeric lignin. However, the lignin deposition process and the factors controlling it are unclear. In this study, the biochemical and developmental dependencies of lignification were investigated using a click-compatible monolignol analog, 3-O-propargylcaffeyl alcohol (3-OPC), which can incorporate into both in vitro polymerized lignin and Arabidopsis thaliana tissues. Fluorescence labeling of 3-OPC using click chemistry followed by confocal fluorescence microscopy enabled the detection and imaging of 3-OPC incorporation patterns. These patterns were consistent with endogenous lignification observed in different developmental stages of Arabidopsis stems. However, the concentration of supplied monolignols influenced where lignification occurred at the subcellular level, with low concentrations being deposited in cell corners and middle lamellae and high concentrations also being deposited in secondary walls. Experimental inhibition of multiple lignification factors confirmed that 3-OPC incorporation proceeds via a free radical coupling mechanism involving peroxidases/laccases and reactive oxygen species (ROS). Finally, the presence of peroxide-producing enzymes determined which cell walls lignified: adding exogenous peroxide and peroxidase caused cells that do not naturally lignify in Arabidopsis stems to lignify. In conclusion, 3-OPC accurately mimics natural lignification patterns in different developmental stages of Arabidopsis stems and allows for the dissection of key biochemical and enzymatic factors controlling lignification.},
doi = {10.3389/fpls.2016.01309},
journal = {Frontiers in Plant Science},
number = ,
volume = 7,
place = {United States},
year = {Wed Aug 31 00:00:00 EDT 2016},
month = {Wed Aug 31 00:00:00 EDT 2016}
}
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Laccase Down-Regulation Causes Alterations in Phenolic Metabolism and Cell Wall Structure in Poplar
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Propidium Iodide Competes with Ca 2+ to Label Pectin in Pollen Tubes and Arabidopsis Root Hairs
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Laccases Direct Lignification in the Discrete Secondary Cell Wall Domains of Protoxylem
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Laccase from Sycamore Maple ( Acer pseudoplatanus ) Polymerizes Monolignols
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Identification of Novel Genes in Arabidopsis Involved in Secondary Cell Wall Formation Using Expression Profiling and Reverse Genetics
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Disruption of LACCASE4 and 17 Results in Tissue-Specific Alterations to Lignification of Arabidopsis thaliana Stems
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Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans
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LACCASE Is Necessary and Nonredundant with PEROXIDASE for Lignin Polymerization during Vascular Development in Arabidopsis
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- The Plant Cell, Vol. 25, Issue 10
Identification of a Ca 2+ -Pectate Binding Site on an Apoplastic Peroxidase
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- The Plant Cell, Vol. 13, Issue 3
Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis
journal, January 2010
- Tronchet, Maurice; BalaguÃ, Claudine; Kroj, Thomas
- Molecular Plant Pathology, Vol. 11, Issue 1
Visualization of plant cell wall lignification using fluorescence-tagged monolignols
journal, August 2013
- Tobimatsu, Yuki; Wagner, Armin; Donaldson, Lloyd
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Lignin Biosynthesis
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Enzymatic "Combustion": The Microbial Degradation of Lignin
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Lignin: Occurrence, Biogenesis and Biodegradation
journal, June 1990
- Lewis, N. G.; Yamamoto, E.
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Lignin Distribution During Latewood Formation in Pinus Radiata D. Don
journal, January 1992
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A Versatile Click-Compatible Monolignol Probe to Study Lignin Deposition in Plant Cell Walls
journal, April 2015
- Pandey, Jyotsna L.; Wang, Bo; Diehl, Brett G.
- PLOS ONE, Vol. 10, Issue 4
Heterogeneity in Formation of Lignin. X. Visualization of Lignification Process in Differentiating Xylem of Pine by Microautoradiography
journal, January 1988
- Terashima, Noritsugu; Fukushima, Kazuhiko; Sano, Yoshiaki
- Holzforschung, Vol. 42, Issue 6
Plant cell wall lignification and monolignol metabolism
journal, January 2013
- Wang, Yin; Chantreau, Maxime; Sibout, Richard
- Frontiers in Plant Science, Vol. 4
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