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Title: Spatio-temporal control of phenylpropanoid biosynthesis by inducible complementation of a cinnamate 4-hydroxylase mutant

Abstract

Abstract Cinnamate 4-hydroxylase (C4H) is a cytochrome P450-dependent monooxygenase that catalyzes the second step of the general phenylpropanoid pathway. Arabidopsis reduced epidermal fluorescence 3 (ref3) mutants, which carry hypomorphic mutations in C4H, exhibit global alterations in phenylpropanoid biosynthesis and have developmental abnormalities including dwarfing. Here we report the characterization of a conditional Arabidopsis C4H line (ref3-2pOpC4H), in which wild-type C4H is expressed in the ref3-2 background. Expression of C4H in plants with well-developed primary inflorescence stems resulted in restoration of fertility and the production of substantial amounts of lignin, revealing that the developmental window for lignification is remarkably plastic. Following induction of C4H expression in ref3-2pOpC4H, we observed rapid and significant reductions in the levels of numerous metabolites, including several benzoyl and cinnamoyl esters and amino acid conjugates. These atypical conjugates were quickly replaced with their sinapoylated equivalents, suggesting that phenolic esters are subjected to substantial amounts of turnover in wild-type plants. Furthermore, using localized application of dexamethasone to ref3-2pOpC4H, we show that phenylpropanoids are not transported appreciably from their site of synthesis. Finally, we identified a defective Casparian strip diffusion barrier in the ref3-2 mutant root endodermis, which is restored by induction of C4H expression.

Authors:
 [1];  [2];  [3];  [2]; ORCiD logo [4];  [5]
  1. Department of Biochemistry, Purdue University, West Lafayette, IN, USA, The Center for Direct Catalytic Conversion of Biomass to Biofuels (C3Bio), Discovery Park, Purdue University, West Lafayette, IN, USA
  2. Institute of Cellular and Molecular Botany, University of Bonn, Bonn, Germany
  3. Department of Biochemistry, Purdue University, West Lafayette, IN, USA
  4. Department of Biochemistry, Purdue University, West Lafayette, IN, USA, The Center for Direct Catalytic Conversion of Biomass to Biofuels (C3Bio), Discovery Park, Purdue University, West Lafayette, IN, USA, Center for Plant Biology, Purdue University, West Lafayette, IN, USA
  5. Tsinghua University, China
Publication Date:
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1774671
Grant/Contract Number:  
SC0000997
Resource Type:
Published Article
Journal Name:
Journal of Experimental Botany
Additional Journal Information:
Journal Name: Journal of Experimental Botany Journal Volume: 72 Journal Issue: 8; Journal ID: ISSN 0022-0957
Publisher:
Oxford University Press
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Kim, Jeong Im, Hidalgo-Shrestha, Christopher, Bonawitz, Nicholas D., Franke, Rochus B., Chapple, Clint, and Zhao, ed., Qiao. Spatio-temporal control of phenylpropanoid biosynthesis by inducible complementation of a cinnamate 4-hydroxylase mutant. United Kingdom: N. p., 2021. Web. doi:10.1093/jxb/erab055.
Kim, Jeong Im, Hidalgo-Shrestha, Christopher, Bonawitz, Nicholas D., Franke, Rochus B., Chapple, Clint, & Zhao, ed., Qiao. Spatio-temporal control of phenylpropanoid biosynthesis by inducible complementation of a cinnamate 4-hydroxylase mutant. United Kingdom. https://doi.org/10.1093/jxb/erab055
Kim, Jeong Im, Hidalgo-Shrestha, Christopher, Bonawitz, Nicholas D., Franke, Rochus B., Chapple, Clint, and Zhao, ed., Qiao. Mon . "Spatio-temporal control of phenylpropanoid biosynthesis by inducible complementation of a cinnamate 4-hydroxylase mutant". United Kingdom. https://doi.org/10.1093/jxb/erab055.
@article{osti_1774671,
title = {Spatio-temporal control of phenylpropanoid biosynthesis by inducible complementation of a cinnamate 4-hydroxylase mutant},
author = {Kim, Jeong Im and Hidalgo-Shrestha, Christopher and Bonawitz, Nicholas D. and Franke, Rochus B. and Chapple, Clint and Zhao, ed., Qiao},
abstractNote = {Abstract Cinnamate 4-hydroxylase (C4H) is a cytochrome P450-dependent monooxygenase that catalyzes the second step of the general phenylpropanoid pathway. Arabidopsis reduced epidermal fluorescence 3 (ref3) mutants, which carry hypomorphic mutations in C4H, exhibit global alterations in phenylpropanoid biosynthesis and have developmental abnormalities including dwarfing. Here we report the characterization of a conditional Arabidopsis C4H line (ref3-2pOpC4H), in which wild-type C4H is expressed in the ref3-2 background. Expression of C4H in plants with well-developed primary inflorescence stems resulted in restoration of fertility and the production of substantial amounts of lignin, revealing that the developmental window for lignification is remarkably plastic. Following induction of C4H expression in ref3-2pOpC4H, we observed rapid and significant reductions in the levels of numerous metabolites, including several benzoyl and cinnamoyl esters and amino acid conjugates. These atypical conjugates were quickly replaced with their sinapoylated equivalents, suggesting that phenolic esters are subjected to substantial amounts of turnover in wild-type plants. Furthermore, using localized application of dexamethasone to ref3-2pOpC4H, we show that phenylpropanoids are not transported appreciably from their site of synthesis. Finally, we identified a defective Casparian strip diffusion barrier in the ref3-2 mutant root endodermis, which is restored by induction of C4H expression.},
doi = {10.1093/jxb/erab055},
journal = {Journal of Experimental Botany},
number = 8,
volume = 72,
place = {United Kingdom},
year = {Mon Feb 15 00:00:00 EST 2021},
month = {Mon Feb 15 00:00:00 EST 2021}
}

Journal Article:
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Publisher's Version of Record
https://doi.org/10.1093/jxb/erab055

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