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Title: Pinoresinol reductase 1 impacts lignin distribution during secondary cell wall biosynthesis in Arabidopsis

Abstract

In this paper, pinoresinol reductase (PrR) catalyzes the conversion of the lignan (-)-pinoresinol to (-)-lariciresinol in Arabidopsis thaliana, where it is encoded by two genes, PrR1 and PrR2, that appear to act redundantly. PrR1 is highly expressed in lignified inflorescence stem tissue, whereas PrR2 expression is barely detectable in stems. Co-expression analysis has indicated that PrR1 is co-expressed with many characterized genes involved in secondary cell wall biosynthesis, whereas PrR2 expression clusters with a different set of genes. The promoter of the PrR1 gene is regulated by the secondary cell wall related transcription factors SND1 and MYB46. The loss-of-function mutant of PrR1 shows, in addition to elevated levels of pinoresinol, significantly decreased lignin content and a slightly altered lignin structure with lower abundance of cinnamyl alcohol end groups. Stimulated Raman scattering (SRS) microscopy analysis indicated that the lignin content of the prr1-1 loss-of-function mutant is similar to that of wild-type plants in xylem cells, which exhibit a normal phenotype, but is reduced in the fiber cells. Finally, together, these data suggest an association of the lignan biosynthetic enzyme encoded by PrR1 with secondary cell wall biosynthesis in fiber cells.

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [6];  [6];  [2];  [4];  [7]
  1. Samuel Roberts Noble Foundation, Ardmore, OK (United States). Plant Biology Division
  2. National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
  3. Northern Illinois Univ., DeKalb, IL (United States). Dept. of Biological Sciences
  4. Georgia Inst. of Technology, Atlanta, GA (United States). Inst. of Paper Science and Technology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
  5. Samuel Roberts Noble Foundation, Ardmore, OK (United States). Plant Biology Division; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  7. Samuel Roberts Noble Foundation, Ardmore, OK (United States). Plant Biology Division; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Univ. of North Texas, Denton, TX (United States). Dept. of Biological Sciences
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Contributing Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States); Samuel Roberts Noble Foundation, Ardmore, OK (United States)
OSTI Identifier:
1286734
Alternate Identifier(s):
OSTI ID: 1251923
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Phytochemistry
Additional Journal Information:
Journal Volume: 112; Journal ID: ISSN 0031-9422
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Lignan; Lignin; Interfascicular fiber; Mutant; Stimulated Raman scattering microscopy

Citation Formats

Zhao, Qiao, Zeng, Yining, Yin, Yanbin, Pu, Yunqiao, Jackson, Lisa A., Engle, Nancy L., Martin, Madhavi Z., Tschaplinski, Timothy J., Ding, Shi-You, Ragauskas, Arthur J., and Dixon, Richard A. Pinoresinol reductase 1 impacts lignin distribution during secondary cell wall biosynthesis in Arabidopsis. United States: N. p., 2014. Web. doi:10.1016/j.phytochem.2014.07.008.
Zhao, Qiao, Zeng, Yining, Yin, Yanbin, Pu, Yunqiao, Jackson, Lisa A., Engle, Nancy L., Martin, Madhavi Z., Tschaplinski, Timothy J., Ding, Shi-You, Ragauskas, Arthur J., & Dixon, Richard A. Pinoresinol reductase 1 impacts lignin distribution during secondary cell wall biosynthesis in Arabidopsis. United States. https://doi.org/10.1016/j.phytochem.2014.07.008
Zhao, Qiao, Zeng, Yining, Yin, Yanbin, Pu, Yunqiao, Jackson, Lisa A., Engle, Nancy L., Martin, Madhavi Z., Tschaplinski, Timothy J., Ding, Shi-You, Ragauskas, Arthur J., and Dixon, Richard A. 2014. "Pinoresinol reductase 1 impacts lignin distribution during secondary cell wall biosynthesis in Arabidopsis". United States. https://doi.org/10.1016/j.phytochem.2014.07.008. https://www.osti.gov/servlets/purl/1286734.
@article{osti_1286734,
title = {Pinoresinol reductase 1 impacts lignin distribution during secondary cell wall biosynthesis in Arabidopsis},
author = {Zhao, Qiao and Zeng, Yining and Yin, Yanbin and Pu, Yunqiao and Jackson, Lisa A. and Engle, Nancy L. and Martin, Madhavi Z. and Tschaplinski, Timothy J. and Ding, Shi-You and Ragauskas, Arthur J. and Dixon, Richard A.},
abstractNote = {In this paper, pinoresinol reductase (PrR) catalyzes the conversion of the lignan (-)-pinoresinol to (-)-lariciresinol in Arabidopsis thaliana, where it is encoded by two genes, PrR1 and PrR2, that appear to act redundantly. PrR1 is highly expressed in lignified inflorescence stem tissue, whereas PrR2 expression is barely detectable in stems. Co-expression analysis has indicated that PrR1 is co-expressed with many characterized genes involved in secondary cell wall biosynthesis, whereas PrR2 expression clusters with a different set of genes. The promoter of the PrR1 gene is regulated by the secondary cell wall related transcription factors SND1 and MYB46. The loss-of-function mutant of PrR1 shows, in addition to elevated levels of pinoresinol, significantly decreased lignin content and a slightly altered lignin structure with lower abundance of cinnamyl alcohol end groups. Stimulated Raman scattering (SRS) microscopy analysis indicated that the lignin content of the prr1-1 loss-of-function mutant is similar to that of wild-type plants in xylem cells, which exhibit a normal phenotype, but is reduced in the fiber cells. Finally, together, these data suggest an association of the lignan biosynthetic enzyme encoded by PrR1 with secondary cell wall biosynthesis in fiber cells.},
doi = {10.1016/j.phytochem.2014.07.008},
url = {https://www.osti.gov/biblio/1286734}, journal = {Phytochemistry},
issn = {0031-9422},
number = ,
volume = 112,
place = {United States},
year = {Tue Aug 05 00:00:00 EDT 2014},
month = {Tue Aug 05 00:00:00 EDT 2014}
}

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Cited by: 22 works
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Works referenced in this record:

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Works referencing / citing this record:

Lignin biosynthesis: old roads revisited and new roads explored
journal, December 2019


Pinoresinol–lariciresinol reductases, key to the lignan synthesis in plants
journal, March 2019


Natural allelic variation of GVS 1 confers diversity in the regulation of leaf senescence in Arabidopsis
journal, October 2018


TcMYB1, TcMYB4, and TcMYB8 participate in the regulation of lignan biosynthesis in Taiwania cryptomerioides Hayata
journal, August 2019


Dirigent proteins in plants: modulating cell wall metabolism during abiotic and biotic stress exposure
journal, May 2017


Insights into the molecular regulation of monolignol-derived product biosynthesis in the growing hemp hypocotyl
journal, January 2018