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Title: Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis

Abstract

One-carbon (C1) metabolism is important for synthesizing a range of biologically important compounds that are essential for life. In plants, the C1 pathway is crucial for the synthesis of a large number of secondary metabolites, including lignin. Tetrahydrofolate and its derivatives, collectively referred to as folates, are crucial co-factors for C1 metabolic pathway enzymes. Given the link between the C1 and phenylpropanoid pathways, we evaluated whether folylpolyglutamate synthetase (FPGS), an enzyme that catalyzes the addition of a glutamate tail to folates to form folylpolyglutamates, can be a viable target for reducing cell wall recalcitrance in plants. Consistent with its role in lignocellulosic formation, FPGS1 was preferentially expressed in vascular tissues. Total lignin was low in fpgs1 plants leading to higher saccharification efficiency of the mutant. The decrease in total lignin in fpgs1 was mainly due to lower guaiacyl (G) lignin levels. Glycome profiling revealed subtle alterations in the cell walls of fpgs1. Further analyses of hemicellulosic polysaccharides by NMR showed that the degree of methylation of 4-O-methyl glucuronoxylan was reduced in the fpgs1 mutant. Microarray analysis and real-time qRT-PCR revealed that transcripts of a number of genes in the C1 and lignin pathways had altered expression in fpgs1 mutants. Consistentmore » with the transcript changes of C1-related genes, a significant reduction in S-adenosyl-l-methionine content was detected in the fpgs1 mutant. The modified expression of the various methyltransferases and lignin-related genes indicate possible feedback regulation of C1 pathway-mediated lignin biosynthesis. In conclusion, our observations provide genetic and biochemical support for the importance of folylpolyglutamates in the lignocellulosic pathway and reinforces previous observations that targeting a single FPGS isoform for down-regulation leads to reduced lignin in plants. Because fpgs1 mutants had no dramatic defects in above ground biomass, selective down-regulation of individual components of C1 metabolism is an approach that should be explored further for the improvement of lignocellulosic feedstocks.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [4];  [5];  [3];  [4];  [4];  [6];  [3];  [5];  [3];  [4];  [4];  [2];  [1];  [1]
+ Show Author Affiliations
  1. 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)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Univ. of North Texas, Denton, TX (United States)
  3. Samuel Roberts Noble Foundation, Ardmore, OK (United States). Plant Biology Division
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Univ. of Georgia, Athens, GA (United States)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Univ. of California, Riverside, CA (United States). Bourns College of Engineering
  6. Univ. of Georgia, Athens, GA (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1260597
Grant/Contract Number:  
DBI-0421683; IOS-0923992
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Arabidopsis; Bioenergy; C1 metabolism; Cell-wall recalcitrance; FPGS1; Lignin; Folylpolyglutamate synthetase

Citation Formats

Srivastava, Avinash C., Chen, Fang, Ray, Tui, Pattathil, Sivakumar, Peña, Maria J., Avci, Utku, Li, Hongjia, Huhman, David V., Backe, Jason, Urbanowicz, Breeanna, Miller, Jeffrey S., Bedair, Mohamed, Wyman, Charles E., Sumner, Lloyd W., York, William S., Hahn, Michael G., Dixon, Richard A., Blancaflor, Elison B., and Tang, Yuhong. Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis. United States: N. p., 2015. Web. doi:10.1186/s13068-015-0403-z.
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Srivastava, Avinash C., Chen, Fang, Ray, Tui, Pattathil, Sivakumar, Peña, Maria J., Avci, Utku, Li, Hongjia, Huhman, David V., Backe, Jason, Urbanowicz, Breeanna, Miller, Jeffrey S., Bedair, Mohamed, Wyman, Charles E., Sumner, Lloyd W., York, William S., Hahn, Michael G., Dixon, Richard A., Blancaflor, Elison B., & Tang, Yuhong. Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis. United States. https://doi.org/10.1186/s13068-015-0403-z
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Srivastava, Avinash C., Chen, Fang, Ray, Tui, Pattathil, Sivakumar, Peña, Maria J., Avci, Utku, Li, Hongjia, Huhman, David V., Backe, Jason, Urbanowicz, Breeanna, Miller, Jeffrey S., Bedair, Mohamed, Wyman, Charles E., Sumner, Lloyd W., York, William S., Hahn, Michael G., Dixon, Richard A., Blancaflor, Elison B., and Tang, Yuhong. Mon . "Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis". United States. https://doi.org/10.1186/s13068-015-0403-z. https://www.osti.gov/servlets/purl/1260597.
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@article{osti_1260597,
title = {Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis},
author = {Srivastava, Avinash C. and Chen, Fang and Ray, Tui and Pattathil, Sivakumar and Peña, Maria J. and Avci, Utku and Li, Hongjia and Huhman, David V. and Backe, Jason and Urbanowicz, Breeanna and Miller, Jeffrey S. and Bedair, Mohamed and Wyman, Charles E. and Sumner, Lloyd W. and York, William S. and Hahn, Michael G. and Dixon, Richard A. and Blancaflor, Elison B. and Tang, Yuhong},
abstractNote = {One-carbon (C1) metabolism is important for synthesizing a range of biologically important compounds that are essential for life. In plants, the C1 pathway is crucial for the synthesis of a large number of secondary metabolites, including lignin. Tetrahydrofolate and its derivatives, collectively referred to as folates, are crucial co-factors for C1 metabolic pathway enzymes. Given the link between the C1 and phenylpropanoid pathways, we evaluated whether folylpolyglutamate synthetase (FPGS), an enzyme that catalyzes the addition of a glutamate tail to folates to form folylpolyglutamates, can be a viable target for reducing cell wall recalcitrance in plants. Consistent with its role in lignocellulosic formation, FPGS1 was preferentially expressed in vascular tissues. Total lignin was low in fpgs1 plants leading to higher saccharification efficiency of the mutant. The decrease in total lignin in fpgs1 was mainly due to lower guaiacyl (G) lignin levels. Glycome profiling revealed subtle alterations in the cell walls of fpgs1. Further analyses of hemicellulosic polysaccharides by NMR showed that the degree of methylation of 4-O-methyl glucuronoxylan was reduced in the fpgs1 mutant. Microarray analysis and real-time qRT-PCR revealed that transcripts of a number of genes in the C1 and lignin pathways had altered expression in fpgs1 mutants. Consistent with the transcript changes of C1-related genes, a significant reduction in S-adenosyl-l-methionine content was detected in the fpgs1 mutant. The modified expression of the various methyltransferases and lignin-related genes indicate possible feedback regulation of C1 pathway-mediated lignin biosynthesis. In conclusion, our observations provide genetic and biochemical support for the importance of folylpolyglutamates in the lignocellulosic pathway and reinforces previous observations that targeting a single FPGS isoform for down-regulation leads to reduced lignin in plants. Because fpgs1 mutants had no dramatic defects in above ground biomass, selective down-regulation of individual components of C1 metabolism is an approach that should be explored further for the improvement of lignocellulosic feedstocks.},
doi = {10.1186/s13068-015-0403-z},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 8,
place = {United States},
year = {2015},
month = {12}
}
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Journal Article:
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Publisher's Version of Record
https://doi.org/10.1186/s13068-015-0403-z
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Cited by: 20 works
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Figures / Tables:

Fig. 1 Fig. 1: Expression pattern of AtFPGS1. a, b Plants transformed with pFPGS1::GUS constructs showing FPGS1 expression in the vascular bundles of cotyledons and hypocotyls (a) and roots (b) of young seedlings. c, d Cross sections of the stained transgenic inflorescence stems showing FPGS1 expression in the fascicular cambium and xylemmore » tissue between protoxylem and metaxylem. e Longitudinal section of pFPGS1::GUS transgenic plants showing FPGS1 expression in the fascicular cambium and xylem region adjacent to metaxylem. f Longitudinal inflorescence stem-sections (100 µm) of plants expressing pFPGS1::FPGS1-GFP were examined for GFP fluorescence. GFP signals were mainly detected in the developing vessel elements adjacent to the differentiated metaxylem. Superimposed image of GFP over a light microscopy image shows the locations of metaxylem and the GFP expressing cells. Arrows highlight the vascular tissue where FPGS1 expression signal is detected in the cytosol. Phloem (PH), protoxylem (PX), metaxylem (MX), developing vessel element (DVE), sclerenchyma fiber (SF), and fascicular cambium (FC). Scale bar 20 µm« less
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