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

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

doi:10.1186/s13068-015-0403-z

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

Journal Article · Mon Dec 21 00:00:00 EST 2015 · Biotechnology for Biofuels

DOI:https://doi.org/10.1186/s13068-015-0403-z· OSTI ID:1260597

Srivastava, Avinash C. ^[1]; Chen, Fang ^[2]; Ray, Tui ^[3]; Pattathil, Sivakumar ^[4]; Peña, Maria J. ^[4]; Avci, Utku ^[4]; Li, Hongjia ^[5]; Huhman, David V. ^[3]; Backe, Jason ^[4]; Urbanowicz, Breeanna ^[4]; Miller, Jeffrey S. ^[6]; Bedair, Mohamed ^[3]; Wyman, Charles E. ^[5]; Sumner, Lloyd W. ^[3]; York, William S. ^[4]; Hahn, Michael G. ^[4]; Dixon, Richard A. ^[2]; Blancaflor, Elison B. ^[1]; Tang, Yuhong ^[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)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Univ. of North Texas, Denton, TX (United States)
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 Georgia, Athens, GA (United States)
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
Univ. of Georgia, Athens, GA (United States)

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.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: DBI-0421683; IOS-0923992

OSTI ID:: 1260597

Journal Information:: Biotechnology for Biofuels, Vol. 8, Issue 1; ISSN 1754-6834

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 20 works

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Caffeoyl coenzyme A O-methyltransferase and lignin biosynthesis Ye, Zheng-Hua; Zhong, Ruiqin; Morrison III, W. Herbert Phytochemistry, Vol. 57, Issue 7 https://doi.org/10.1016/s0031-9422(01)00051-6	journal	August 2001
The maize brown midrib2 ( bm2 ) gene encodes a methylenetetrahydrofolate reductase that contributes to lignin accumulation Tang, Ho Man; Liu, Sanzhen; Hill-Skinner, Sarah The Plant Journal, Vol. 77, Issue 3 https://doi.org/10.1111/tpj.12394	journal	January 2014
Transcriptional regulation of lignin biosynthesis Zhong, Ruiqin; Ye, Zheng-Hua Plant Signaling & Behavior, Vol. 4, Issue 11 https://doi.org/10.4161/psb.4.11.9875	journal	November 2009
High free-methionine and decreased lignin content result from a mutation in the Arabidopsis S -adenosyl-L-methionine synthetase 3 gene Shen, Bo; Li, Changjiang; Tarczynski, Mitchell C. The Plant Journal, Vol. 29, Issue 3 https://doi.org/10.1046/j.1365-313X.2002.01221.x	journal	February 2002
New insights into the molecular architecture of hardwood lignins by chemical degradative methods Lapierre, Catherine; Pollet, Brigitte; Rolando, Christian Research on Chemical Intermediates, Vol. 21, Issue 3-5, p. 397-412 https://doi.org/10.1007/BF03052266	journal	March 1995
Systems Rebalancing of Metabolism in Response to Sulfur Deprivation, as Revealed by Metabolome Analysis of Arabidopsis Plants Nikiforova, Victoria J.; Kopka, Joachim; Tolstikov, Vladimir Plant Physiology, Vol. 138, Issue 1 https://doi.org/10.1104/pp.104.053793	journal	April 2005
Arabidopsis irregular xylem8 and irregular xylem9 : Implications for the Complexity of Glucuronoxylan Biosynthesis Peña, Maria J.; Zhong, Ruiqin; Zhou, Gong-Ke The Plant Cell, Vol. 19, Issue 2 https://doi.org/10.1105/tpc.106.049320	journal	February 2007
The S-methylmethionine cycle in angiosperms: ubiquity, antiquity and activity: S-methylmethionine cycle Ranocha, Philippe; McNeil, Scott D.; Ziemak, Michael J. The Plant Journal, Vol. 25, Issue 5 https://doi.org/10.1046/j.1365-313x.2001.00988.x	journal	March 2001
Rewriting the lignin roadmap Humphreys, John M.; Chapple, Clint Current Opinion in Plant Biology, Vol. 5, Issue 3 https://doi.org/10.1016/S1369-5266(02)00257-1	journal	June 2002
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Modifications in Lignin and Accumulation of Phenolic Glucosides in Poplar Xylem upon Down-regulation of Caffeoyl-Coenzyme A O-Methyltransferase, an Enzyme Involved in Lignin Biosynthesis Meyermans, Hugo; Morreel, Kris; Lapierre, Catherine Journal of Biological Chemistry, Vol. 275, Issue 47, p. 36899-36909 https://doi.org/10.1074/jbc.M006915200	journal	August 2000
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Similar Records

Silencing Folylpolyglutamate Synthetase1 (FPGS1) in Switchgrass (Panicum virgatum L.) Improves Lignocellulosic Biofuel Production

Journal Article · Fri Jun 19 00:00:00 EDT 2020 · Frontiers in Plant Science · OSTI ID:1260597

Mazarei, Mitra; Baxter, Holly L.; Srivastava, Avinash; +15 more

Combining loss of function of FOLYLPOLYGLUTAMATE SYNTHETASE1 and CAFFEOYL-COA 3-O-METHYLTRANSFERASE1 for lignin reduction and improved saccharification efficiency in Arabidopsis thaliana

Journal Article · Fri May 03 00:00:00 EDT 2019 · Biotechnology for Biofuels · OSTI ID:1260597

Xie, Hongli; Engle, Nancy L.; Venketachalam, Sivasankari; +16 more

In situ autoradiographic detection of folylpolyglutamate synthetase activity

Journal Article · Sat Nov 01 00:00:00 EST 1986 · Anal. Biochem.; (United States) · OSTI ID:1260597

Sussman, D J; Milman, G; Osborne, C; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Arabidopsis
Bioenergy
C1 metabolism
Cell-wall recalcitrance
FPGS1
Lignin
Folylpolyglutamate synthetase

MOESM2 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d4 The current record is supplemented by this image	image	January 2015
MOESM3 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d3 The current record is supplemented by this dataset	dataset	January 2015
MOESM10 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d2 The current record is supplemented by this text	text	January 2015
MOESM4 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d1 The current record is supplemented by this image	image	January 2015
MOESM6 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d9 The current record is supplemented by this image	image	January 2015
MOESM8 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d7 The current record is supplemented by this image	image	January 2015
MOESM7 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d6 The current record is supplemented by this image	image	January 2015
MOESM9 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d5 The current record is supplemented by this text	text	January 2015
MOESM7 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis PeAaa, Maria; Avci, Utku; Li, Hongjia https://doi.org/10.6084/m9.figshare.c.3599840_d6.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM4 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Pattathil, Sivakumar https://doi.org/10.6084/m9.figshare.c.3599840_d1.v1 The current record is supplemented by this figure	figure	December 2015
Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM1 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/M9.FIGSHARE.C.3599840_D10 The current record is supplemented by this image	image	January 2015
Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis [Supplementary Data] Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840 The current record is supplemented by this dataset	dataset	December 2015
MOESM2 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d4.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM9 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d5.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM3 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d3.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM6 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d9.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM1 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Pattathil, Sivakumar https://doi.org/10.6084/m9.figshare.c.3599840_d10.v1 The current record is supplemented by this figure	figure	December 2015
MOESM5 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/M9.FIGSHARE.C.3599840_D8 The current record is supplemented by this dataset	dataset	January 2015
MOESM8 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d7.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM10 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Pattathil, Sivakumar https://doi.org/10.6084/m9.figshare.c.3599840_d2.v1 The current record is supplemented by this dataset	dataset	December 2015
MOESM5 of Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis Srivastava, Avinash; Chen, Fang; Ray, Tui https://doi.org/10.6084/m9.figshare.c.3599840_d8.v1 The current record is supplemented by this dataset	dataset	December 2015