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

Switchgrass (Panicum virgatum L.) is a lignocellulosic perennial grass with great potential in bioenergy field. Lignocellulosic bioenergy crops are mostly resistant to cell wall deconstruction, and therefore yield suboptimal levels of biofuel. The one-carbon pathway (also known as C1 metabolism) is...

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Main Authors: Mitra Mazarei, Holly L. Baxter, Avinash Srivastava, Guifen Li, Hongli Xie, Alexandru Dumitrache, Miguel Rodriguez, Jace M. Natzke, Ji-Yi Zhang, Geoffrey B. Turner, Robert W. Sykes, Mark F. Davis, Michael K. Udvardi, Zeng-Yu Wang, Brian H. Davison, Elison B. Blancaflor, Yuhong Tang, Charles Neal Stewart
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.00843/full
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author Mitra Mazarei
Mitra Mazarei
Mitra Mazarei
Holly L. Baxter
Holly L. Baxter
Avinash Srivastava
Avinash Srivastava
Guifen Li
Guifen Li
Hongli Xie
Hongli Xie
Alexandru Dumitrache
Alexandru Dumitrache
Miguel Rodriguez
Miguel Rodriguez
Miguel Rodriguez
Jace M. Natzke
Jace M. Natzke
Ji-Yi Zhang
Ji-Yi Zhang
Geoffrey B. Turner
Geoffrey B. Turner
Robert W. Sykes
Robert W. Sykes
Mark F. Davis
Mark F. Davis
Mark F. Davis
Michael K. Udvardi
Michael K. Udvardi
Michael K. Udvardi
Zeng-Yu Wang
Zeng-Yu Wang
Brian H. Davison
Brian H. Davison
Brian H. Davison
Elison B. Blancaflor
Elison B. Blancaflor
Yuhong Tang
Yuhong Tang
Charles Neal Stewart
Charles Neal Stewart
Charles Neal Stewart
author_facet Mitra Mazarei
Mitra Mazarei
Mitra Mazarei
Holly L. Baxter
Holly L. Baxter
Avinash Srivastava
Avinash Srivastava
Guifen Li
Guifen Li
Hongli Xie
Hongli Xie
Alexandru Dumitrache
Alexandru Dumitrache
Miguel Rodriguez
Miguel Rodriguez
Miguel Rodriguez
Jace M. Natzke
Jace M. Natzke
Ji-Yi Zhang
Ji-Yi Zhang
Geoffrey B. Turner
Geoffrey B. Turner
Robert W. Sykes
Robert W. Sykes
Mark F. Davis
Mark F. Davis
Mark F. Davis
Michael K. Udvardi
Michael K. Udvardi
Michael K. Udvardi
Zeng-Yu Wang
Zeng-Yu Wang
Brian H. Davison
Brian H. Davison
Brian H. Davison
Elison B. Blancaflor
Elison B. Blancaflor
Yuhong Tang
Yuhong Tang
Charles Neal Stewart
Charles Neal Stewart
Charles Neal Stewart
author_sort Mitra Mazarei
collection DOAJ
description Switchgrass (Panicum virgatum L.) is a lignocellulosic perennial grass with great potential in bioenergy field. Lignocellulosic bioenergy crops are mostly resistant to cell wall deconstruction, and therefore yield suboptimal levels of biofuel. The one-carbon pathway (also known as C1 metabolism) is critical for polymer methylation, including that of lignin and hemicelluloses in cell walls. Folylpolyglutamate synthetase (FPGS) catalyzes a biochemical reaction that leads to the formation of folylpolyglutamate, an important cofactor for many enzymes in the C1 pathway. In this study, the putatively novel switchgrass PvFPGS1 gene was identified and its functional role in cell wall composition and biofuel production was examined by RNAi knockdown analysis. The PvFPGS1-downregulated plants were analyzed in the field over three growing seasons. Transgenic plants with the highest reduction in PvFPGS1 expression grew slower and produced lower end-of-season biomass. Transgenic plants with low-to-moderate reduction in PvFPGS1 transcript levels produced equivalent biomass as controls. There were no significant differences observed for lignin content and syringyl/guaiacyl lignin monomer ratio in the low-to-moderately reduced PvFPGS1 transgenic lines compared with the controls. Similarly, sugar release efficiency was also not significantly different in these transgenic lines compared with the control lines. However, transgenic plants produced up to 18% more ethanol while maintaining congruent growth and biomass as non-transgenic controls. Severity of rust disease among transgenic and control lines were not different during the time course of the field experiments. Altogether, the unchanged lignin content and composition in the low-to-moderate PvFPGS1-downregulated lines may suggest that partial downregulation of PvFPGS1 expression did not impact lignin biosynthesis in switchgrass. In conclusion, the manipulation of PvFPGS1 expression in bioenergy crops may be useful to increase biofuel potential with no growth penalty or increased susceptibility to rust in feedstock.
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spelling doaj.art-427088f1a4834c50a7346fd1fb79b9192022-12-21T18:21:56ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-06-011110.3389/fpls.2020.00843545931Silencing Folylpolyglutamate Synthetase1 (FPGS1) in Switchgrass (Panicum virgatum L.) Improves Lignocellulosic Biofuel ProductionMitra Mazarei0Mitra Mazarei1Mitra Mazarei2Holly L. Baxter3Holly L. Baxter4Avinash Srivastava5Avinash Srivastava6Guifen Li7Guifen Li8Hongli Xie9Hongli Xie10Alexandru Dumitrache11Alexandru Dumitrache12Miguel Rodriguez13Miguel Rodriguez14Miguel Rodriguez15Jace M. Natzke16Jace M. Natzke17Ji-Yi Zhang18Ji-Yi Zhang19Geoffrey B. Turner20Geoffrey B. Turner21Robert W. Sykes22Robert W. Sykes23Mark F. Davis24Mark F. Davis25Mark F. Davis26Michael K. Udvardi27Michael K. Udvardi28Michael K. Udvardi29Zeng-Yu Wang30Zeng-Yu Wang31Brian H. Davison32Brian H. Davison33Brian H. Davison34Elison B. Blancaflor35Elison B. Blancaflor36Yuhong Tang37Yuhong Tang38Charles Neal Stewart39Charles Neal Stewart40Charles Neal Stewart41Department of Plant Sciences, The University of Tennessee, Knoxville, TN, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesThe Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesDepartment of Plant Sciences, The University of Tennessee, Knoxville, TN, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNoble Research Institute, Ardmore, OK, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNoble Research Institute, Ardmore, OK, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNoble Research Institute, Ardmore, OK, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesBiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesThe Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesBiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesBiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNoble Research Institute, Ardmore, OK, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNational Renewable Energy Laboratory, Golden, CO, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNational Renewable Energy Laboratory, Golden, CO, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesThe Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNational Renewable Energy Laboratory, Golden, CO, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesThe Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNoble Research Institute, Ardmore, OK, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNoble Research Institute, Ardmore, OK, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesThe Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesBiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNoble Research Institute, Ardmore, OK, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesNoble Research Institute, Ardmore, OK, United StatesDepartment of Plant Sciences, The University of Tennessee, Knoxville, TN, United StatesBioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesThe Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN, United StatesSwitchgrass (Panicum virgatum L.) is a lignocellulosic perennial grass with great potential in bioenergy field. Lignocellulosic bioenergy crops are mostly resistant to cell wall deconstruction, and therefore yield suboptimal levels of biofuel. The one-carbon pathway (also known as C1 metabolism) is critical for polymer methylation, including that of lignin and hemicelluloses in cell walls. Folylpolyglutamate synthetase (FPGS) catalyzes a biochemical reaction that leads to the formation of folylpolyglutamate, an important cofactor for many enzymes in the C1 pathway. In this study, the putatively novel switchgrass PvFPGS1 gene was identified and its functional role in cell wall composition and biofuel production was examined by RNAi knockdown analysis. The PvFPGS1-downregulated plants were analyzed in the field over three growing seasons. Transgenic plants with the highest reduction in PvFPGS1 expression grew slower and produced lower end-of-season biomass. Transgenic plants with low-to-moderate reduction in PvFPGS1 transcript levels produced equivalent biomass as controls. There were no significant differences observed for lignin content and syringyl/guaiacyl lignin monomer ratio in the low-to-moderately reduced PvFPGS1 transgenic lines compared with the controls. Similarly, sugar release efficiency was also not significantly different in these transgenic lines compared with the control lines. However, transgenic plants produced up to 18% more ethanol while maintaining congruent growth and biomass as non-transgenic controls. Severity of rust disease among transgenic and control lines were not different during the time course of the field experiments. Altogether, the unchanged lignin content and composition in the low-to-moderate PvFPGS1-downregulated lines may suggest that partial downregulation of PvFPGS1 expression did not impact lignin biosynthesis in switchgrass. In conclusion, the manipulation of PvFPGS1 expression in bioenergy crops may be useful to increase biofuel potential with no growth penalty or increased susceptibility to rust in feedstock.https://www.frontiersin.org/article/10.3389/fpls.2020.00843/fullfolylpolyglutamate synthetaseswitchgrassRNAi-gene silencingPvFPGS1lignocellulosicbiofuel
spellingShingle Mitra Mazarei
Mitra Mazarei
Mitra Mazarei
Holly L. Baxter
Holly L. Baxter
Avinash Srivastava
Avinash Srivastava
Guifen Li
Guifen Li
Hongli Xie
Hongli Xie
Alexandru Dumitrache
Alexandru Dumitrache
Miguel Rodriguez
Miguel Rodriguez
Miguel Rodriguez
Jace M. Natzke
Jace M. Natzke
Ji-Yi Zhang
Ji-Yi Zhang
Geoffrey B. Turner
Geoffrey B. Turner
Robert W. Sykes
Robert W. Sykes
Mark F. Davis
Mark F. Davis
Mark F. Davis
Michael K. Udvardi
Michael K. Udvardi
Michael K. Udvardi
Zeng-Yu Wang
Zeng-Yu Wang
Brian H. Davison
Brian H. Davison
Brian H. Davison
Elison B. Blancaflor
Elison B. Blancaflor
Yuhong Tang
Yuhong Tang
Charles Neal Stewart
Charles Neal Stewart
Charles Neal Stewart
Silencing Folylpolyglutamate Synthetase1 (FPGS1) in Switchgrass (Panicum virgatum L.) Improves Lignocellulosic Biofuel Production
Frontiers in Plant Science
folylpolyglutamate synthetase
switchgrass
RNAi-gene silencing
PvFPGS1
lignocellulosic
biofuel
title Silencing Folylpolyglutamate Synthetase1 (FPGS1) in Switchgrass (Panicum virgatum L.) Improves Lignocellulosic Biofuel Production
title_full Silencing Folylpolyglutamate Synthetase1 (FPGS1) in Switchgrass (Panicum virgatum L.) Improves Lignocellulosic Biofuel Production
title_fullStr Silencing Folylpolyglutamate Synthetase1 (FPGS1) in Switchgrass (Panicum virgatum L.) Improves Lignocellulosic Biofuel Production
title_full_unstemmed Silencing Folylpolyglutamate Synthetase1 (FPGS1) in Switchgrass (Panicum virgatum L.) Improves Lignocellulosic Biofuel Production
title_short Silencing Folylpolyglutamate Synthetase1 (FPGS1) in Switchgrass (Panicum virgatum L.) Improves Lignocellulosic Biofuel Production
title_sort silencing folylpolyglutamate synthetase1 fpgs1 in switchgrass panicum virgatum l improves lignocellulosic biofuel production
topic folylpolyglutamate synthetase
switchgrass
RNAi-gene silencing
PvFPGS1
lignocellulosic
biofuel
url https://www.frontiersin.org/article/10.3389/fpls.2020.00843/full
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