Downregulation of barley ferulate 5-hydroxylase dramatically alters straw lignin structure without impact on mechanical properties

Shafiei, Reza; Hooper, Matthew; McClellan, Christopher; Oakey, Helena; Stephens, Jennifer; Lapierre, Catherine; Tsuji, Yukiko; Goeminne, Geert; Vanholme, Ruben; Boerjan, Wout; Ralph, John; Halpin, Claire

doi:10.3389/fpls.2022.1125003

Title: Downregulation of barley ferulate 5-hydroxylase dramatically alters straw lignin structure without impact on mechanical properties

Journal Article · Mon Jan 16 00:00:00 EST 2023 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2022.1125003· OSTI ID:1970481

Shafiei, Reza ^[1]; Hooper, Matthew ^[1]; McClellan, Christopher ^[1]; Oakey, Helena ^[2]; Stephens, Jennifer ^[3]; Lapierre, Catherine ^[4]; Tsuji, Yukiko ^[5]; Goeminne, Geert ^[6]; Vanholme, Ruben ^[7]; Boerjan, Wout ^[7]; Ralph, John ^[5]; Halpin, Claire ^[1]

Univ. of Dundee at the James Hutton Inst. (United Kingdom)
Univ. of Dundee at the James Hutton Inst. (United Kingdom); Univ. of Adelaide, SA (Australia)
James Hutton Inst., Dundee (United Kingdom)
Univ. Paris-Saclay, Versailles (France)
Univ. of Wisconsin, Madison, WI (United States)
VIB-UGent (Belgium)
Ghent Univ. (Belgium)

Barley is a major cereal crop for temperate climates, and a diploid genetic model for polyploid wheat. Cereal straw biomass is an attractive source of feedstock for green technologies but lignin, a key determinant of feedstock recalcitrance, complicates bio-conversion processes. However, manipulating lignin content to improve the conversion process could negatively affect agronomic traits. An alternative approach is to manipulate lignin composition which influences the physical and chemical properties of straw. This study validates the function of a barley ferulate 5-hydroxylase gene and demonstrates that its downregulation using the RNA-interference approach substantially impacts lignin composition. We identified five barley genes having putative ferulate 5-hydroxylase activity. Downregulation of HvF5H1 substantially reduced the lignin syringyl/guaiacyl (S/G) ratio in straw while the lignin content, straw mechanical properties, plant growth habit, and grain characteristics all remained unaffected. Metabolic profiling revealed significant changes in the abundance of 173 features in the HvF5H1-RNAi lines. The drastic changes in the lignin polymer of transgenic lines highlight the plasticity of barley lignification processes and the associated potential for manipulating and improving lignocellulosic biomass as a feedstock for green technologies. On the other hand, our results highlight some differences between the lignin biosynthetic pathway in barley, a temperate climate grass, and the warm climate grass, rice, and underscore potential diversity in the lignin biosynthetic pathways in grasses.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)

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

Grant/Contract Number:: SC0018409; BB/N023455/1; BB/G016232/1

OSTI ID:: 1970481

Journal Information:: Frontiers in Plant Science, Vol. 13; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms Kumar, Sudhir; Stecher, Glen; Li, Michael Molecular Biology and Evolution, Vol. 35, Issue 6 https://doi.org/10.1093/molbev/msy096	journal	May 2018
A chromosome conformation capture ordered sequence of the barley genome Mascher, Martin; Gundlach, Heidrun; Himmelbach, Axel Nature, Vol. 544, Issue 7651 https://doi.org/10.1038/nature22043	journal	April 2017
Identification of crop cultivars with consistently high lignocellulosic sugar release requires the use of appropriate statistical design and modelling Oakey, Helena; Shafiei, Reza; Comadran, Jordi Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-185	journal	January 2013
Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase Franke, Rochus; McMichael, Colleen M.; Meyer, Knut The Plant Journal, Vol. 22, Issue 3, p. 223-234 https://doi.org/10.1046/j.1365-313x.2000.00727.x	journal	May 2000
Lignin monomer composition affects Arabidopsis cell-wall degradability after liquid hot water pretreatment Li, Xu; Ximenes, Eduardo; Kim, Youngmi Biotechnology for Biofuels, Vol. 3, Issue 1 https://doi.org/10.1186/1754-6834-3-27	journal	January 2010
RNAi-suppression of barley caffeic acid O -methyltransferase modifies lignin despite redundancy in the gene family Daly, Paul; McClellan, Christopher; Maluk, Marta Plant Biotechnology Journal, Vol. 17, Issue 3 https://doi.org/10.1111/pbi.13001	journal	October 2018
Lignin engineering to improve saccharification and digestibility in grasses Halpin, Claire Current Opinion in Biotechnology, Vol. 56 https://doi.org/10.1016/j.copbio.2019.02.013	journal	April 2019
The effect of altered lignin composition on mechanical properties of CINNAMYL ALCOHOL DEHYDROGENASE (CAD) deficient poplars Özparpucu, Merve; Gierlinger, Notburga; Burgert, Ingo Planta, Vol. 247, Issue 4 https://doi.org/10.1007/s00425-017-2828-z	journal	December 2017
Cell wall fermentation kinetics are impacted more by lignin content and ferulate cross-linking than by lignin composition Grabber, John H.; Mertens, David R.; Kim, Hoon Journal of the Science of Food and Agriculture, Vol. 89, Issue 1 https://doi.org/10.1002/jsfa.3418	journal	January 2009
Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis Meyer, K.; Shirley, A. M.; Cusumano, J. C. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.6619	journal	June 1998
Lignin structure and its engineering Ralph, John; Lapierre, Catherine; Boerjan, Wout Current Opinion in Biotechnology, Vol. 56 https://doi.org/10.1016/j.copbio.2019.02.019	journal	April 2019
Ferulate-5-hydroxylase from Arabidopsis thaliana defines a new family of cytochrome P450-dependent monooxygenases. Meyer, K.; Cusumano, J. C.; Somerville, C. Proceedings of the National Academy of Sciences, Vol. 93, Issue 14 https://doi.org/10.1073/pnas.93.14.6869	journal	July 1996
p -Coumaroylation of poplar lignins impacts lignin structure and improves wood saccharification Lapierre, Catherine; Sibout, Richard; Laurans, Françoise Plant Physiology, Vol. 187, Issue 3 https://doi.org/10.1093/plphys/kiab359	journal	August 2021
Integrative analysis and expression profiling of secondary cell wall genes in C4 biofuel model Setaria italica reveals targets for lignocellulose bioengineering Muthamilarasan, Mehanathan; Khan, Yusuf; Jaishankar, Jananee Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00965	journal	November 2015
Unravelling the impact of lignin on cell wall mechanics: a comprehensive study on young poplar trees downregulated for CINNAMYL ALCOHOL DEHYDROGENASE (CAD) Özparpucu, Merve; Rüggeberg, Markus; Gierlinger, Notburga The Plant Journal, Vol. 91, Issue 3 https://doi.org/10.1111/tpj.13584	journal	June 2017
Knockout of the lignin pathway gene BnF5H decreases the S/G lignin compositional ratio and improves Sclerotinia sclerotiorum resistance in Brassica napus Cao, Yanru; Yan, Xingying; Ran, Shuyao Plant, Cell & Environment, Vol. 45, Issue 1 https://doi.org/10.1111/pce.14208	journal	December 2021
Caffeoyl Shikimate Esterase (CSE) Is an Enzyme in the Lignin Biosynthetic Pathway in Arabidopsis Vanholme, R.; Cesarino, I.; Rataj, K. Science, Vol. 341, Issue 6150 https://doi.org/10.1126/science.1241602	journal	August 2013
RNAi downregulation of three key lignin genes in sugarcane improves glucose release without reduction in sugar production Bewg, William P.; Poovaiah, Charleson; Lan, Wu Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0683-y	journal	December 2016
The decimal code for the growth stages of cereals, with illustrations Tottman, D. R. Annals of Applied Biology, Vol. 110, Issue 2 https://doi.org/10.1111/j.1744-7348.1987.tb03275.x	journal	April 1987
Identification of Grass-specific Enzyme That Acylates Monolignols with p-Coumarate Withers, Saunia; Lu, Fachuang; Kim, Hoon Journal of Biological Chemistry, Vol. 287, Issue 11, p. 8347-8355 https://doi.org/10.1074/jbc.M111.284497	journal	January 2012
Survey of wheat straw stem characteristics for enhanced resistance to lodging Muhammad, Ali; Hao, Huanhuan; Xue, Yali Cellulose, Vol. 27, Issue 5 https://doi.org/10.1007/s10570-020-02972-7	journal	January 2020
Preparative Thioacidolysis of Spruce Lignin: Isolation and Identification of Main Monomeric Products Lapierre, Catherine; Monties, Bernard; Rolando, Christian Holzforschung, Vol. 40, Issue 1 https://doi.org/10.1515/hfsg.1986.40.1.47	journal	January 1986
Characterization of phenylpropanoid pathway genes within European maize (Zea mays L.) inbreds Andersen, Jeppe; Zein, Imad; Wenzel, Gerhard BMC Plant Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2229-8-2	journal	January 2008
Expression atlas and comparative coexpression network analyses reveal important genes involved in the formation of lignified cell wall in Brachypodium distachyon Sibout, Richard; Proost, Sebastian; Hansen, Bjoern Oest New Phytologist, Vol. 215, Issue 3 https://doi.org/10.1111/nph.14635	journal	June 2017
p -Coumaroyl-CoA:monolignol transferase (PMT) acts specifically in the lignin biosynthetic pathway in Brachypodium distachyon Petrik, Deborah L.; Karlen, Steven D.; Cass, Cynthia L. The Plant Journal, Vol. 77, Issue 5 https://doi.org/10.1111/tpj.12420	journal	February 2014
Identification of enzymatic genes with the potential to reduce biomass recalcitrance through lignin manipulation in Arabidopsis Sakamoto, Shingo; Kamimura, Naofumi; Tokue, Yosuke Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-01736-6	journal	May 2020
Coexistence but Independent Biosynthesis of Catechyl and Guaiacyl/Syringyl Lignin Polymers in Seed Coats Tobimatsu, Y.; Chen, F.; Nakashima, J. The Plant Cell, Vol. 25, Issue 7 https://doi.org/10.1105/tpc.113.113142	journal	July 2013
EORNA, a barley gene and transcript abundance database Milne, Linda; Bayer, Micha; Rapazote-Flores, Paulo Scientific Data, Vol. 8, Issue 1 https://doi.org/10.1038/s41597-021-00872-4	journal	March 2021
Lignin Biosynthesis and Structure Vanholme, R.; Demedts, B.; Morreel, K. Plant Physiology, Vol. 153, Issue 3, p. 895-905 https://doi.org/10.1104/pp.110.155119	journal	May 2010
Molecular-Genetic Analysis of Plant Cytochrome P450-Dependent Monooxygenases Chapple, Clint Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 49, Issue 1 https://doi.org/10.1146/annurev.arplant.49.1.311	journal	June 1998
Structural Redesigning Arabidopsis Lignins into Alkali-Soluble Lignins through the Expression of p- Coumaroyl-CoA:Monolignol Transferase PMT Sibout, Richard; Le Bris, Philippe; Legée, Frédéric Plant Physiology, Vol. 170, Issue 3 https://doi.org/10.1104/pp.15.01877	journal	January 2016
Simultaneous regulation of F5H in COMT ‐ RNA i transgenic switchgrass alters effects of COMT suppression on syringyl lignin biosynthesis Wu, Zhenying; Wang, Nengfei; Hisano, Hiroshi Plant Biotechnology Journal, Vol. 17, Issue 4 https://doi.org/10.1111/pbi.13019	journal	October 2018
p -Hydroxyphenyl, Guaiacyl, and Syringyl Lignins Have Similar Inhibitory Effects on Wall Degradability Grabber, John H.; Ralph, John; Hatfield, Ronald D. Journal of Agricultural and Food Chemistry, Vol. 45, Issue 7 https://doi.org/10.1021/jf970029v	journal	July 1997
An Arabidopsis mutant defective in the general phenylpropanoid pathway. Chapple, C. C.; Vogt, T.; Ellis, B. E. The Plant Cell, Vol. 4, Issue 11 https://doi.org/10.1105/tpc.4.11.1413	journal	November 1992
Lignin characterization of rice CONIFERALDEHYDE 5-HYDROXYLASE loss-of-function mutants generated with the CRISPR/Cas9 system Takeda, Yuri; Suzuki, Shiro; Tobimatsu, Yuki The Plant Journal, Vol. 97, Issue 3 https://doi.org/10.1111/tpj.14141	journal	December 2018
MicroRNA6443‐mediated regulation of FERULATE 5‐HYDROXYLASE gene alters lignin composition and enhances saccharification in Populus tomentosa Fan, Di; Li, Chaofeng; Fan, Chunfen New Phytologist, Vol. 226, Issue 2 https://doi.org/10.1111/nph.16379	journal	January 2020
Cloning, characterization, and expression of two cDNA clones for a rice ferulate-5-hydroxylase gene, a cytochrome P450-dependent monooxygenase Kim, Jin-Hong; Yang, Dae Hwa; Kim, Jae-Sung Journal of Plant Biology, Vol. 49, Issue 3 https://doi.org/10.1007/BF03030533	journal	June 2006
Whole plant cell wall characterization using solution-state 2D NMR Mansfield, Shawn D.; Kim, Hoon; Lu, Fachuang Nature Protocols, Vol. 7, Issue 9 https://doi.org/10.1038/nprot.2012.064	journal	August 2012
Role of bifunctional ammonia-lyase in grass cell wall biosynthesis Barros, Jaime; Serrani-Yarce, Juan C.; Chen, Fang Nature Plants, Vol. 2, Issue 6 https://doi.org/10.1038/nplants.2016.50	journal	May 2016
Comparative evaluations of lignocellulose reactivity and usability in transgenic rice plants with altered lignin composition Takeda, Yuri; Tobimatsu, Yuki; Yamamura, Masaomi Journal of Wood Science, Vol. 65, Issue 1 https://doi.org/10.1186/s10086-019-1784-6	journal	February 2019
Identification and suppression of the p‐ coumaroyl CoA:hydroxycinnamyl alcohol transferase in Zea mays L. Marita, Jane M.; Hatfield, Ronald D.; Rancour, David M. The Plant Journal, Vol. 78, Issue 5 https://doi.org/10.1111/tpj.12510	journal	May 2014
Engineering plant cell walls: tuning lignin monomer composition for deconstructable biofuel feedstocks or resilient biomaterials Ciesielski, Peter N.; Resch, Michael G.; Hewetson, Barron Green Chemistry, Vol. 16, Issue 5, p. 2627-2635 https://doi.org/10.1039/c3gc42422g	journal	January 2014
Regulation of CONIFERALDEHYDE 5-HYDROXYLASE expression to modulate cell wall lignin structure in rice Takeda, Yuri; Koshiba, Taichi; Tobimatsu, Yuki Planta, Vol. 246, Issue 2 https://doi.org/10.1007/s00425-017-2692-x	journal	April 2017
Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5 Kim, Hoon; Ralph, John Org. Biomol. Chem., Vol. 8, Issue 3 https://doi.org/10.1039/B916070A	journal	January 2010
Plant biomechanics and resilience to environmental changes are controlled by specific lignin chemistries in each vascular cell type and morphotype Ménard, Delphine; Blaschek, Leonard; Kriechbaum, Konstantin The Plant Cell, Vol. 34, Issue 12 https://doi.org/10.1093/plcell/koac284	journal	September 2022
A decimal code for the growth stages of cereals Zadoks, J. C.; Chang, T. T.; Konzak, C. F. Weed Research, Vol. 14, Issue 6 https://doi.org/10.1111/j.1365-3180.1974.tb01084.x	journal	December 1974
The Effects on Lignin Structure of Overexpression of Ferulate 5-Hydroxylase in Hybrid Poplar ¹ Stewart, Jaclyn J.; Akiyama, Takuya; Chapple, Clint Plant Physiology, Vol. 150, Issue 2 https://doi.org/10.1104/pp.109.137059	journal	April 2009
Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana Van Acker, Rebecca; Vanholme, Ruben; Storme, Véronique Biotechnology for Biofuels, Vol. 6, Article No. 46 https://doi.org/10.1186/1754-6834-6-46	journal	January 2013
Assembly of an Evolutionarily New Pathway for α-Pyrone Biosynthesis in Arabidopsis Weng, Jing-Ke; Li, Yi; Mo, Huaping Science, Vol. 337, Issue 6097 https://doi.org/10.1126/science.1221614	journal	August 2012
Targeted down-regulation of cytochrome P450 enzymes for forage quality improvement in alfalfa (Medicago sativa L.) Reddy, M. S. S.; Chen, F.; Shadle, G. Proceedings of the National Academy of Sciences, Vol. 102, Issue 46 https://doi.org/10.1073/pnas.0505749102	journal	November 2005
Plant Phenylalanine/Tyrosine Ammonia-lyases Barros, Jaime; Dixon, Richard A. Trends in Plant Science, Vol. 25, Issue 1 https://doi.org/10.1016/j.tplants.2019.09.011	journal	January 2020
Pathway of p-Coumaric Acid Incorporation into Maize Lignin As Revealed by NMR Ralph, John; Hatfield, Ronald D.; Quideau, Stephane Journal of the American Chemical Society, Vol. 116, Issue 21, p. 9448-9456 https://doi.org/10.1021/ja00100a006	journal	October 1994
Detection and Determination of p-Coumaroylated Units in Lignins Lu, Fachuang; Ralph, John Journal of Agricultural and Food Chemistry, Vol. 47, Issue 5, p. 1988-1992 https://doi.org/10.1021/jf981140j	journal	May 1999
An essential role of caffeoyl shikimate esterase in monolignol biosynthesis in Medicago truncatula Ha, Chan Man; Escamilla-Trevino, Luis; Yarce, Juan Carlos Serrani The Plant Journal, Vol. 86, Issue 5 https://doi.org/10.1111/tpj.13177	journal	June 2016
Independent origins of syringyl lignin in vascular plants Weng, J. -K.; Li, X.; Stout, J. Proceedings of the National Academy of Sciences, Vol. 105, Issue 22 https://doi.org/10.1073/pnas.0801696105	journal	May 2008
Cytochromes P450 Bak, Søren; Beisson, Fred; Bishop, Gerard The Arabidopsis Book, Vol. 9 https://doi.org/10.1199/tab.0144	journal	January 2011
Manipulation of Lignin Monomer Composition Combined with the Introduction of Monolignol Conjugate Biosynthesis Leads to Synergistic Changes in Lignin Structure Smith, Rebecca A.; Lu, Fachuang; Muro-Villanueva, Fabiola Plant and Cell Physiology, Vol. 63, Issue 6 https://doi.org/10.1093/pcp/pcac031	journal	March 2022

Similar Records

Downregulation of p-COUMAROYL ESTER 3-HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification

Journal Article · Mon Jun 11 00:00:00 EDT 2018 · The Plant Journal · OSTI ID:1970481

Takeda, Yuri; Tobimatsu, Yuki; Karlen, Steven D.; +10 more

Compensatory Guaiacyl Lignin Biosynthesis at the Expense of Syringyl Lignin in 4CL1-Knockout Poplar -Knockout Poplar

Journal Article · Fri May 08 00:00:00 EDT 2020 · Plant Physiology (Bethesda) · OSTI ID:1970481

Tsai, Chung-Jui; Xu, Peng; Xue, Liang-Jiao; +14 more

Time course field analysis of COMT-downregulated switchgrass: Lignification, recalcitrance, and rust susceptibility

Journal Article · Wed May 18 00:00:00 EDT 2016 · BioEnergy Research · OSTI ID:1970481

Baxter, Holly L.; Mazarei, Mitra; Fu, Chunxiang; +8 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
syringyl
guaiacyl
ferulate 5-hydroxylase
RNAi
saccharification
feedstock
recalcitrance

Title: Downregulation of barley ferulate 5-hydroxylase dramatically alters straw lignin structure without impact on mechanical properties

Citation Formats

References (57)

Similar Records

Related Subjects