Transgenic miR156 switchgrass in the field: growth, recalcitrance and rust susceptibility

Baxter, Holly L.; Mazarei, Mitra; Dumitrache, Alexandru; Natzke, Jace M.; Rodriguez, Miguel; Gou, Jiqing; Fu, Chunxiang; Sykes, Robert W.; Turner, Geoffrey B.; Davis, Mark F.; Brown, Steven D.; Davison, Brian H.; Wang, Zeng-Yu; Stewart, C. Neal

doi:10.1111/pbi.12747

Title: Transgenic miR156 switchgrass in the field: growth, recalcitrance and rust susceptibility

Journal Article · Mon Apr 24 00:00:00 EDT 2017 · Plant Biotechnology Journal

DOI:https://doi.org/10.1111/pbi.12747· OSTI ID:1364675

Baxter, Holly L. ^[1]; Mazarei, Mitra ^[1]; Dumitrache, Alexandru ^[2]; Natzke, Jace M. ^[2]; Rodriguez, Miguel ^[2]; Gou, Jiqing ^[3]; Fu, Chunxiang ^[3]; Sykes, Robert W. ^[4]; Turner, Geoffrey B. ^[4]; Davis, Mark F. ^[4]; Brown, Steven D. ^[2];

^[2]; Wang, Zeng-Yu ^[3]; Stewart, C. Neal ^[1]

Department of Plant Sciences, University of Tennessee, Knoxville TN USA; BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge TN USA
BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge TN USA; Biosciences Division, Oak Ridge National Laboratory, Oak Ridge TN USA
BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge TN USA; Samuel Roberts Noble Foundation, Ardmore OK USA
BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge TN USA; National Renewable Energy Laboratory, Golden CO USA

Sustainable utilization of lignocellulosic perennial grass feedstocks will be enabled by high biomass production and optimized cell wall chemistry for efficient conversion into biofuels. MicroRNAs are regulatory elements that modulate the expression of genes involved in various biological functions in plants, including growth and development. In greenhouse studies, overexpressing a microRNA (miR156) gene in switchgrass had dramatic effects on plant architecture and flowering, which appeared to be driven by transgene expression levels. High expressing lines were extremely dwarfed, whereas low and moderate expressing lines had higher biomass yields, improved sugar release, and delayed flowering. Four lines with moderate or low miR156 overexpression from the prior greenhouse study were selected for a field experiment to assess the relationship between miR156 expression and biomass production over three years. We also analyzed important bioenergy feedstock traits such as flowering, disease resistance, cell wall chemistry, and biofuel production. Phenotypes of the transgenic lines were inconsistent between the greenhouse and the field as well as among different field growing seasons. One low expressing transgenic line consistently produced more biomass (25-56%) than the control across all three seasons, which translated to the production of 30% more biofuel per plant during the final season. The other three transgenic lines produced less biomass than the control by the final season, and the two lines with moderate expression levels also exhibited altered disease susceptibilities. Results of this study emphasize the importance of performing multi-year field studies for plants with altered regulatory transgenes that target plant growth and development.

View Journal Article

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); National Renewable Energy Laboratory (NREL), Golden, CO (United States)

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

Grant/Contract Number:: AC05-00OR22725; AC36-08GO28308

OSTI ID:: 1364675

Alternate ID(s):: OSTI ID: 1364676; OSTI ID: 1376550; OSTI ID: 1395091

Report Number(s):: NREL/JA-5100-68393

Journal Information:: Plant Biotechnology Journal, Journal Name: Plant Biotechnology Journal Vol. 16 Journal Issue: 1; ISSN 1467-7644

Publisher:: Society for Experimental Biology; Association of Applied BiologyCopyright Statement

Country of Publication:: United Kingdom

Language:: English

Citation Metrics:

Cited by: 14 works

Citation information provided by
Web of Science

References (55)

Downregulation of Cinnamyl-Alcohol Dehydrogenase in Switchgrass by RNA Silencing Results in Enhanced Glucose Release after Cellulase Treatment Saathoff, Aaron J.; Sarath, Gautam; Chow, Elaine K. PLoS ONE, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pone.0016416	journal	January 2011
Characterization of the Rust Fungus, Puccinia emaculata, and Evaluation of Genetic Variability for Rust Resistance in Switchgrass Populations Uppalapati, Srinivasa Rao; Serba, Desalegn D.; Ishiga, Yasuhiro BioEnergy Research, Vol. 6, Issue 2 https://doi.org/10.1007/s12155-012-9263-6	journal	October 2012
Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana Liu, H. -H.; Tian, X.; Li, Y. -J. RNA, Vol. 14, Issue 5 https://doi.org/10.1261/rna.895308	journal	March 2008
Two-year field analysis of reduced recalcitrance transgenic switchgrass Baxter, Holly L.; Mazarei, Mitra; Labbe, Nicole Plant Biotechnology Journal, Vol. 12, Issue 7 https://doi.org/10.1111/pbi.12195	journal	April 2014
Constitutive expression of the Corngrass1 microRNA in poplar affects plant architecture and stem lignin content and composition Rubinelli, Peter M.; Chuck, George; Li, Xu Biomass and Bioenergy, Vol. 54 https://doi.org/10.1016/j.biombioe.2012.03.001	journal	July 2013
Cell-wall carbohydrates and their modification as a resource for biofuels Pauly, Markus; Keegstra, Kenneth The Plant Journal, Vol. 54, Issue 4, p. 559-568 https://doi.org/10.1111/j.1365-313X.2008.03463.x	journal	May 2008
Transgenic perennial biofuel feedstocks and strategies for bioconfinement Kausch, Albert P.; Hague, Joel; Oliver, Melvin Biofuels, Vol. 1, Issue 1 https://doi.org/10.4155/bfs.09.11	journal	January 2010
First Report of Rust on Switchgrass ( Panicum virgatum ) Caused by Puccinia emaculata in Tennessee Zale, J.; Freshour, L.; Agarwal, S. Plant Disease, Vol. 92, Issue 12 https://doi.org/10.1094/PDIS-92-12-1710B	journal	December 2008
Lignin modification improves fermentable sugar yields for biofuel production Chen, Fang; Dixon, Richard A. Nature Biotechnology, Vol. 25, Issue 7, p. 759-761 https://doi.org/10.1038/nbt1316	journal	June 2007
Reducing the Effect of Variable Starch Levels in Biomass Recalcitrance Screening Decker, Stephen R.; Carlile, Melissa; Selig, Michael J. Biomass Conversion https://doi.org/10.1007/978-1-61779-956-3_17	book	January 2012
The effect of shading on photosynthesis, growth, and regrowth following defoliation for Bromus tectorum Pierson, Elizabeth A.; Mack, Richard N.; Black, R. Alan Oecologia, Vol. 84, Issue 4 https://doi.org/10.1007/BF00328171	journal	October 1990
High-Throughput Screening of Plant Cell-Wall Composition Using Pyrolysis Molecular Beam Mass Spectroscopy Sykes, Robert; Yung, Matthew; Novaes, Evandro Biofuels https://doi.org/10.1007/978-1-60761-214-8_12	book	January 2009
Development and Genetic Control of Plant Architecture and Biomass in the Panicoid Grass, Setaria Mauro-Herrera, Margarita; Doust, Andrew N. PLOS ONE, Vol. 11, Issue 3 https://doi.org/10.1371/journal.pone.0151346	journal	March 2016
Identifying disease threats and management practices for bio-energy crops Stewart, Alison; Cromey, Matthew Current Opinion in Environmental Sustainability, Vol. 3, Issue 1-2 https://doi.org/10.1016/j.cosust.2010.10.008	journal	March 2011
Leaf spot on switch grass ( Panicum virgatum ), symptoms of a new disease caused by Bipolaris oryzae Krupinsky, J. M.; Berdahl, J. D.; Schoch, C. L. Canadian Journal of Plant Pathology, Vol. 26, Issue 3 https://doi.org/10.1080/07060660409507155	journal	September 2004
ORIGINAL RESEARCH: Lignocellulose recalcitrance screening by integrated high-throughput hydrothermal pretreatment and enzymatic saccharification Selig, Michael J.; Tucker, Melvin P.; Sykes, Robert W. Industrial Biotechnology, Vol. 6, Issue 2 https://doi.org/10.1089/ind.2010.0009	journal	April 2010
Manipulating microRNAs for improved biomass and biofuels from plant feedstocks Trumbo, Jennifer Lynn; Zhang, Baohong; Stewart, Charles Neal Plant Biotechnology Journal, Vol. 13, Issue 3 https://doi.org/10.1111/pbi.12319	journal	February 2015
Enhancing digestibility and ethanol yield of Populus wood via expression of an engineered monolignol 4-O-methyltransferase Cai, Yuanheng; Zhang, Kewei; Kim, Hoon Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11989	journal	June 2016
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
Silencing of 4-coumarate:coenzyme A ligase in switchgrass leads to reduced lignin content and improved fermentable sugar yields for biofuel production Xu, Bin; Escamilla-Treviño, Luis L.; Sathitsuksanoh, Noppadon New Phytologist, Vol. 192, Issue 3 https://doi.org/10.1111/j.1469-8137.2011.03830.x	journal	July 2011
Downregulation of Cinnamyl Alcohol Dehydrogenase (CAD) Leads to Improved Saccharification Efficiency in Switchgrass Fu, Chunxiang; Xiao, Xirong; Xi, Yajun BioEnergy Research, Vol. 4, Issue 3, p. 153-164 https://doi.org/10.1007/s12155-010-9109-z	journal	January 2011
A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling Navarro, L.; Dunoyer, P.; Jay, F. Science, Vol. 312, Issue 5772 https://doi.org/10.1126/science.1126088	journal	April 2006
Sugarcane transgenics expressing MYB transcription factors show improved glucose release Poovaiah, Charleson R.; Bewg, William P.; Lan, Wu Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0559-1	journal	July 2016
Altered Lignin Biosynthesis Improves Cellulosic Bioethanol Production in Transgenic Maize Plants Down-Regulated for Cinnamyl Alcohol Dehydrogenase Fornalé, Silvia; Capellades, Montserrat; Encina, Antonio Molecular Plant, Vol. 5, Issue 4 https://doi.org/10.1093/mp/ssr097	journal	July 2012
First Report of Leaf Spot caused by Bipolaris oryzae on Switchgrass in Tennessee Vu, A. L.; Dee, M. M.; Zale, J. Plant Disease, Vol. 97, Issue 12 https://doi.org/10.1094/PDIS-01-13-0070-PDN	journal	December 2013
MicroRNA-Directed Regulation of Arabidopsis AUXIN RESPONSE FACTOR17 Is Essential for Proper Development and Modulates Expression of Early Auxin Response Genes Mallory, Allison C.; Bartel, David P.; Bartel, Bonnie The Plant Cell, Vol. 17, Issue 5 https://doi.org/10.1105/tpc.105.031716	journal	April 2005
Manipulation of plant architecture to enhance lignocellulosic biomass Stamm, P.; Verma, V.; Ramamoorthy, R. AoB Plants, Vol. 2012, Issue 0 https://doi.org/10.1093/aobpla/pls026	journal	January 2012
Switchgrass SBP-box transcription factors PvSPL1 and 2 function redundantly to initiate side tillers and affect biomass yield of energy crop Wu, Zhenying; Cao, Yingping; Yang, Ruijuan Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0516-z	journal	May 2016
Overexpression of miR156 in switchgrass (Panicum virgatum L.) results in various morphological alterations and leads to improved biomass production: Overexpression of miR156 improved switchgrass biomass Fu, Chunxiang; Sunkar, Ramanjulu; Zhou, Chuanen Plant Biotechnology Journal, Vol. 10, Issue 4 https://doi.org/10.1111/j.1467-7652.2011.00677.x	journal	January 2012
Identification and Molecular Characterization of the Switchgrass AP2/ERF Transcription Factor Superfamily, and Overexpression of PvERF001 for Improvement of Biomass Characteristics for Biofuel Wuddineh, Wegi A.; Mazarei, Mitra; Turner, Geoffrey B. Frontiers in Bioengineering and Biotechnology, Vol. 3 https://doi.org/10.3389/fbioe.2015.00101	journal	July 2015
Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks Shen, Hui; He, Xianzhi; Poovaiah, Charleson R. New Phytologist, Vol. 193, Issue 1, p. 121-136 https://doi.org/10.1111/j.1469-8137.2011.03922.x	journal	October 2011
Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass Fu, Chunxiang; Mielenz, Jonathan R.; Xiao, Xirong Proceedings of the National Academy of Sciences, Vol. 108, Issue 9, p. 3803-3808 https://doi.org/10.1073/pnas.1100310108	journal	February 2011
Time Course Field Analysis of COMT-Downregulated Switchgrass: Lignification, Recalcitrance, and Rust Susceptibility Baxter, Holly L.; Mazarei, Mitra; Fu, Chunxiang BioEnergy Research, Vol. 9, Issue 4 https://doi.org/10.1007/s12155-016-9751-1	journal	May 2016
MicroRNA Regulation of NAC-Domain Targets Is Required for Proper Formation and Separation of Adjacent Embryonic, Vegetative, and Floral Organs Mallory, Allison C.; Dugas, Diana V.; Bartel, David P. Current Biology, Vol. 14, Issue 12 https://doi.org/10.1016/j.cub.2004.06.022	journal	June 2004
Overexpression of the maize Corngrass1 microRNA prevents flowering, improves digestibility, and increases starch content of switchgrass Chuck, G. S.; Tobias, C.; Sun, L. Proceedings of the National Academy of Sciences, Vol. 108, Issue 42, p. 17550-17555 https://doi.org/10.1073/pnas.1113971108	journal	October 2011
Biomass recalcitrance. Part I: the chemical compositions and physical structures affecting the enzymatic hydrolysis of lignocellulose Zhao, Xuebing; Zhang, Lihua; Liu, Dehua Biofuels, Bioproducts and Biorefining, Vol. 6, Issue 4 https://doi.org/10.1002/bbb.1331	journal	March 2012
Standardization of Switchgrass Sample Collection for Cell Wall and Biomass Trait Analysis Hardin, C. Frank; Fu, Chunxiang; Hisano, Hiroshi BioEnergy Research, Vol. 6, Issue 2 https://doi.org/10.1007/s12155-012-9292-1	journal	January 2013
Enhanced characteristics of genetically modified switchgrass (Panicum virgatum L.) for high biofuel production Shen, Hui; Poovaiah, Charleson R.; Ziebell, Angela Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-71	journal	January 2013
The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA Chuck, George; Cigan, A. Mark; Saeteurn, Koy Nature Genetics, Vol. 39, Issue 4, p. 544-549 https://doi.org/10.1038/ng2001	journal	March 2007
The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants Cui, Long-Gang; Shan, Jun-Xiang; Shi, Min The Plant Journal, Vol. 80, Issue 6 https://doi.org/10.1111/tpj.12712	journal	November 2014
Overexpression of GA20-OXIDASE1 impacts plant height, biomass allocation and saccharification efficiency in maize Voorend, Wannes; Nelissen, Hilde; Vanholme, Ruben Plant Biotechnology Journal, Vol. 14, Issue 3 https://doi.org/10.1111/pbi.12458	journal	September 2015
Mechanism of Leaf-Shape Determination Tsukaya, Hirokazu Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105320	journal	June 2006
First Report of Leaf Spot Caused by Bipolaris spicifera on Switchgrass in the United States Vu, A. L.; Dee, M. M.; Gualandi, R. J. Plant Disease, Vol. 95, Issue 9 https://doi.org/10.1094/PDIS-10-10-0774	journal	September 2011
The Sequential Action of miR156 and miR172 Regulates Developmental Timing in Arabidopsis Wu, Gang; Park, Mee Yeon; Conway, Susan R. Cell, Vol. 138, Issue 4 https://doi.org/10.1016/j.cell.2009.06.031	journal	August 2009
Field Evaluation of Transgenic Switchgrass Plants Overexpressing PvMYB4 for Reduced Biomass Recalcitrance Baxter, Holly L.; Poovaiah, Charleson R.; Yee, Kelsey L. BioEnergy Research, Vol. 8, Issue 3 https://doi.org/10.1007/s12155-014-9570-1	journal	January 2015
Investigating plant cell wall components that affect biomass recalcitrance in poplar and switchgrass DeMartini, Jaclyn D.; Pattathil, Sivakumar; Miller, Jeffrey S. Energy & Environmental Science, Vol. 6, Issue 3 https://doi.org/10.1039/c3ee23801f	journal	January 2013
Transgenic switchgrass ( Panicum virgatum L.) biomass is increased by overexpression of switchgrass sucrose synthase ( PvSUS1 ) Poovaiah, Charleson R.; Mazarei, Mitra; Decker, Stephen R. Biotechnology Journal, Vol. 10, Issue 4 https://doi.org/10.1002/biot.201400499	journal	November 2014
Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3 Wu, G. Development, Vol. 133, Issue 18 https://doi.org/10.1242/dev.02521	journal	September 2006
RNAi suppression of lignin biosynthesis in sugarcane reduces recalcitrance for biofuel production from lignocellulosic biomass: RNAi suppression of Jung, Je Hyeong; Fouad, Walid M.; Vermerris, Wilfred Plant Biotechnology Journal, Vol. 10, Issue 9 https://doi.org/10.1111/j.1467-7652.2012.00734.x	journal	August 2012
Cessation of Tillering in Spring Wheat in Relation to Light Interception and Red : Far-red Ratio Evers, Jochem B.; Vos, Jan; Andrieu, Bruno Annals of Botany, Vol. 97, Issue 4 https://doi.org/10.1093/aob/mcl020	journal	February 2006
Greenhouse and field evaluation of transgenic poplars with modified gibberellin metabolism and signaling genes Viswanath, Venkatesh; Ma, Cathleen; Etherington, Elizabeth BMC Proceedings, Vol. 5, Issue S7 https://doi.org/10.1186/1753-6561-5-S7-O22	journal	September 2011
Functional Evolution in the Plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) Gene Family Preston, Jill C.; Hileman, Lena C. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00080	journal	January 2013
Transgenic switchgrass ( Panicum virgatum L.) targeted for reduced recalcitrance to bioconversion: a 2-year comparative analysis of field-grown lines modified for target gene or genetic element expression Dumitrache, Alexandru; Natzke, Jace; Rodriguez, Miguel Plant Biotechnology Journal, Vol. 15, Issue 6 https://doi.org/10.1111/pbi.12666	journal	February 2017
Two WUSCHEL-related homeobox Genes, narrow leaf2 and narrow leaf3, Control Leaf Width in Rice Ishiwata, Aiko; Ozawa, Misa; Nagasaki, Hiroshi Plant and Cell Physiology, Vol. 54, Issue 5 https://doi.org/10.1093/pcp/pct032	journal	March 2013
The Biology and Agronomy of Switchgrass for Biofuels Parrish, David J.; Fike, John H. Critical Reviews in Plant Sciences, Vol. 24, Issue 5-6 https://doi.org/10.1080/07352680500316433	journal	September 2005

Similar Records

Light and temperature effects on miR156 transgenic switchgrass flowering: A simulated latitudinal study

Journal Article · Fri Nov 03 00:00:00 EDT 2017 · Plant Direct · OSTI ID:1364675

Johnson, Chelsea R.; Millwood, Reginald J.; Wang, Zeng-Yu; +1 more

Field-grown miR156 transgenic switchgrass reproduction, yield, global gene expression analysis, and bioconfinement

Journal Article · Thu Nov 30 00:00:00 EST 2017 · Biotechnology for Biofuels · OSTI ID:1364675

Johnson, Chelsea R.; Millwood, Reginald J.; Tang, Yuhong; +7 more

Field Evaluation of Transgenic Switchgrass Plants Overexpressing PvMYB₄ for Reduced Biomass Recalcitrance

Journal Article · Wed Jan 07 00:00:00 EST 2015 · BioEnergy Research · OSTI ID:1364675

Baxter, Holly L.; Poovaiah, Charleson R.; Yee, Kelsey L.; +13 more

Related Subjects

60 APPLIED LIFE SCIENCES
microRNA156
biomass
transgene regulation
switchgrass
flowering
bioconfinement
09 BIOMASS FUELS
gene expression

Title: Transgenic miR156 switchgrass in the field: growth, recalcitrance and rust susceptibility

Citation Formats

References (55)

Similar Records

Related Subjects