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

Abstract

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 threemore » 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.« less

Authors:
 [1];  [1];  [2];  [2];  [2];  [3];  [3];  [4];  [4];  [4];  [2]; ORCiD logo [2];  [3];  [1]
  1. Department of Plant Sciences, University of Tennessee, Knoxville TN USA; BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge TN USA
  2. BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge TN USA; Biosciences Division, Oak Ridge National Laboratory, Oak Ridge TN USA
  3. BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge TN USA; Samuel Roberts Noble Foundation, Ardmore OK USA
  4. BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge TN USA; National Renewable Energy Laboratory, Golden CO USA
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); National Renewable Energy Laboratory (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1364675
Alternate Identifier(s):
OSTI ID: 1364676; OSTI ID: 1376550; OSTI ID: 1395091
Report Number(s):
NREL/JA-5100-68393
Journal ID: ISSN 1467-7644
Grant/Contract Number:  
AC05-00OR22725; AC36-08GO28308
Resource Type:
Published Article
Journal Name:
Plant Biotechnology Journal
Additional Journal Information:
Journal Name: Plant Biotechnology Journal Journal Volume: 16 Journal Issue: 1; Journal ID: ISSN 1467-7644
Publisher:
Society for Experimental Biology; Association of Applied Biology
Country of Publication:
United Kingdom
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; microRNA156; biomass; transgene regulation; switchgrass; flowering; bioconfinement; 09 BIOMASS FUELS; gene expression

Citation Formats

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, and Stewart, C. Neal. Transgenic miR156 switchgrass in the field: growth, recalcitrance and rust susceptibility. United Kingdom: N. p., 2017. Web. doi:10.1111/pbi.12747.
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. Transgenic miR156 switchgrass in the field: growth, recalcitrance and rust susceptibility. United Kingdom. https://doi.org/10.1111/pbi.12747
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, and Stewart, C. Neal. Mon . "Transgenic miR156 switchgrass in the field: growth, recalcitrance and rust susceptibility". United Kingdom. https://doi.org/10.1111/pbi.12747.
@article{osti_1364675,
title = {Transgenic miR156 switchgrass in the field: growth, recalcitrance and rust susceptibility},
author = {Baxter, Holly L. and Mazarei, Mitra and Dumitrache, Alexandru and Natzke, Jace M. and Rodriguez, Miguel and Gou, Jiqing and Fu, Chunxiang and Sykes, Robert W. and Turner, Geoffrey B. and Davis, Mark F. and Brown, Steven D. and Davison, Brian H. and Wang, Zeng-Yu and Stewart, C. Neal},
abstractNote = {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.},
doi = {10.1111/pbi.12747},
journal = {Plant Biotechnology Journal},
number = 1,
volume = 16,
place = {United Kingdom},
year = {Mon Apr 24 00:00:00 EDT 2017},
month = {Mon Apr 24 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/pbi.12747

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Cited by: 14 works
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Works referenced in this record:

Characterization of the Rust Fungus, Puccinia emaculata, and Evaluation of Genetic Variability for Rust Resistance in Switchgrass Populations
journal, October 2012

  • Uppalapati, Srinivasa Rao; Serba, Desalegn D.; Ishiga, Yasuhiro
  • BioEnergy Research, Vol. 6, Issue 2
  • DOI: 10.1007/s12155-012-9263-6

Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana
journal, March 2008


Two-year field analysis of reduced recalcitrance transgenic switchgrass
journal, April 2014

  • Baxter, Holly L.; Mazarei, Mitra; Labbe, Nicole
  • Plant Biotechnology Journal, Vol. 12, Issue 7
  • DOI: 10.1111/pbi.12195

Cell-wall carbohydrates and their modification as a resource for biofuels
journal, May 2008


Transgenic perennial biofuel feedstocks and strategies for bioconfinement
journal, January 2010

  • Kausch, Albert P.; Hague, Joel; Oliver, Melvin
  • Biofuels, Vol. 1, Issue 1
  • DOI: 10.4155/bfs.09.11

First Report of Rust on Switchgrass ( Panicum virgatum ) Caused by Puccinia emaculata in Tennessee
journal, December 2008


Lignin modification improves fermentable sugar yields for biofuel production
journal, June 2007

  • Chen, Fang; Dixon, Richard A.
  • Nature Biotechnology, Vol. 25, Issue 7, p. 759-761
  • DOI: 10.1038/nbt1316

Reducing the Effect of Variable Starch Levels in Biomass Recalcitrance Screening
book, January 2012


The effect of shading on photosynthesis, growth, and regrowth following defoliation for Bromus tectorum
journal, October 1990

  • Pierson, Elizabeth A.; Mack, Richard N.; Black, R. Alan
  • Oecologia, Vol. 84, Issue 4
  • DOI: 10.1007/BF00328171

Development and Genetic Control of Plant Architecture and Biomass in the Panicoid Grass, Setaria
journal, March 2016


Identifying disease threats and management practices for bio-energy crops
journal, March 2011


Leaf spot on switch grass ( Panicum virgatum ), symptoms of a new disease caused by Bipolaris oryzae
journal, September 2004

  • Krupinsky, J. M.; Berdahl, J. D.; Schoch, C. L.
  • Canadian Journal of Plant Pathology, Vol. 26, Issue 3
  • DOI: 10.1080/07060660409507155

ORIGINAL RESEARCH: Lignocellulose recalcitrance screening by integrated high-throughput hydrothermal pretreatment and enzymatic saccharification
journal, April 2010

  • Selig, Michael J.; Tucker, Melvin P.; Sykes, Robert W.
  • Industrial Biotechnology, Vol. 6, Issue 2
  • DOI: 10.1089/ind.2010.0009

Manipulating microRNAs for improved biomass and biofuels from plant feedstocks
journal, February 2015

  • Trumbo, Jennifer Lynn; Zhang, Baohong; Stewart, Charles Neal
  • Plant Biotechnology Journal, Vol. 13, Issue 3
  • DOI: 10.1111/pbi.12319

Enhancing digestibility and ethanol yield of Populus wood via expression of an engineered monolignol 4-O-methyltransferase
journal, June 2016

  • Cai, Yuanheng; Zhang, Kewei; Kim, Hoon
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11989

Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007

  • Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
  • Science, Vol. 315, Issue 5813, p. 804-807
  • DOI: 10.1126/science.1137016

Silencing of 4-coumarate:coenzyme A ligase in switchgrass leads to reduced lignin content and improved fermentable sugar yields for biofuel production
journal, July 2011


Downregulation of Cinnamyl Alcohol Dehydrogenase (CAD) Leads to Improved Saccharification Efficiency in Switchgrass
journal, January 2011


A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling
journal, April 2006


Sugarcane transgenics expressing MYB transcription factors show improved glucose release
journal, July 2016

  • Poovaiah, Charleson R.; Bewg, William P.; Lan, Wu
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0559-1

Altered Lignin Biosynthesis Improves Cellulosic Bioethanol Production in Transgenic Maize Plants Down-Regulated for Cinnamyl Alcohol Dehydrogenase
journal, July 2012

  • Fornalé, Silvia; Capellades, Montserrat; Encina, Antonio
  • Molecular Plant, Vol. 5, Issue 4
  • DOI: 10.1093/mp/ssr097

First Report of Leaf Spot caused by Bipolaris oryzae on Switchgrass in Tennessee
journal, December 2013


Manipulation of plant architecture to enhance lignocellulosic biomass
journal, January 2012


Switchgrass SBP-box transcription factors PvSPL1 and 2 function redundantly to initiate side tillers and affect biomass yield of energy crop
journal, May 2016


Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks
journal, October 2011


Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass
journal, February 2011

  • Fu, Chunxiang; Mielenz, Jonathan R.; Xiao, Xirong
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 9, p. 3803-3808
  • DOI: 10.1073/pnas.1100310108

Time Course Field Analysis of COMT-Downregulated Switchgrass: Lignification, Recalcitrance, and Rust Susceptibility
journal, May 2016


MicroRNA Regulation of NAC-Domain Targets Is Required for Proper Formation and Separation of Adjacent Embryonic, Vegetative, and Floral Organs
journal, June 2004


Overexpression of the maize Corngrass1 microRNA prevents flowering, improves digestibility, and increases starch content of switchgrass
journal, October 2011

  • Chuck, G. S.; Tobias, C.; Sun, L.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 42, p. 17550-17555
  • DOI: 10.1073/pnas.1113971108

Biomass recalcitrance. Part I: the chemical compositions and physical structures affecting the enzymatic hydrolysis of lignocellulose
journal, March 2012

  • Zhao, Xuebing; Zhang, Lihua; Liu, Dehua
  • Biofuels, Bioproducts and Biorefining, Vol. 6, Issue 4
  • DOI: 10.1002/bbb.1331

Standardization of Switchgrass Sample Collection for Cell Wall and Biomass Trait Analysis
journal, January 2013


Enhanced characteristics of genetically modified switchgrass (Panicum virgatum L.) for high biofuel production
journal, January 2013

  • Shen, Hui; Poovaiah, Charleson R.; Ziebell, Angela
  • Biotechnology for Biofuels, Vol. 6, Issue 1
  • DOI: 10.1186/1754-6834-6-71

The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA
journal, March 2007

  • Chuck, George; Cigan, A. Mark; Saeteurn, Koy
  • Nature Genetics, Vol. 39, Issue 4, p. 544-549
  • DOI: 10.1038/ng2001

The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants
journal, November 2014

  • Cui, Long-Gang; Shan, Jun-Xiang; Shi, Min
  • The Plant Journal, Vol. 80, Issue 6
  • DOI: 10.1111/tpj.12712

Overexpression of GA20-OXIDASE1 impacts plant height, biomass allocation and saccharification efficiency in maize
journal, September 2015

  • Voorend, Wannes; Nelissen, Hilde; Vanholme, Ruben
  • Plant Biotechnology Journal, Vol. 14, Issue 3
  • DOI: 10.1111/pbi.12458

Mechanism of Leaf-Shape Determination
journal, June 2006


First Report of Leaf Spot Caused by Bipolaris spicifera on Switchgrass in the United States
journal, September 2011


The Sequential Action of miR156 and miR172 Regulates Developmental Timing in Arabidopsis
journal, August 2009


Field Evaluation of Transgenic Switchgrass Plants Overexpressing PvMYB4 for Reduced Biomass Recalcitrance
journal, January 2015

  • Baxter, Holly L.; Poovaiah, Charleson R.; Yee, Kelsey L.
  • BioEnergy Research, Vol. 8, Issue 3
  • DOI: 10.1007/s12155-014-9570-1

Investigating plant cell wall components that affect biomass recalcitrance in poplar and switchgrass
journal, January 2013

  • DeMartini, Jaclyn D.; Pattathil, Sivakumar; Miller, Jeffrey S.
  • Energy & Environmental Science, Vol. 6, Issue 3
  • DOI: 10.1039/c3ee23801f

Transgenic switchgrass ( Panicum virgatum L.) biomass is increased by overexpression of switchgrass sucrose synthase ( PvSUS1 )
journal, November 2014

  • Poovaiah, Charleson R.; Mazarei, Mitra; Decker, Stephen R.
  • Biotechnology Journal, Vol. 10, Issue 4
  • DOI: 10.1002/biot.201400499

RNAi suppression of lignin biosynthesis in sugarcane reduces recalcitrance for biofuel production from lignocellulosic biomass: RNAi suppression of
journal, August 2012


Cessation of Tillering in Spring Wheat in Relation to Light Interception and Red : Far-red Ratio
journal, February 2006

  • Evers, Jochem B.; Vos, Jan; Andrieu, Bruno
  • Annals of Botany, Vol. 97, Issue 4
  • DOI: 10.1093/aob/mcl020

Greenhouse and field evaluation of transgenic poplars with modified gibberellin metabolism and signaling genes
journal, September 2011


Functional Evolution in the Plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) Gene Family
journal, January 2013


Two WUSCHEL-related homeobox Genes, narrow leaf2 and narrow leaf3, Control Leaf Width in Rice
journal, March 2013

  • Ishiwata, Aiko; Ozawa, Misa; Nagasaki, Hiroshi
  • Plant and Cell Physiology, Vol. 54, Issue 5
  • DOI: 10.1093/pcp/pct032

The Biology and Agronomy of Switchgrass for Biofuels
journal, September 2005