Agronomic performance of Populus deltoides trees engineered for biofuel production
Abstract
Background: One of the major barriers to the development of lignocellulosic feedstocks is the recalcitrance of plant cell walls to deconstruction and saccharification. Recalcitrance can be reduced by targeting genes involved in cell wall biosynthesis, but this can have unintended consequences that compromise the agronomic performance of the trees under field conditions. Here we report the results of a field trial of fourteen distinct transgenic Populus deltoides lines that had previously demonstrated reduced recalcitrance without yield penalties under greenhouse conditions.Results: Survival and productivity of the trial were excellent in the first year, and there was little evidence for reduced performance of the transgenic lines with modified target gene expression. Surprisingly, the most striking phenotypic effects in this trial were for two empty-vector control lines that had modified bud set and bud flush. This is most likely due to somaclonal variation or insertional mutagenesis. Traits related to yield, crown architecture, herbivory, pathogen response, and frost damage showed few significant differences between target gene transgenics and empty vector controls. However, there were a few interesting exceptions. Lines overexpressing the DUF231 gene, a putative O-acetyltransferase, showed early bud flush and marginally increased height growth. Lines overexpressing the DUF266 gene, a putative glycosyltransferase, hadmore »
- Authors:
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1618697
- Alternate Identifier(s):
- OSTI ID: 1435303
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Published Article
- Journal Name:
- Biotechnology for Biofuels
- Additional Journal Information:
- Journal Name: Biotechnology for Biofuels Journal Volume: 10 Journal Issue: 1; Journal ID: ISSN 1754-6834
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 09 BIOMASS FUELS
Citation Formats
Macaya-Sanz, David, Chen, Jin‐Gui, Kalluri, Udaya C., Muchero, Wellington, Tschaplinski, Timothy J., Gunter, Lee E., Simon, Sandra J., Biswal, Ajaya K., Bryan, Anthony C., Payyavula, Raja, Xie, Meng, Yang, Yongil, Zhang, Jin, Mohnen, Debra, Tuskan, Gerald A., and DiFazio, Stephen P. Agronomic performance of Populus deltoides trees engineered for biofuel production. Netherlands: N. p., 2017.
Web. doi:10.1186/s13068-017-0934-6.
Macaya-Sanz, David, Chen, Jin‐Gui, Kalluri, Udaya C., Muchero, Wellington, Tschaplinski, Timothy J., Gunter, Lee E., Simon, Sandra J., Biswal, Ajaya K., Bryan, Anthony C., Payyavula, Raja, Xie, Meng, Yang, Yongil, Zhang, Jin, Mohnen, Debra, Tuskan, Gerald A., & DiFazio, Stephen P. Agronomic performance of Populus deltoides trees engineered for biofuel production. Netherlands. https://doi.org/10.1186/s13068-017-0934-6
Macaya-Sanz, David, Chen, Jin‐Gui, Kalluri, Udaya C., Muchero, Wellington, Tschaplinski, Timothy J., Gunter, Lee E., Simon, Sandra J., Biswal, Ajaya K., Bryan, Anthony C., Payyavula, Raja, Xie, Meng, Yang, Yongil, Zhang, Jin, Mohnen, Debra, Tuskan, Gerald A., and DiFazio, Stephen P. Thu .
"Agronomic performance of Populus deltoides trees engineered for biofuel production". Netherlands. https://doi.org/10.1186/s13068-017-0934-6.
@article{osti_1618697,
title = {Agronomic performance of Populus deltoides trees engineered for biofuel production},
author = {Macaya-Sanz, David and Chen, Jin‐Gui and Kalluri, Udaya C. and Muchero, Wellington and Tschaplinski, Timothy J. and Gunter, Lee E. and Simon, Sandra J. and Biswal, Ajaya K. and Bryan, Anthony C. and Payyavula, Raja and Xie, Meng and Yang, Yongil and Zhang, Jin and Mohnen, Debra and Tuskan, Gerald A. and DiFazio, Stephen P.},
abstractNote = {Background: One of the major barriers to the development of lignocellulosic feedstocks is the recalcitrance of plant cell walls to deconstruction and saccharification. Recalcitrance can be reduced by targeting genes involved in cell wall biosynthesis, but this can have unintended consequences that compromise the agronomic performance of the trees under field conditions. Here we report the results of a field trial of fourteen distinct transgenic Populus deltoides lines that had previously demonstrated reduced recalcitrance without yield penalties under greenhouse conditions.Results: Survival and productivity of the trial were excellent in the first year, and there was little evidence for reduced performance of the transgenic lines with modified target gene expression. Surprisingly, the most striking phenotypic effects in this trial were for two empty-vector control lines that had modified bud set and bud flush. This is most likely due to somaclonal variation or insertional mutagenesis. Traits related to yield, crown architecture, herbivory, pathogen response, and frost damage showed few significant differences between target gene transgenics and empty vector controls. However, there were a few interesting exceptions. Lines overexpressing the DUF231 gene, a putative O-acetyltransferase, showed early bud flush and marginally increased height growth. Lines overexpressing the DUF266 gene, a putative glycosyltransferase, had significantly decreased stem internode length and slightly higher volume index. Finally, lines overexpressing the PFD2 gene, a putative member of the prefoldin complex, had a slightly reduced volume index.Conclusions: This field trial demonstrates that these cell wall modifications, which decreased cell wall recalcitrance under laboratory conditions, did not seriously compromise first-year performance in the field, despite substantial challenges, including an outbreak of a stem boring insect (Gypsonoma haimbachiana), attack by a leaf rust pathogen (Melampsora spp.), and a late frost event. This bodes well for the potential utility of these lines as advanced biofuels feedstocks.},
doi = {10.1186/s13068-017-0934-6},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 10,
place = {Netherlands},
year = {Thu Nov 30 00:00:00 EST 2017},
month = {Thu Nov 30 00:00:00 EST 2017}
}
https://doi.org/10.1186/s13068-017-0934-6
Web of Science
Works referenced in this record:
Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees
journal, August 1999
- Hu, Wen-Jing; Harding, Scott A.; Lung, Jrhau
- Nature Biotechnology, Vol. 17, Issue 8, p. 808-812
Gene-trap mutagenesis: past, present and beyond
journal, October 2001
- Stanford, William L.; Cohn, Jason B.; Cordes, Sabine P.
- Nature Reviews Genetics, Vol. 2, Issue 10
Chlamydomonas reinhardtii Has Multiple Prolyl 4-Hydroxylases, One of Which Is Essential for Proper Cell Wall Assembly
journal, January 2007
- Keskiaho, Katriina; Hieta, Reija; Sormunen, Raija
- The Plant Cell, Vol. 19, Issue 1
Bioenergy research: a new paradigm in multidisciplinary research
journal, April 2010
- Kalluri, Udaya C.; Keller, Martin
- Journal of The Royal Society Interface, Vol. 7, Issue 51
Defining the Boundaries and Characterizing the Landscape of Functional Genome Expression in Vascular Tissues of Populus using Shotgun Proteomics
journal, November 2011
- Abraham, Paul; Adams, Rachel; Giannone, Richard J.
- Journal of Proteome Research, Vol. 11, Issue 1
The Shikimate Pathway and Aromatic Amino Acid Biosynthesis in Plants
journal, June 2012
- Maeda, Hiroshi; Dudareva, Natalia
- Annual Review of Plant Biology, Vol. 63, Issue 1
Dynamic Regulation of Cortical Microtubule Organization through Prefoldin-DELLA Interaction
journal, May 2013
- Locascio, Antonella; Blázquez, Miguel A.; Alabadí, David
- Current Biology, Vol. 23, Issue 9
Elimination of metabolic pathways to all traditional fermentation products increases ethanol yields in Clostridium thermocellum
journal, November 2015
- Papanek, Beth; Biswas, Ranjita; Rydzak, Thomas
- Metabolic Engineering, Vol. 32
T-DNA insertional mutagenesis for functional genomics in rice
journal, June 2000
- Jeon, Jong-Seong; Lee, Sichul; Jung, Ki-Hong
- The Plant Journal, Vol. 22, Issue 6
13C Nuclear Magnetic Resonance Detection of Interactions of Serine Hydroxymethyltransferase with C1-Tetrahydrofolate Synthase and Glycine Decarboxylase Complex Activities in Arabidopsis
journal, September 1996
- Prabhu, V.; Chatson, K. B.; Abrams, G. D.
- Plant Physiology, Vol. 112, Issue 1
Initial characterization of shade avoidance response suggests functional diversity between Populus phytochrome B genes
journal, September 2012
- Karve, Abhijit A.; Jawdy, Sara S.; Gunter, Lee E.
- New Phytologist, Vol. 196, Issue 3
Identification of candidate genes in Arabidopsis and Populus cell wall biosynthesis using text-mining, co-expression network analysis and comparative genomics
journal, December 2011
- Yang, Xiaohan; Ye, Chu-Yu; Bisaria, Anjali
- Plant Science, Vol. 181, Issue 6
Consolidated bioprocessing of cellulosic biomass: an update
journal, October 2005
- Lynd, Lee R.; van Zyl, Willem H.; McBride, John E.
- Current Opinion in Biotechnology, Vol. 16, Issue 5, p. 577-583
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
Bud set in poplar - genetic dissection of a complex trait in natural and hybrid populations
journal, October 2010
- Rohde, Antje; Storme, Véronique; Jorge, Véronique
- New Phytologist, Vol. 189, Issue 1
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
Growth under field conditions affects lignin content and productivity in transgenic Populus trichocarpa with altered lignin biosynthesis
journal, September 2014
- Stout, Anna T.; Davis, Aletta A.; Domec, Jean-Christophe
- Biomass and Bioenergy, Vol. 68
The Genetics of Lignin Biosynthesis: Connecting Genotype to Phenotype
journal, December 2010
- Bonawitz, Nicholas D.; Chapple, Clint
- Annual Review of Genetics, Vol. 44, Issue 1, p. 337-363
Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
journal, August 2014
- Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli
- Nature Genetics, Vol. 46, Issue 10
Phytozome: a comparative platform for green plant genomics
journal, November 2011
- Goodstein, David M.; Shu, Shengqiang; Howson, Russell
- Nucleic Acids Research, Vol. 40, Issue D1
The Populus Class III HD ZIP Transcription Factor POPCORONA Affects Cell Differentiation during Secondary Growth of Woody Stems
journal, February 2011
- Du, Juan; Miura, Eriko; Robischon, Marcel
- PLoS ONE, Vol. 6, Issue 2
Downregulation of GAUT12 in Populus deltoides by RNA silencing results in reduced recalcitrance, increased growth and reduced xylan and pectin in a woody biofuel feedstock
journal, January 2015
- Biswal, Ajaya K.; Hao, Zhangying; Pattathil, Sivakumar
- Biotechnology for Biofuels, Vol. 8, Issue 1
Recent progress in consolidated bioprocessing
journal, June 2012
- Olson, Daniel G.; McBride, John E.; Joe Shaw, A.
- Current Opinion in Biotechnology, Vol. 23, Issue 3, p. 396-405
Cortical microtubule rearrangements and cell wall patterning
journal, April 2015
- Oda, Yoshihisa
- Frontiers in Plant Science, Vol. 6
Deconstruction of Lignocellulosic Biomass to Fuels and Chemicals
journal, July 2011
- Chundawat, Shishir P. S.; Beckham, Gregg T.; Himmel, Michael E.
- Annual Review of Chemical and Biomolecular Engineering, Vol. 2, Issue 1, p. 121-145
Pampered inside, pestered outside? Differences and similarities between plants growing in controlled conditions and in the field
journal, October 2016
- Poorter, Hendrik; Fiorani, Fabio; Pieruschka, Roland
- New Phytologist, Vol. 212, Issue 4
Cellulosic Biofuels
journal, June 2009
- Carroll, Andrew; Somerville, Chris
- Annual Review of Plant Biology, Vol. 60, Issue 1
Shotgun proteome profile of Populus developing xylem
journal, November 2009
- Kalluri, Udaya C.; Hurst, Gregory B.; Lankford, Patricia K.
- PROTEOMICS, Vol. 9, Issue 21, p. 4871-4880
Stability of Herbicide Resistance over 8 Years of Coppice in Field-Grown, Genetically Engineered Poplars
journal, April 2008
- Li, Jingyi; Meilan, Richard; Ma, Cathleen
- Western Journal of Applied Forestry, Vol. 23, Issue 2
Retrotransposons of rice involved in mutations induced by tissue culture.
journal, July 1996
- Hirochika, H.; Sugimoto, K.; Otsuki, Y.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 15
Lignin content in natural Populus variants affects sugar release
journal, March 2011
- Studer, M. H.; DeMartini, J. D.; Davis, M. F.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 15, p. 6300-6305
TRICHOME BIREFRINGENCE and Its Homolog AT5G01360 Encode Plant-Specific DUF231 Proteins Required for Cellulose Biosynthesis in Arabidopsis
journal, April 2010
- Bischoff, Volker; Nita, Silvia; Neumetzler, Lutz
- Plant Physiology, Vol. 153, Issue 2
Stability of transgenes in trees: expression of two reporter genes in poplar over three field seasons
journal, December 2008
- Li, J.; Brunner, A. M.; Meilan, R.
- Tree Physiology, Vol. 29, Issue 2
Dissection of the Transcriptional Program Regulating Secondary Wall Biosynthesis during Wood Formation in Poplar
journal, September 2011
- Zhong, Ruiqin; McCarthy, Ryan L.; Lee, Chanhui
- Plant Physiology, Vol. 157, Issue 3
Direct conversion of plant biomass to ethanol by engineered Caldicellulosiruptor bescii
journal, June 2014
- Chung, D.; Cha, M.; Guss, A. M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 24, p. 8931-8936
Bioinformatics-Based Identification of Candidate Genes from QTLs Associated with Cell Wall Traits in Populus
journal, November 2009
- Ranjan, Priya; Yin, Tongming; Zhang, Xinye
- BioEnergy Research, Vol. 3, Issue 2, p. 172-182
Vernalization and the chilling requirement to exit bud dormancy: shared or separate regulation?
journal, December 2014
- Brunner, Amy M.; Evans, Luke M.; Hsu, Chuan-Yu
- Frontiers in Plant Science, Vol. 5
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
Feasibilities of consolidated bioprocessing microbes: From pretreatment to biofuel production
journal, June 2014
- Parisutham, Vinuselvi; Kim, Tae Hyun; Lee, Sung Kuk
- Bioresource Technology, Vol. 161
Poplar genetic engineering: promoting desirable wood characteristics and pest resistance
journal, May 2013
- Polle, A.; Janz, D.; Teichmann, T.
- Applied Microbiology and Biotechnology, Vol. 97, Issue 13
Field and pulping performances of transgenic trees with altered lignification
journal, June 2002
- Pilate, Gilles; Guiney, Emma; Holt, Karen
- Nature Biotechnology, Vol. 20, Issue 6
The emerging function of IQD proteins as scaffolds in cellular signaling and trafficking
journal, June 2013
- Abel, Steffen; Bürstenbinder, Katharina; Müller, Jens
- Plant Signaling & Behavior, Vol. 8, Issue 6
Transgenic poplars with reduced lignin show impaired xylem conductivity, growth efficiency and survival: Transgenic poplars with reduced lignin
journal, February 2011
- Voelker, Steven L.; Lachenbruch, Barbara; Meinzer, Frederick C.
- Plant, Cell & Environment, Vol. 34, Issue 4
Reduced Wall Acetylation Proteins Play Vital and Distinct Roles in Cell Wall O -Acetylation in Arabidopsis
journal, September 2013
- Manabe, Yuzuki; Verhertbruggen, Yves; Gille, Sascha
- Plant Physiology, Vol. 163, Issue 3
The cinnamyl alcohol dehydrogenase gene family in Populus: phylogeny, organization, and expression
journal, January 2009
- Barakat, Abdelali; Bagniewska-Zadworna, Agnieszka; Choi, Alex
- BMC Plant Biology, Vol. 9, Issue 1
Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase
journal, December 2013
- Van Acker, R.; Leple, J. -C.; Aerts, D.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 2
The Chromosomal Basis of Somaclonal Variation
journal, June 1988
- Lee, M.; Phillips, R. L.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 39, Issue 1
Chilling of Dormant Buds Hyperinduces FLOWERING LOCUS T and Recruits GA-Inducible 1,3-β-Glucanases to Reopen Signal Conduits and Release Dormancy in Populus
journal, January 2011
- Rinne, Päivi L. H.; Welling, Annikki; Vahala, Jorma
- The Plant Cell, Vol. 23, Issue 1
The 20-year environmental safety record of GM trees
journal, July 2010
- Walter, Christian; Fladung, Matthias; Boerjan, Wout
- Nature Biotechnology, Vol. 28, Issue 7
Overexpression of a Domain of Unknown Function 266-containing protein results in high cellulose content, reduced recalcitrance, and enhanced plant growth in the bioenergy crop Populus
journal, March 2017
- Yang, Yongil; Yoo, Chang Geun; Guo, Hao-Bo
- Biotechnology for Biofuels, Vol. 10, Issue 1
DELLAs Contribute to Plant Photomorphogenesis
journal, January 2007
- Achard, Patrick; Liao, Lili; Jiang, Caifu
- Plant Physiology, Vol. 143, Issue 3
Photoperiod- and temperature-mediated control of phenology in trees - a molecular perspective
journal, November 2016
- Singh, Rajesh Kumar; Svystun, Tetiana; AlDahmash, Badr
- New Phytologist, Vol. 213, Issue 2
Genetic instability of plant tissue cultures: breakdown of normal controls.
journal, June 1994
- Phillips, R. L.; Kaeppler, S. M.; Olhoft, P.
- Proceedings of the National Academy of Sciences, Vol. 91, Issue 12
Tyloses and Phenolic Deposits in Xylem Vessels Impede Water Transport in Low-Lignin Transgenic Poplars: A Study by Cryo-Fluorescence Microscopy
journal, July 2010
- Kitin, Peter; Voelker, Steven L.; Meinzer, Frederick C.
- Plant Physiology, Vol. 154, Issue 2
Tissue culture-induced DNA methylation variation in maize.
journal, October 1993
- Kaeppler, S. M.; Phillips, R. L.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 19
Diverse developmental mutants revealed in an activation-tagged population of poplarThis article is one of a selection of papers published on the Special Issue of Poplar Research in Canada.
journal, November 2007
- Harrison, Edward J.; Bush, Michael; Plett, Jonathan M.
- Canadian Journal of Botany, Vol. 85, Issue 11
Two High-Throughput Techniques for Determining Wood Properties as Part of a Molecular Genetics Analysis of Hybrid Poplar and Loblolly Pine
journal, January 1999
- Tuskan, Gerald; West, Darrell; Bradshaw, Harvy D.
- Applied Biochemistry and Biotechnology, Vol. 77, Issue 1-3
Activation tagging is an effective gene tagging system in Populus
journal, July 2010
- Busov, Victor; Yordanov, Yordan; Gou, Jiqing
- Tree Genetics & Genomes, Vol. 7, Issue 1
Role of the Extensin Superfamily in Primary Cell Wall Architecture
journal, March 2011
- Lamport, Derek T. A.; Kieliszewski, Marcia J.; Chen, Yuning
- Plant Physiology, Vol. 156, Issue 1
Works referencing / citing this record:
Overexpression of a serine hydroxymethyltransferase increases biomass production and reduces recalcitrance in the bioenergy crop Populus
journal, January 2019
- Zhang, Jin; Li, Mi; Bryan, Anthony C.
- Sustainable Energy & Fuels, Vol. 3, Issue 1
Agronomic performance of 27 Populus clones evaluated after two 3‐year coppice rotations in Henan, China
journal, December 2019
- Zhang, Jin; Song, Xueqin; Zhang, Lei
- GCB Bioenergy, Vol. 12, Issue 2
Harnessing Soil Microbes to Improve Plant Phosphate Efficiency in Cropping Systems
journal, March 2019
- Kafle, Arjun; Cope, Kevin; Raths, Rachel
- Agronomy, Vol. 9, Issue 3