CRISPR/Cas9-Induced fad2 and rod1 Mutations Stacked With fae1 Confer High Oleic Acid Seed Oil in Pennycress (Thlaspi arvense L.)

Jarvis, Brice A.; Romsdahl, Trevor B.; McGinn, Michaela G.; Nazarenus, Tara J.; Cahoon, Edgar B.; Chapman, Kent D.; Sedbrook, John C.

doi:10.3389/fpls.2021.652319

Title: CRISPR/Cas9-Induced fad2 and rod1 Mutations Stacked With fae1 Confer High Oleic Acid Seed Oil in Pennycress (Thlaspi arvense L.)

Journal Article · Thu Apr 22 00:00:00 EDT 2021 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2021.652319· OSTI ID:1853580

Jarvis, Brice A. ^[1]; Romsdahl, Trevor B. ^[2]; McGinn, Michaela G. ^[1]; Nazarenus, Tara J. ^[3]; Cahoon, Edgar B. ^[3]; Chapman, Kent D. ^[2]; Sedbrook, John C. ^[1]

Illinois State University (ISU), Normal, IL (United States). School of Biological Sciences
Univ. of North Texas, Denton, TX (United States). Dept. of Biological Sciences. BioDiscovery Inst.
Univ. of Nebraska, Lincoln, NE (United States). Center for Plant Science Innovation. Dept. of Biochemistry

Pennycress (Thlaspi arvense L.) is being domesticated as an oilseed cash cover crop to be grown in the off-season throughout temperate regions of the world. With its diploid genome and ease of directed mutagenesis using molecular approaches, pennycress seed oil composition can be rapidly tailored for a plethora of food, feed, oleochemical and fuel uses. Here, we utilized Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/Cas9 technology to produce knockout mutations in the FATTY ACID DESATURASE2 (FAD2) and REDUCED OLEATE DESATURATION1 (ROD1) genes to increase oleic acid content. High oleic acid (18:1) oil is valued for its oxidative stability that is superior to the polyunsaturated fatty acids (PUFAs) linoleic (18:2) and linolenic (18:3), and better cold flow properties than the very long chain fatty acid (VLCFA) erucic (22:1). When combined with a FATTY ACID ELONGATION1 (fae1) knockout mutation, fad2 fae1 and rod1 fae1 double mutants produced ~90% and ~60% oleic acid in seed oil, respectively, with PUFAs in fad2 fae1 as well as fad2 single mutants reduced to less than 5%. MALDI-MS spatial imaging analyses of phosphatidylcholine (PC) and triacylglycerol (TAG) molecular species in wild-type pennycress embryo sections from mature seeds revealed that erucic acid is highly enriched in cotyledons which serve as storage organs, suggestive of a role in providing energy for the germinating seedling. In contrast, PUFA-containing TAGs are enriched in the embryonic axis, which may be utilized for cellular membrane expansion during seed germination and seedling emergence. Under standard growth chamber conditions, rod1 fae1 plants grew like wild type whereas fad2 single and fad2 fae1 double mutant plants exhibited delayed growth and overall reduced heights and seed yields, suggesting that reducing PUFAs below a threshold in pennycress had negative physiological effects. Taken together, our results suggest that combinatorial knockout of ROD1 and FAE1 may be a viable route to commercially increase oleic acid content in pennycress seed oil whereas mutations in FAD2 will likely require at least partial function to avoid fitness trade-offs.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of North Texas, Denton, TX (United States); Illinois State University (ISU), Normal, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0020325; SC0021286

OSTI ID:: 1853580

Journal Information:: Frontiers in Plant Science, Vol. 12; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (94)

Direct stacking of sequence-specific nuclease-induced mutations to produce high oleic and low linolenic soybean oil Demorest, Zachary L.; Coffman, Andrew; Baltes, Nicholas J. BMC Plant Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12870-016-0906-1	journal	October 2016
Cellular Plasticity in Response to Suppression of Storage Proteins in the Brassica napus Embryo Rolletschek, Hardy; Schwender, Jörg; König, Christina The Plant Cell, Vol. 32, Issue 7 https://doi.org/10.1105/tpc.19.00879	journal	April 2020
Generation of camelina mid-oleic acid seed oil by identification and stacking of fatty acid biosynthetic mutants Neumann, Nicholas G.; Nazarenus, Tara J.; Aznar-Moreno, Jose A. Industrial Crops and Products, Vol. 159 https://doi.org/10.1016/j.indcrop.2020.113074	journal	January 2021
Effects of fatty acid derivatives on the ignition quality and cold flow of diesel fuel Stournas, S.; Lois, E.; Serdari, A. Journal of the American Oil Chemists' Society, Vol. 72, Issue 4 https://doi.org/10.1007/BF02636084	journal	April 1995
Extraction of proteins from pennycress seeds and press cake Selling, Gordon W.; Hojilla-Evangelista, Mila P.; Evangelista, Roque L. Industrial Crops and Products, Vol. 41 https://doi.org/10.1016/j.indcrop.2012.04.009	journal	January 2013
Significant variation for seed oil content, fatty acid profile, and seed weight in natural populations of field pennycress (Thlaspi arvense L.) Altendorf, Kayla; Isbell, Terry; Wyse, Donald L. Industrial Crops and Products, Vol. 129 https://doi.org/10.1016/j.indcrop.2018.11.054	journal	March 2019
Hydrocracking of used cooking oil for biofuels production Bezergianni, Stella; Kalogianni, Aggeliki Bioresource Technology, Vol. 100, Issue 17 https://doi.org/10.1016/j.biortech.2009.03.039	journal	September 2009
Conjugated fatty acids accumulate to high levels in phospholipids of metabolically engineered soybean and Arabidopsis seeds Cahoon, Edgar B.; Dietrich, Charles R.; Meyer, Knut Phytochemistry, Vol. 67, Issue 12 https://doi.org/10.1016/j.phytochem.2006.04.013	journal	June 2006
Pennycress, carbon wise: labeling experiments reveal how pennycress seeds efficiently incorporate carbon into biomass Sedbrook, John C.; Durrett, Timothy P. Journal of Experimental Botany, Vol. 71, Issue 10 https://doi.org/10.1093/jxb/eraa136	journal	May 2020
Identification and stacking of crucial traits required for the domestication of pennycress Chopra, Ratan; Johnson, Evan B.; Emenecker, Ryan Nature Food, Vol. 1, Issue 1 https://doi.org/10.1038/s43016-019-0007-z	journal	January 2020
Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants: CRISPR/Cas9-induced potyvirus resistance Pyott, Douglas E.; Sheehan, Emma; Molnar, Attila Molecular Plant Pathology, Vol. 17, Issue 8 https://doi.org/10.1111/mpp.12417	journal	June 2016
Management of pennycress as a winter annual cash cover crop. A review Cubins, Julija A.; Wells, M. Scott; Frels, Katherine Agronomy for Sustainable Development, Vol. 39, Issue 5 https://doi.org/10.1007/s13593-019-0592-0	journal	September 2019
Simultaneous silencing of FAD2 and FAE1 genes affects both oleic acid and erucic acid contents in Brassica napus seeds Peng, Qi; Hu, Yan; Wei, Ran Plant Cell Reports, Vol. 29, Issue 4 https://doi.org/10.1007/s00299-010-0823-y	journal	February 2010
Molecular tools enabling pennycress ( Thlaspi arvense ) as a model plant and oilseed cash cover crop McGinn, Michaela; Phippen, Winthrop B.; Chopra, Ratan Plant Biotechnology Journal, Vol. 17, Issue 4 https://doi.org/10.1111/pbi.13014	journal	October 2018
Two Acyltransferases Contribute Differently to Linolenic Acid Levels in Seed Oil Marmon, Sofia; Sturtevant, Drew; Herrfurth, Cornelia Plant Physiology, Vol. 173, Issue 4 https://doi.org/10.1104/pp.16.01865	journal	February 2017
Generating Pennycress (Thlaspi arvense) Seed Triacylglycerols and Acetyl-Triacylglycerols Containing Medium-Chain Fatty Acids Esfahanian, Maliheh; Nazarenus, Tara J.; Freund, Meghan M. Frontiers in Energy Research, Vol. 9 https://doi.org/10.3389/fenrg.2021.620118	journal	January 2021
Genome Wide Analysis of Fatty Acid Desaturation and Its Response to Temperature Menard, Guillaume N.; Moreno, Jose Martin; Bryant, Fiona M. Plant Physiology, Vol. 173, Issue 3 https://doi.org/10.1104/pp.16.01907	journal	January 2017
De novo assembly of the pennycress ( Thlaspi arvense ) transcriptome provides tools for the development of a winter cover crop and biodiesel feedstock Dorn, Kevin M.; Fankhauser, Johnathon D.; Wyse, Donald L. The Plant Journal, Vol. 75, Issue 6 https://doi.org/10.1111/tpj.12267	journal	August 2013
Very-long-chain fatty acid biosynthesis is controlled through the expression and specificity of the condensing enzyme Millar, Anthony A.; Kunst, Ljerka The Plant Journal, Vol. 12, Issue 1 https://doi.org/10.1046/j.1365-313X.1997.12010121.x	journal	July 1997
Development of high oleic and low linoleic acid transgenics in a zero erucic acid Brassica juncea L. (Indian mustard) line by antisense suppression of the fad2 gene Sivaraman, Indira; Arumugam, Neelakantan; Sodhi, Yashpal Singh Molecular Breeding, Vol. 13, Issue 4 https://doi.org/10.1023/B:MOLB.0000034092.47934.d6	journal	May 2004
Effects of free fatty acids on oxidative stability of vegetable oil Frega, N.; Mozzon, M.; Lercker, G. Journal of the American Oil Chemists' Society, Vol. 76, Issue 3 https://doi.org/10.1007/s11746-999-0239-4	journal	March 1999
Glycerolipid Synthesis: Biochemistry and Regulation Browse, J.; Somerville, C. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 42, Issue 1 https://doi.org/10.1146/annurev.pp.42.060191.002343	journal	June 1991
Highly efficient heritable plant genome engineering using Cas9 orthologues from Streptococcus thermophilus and Staphylococcus aureus Steinert, Jeannette; Schiml, Simon; Fauser, Friedrich The Plant Journal, Vol. 84, Issue 6 https://doi.org/10.1111/tpj.13078	journal	December 2015
A life cycle assessment of pennycress (Thlaspi arvense L.) -derived jet fuel and diesel Fan, Jiqing; Shonnard, David R.; Kalnes, Tom N. Biomass and Bioenergy, Vol. 55 https://doi.org/10.1016/j.biombioe.2012.12.040	journal	August 2013
Production and Evaluation of Biodiesel from Field Pennycress ( Thlaspi arvense L.) Oil ^† Moser, Bryan R.; Knothe, Gerhard; Vaughn, Steven F. Energy & Fuels, Vol. 23, Issue 8 https://doi.org/10.1021/ef900337g	journal	August 2009
Identification of three genes encoding microsomal oleate desaturases (FAD2) from the oilseed crop Camelina sativa Kang, Jinling; Snapp, Anna R.; Lu, Chaofu Plant Physiology and Biochemistry, Vol. 49, Issue 2 https://doi.org/10.1016/j.plaphy.2010.12.004	journal	February 2011
New insights into the health effects of dietary saturated and omega-6 and omega-3 polyunsaturated fatty acids de Lorgeril, Michel; Salen, Patricia BMC Medicine, Vol. 10, Issue 1 https://doi.org/10.1186/1741-7015-10-50	journal	May 2012
Lifestyle and nutritional imbalances associated with Western diseases: causes and consequences of chronic systemic low-grade inflammation in an evolutionary context Ruiz-Núñez, Begoña; Pruimboom, Leo; Dijck-Brouwer, D. A. Janneke The Journal of Nutritional Biochemistry, Vol. 24, Issue 7 https://doi.org/10.1016/j.jnutbio.2013.02.009	journal	July 2013
Evaluation and enhancement of cold flow properties of palm oil and its biodiesel Verma, Puneet; Sharma, M. P.; Dwivedi, Gaurav Energy Reports, Vol. 2 https://doi.org/10.1016/j.egyr.2015.12.001	journal	November 2016
Biochemical pathways in seed oil synthesis Bates, Philip D.; Stymne, Sten; Ohlrogge, John Current Opinion in Plant Biology, Vol. 16, Issue 3 https://doi.org/10.1016/j.pbi.2013.02.015	journal	June 2013
Jasmonate action in plant growth and development Huang, Huang; Liu, Bei; Liu, Liangyu Journal of Experimental Botany, Vol. 68, Issue 6 https://doi.org/10.1093/jxb/erw495	journal	February 2017
Combination of modern plant breeding and enzyme technology to obtain highly enriched erucic acid from Crambe oil Volkova, Natalia; Li, Xueyuan; Zhu, Li-Hua Sustainable Chemical Processes, Vol. 4, Issue 1 https://doi.org/10.1186/s40508-016-0045-x	journal	January 2016
Camelina seed transcriptome: a tool for meal and oil improvement and translational research Nguyen, Huu T.; Silva, Jillian E.; Podicheti, Ram Plant Biotechnology Journal, Vol. 11, Issue 6 https://doi.org/10.1111/pbi.12068	journal	April 2013
The need for biofuels as part of a low carbon energy future Fulton, Lewis M.; Lynd, Lee R.; Körner, Alexander Biofuels, Bioproducts and Biorefining, Vol. 9, Issue 5 https://doi.org/10.1002/bbb.1559	journal	June 2015
Mutants of Arabidopsis deficient in the synthesis of alpha-linolenate. Biochemical and genetic characterization of the endoplasmic reticulum linoleoyl desaturase Browse, J.; McConn, M.; James, D. Journal of Biological Chemistry, Vol. 268, Issue 22 https://doi.org/10.1016/S0021-9258(19)85427-3	journal	August 1993
The biochemistry of headgroup exchange during triacylglycerol synthesis in canola Bai, Shuangyi; Wallis, James G.; Denolf, Peter The Plant Journal, Vol. 103, Issue 1 https://doi.org/10.1111/tpj.14709	journal	February 2020
Fatty acid-derived signals in plants Weber, Hans Trends in Plant Science, Vol. 7, Issue 5 https://doi.org/10.1016/S1360-1385(02)02250-1	journal	May 2002
Influence of variety and weather conditions on fatty acid composition of winter and spring Camelina sativa varieties in Poland Kurasiak-Popowska, Danuta; Graczyk, Małgorzata; Przybylska-Balcerek, Anna European Food Research and Technology, Vol. 247, Issue 2 https://doi.org/10.1007/s00217-020-03639-0	journal	November 2020
Arabidopsis Fatty Acid Desaturase FAD2 Is Required for Salt Tolerance during Seed Germination and Early Seedling Growth Zhang, Jiantao; Liu, Hua; Sun, Jian PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0030355	journal	January 2012
Techno-economic analysis of pennycress production, harvest and post-harvest logistics for renewable jet fuel Mousavi-Avval, Seyed Hashem; Shah, Ajay Renewable and Sustainable Energy Reviews, Vol. 123 https://doi.org/10.1016/j.rser.2020.109764	journal	May 2020
High-value oils from plants Dyer, John M.; Stymne, Sten; Green, Allan G. The Plant Journal, Vol. 54, Issue 4 https://doi.org/10.1111/j.1365-313X.2008.03430.x	journal	May 2008
Identification of target genes and processes involved in erucic acid accumulation during seed development in the biodiesel feedstock Pennycress (Thlaspi arvense L.) Claver, Ana; Rey, Raquel; López, M. Victoria Journal of Plant Physiology, Vol. 208 https://doi.org/10.1016/j.jplph.2016.10.011	journal	January 2017
Exploiting the wild crucifer Thlaspi arvense to identify conserved and novel genes expressed during a plant’s response to cold stress Sharma, Nirmala; Cram, Dustin; Huebert, Terry Plant Molecular Biology, Vol. 63, Issue 2 https://doi.org/10.1007/s11103-006-9080-4	journal	September 2006
Translational genomics using Arabidopsis as a model enables the characterization of pennycress genes through forward and reverse genetics Chopra, Ratan; Johnson, Evan B.; Daniels, Erin The Plant Journal, Vol. 96, Issue 6 https://doi.org/10.1111/tpj.14147	journal	December 2018
Fatty Acid Desaturation during Chilling Acclimation Is One of the Factors Involved in Conferring Low-Temperature Tolerance to Young Tobacco Leaves Kodama, H.; Horiguchi, G.; Nishiuchi, T. Plant Physiology, Vol. 107, Issue 4 https://doi.org/10.1104/pp.107.4.1177	journal	April 1995
Feedback regulation of plastidic acetyl-CoA carboxylase by 18:1-acyl carrier protein in Brassica napus Andre, C.; Haslam, R. P.; Shanklin, J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 25 https://doi.org/10.1073/pnas.1204604109	journal	June 2012
Matrix assisted laser desorption/ionization-mass spectrometry imaging (MALDI-MSI) for direct visualization of plant metabolites in situ Sturtevant, Drew; Lee, Young-Jin; Chapman, Kent D. Current Opinion in Biotechnology, Vol. 37 https://doi.org/10.1016/j.copbio.2015.10.004	journal	February 2016
Visualizing the oilseed lipidome Sturtevant, Drew; Aziz, Mina; Chapman, Kent INFORM International News on Fats, Oils, and Related Materials, Vol. 29, Issue 4 https://doi.org/10.21748/inform.04.2018.21	journal	April 2018
Enrichment of erucic acid from pennycress (Thlaspi arvense L.) seed oil Isbell, Terry A.; Evangelista, Roque; Glenn, Steve E. Industrial Crops and Products, Vol. 66 https://doi.org/10.1016/j.indcrop.2014.12.050	journal	April 2015
Influence of blending vegetable oil methyl esters on biodiesel fuel properties: Oxidative stability and cold flow properties Serrano, Marta; Oliveros, Rubén; Sánchez, Marcos Energy, Vol. 65 https://doi.org/10.1016/j.energy.2013.11.072	journal	February 2014
The Effect of Climate Change on Linolenic Fatty Acid in Oilseed Rape Wójtowicz, Marek; Wójtowicz, Andrzej Agronomy, Vol. 10, Issue 12 https://doi.org/10.3390/agronomy10122003	journal	December 2020
Extending the story of very-long-chain fatty acid elongation Haslam, Tegan M.; Kunst, Ljerka Plant Science, Vol. 210 https://doi.org/10.1016/j.plantsci.2013.05.008	journal	September 2013
Depressed expression of FAE1 and FAD2 genes modifies fatty acid profiles and storage compounds accumulation in Brassica napus seeds Shi, Jianghua; Lang, Chunxiu; Wang, Fulin Plant Science, Vol. 263 https://doi.org/10.1016/j.plantsci.2017.07.014	journal	October 2017
Biotin attachment domain-containing proteins mediate hydroxy fatty acid-dependent inhibition of acetyl CoA carboxylase Yu, Xiao-Hong; Cai, Yuanheng; Keereetaweep, Jantana Plant Physiology, Vol. 185, Issue 3 https://doi.org/10.1093/plphys/kiaa109	journal	January 2021
Tissue-specific differences in metabolites and transcripts contribute to the heterogeneity of ricinoleic acid accumulation in Ricinus communis L. (castor) seeds Sturtevant, Drew; Romsdahl, Trevor B.; Yu, Xiao-Hong Metabolomics, Vol. 15, Issue 1 https://doi.org/10.1007/s11306-018-1464-3	journal	January 2019
The carbon fertilization effect over a century of anthropogenic CO ₂ emissions: higher intracellular CO ₂ and more drought resistance among invasive and native grass species contrasts with increased water use efficiency for woody plants in the US Southwest Drake, Brandon L.; Hanson, David T.; Lowrey, Timothy K. Global Change Biology, Vol. 23, Issue 2 https://doi.org/10.1111/gcb.13449	journal	September 2016
Heterogeneous Distribution of Erucic Acid in Brassica napus Seeds Lu, Shaoping; Aziz, Mina; Sturtevant, Drew Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01744	journal	January 2020
Compartmentation of Triacylglycerol Accumulation in Plants Chapman, Kent D.; Ohlrogge, John B. Journal of Biological Chemistry, Vol. 287, Issue 4, p. 2288-2294 https://doi.org/10.1074/jbc.R111.290072	journal	November 2011
Spatial and Temporal Mapping of Key Lipid Species in Brassica napus Seeds Woodfield, Helen K.; Sturtevant, Drew; Borisjuk, Ljudmilla Plant Physiology, Vol. 173, Issue 4 https://doi.org/10.1104/pp.16.01705	journal	February 2017
Non-conventional pathways enable pennycress (Thlaspi arvense L.) embryos to achieve high efficiency of oil biosynthesis Tsogtbaatar, Enkhtuul; Cocuron, Jean-Christophe; Alonso, Ana Paula Journal of Experimental Botany, Vol. 71, Issue 10 https://doi.org/10.1093/jxb/eraa060	journal	February 2020
New approaches to facilitate rapid domestication of a wild plant to an oilseed crop: Example pennycress (Thlaspi arvense L.) Sedbrook, John C.; Phippen, Winthrop B.; Marks, M. David Plant Science, Vol. 227 https://doi.org/10.1016/j.plantsci.2014.07.008	journal	October 2014
A review of the effect of the composition of biodiesel on NO x emission, oxidative stability and cold flow properties Lanjekar, R. D.; Deshmukh, D. Renewable and Sustainable Energy Reviews, Vol. 54 https://doi.org/10.1016/j.rser.2015.10.034	journal	February 2016
The FAD2 Gene in Plants: Occurrence, Regulation, and Role Dar, Aejaz A.; Choudhury, Abhikshit R.; Kancharla, Pavan K. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01789	journal	October 2017
Cetyltrimethyl Ammonium Bromide (CTAB) DNA Miniprep for Plant DNA Isolation Clarke, Joseph D. Cold Spring Harbor Protocols, Vol. 2009, Issue 3 https://doi.org/10.1101/pdb.prot5177	journal	March 2009
Brassica carinata genotypes demonstrate potential as a winter biofuel crop in South East United States Kumar, Shivendra; Seepaul, Ramdeo; Mulvaney, Michael J. Industrial Crops and Products, Vol. 150 https://doi.org/10.1016/j.indcrop.2020.112353	journal	August 2020
Evaluation on biodiesel cold flow properties, oxidative stability and enhancement strategies: A review Sia, Chee Bing; Kansedo, Jibrail; Tan, Yie Hua Biocatalysis and Agricultural Biotechnology, Vol. 24 https://doi.org/10.1016/j.bcab.2020.101514	journal	March 2020
Comparative analysis of oil and protein content and seed yield of five Brassicaceae oilseeds on the Canadian prairie Hossain, Zakir; Johnson, Eric N.; Wang, Li Industrial Crops and Products, Vol. 136 https://doi.org/10.1016/j.indcrop.2019.05.001	journal	September 2019
Spatial analysis of lipid metabolites and expressed genes reveals tissue-specific heterogeneity of lipid metabolism in high- and low-oil Brassica napus L. seeds Lu, Shaoping; Sturtevant, Drew; Aziz, Mina The Plant Journal, Vol. 94, Issue 6 https://doi.org/10.1111/tpj.13959	journal	June 2018
Nonsense-mediated mRNA decay: molecular insights and mechanistic variations across species Conti, Elena; Izaurralde, Elisa Current Opinion in Cell Biology, Vol. 17, Issue 3 https://doi.org/10.1016/j.ceb.2005.04.005	journal	June 2005
Identification of a Gene that Complements an Arabidopsis Mutant Deficient in Chloroplast [omega]6 Desaturase Activity Falcone, D. L.; Gibson, S.; Lemieux, B. Plant Physiology, Vol. 106, Issue 4 https://doi.org/10.1104/pp.106.4.1453	journal	December 1994
Soybean Seed Yield and Quality as a Response to Field Pennycress Residue Phippen, Winthrop B.; Phippen, Mary E. Crop Science, Vol. 52, Issue 6 https://doi.org/10.2135/cropsci2012.03.0192	journal	January 2012
Biodiesel production through the use of different sources and characterization of oils and their esters as the substitute of diesel: A review Singh, S. P.; Singh, Dipti Renewable and Sustainable Energy Reviews, Vol. 14, Issue 1 https://doi.org/10.1016/j.rser.2009.07.017	journal	January 2010
Bottlenecks in erucic acid accumulation in genetically engineered ultrahigh erucic acid C rambe abyssinica Guan, Rui; Lager, Ida; Li, Xueyuan Plant Biotechnology Journal, Vol. 12, Issue 2 https://doi.org/10.1111/pbi.12128	journal	October 2013
The Significance of Different Diacylgycerol Synthesis Pathways on Plant Oil Composition and Bioengineering Bates, Philip D.; Browse, John Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00147	journal	January 2012
Light Enables a Very High Efficiency of Carbon Storage in Developing Embryos of Rapeseed Goffman, Fernando D.; Alonso, Ana P.; Schwender, Jörg Plant Physiology, Vol. 138, Issue 4 https://doi.org/10.1104/pp.105.063628	journal	July 2005
Characterization of the FAD2 Gene Family in Soybean Reveals the Limitations of Gel-Based TILLING in Genes with High Copy Number Lakhssassi, Naoufal; Zhou, Zhou; Liu, Shiming Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00324	journal	March 2017
Producing Stable Pyrolysis Liquids from the Oil-Seed Presscakes of Mustard Family Plants: Pennycress (Thlaspi arvense L.) and Camelina (Camelina sativa) ^† Boateng, A. A.; Mullen, C. A.; Goldberg, N. M. Energy & Fuels, Vol. 24, Issue 12 https://doi.org/10.1021/ef101223a	journal	December 2010
Imaging heterogeneity of membrane and storage lipids in transgenic Camelina sativa seeds with altered fatty acid profiles Horn, Patrick J.; Silva, Jillian E.; Anderson, Danielle The Plant Journal https://doi.org/10.1111/tpj.12278	journal	July 2013
Studies on the Flowering of Thlaspi arvense L. IV. Genetic and Ecological Differences between Early- and Late-Flowering Strains Best, K. F. Botanical Gazette, Vol. 139, Issue 2 https://doi.org/10.1086/336986	journal	June 1978
Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana Fauser, Friedrich; Schiml, Simon; Puchta, Holger The Plant Journal, Vol. 79, Issue 2 https://doi.org/10.1111/tpj.12554	journal	June 2014
Membrane lipid polyunsaturation mediated by FATTY ACID DESATURASE 2 ( FAD 2 ) is involved in endoplasmic reticulum stress tolerance in Arabidopsis thaliana Nguyen, Van Cam; Nakamura, Yuki; Kanehara, Kazue The Plant Journal, Vol. 99, Issue 3 https://doi.org/10.1111/tpj.14338	journal	June 2019
The adaptable use of Brassica NIRS calibration equations to identify pennycress variants to facilitate the rapid domestication of a new winter oilseed crop Chopra, Ratan; Folstad, Nicole; Lyons, Joseph Industrial Crops and Products, Vol. 128 https://doi.org/10.1016/j.indcrop.2018.10.079	journal	February 2019
Down-regulation of crambe fatty acid desaturase and elongase in Arabidopsis and crambe resulted in significantly increased oleic acid content in seed oil Li, Xueyuan; Mei, Desheng; Liu, Qing Plant Biotechnology Journal, Vol. 14, Issue 1 https://doi.org/10.1111/pbi.12386	journal	May 2015
Significant enhancement of fatty acid composition in seeds of the allohexaploid, Camelina sativa , using CRISPR/Cas9 gene editing Jiang, Wen Zhi; Henry, Isabelle M.; Lynagh, Peter G. Plant Biotechnology Journal, Vol. 15, Issue 5 https://doi.org/10.1111/pbi.12663	journal	January 2017
Development of ultra-high erucic acid oil in the industrial oil crop Crambe abyssinica : Development of ultra-high erucic acid oil Li, Xueyuan; van Loo, Eibertus N.; Gruber, Jens Plant Biotechnology Journal, Vol. 10, Issue 7 https://doi.org/10.1111/j.1467-7652.2012.00709.x	journal	May 2012
Arabidopsis Genes Involved in Acyl Lipid Metabolism. A 2003 Census of the Candidates, a Study of the Distribution of Expressed Sequence Tags in Organs, and a Web-Based Database Beisson, Frédéric; Koo, Abraham J. K.; Ruuska, Sari Plant Physiology, Vol. 132, Issue 2 https://doi.org/10.1104/pp.103.022988	journal	June 2003
Climate consequences of low-carbon fuels: The United States Renewable Fuel Standard Hill, Jason; Tajibaeva, Liaila; Polasky, Stephen Energy Policy, Vol. 97 https://doi.org/10.1016/j.enpol.2016.07.035	journal	October 2016
Transfection and transformation of Agrobacterium tumefaciens Holsters, M.; de Waele, D.; Depicker, A. Molecular and General Genetics MGG, Vol. 163, Issue 2 https://doi.org/10.1007/BF00267408	journal	January 1978
An improved method for rapid analysis of the fatty acids of glycerolipids Ichihara, Ken'ichi; Shibahara, Akira; Yamamoto, Kohei Lipids, Vol. 31, Issue 8 https://doi.org/10.1007/BF02522986	journal	August 1996
Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis. Okuley, J.; Lightner, J.; Feldmann, K. The Plant Cell, Vol. 6, Issue 1 https://doi.org/10.1105/tpc.6.1.147	journal	January 1994
Understanding the control of acyl flux through the lipid metabolic network of plant oil biosynthesis Bates, Philip D. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1861, Issue 9 https://doi.org/10.1016/j.bbalip.2016.03.021	journal	September 2016
An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis Lu, C.; Xin, Z.; Ren, Z. Proceedings of the National Academy of Sciences, Vol. 106, Issue 44 https://doi.org/10.1073/pnas.0908848106	journal	October 2009
Functional analysis of β-ketoacyl-CoA synthase from biofuel feedstock Thlaspi arvense reveals differences in the triacylglycerol biosynthetic pathway among Brassicaceae Claver, Ana; de la Vega, Marina; Rey-Giménez, Raquel Plant Molecular Biology, Vol. 104, Issue 3 https://doi.org/10.1007/s11103-020-01042-7	journal	August 2020
A draft genome of field pennycress (Thlaspi arvense) provides tools for the domestication of a new winter biofuel crop Dorn, K. M.; Fankhauser, J. D.; Wyse, D. L. DNA Research, Vol. 22, Issue 2 https://doi.org/10.1093/dnares/dsu045	journal	January 2015

Similar Records

Generation of camelina mid-oleic acid seed oil by identification and stacking of fatty acid biosynthetic mutants

Journal Article · Wed Nov 18 00:00:00 EST 2020 · Industrial Crops and Products · OSTI ID:1853580

Neumann, Nicholas G.; Nazarenus, Tara J.; Aznar-Moreno, Jose A.; +5 more

Molecular tools enabling pennycress (Thlaspi arvense) as a model plant and oilseed cash cover crop

Journal Article · Wed Sep 19 00:00:00 EDT 2018 · Plant Biotechnology Journal · OSTI ID:1853580

McGinn, Michaela; Phippen, Winthrop B.; Chopra, Ratan; +10 more

Metabolic engineering of oilseed crops to produce high levels of novel acetyl glyceride oils with reduced viscosity, freezing point and calorific value

Journal Article · Tue Mar 10 00:00:00 EDT 2015 · Plant Biotechnology Journal · OSTI ID:1853580

Liu, Jinjie; Rice, Adam; McGlew, Kathleen; +6 more

Related Subjects

09 BIOMASS FUELS
plant sciences
CRISPR
MALDI-MSI
oilseed
oleic acid
pennycress
polyunsaturated fatty acid
Thlaspi arvense
triacylglycerol

Title: CRISPR/Cas9-Induced fad2 and rod1 Mutations Stacked With fae1 Confer High Oleic Acid Seed Oil in Pennycress (Thlaspi arvense L.)

Citation Formats

References (94)

Similar Records

Related Subjects