Enhancing microRNA 167A expression in seed decreases the α-linolenic acid content and increases seed size in Camelina sativa

Na, GunNam; Mu, Xiaopeng; Grabowski, Paul; Schmutz, Jeremy; Lu, Chaofu

doi:10.1111/tpj.14223

Enhancing microRNA 167A expression in seed decreases the α-linolenic acid content and increases seed size in Camelina sativa

Journal Article · Wed Jan 02 23:00:00 EST 2019 · The Plant Journal

DOI:https://doi.org/10.1111/tpj.14223· OSTI ID:1616082

Na, GunNam ^[1]; Mu, Xiaopeng ^[2]; Grabowski, Paul ^[3]; Schmutz, Jeremy ^[4]; ^[1]

Montana State Univ., Bozeman, MT (United States)
Montana State Univ., Bozeman, MT (United States); Shanxi Agricultural Univ., Taigu (China)
HudsonAlpha Inst. of Biotechnology, Huntsville, AL (United States)
HudsonAlpha Inst. of Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Despite well established roles of microRNAs in plant development, few aspects have been addressed to understand their effects in seeds especially on lipid metabolism. In this study, we showed that overexpressing microRNA167A (miR167OE) in camelina (Camelina sativa) under a seed-specific promoter changed fatty acid composition and increased seed size. Specifically, the miR167OE seeds had a lower α-linolenic acid with a concomitantly higher linoleic acid content than the wild-type. This decreased level of fatty acid desaturation corresponded to a decreased transcriptional expression of the camelina fatty acid desaturase3 (CsFAD3) in developing seeds. MiR167 targeted the transcription factor auxin response factor (CsARF8) in camelina, as had been reported previously in Arabidopsis. Chromatin immunoprecipitation experiments combined with transcriptome analysis indicated that CsARF8 bound to promoters of camelina bZIP67 and ABI3 genes. These transcription factors directly or through the ABI3-bZIP12 pathway regulate CsFAD3 expression and affect α-linolenic acid accumulation. In addition, to decipher the miR167A-CsARF8 mediated transcriptional cascade for CsFAD3 suppression, transcriptome analysis was conducted to implicate mechanisms that regulate seed size in camelina. Expression levels of many genes were altered in miR167OE, including orthologs that have previously been identified to affect seed size in other plants. Most notably, genes for seed coat development such as suberin and lignin biosynthesis were down-regulated. Finally, this study provides valuable insights into the regulatory mechanism of fatty acid metabolism and seed size determination, and suggests possible approaches to improve these important traits in camelina.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Montana State Univ., Bozeman, MT (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); USDA

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1616082

Alternate ID(s):: OSTI ID: 1612534
OSTI ID: 1647217
OSTI ID: 1494844

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Journal Issue: 2 Vol. 98; ISSN 0960-7412

Publisher:: Society for Experimental BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (110)

Camelina-derived jet fuel and diesel: Sustainable advanced biofuels Shonnard, David R.; Williams, Larry; Kalnes, Tom N. Environmental Progress & Sustainable Energy, Vol. 29, Issue 3 https://doi.org/10.1002/ep.10461	journal	June 2010
The Bicinchoninic Acid (BCA) Assay for Protein Quantitation Walker, John M. Springer Protocols Handbooks https://doi.org/10.1007/978-1-59745-198-7_3	book	January 2009
Generation of transgenic plants of a potential oilseed crop Camelina sativa by Agrobacterium-mediated transformation Lu, Chaofu; Kang, Jinling Plant Cell Reports, Vol. 27, Issue 2 https://doi.org/10.1007/s00299-007-0454-0	journal	September 2007
Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis Gaj, Malgorzata D.; Zhang, Shibo; Harada, John J. Planta, Vol. 222, Issue 6 https://doi.org/10.1007/s00425-005-0041-y	journal	July 2005
A fatty acid condensing enzyme from Physaria fendleri increases hydroxy fatty acid accumulation in transgenic oilseeds of Camelina sativa Snapp, Anna R.; Kang, Jinling; Qi, Xiaoli Planta, Vol. 240, Issue 3 https://doi.org/10.1007/s00425-014-2122-2	journal	July 2014
Hormonal regulation of tissue-specific ectopic expression of an Arabidopsis endoplasmic reticulum-type ω-3 fatty acid desaturase (FAD3) gene Matsuda, Osamu; Watanabe, Chizuru; Iba, Koh Planta, Vol. 213, Issue 6 https://doi.org/10.1007/s004250100575	journal	October 2001
Networks controlling seed size in Arabidopsis Orozco-Arroyo, Gregorio; Paolo, Dario; Ezquer, Ignacio Plant Reproduction, Vol. 28, Issue 1 https://doi.org/10.1007/s00497-015-0255-5	journal	February 2015
Identification and molecular characterization of miRNAs and their target genes associated with seed development through small RNA sequencing in chickpea Pradhan, Seema; Verma, Subodh; Chakraborty, Anirban Functional & Integrative Genomics, Vol. 21, Issue 2 https://doi.org/10.1007/s10142-021-00777-w	journal	February 2021
Dual DNA Binding Property of ABA insensitive 3 Like Factors Targeted to Promoters Responsive to ABA and Auxin Nag, Ronita; Maity, Manas Kanti; DasGupta, Maitrayee Plant Molecular Biology, Vol. 59, Issue 5 https://doi.org/10.1007/s11103-005-1387-z	journal	November 2005
Abscisic acid or high osmoticum promote accumulation of long-chain fatty acids in developing embryos of Brassica napus Finkelstein, Ruth; Somerville, Chris Plant Science, Vol. 61, Issue 2 https://doi.org/10.1016/0168-9452(89)90227-6	journal	January 1989
Auxin-regulated changes of fatty acid content and composition in soybean zygotic embryo cotyledons Liu, Wennuan; Hildebrand, David F.; Collins, Glenn B. Plant Science, Vol. 106, Issue 1 https://doi.org/10.1016/0168-9452(95)04067-5	journal	March 1995
Regulation and evolution of the interaction of the seed B3 transcription factors with NF-Y subunits Boulard, C.; Fatihi, A.; Lepiniec, L. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1860, Issue 10 https://doi.org/10.1016/j.bbagrm.2017.08.008	journal	October 2017
New frontiers in oilseed biotechnology: meeting the global demand for vegetable oils for food, feed, biofuel, and industrial applications Lu, Chaofu; Napier, Johnathan A.; Clemente, Thomas E. Current Opinion in Biotechnology, Vol. 22, Issue 2 https://doi.org/10.1016/j.copbio.2010.11.006	journal	April 2011
The Transcription Factor FUSCA3 Controls Developmental Timing in Arabidopsis through the Hormones Gibberellin and Abscisic Acid Gazzarrini, Sonia; Tsuchiya, Yuichiro; Lumba, Shelley Developmental Cell, Vol. 7, Issue 3 https://doi.org/10.1016/j.devcel.2004.06.017	journal	September 2004
Biodiesel from Camelina sativa: A comprehensive characterisation Ciubota-Rosie, Camelia; Ruiz, José Ramón; Ramos, María Jesús Fuel, Vol. 105 https://doi.org/10.1016/j.fuel.2012.09.062	journal	March 2013
Characterization of the morphological changes and fatty acid profile of developing Camelina sativa seeds Rodríguez-Rodríguez, Manuel Fernando; Sánchez-García, Alicia; Salas, Joaquín J. Industrial Crops and Products, Vol. 50 https://doi.org/10.1016/j.indcrop.2013.07.042	journal	October 2013
Signaling pathways of seed size control in plants Li, Na; Li, Yunhai Current Opinion in Plant Biology, Vol. 33 https://doi.org/10.1016/j.pbi.2016.05.008	journal	October 2016
Increasing seed mass and oil content in transgenic Arabidopsis by the overexpression of wri1-like gene from Brassica napus Liu, Jing; Hua, Wei; Zhan, Gaomiao Plant Physiology and Biochemistry, Vol. 48, Issue 1 https://doi.org/10.1016/j.plaphy.2009.09.007	journal	January 2010
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
Mutagenesis of the FAE1 genes significantly changes fatty acid composition in seeds of Camelina sativa Ozseyhan, Mehmet E.; Kang, Jinling; Mu, Xiaopeng Plant Physiology and Biochemistry, Vol. 123 https://doi.org/10.1016/j.plaphy.2017.11.021	journal	February 2018
Physiological and developmental regulation of seed oil production Baud, Sébastien; Lepiniec, Loïc Progress in Lipid Research, Vol. 49, Issue 3 https://doi.org/10.1016/j.plipres.2010.01.001	journal	July 2010
TTG1 complex MYBs, MYB5 and TT2, control outer seed coat differentiation Gonzalez, Antonio; Mendenhall, John; Huo, Yujia Developmental Biology, Vol. 325, Issue 2 https://doi.org/10.1016/j.ydbio.2008.10.005	journal	January 2009
“Designer” Biodiesel: Optimizing Fatty Ester Composition to Improve Fuel Properties ^† Knothe, Gerhard Energy & Fuels, Vol. 22, Issue 2 https://doi.org/10.1021/ef700639e	journal	March 2008
Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching Zhang, Yu-Chan; Yu, Yang; Wang, Cong-Ying Nature Biotechnology, Vol. 31, Issue 9 https://doi.org/10.1038/nbt.2646	journal	July 2013
The plasma membrane–bound phospholipase Dδ enhances freezing tolerance in Arabidopsis thaliana Li, Weiqi; Li, Maoyin; Zhang, Wenhua Nature Biotechnology, Vol. 22, Issue 4 https://doi.org/10.1038/nbt949	journal	March 2004
The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure Kagale, Sateesh; Koh, Chushin; Nixon, John Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4706	journal	April 2014
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
microRNA regulation of fruit growth José Ripoll, Juan; Bailey, Lindsay J.; Mai, Quynh-Anh Nature Plants, Vol. 1, Issue 4 https://doi.org/10.1038/nplants.2015.36	journal	March 2015
Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis Yoo, Sang-Dong; Cho, Young-Hee; Sheen, Jen Nature Protocols, Vol. 2, Issue 7 https://doi.org/10.1038/nprot.2007.199	journal	June 2007
An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants Saleh, Abdelaty; Alvarez-Venegas, Raúl; Avramova, Zoya Nature Protocols, Vol. 3, Issue 6 https://doi.org/10.1038/nprot.2008.66	journal	May 2008
Epigenetic mechanisms governing seed development in plants Köhler, Claudia; Makarevich, Grigory EMBO reports, Vol. 7, Issue 12 https://doi.org/10.1038/sj.embor.7400854	journal	December 2006
Manipulation of Auxin Response Factor 19 affects seed size in the woody perennial Jatropha curcas Sun, Yanwei; Wang, Chunming; Wang, Ning Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep40844	journal	January 2017
Flavonoids and the regulation of seed size in Arabidopsis Doughty, James; Aljabri, Maha; Scott, Rod J. Biochemical Society Transactions, Vol. 42, Issue 2 https://doi.org/10.1042/BST20140040	journal	March 2014
Module-specific regulation of the β-phaseolin promoter during embryogenesis Chandrasekharan, Mahesh B.; Bishop, Kenneth J.; Hall, Timothy C. The Plant Journal, Vol. 33, Issue 5 https://doi.org/10.1046/j.1365-313X.2003.01678.x	journal	February 2003
The FUS3 transcription factor functions through the epidermal regulator TTG1 during embryogenesis in Arabidopsis Tsuchiya, Yuichiro; Nambara, Eiji; Naito, Satoshi The Plant Journal, Vol. 37, Issue 1 https://doi.org/10.1046/j.1365-313X.2003.01939.x	journal	January 2004
Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product Reidt, Wim; Wohlfarth, Thomas; Ellerstrom, Mats The Plant Journal, Vol. 21, Issue 5 https://doi.org/10.1046/j.1365-313x.2000.00686.x	journal	March 2000
Seed Development and Differentiation: A Role for Metabolic Regulation Borisjuk, L.; Rolletschek, H.; Radchuk, R. Plant Biology, Vol. 6, Issue 4 https://doi.org/10.1055/s-2004-817908	journal	July 2004
Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis Braybrook, S. A.; Stone, S. L.; Park, S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 9 https://doi.org/10.1073/pnas.0511331103	journal	February 2006
Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers Li, Y.; Beisson, F.; Koo, A. J. K. Proceedings of the National Academy of Sciences, Vol. 104, Issue 46 https://doi.org/10.1073/pnas.0706984104	journal	November 2007
Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: Implications for somatic embryogenesis Stone, S. L.; Braybrook, S. A.; Paula, S. L. Proceedings of the National Academy of Sciences, Vol. 105, Issue 8 https://doi.org/10.1073/pnas.0712364105	journal	February 2008
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
Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis Liu, X.; Zhang, H.; Zhao, Y. Proceedings of the National Academy of Sciences, Vol. 110, Issue 38 https://doi.org/10.1073/pnas.1304651110	journal	August 2013
Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis Li, J.; Nie, X.; Tan, J. L. H. Proceedings of the National Academy of Sciences, Vol. 110, Issue 38 https://doi.org/10.1073/pnas.1305175110	journal	September 2013
Natural variation in ARF18 gene simultaneously affects seed weight and silique length in polyploid rapeseed Liu, Jing; Hua, Wei; Hu, Zhiyong Proceedings of the National Academy of Sciences, Vol. 112, Issue 37 https://doi.org/10.1073/pnas.1502160112	journal	August 2015
Activation and repression of transcription by auxin-response factors Ulmasov, T.; Hagen, G.; Guilfoyle, T. J. Proceedings of the National Academy of Sciences, Vol. 96, Issue 10 https://doi.org/10.1073/pnas.96.10.5844	journal	May 1999
Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana Alonso-Blanco, C.; Blankestijn-de Vries, H.; Hanhart, C. J. Proceedings of the National Academy of Sciences, Vol. 96, Issue 8 https://doi.org/10.1073/pnas.96.8.4710	journal	April 1999
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato Liu, Ning; Wu, Shan; Van Houten, Jason Journal of Experimental Botany, Vol. 65, Issue 9 https://doi.org/10.1093/jxb/eru141	journal	April 2014
The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools Lamesch, Philippe; Berardini, Tanya Z.; Li, Donghui Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1090	journal	December 2011
MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis Nodine, M. D.; Bartel, D. P. Genes & Development, Vol. 24, Issue 23 https://doi.org/10.1101/gad.1986710	journal	December 2010
The turnip Mutant of Arabidopsis Reveals That LEAFY COTYLEDON1 Expression Mediates the Effects of Auxin and Sugars to Promote Embryonic Cell Identity Casson, Stuart A.; Lindsey, Keith Plant Physiology, Vol. 142, Issue 2 https://doi.org/10.1104/pp.106.080895	journal	August 2006
CYP86B1 Is Required for Very Long Chain ω -Hydroxyacid and α , ω -Dicarboxylic Acid Synthesis in Root and Seed Suberin Polyester Compagnon, Vincent; Diehl, Patrik; Benveniste, Irène Plant Physiology, Vol. 150, Issue 4 https://doi.org/10.1104/pp.109.141408	journal	June 2009
The Protein Kinase SnRK2.6 Mediates the Regulation of Sucrose Metabolism and Plant Growth in Arabidopsis Zheng, Zhifu; Xu, Xiaoping; Crosley, Rodney A. Plant Physiology, Vol. 153, Issue 1 https://doi.org/10.1104/pp.109.150789	journal	March 2010
Expression of ZmLEC1 and ZmWRI1 Increases Seed Oil Production in Maize Shen, Bo; Allen, William B.; Zheng, Peizhong Plant Physiology, Vol. 153, Issue 3 https://doi.org/10.1104/pp.110.157537	journal	May 2010
Three Arabidopsis Fatty Acyl-Coenzyme A Reductases, FAR1, FAR4, and FAR5, Generate Primary Fatty Alcohols Associated with Suberin Deposition Domergue, Frédéric; Vishwanath, Sollapura J.; Joubès, Jérôme Plant Physiology, Vol. 153, Issue 4 https://doi.org/10.1104/pp.110.158238	journal	June 2010
MicroRNAs Regulate the Timing of Embryo Maturation in Arabidopsis Willmann, Matthew R.; Mehalick, Andrew J.; Packer, Rachel L. Plant Physiology, Vol. 155, Issue 4 https://doi.org/10.1104/pp.110.171355	journal	February 2011
Acyl Editing and Headgroup Exchange Are the Major Mechanisms That Direct Polyunsaturated Fatty Acid Flux into Triacylglycerols Bates, Philip D.; Fatihi, Abdelhak; Snapp, Anna R. Plant Physiology, Vol. 160, Issue 3 https://doi.org/10.1104/pp.112.204438	journal	August 2012
Identification of Direct Targets of FUSCA3, a Key Regulator of Arabidopsis Seed Development Wang, Fangfang; Perry, Sharyn E. Plant Physiology, Vol. 161, Issue 3 https://doi.org/10.1104/pp.112.212282	journal	January 2013
Brassinosteroid Regulates Seed Size and Shape in Arabidopsis Jiang, Wen-Bo; Huang, Hui-Ya; Hu, Yu-Wei Plant Physiology, Vol. 162, Issue 4 https://doi.org/10.1104/pp.113.217703	journal	June 2013
Overexpression of the FAD3 Desaturase Gene in a Mutant of Arabidopsis Shah, S.; Xin, Z.; Browse, J. Plant Physiology, Vol. 114, Issue 4 https://doi.org/10.1104/pp.114.4.1533	journal	August 1997
The Nonspecific Lipid Transfer Protein AtLtpI-4 Is Involved in Suberin Formation of Arabidopsis thaliana Crown Galls Deeken, Rosalia; Saupe, Stefanie; Klinkenberg, Joern Plant Physiology, Vol. 172, Issue 3 https://doi.org/10.1104/pp.16.01486	journal	September 2016
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
Three Classes of Abscisic Acid (ABA)-Insensitive Mutations of Arabidopsis Define Genes that Control Overlapping Subsets of ABA Responses Finkelstein, Ruth R.; Somerville, Chris R. Plant Physiology, Vol. 94, Issue 3 https://doi.org/10.1104/pp.94.3.1172	journal	November 1990
A New Dynamin-Like Protein, ADL6, Is Involved in Trafficking from the trans -Golgi Network to the Central Vacuole in Arabidopsis Jin, Jing Bo; Kim, Young A.; Kim, Soo Jin The Plant Cell, Vol. 13, Issue 7 https://doi.org/10.1105/TPC.000534	journal	July 2001
The Acyl-CoA Synthetase Encoded by LACS2 Is Essential for Normal Cuticle Development in Arabidopsis Schnurr, Judy; Shockey, Jay; Browse, John The Plant Cell, Vol. 16, Issue 3 https://doi.org/10.1105/tpc.017608	journal	February 2004
AUXIN RESPONSE FACTOR8 Is a Negative Regulator of Fruit Initiation in Arabidopsis Goetz, Marc; Vivian-Smith, Adam; Johnson, Susan D. The Plant Cell, Vol. 18, Issue 8 https://doi.org/10.1105/tpc.105.037192	journal	July 2006
The Acyltransferase GPAT5 Is Required for the Synthesis of Suberin in Seed Coat and Root of Arabidopsis Beisson, Fred; Li, Yonghua; Bonaventure, Gustavo The Plant Cell, Vol. 19, Issue 1 https://doi.org/10.1105/tpc.106.048033	journal	January 2007
MYB58 and MYB63 Are Transcriptional Activators of the Lignin Biosynthetic Pathway during Secondary Cell Wall Formation in Arabidopsis Zhou, Jianli; Lee, Chanhui; Zhong, Ruiqin The Plant Cell, Vol. 21, Issue 1 https://doi.org/10.1105/tpc.108.063321	journal	January 2009
ABI3 and PIL5 Collaboratively Activate the Expression of SOMNUS by Directly Binding to Its Promoter in Imbibed Arabidopsis Seeds Park, Jeongmoo; Lee, Nayoung; Kim, Woohyun The Plant Cell, Vol. 23, Issue 4 https://doi.org/10.1105/tpc.110.080721	journal	April 2011
bZIP67 Regulates the Omega-3 Fatty Acid Content of Arabidopsis Seed Oil by Activating FATTY ACID DESATURASE3 Mendes, Ana; Kelly, Amélie A.; van Erp, Harrie The Plant Cell, Vol. 25, Issue 8 https://doi.org/10.1105/tpc.113.116343	journal	August 2013
MYB118 Represses Endosperm Maturation in Seeds of Arabidopsis Barthole, G.; To, A.; Marchive, C. The Plant Cell, Vol. 26, Issue 9 https://doi.org/10.1105/tpc.114.130021	journal	September 2014
MYB107 and MYB9 Homologs Regulate Suberin Deposition in Angiosperms Lashbrooke, Justin; Cohen, Hagai; Levy-Samocha, Dorit The Plant Cell, Vol. 28, Issue 9 https://doi.org/10.1105/tpc.16.00490	journal	September 2016
Leafy Cotyledon Mutants of Arabidopsis. Meinke, D. W.; Franzmann, L. H.; Nickle, T. C. The Plant Cell https://doi.org/10.1105/tpc.6.8.1049	journal	August 1994
A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele Nambara, Eiji; Naito, Satoshi; McCourt, Peter The Plant Journal, Vol. 2, Issue 4 https://doi.org/10.1111/j.1365-313X.1992.00435.x	journal	July 1992
WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis Cernac, Alex; Benning, Christoph The Plant Journal, Vol. 40, Issue 4, p. 575-585 https://doi.org/10.1111/j.1365-313X.2004.02235.x	journal	September 2004
A high-throughput screen for genes from castor that boost hydroxy fatty acid accumulation in seed oils of transgenic Arabidopsis Lu, Chaofu; Fulda, Martin; Wallis, James G. The Plant Journal, Vol. 45, Issue 5 https://doi.org/10.1111/j.1365-313X.2005.02636.x	journal	March 2006
Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling: TFs of A. thaliana R2R3-MYB subgroup 7 Stracke, Ralf; Ishihara, Hirofumi; Huep, Gunnar The Plant Journal, Vol. 50, Issue 4 https://doi.org/10.1111/j.1365-313X.2007.03078.x	journal	April 2007
WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis: Oil synthesis regulatory network in seeds Baud, Sébastien; Mendoza, Monica Santos; To, Alexandra The Plant Journal, Vol. 50, Issue 5 https://doi.org/10.1111/j.1365-313X.2007.03092.x	journal	April 2007
Deposition and localization of lipid polyester in developing seeds of Brassica napus and Arabidopsis thaliana: Lipid polyesters in seed coats Molina, Isabel; Ohlrogge, John B.; Pollard, Mike The Plant Journal, Vol. 53, Issue 3 https://doi.org/10.1111/j.1365-313X.2007.03348.x	journal	October 2007
Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis Santos-Mendoza, Monica; Dubreucq, Bertrand; Baud, Sébastien The Plant Journal, Vol. 54, Issue 4 https://doi.org/10.1111/j.1365-313X.2008.03461.x	journal	May 2008
Two Arabidopsis 3-ketoacyl CoA synthase genes, KCS20 and KCS2 / DAISY , are functionally redundant in cuticular wax and root suberin biosynthesis, but differentially controlled by osmotic stress Lee, Saet-Buyl; Jung, Su-Jin; Go, Young-Sam The Plant Journal, Vol. 60, Issue 3 https://doi.org/10.1111/j.1365-313X.2009.03973.x	journal	November 2009
Lipid biochemists salute the genome Wallis, James G.; Browse, John The Plant Journal, Vol. 61, Issue 6 https://doi.org/10.1111/j.1365-313X.2010.04125.x	journal	March 2010
Two high linolenic mutants of Arabidopsis thaliana contain megabase-scale genome duplications encompassing the FAD3 locus: High linolenic acid mutants of A. thaliana O’Neill, Carmel M.; Baker, David; Bennett, Gawain The Plant Journal, Vol. 68, Issue 5 https://doi.org/10.1111/j.1365-313X.2011.04742.x	journal	October 2011
Increasing seed oil content in oil-seed rape (Brassica napus L.) by over-expression of a yeast glycerol-3-phosphate dehydrogenase under the control of a seed-specific promoter Vigeolas, Helene; Waldeck, Peter; Zank, Thorsten Plant Biotechnology Journal, Vol. 5, Issue 3 https://doi.org/10.1111/j.1467-7652.2007.00252.x	journal	May 2007
MYB 56 Encoding a R2R3 MYB Transcription Factor Regulates Seed Size in Arabidopsis thaliana : MYB56 and Seed Size Zhang, Yanjie; Liang, Wanqi; Shi, Jianxin Journal of Integrative Plant Biology, Vol. 55, Issue 11 https://doi.org/10.1111/jipb.12094	journal	September 2013
Complexity and robustness of the flavonoid transcriptional regulatory network revealed by comprehensive analyses of MYB-bHLH-WDR complexes and their targets in Arabidopsis seed Xu, Wenjia; Grain, Damaris; Bobet, Sophie New Phytologist, Vol. 202, Issue 1 https://doi.org/10.1111/nph.12620	journal	December 2013
The transcription factor MYB115 contributes to the regulation of proanthocyanidin biosynthesis and enhances fungal resistance in poplar Wang, Lijun; Ran, Lingyu; Hou, Yisu New Phytologist, Vol. 215, Issue 1 https://doi.org/10.1111/nph.14569	journal	April 2017
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
Extension of oil biosynthesis during the mid-phase of seed development enhances oil content in Arabidopsis seeds Kanai, Masatake; Mano, Shoji; Kondo, Maki Plant Biotechnology Journal, Vol. 14, Issue 5 https://doi.org/10.1111/pbi.12489	journal	October 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
Selective gene dosage by CRISPR-Cas9 genome editing in hexaploid Camelina sativa Morineau, Céline; Bellec, Yannick; Tellier, Frédérique Plant Biotechnology Journal, Vol. 15, Issue 6 https://doi.org/10.1111/pbi.12671	journal	April 2017
FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells Zhang, Meng; Cao, Xia; Jia, Qingli The Plant Journal, Vol. 88, Issue 1 https://doi.org/10.1111/tpj.13233	journal	August 2016
Histone acetyltransferase general control non-repressed protein 5 (GCN5) affects the fatty acid composition of Arabidopsis thaliana seeds by acetylating fatty acid desaturase3 ( FAD3 ) Wang, Tianya; Xing, Jiewen; Liu, Xinye The Plant Journal, Vol. 88, Issue 5 https://doi.org/10.1111/tpj.13300	journal	September 2016
Map-based cloning of a gene controlling omega-3 fatty acid desaturation in Arabidopsis Arondel, V.; Lemieux, B.; Hwang, I. Science, Vol. 258, Issue 5086 https://doi.org/10.1126/science.1455229	journal	November 1992
Seed-Development Programs: A Systems Biology–Based Comparison Between Dicots and Monocots Sreenivasulu, Nese; Wobus, Ulrich Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120215	journal	April 2013
Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs Varkonyi-Gasic, Erika; Wu, Rongmei; Wood, Marion Plant Methods, Vol. 3, Issue 1 https://doi.org/10.1186/1746-4811-3-12	journal	January 2007
Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture Rajewski, Alex; Carter-House, Derreck; Stajich, Jason BMC Genomics, Vol. 22, Issue 1 https://doi.org/10.1186/s12864-021-07489-2	journal	March 2021
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
A transgene design for enhancing oil content in Arabidopsis and Camelina seeds Zhu, Yerong; Xie, Linan; Chen, Grace Q. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1049-4	journal	February 2018
Polinton-like viruses are abundant in aquatic ecosystems Bellas, Christopher M.; Sommaruga, Ruben Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00956-0	journal	January 2021
Acyl-Lipid Metabolism Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred The Arabidopsis Book, Vol. 11 https://doi.org/10.1199/tab.0161	journal	January 2013
The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs Schruff, M. C. Development, Vol. 133, Issue 2 https://doi.org/10.1242/dev.02194	journal	December 2005
Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction Wu, M. -F.; Tian, Q.; Reed, J. W. Development, Vol. 133, Issue 21 https://doi.org/10.1242/dev.02602	journal	October 2006
A Regulatory Network for Coordinated Flower Maturation Reeves, Paul H.; Ellis, Christine M.; Ploense, Sara E. PLoS Genetics, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pgen.1002506	journal	February 2012
Identification of MicroRNAs and Transcript Targets in Camelina sativa by Deep Sequencing and Computational Methods Poudel, Saroj; Aryal, Niranjan; Lu, Chaofu PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0121542	journal	March 2015
Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato Zhangjun, Fei,; Ning, Liu,; Biao, Ding, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/98wt-yv70	text	January 2014
Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction Feng, Wu, Miin; Qing, Tian,; W., Reed, Jason The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/db4z-va19	text	January 2006
A Regulatory Network for Coordinated Flower Maturation E., Farmer, Edward; Ina, Haupt,; M., Ellis, Christine The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/qc2e-g010	text	January 2012
Leafy Cotyledon Mutants of Arabidopsis Meinke, David W.; Franzmann, Linda H.; Nickle, Todd C. The Plant Cell, Vol. 6, Issue 8 https://doi.org/10.2307/3869884	journal	August 1994
A New Dynamin-Like Protein, ADL6, Is Involved in Trafficking from the trans-Golgi Network to the Central Vacuole in Arabidopsis Jin, Jing Bo; Kim, Young A.; Kim, Soo Jin The Plant Cell, Vol. 13, Issue 7 https://doi.org/10.2307/3871383	journal	July 2001

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Into the Seed: Auxin Controls Seed Development and Grain Yield Cao, Jinshan; Li, Guoji; Qu, Dejie International Journal of Molecular Sciences, Vol. 21, Issue 5 https://doi.org/10.3390/ijms21051662	journal	February 2020
Additional file 10 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225766	image	January 2020
Additional file 11 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225769.v1	dataset	January 2020
Additional file 1 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225772.v1	dataset	January 2020
Additional file 2 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225775	dataset	January 2020
Additional file 3 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225778.v1	dataset	January 2020
Additional file 4 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225781.v1	dataset	January 2020
Additional file 5 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225784.v1	dataset	January 2020
Additional file 6 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225787.v1	dataset	January 2020
Additional file 7 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225793	dataset	January 2020
Additional file 8 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225796	image	January 2020
Additional file 9 of Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress Song, Yanan; Cui, Hongli; Shi, Ying figshare https://doi.org/10.6084/m9.figshare.13225799.v1	image	January 2020
Additional file 10 of Small RNA profiling for identification of microRNAs involved in regulation of seed development and lipid biosynthesis in yellowhorn Wang, Li; Ruan, Chengjiang; Bao, Aomin figshare https://doi.org/10.6084/m9.figshare.16800305.v1	dataset	January 2021
Additional file 3 of Small RNA profiling for identification of microRNAs involved in regulation of seed development and lipid biosynthesis in yellowhorn Wang, Li; Ruan, Chengjiang; Bao, Aomin figshare https://doi.org/10.6084/m9.figshare.16800326	dataset	January 2021
Additional file 5 of Small RNA profiling for identification of microRNAs involved in regulation of seed development and lipid biosynthesis in yellowhorn Wang, Li; Ruan, Chengjiang; Bao, Aomin figshare https://doi.org/10.6084/m9.figshare.16800332.v1	dataset	January 2021
Additional file 6 of Small RNA profiling for identification of microRNAs involved in regulation of seed development and lipid biosynthesis in yellowhorn Wang, Li; Ruan, Chengjiang; Bao, Aomin figshare https://doi.org/10.6084/m9.figshare.16800335.v1	dataset	January 2021
Additional file 7 of Small RNA profiling for identification of microRNAs involved in regulation of seed development and lipid biosynthesis in yellowhorn Wang, Li; Ruan, Chengjiang; Bao, Aomin figshare https://doi.org/10.6084/m9.figshare.16800338.v1	dataset	January 2021
Additional file 8 of Small RNA profiling for identification of microRNAs involved in regulation of seed development and lipid biosynthesis in yellowhorn Wang, Li; Ruan, Chengjiang; Bao, Aomin figshare https://doi.org/10.6084/m9.figshare.16800341.v1	dataset	January 2021
Additional file 2 of Multiomics comparative analysis of the maize large grain mutant tc19 identified pathways related to kernel development Cai, Qing; Jiao, Fuchao; Wang, Qianqian figshare https://doi.org/10.6084/m9.figshare.24123776	dataset	January 2023
Additional file 3 of Multiomics comparative analysis of the maize large grain mutant tc19 identified pathways related to kernel development Cai, Qing; Jiao, Fuchao; Wang, Qianqian figshare https://doi.org/10.6084/m9.figshare.24123779	dataset	January 2023
Mapping quantitative trait loci for seed traits in Camelina sativa King, Kevin; Li, Huang; Kang, Jinling Theoretical and Applied Genetics, Vol. 132, Issue 9 https://doi.org/10.1007/s00122-019-03371-8	journal	June 2019