FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells
Abstract
Triacylglycerol (TAG) is the main storage lipid in plant seeds and the major form of plant oil used for food and, increasingly, for industrial and biofuel applications. Several transcription factors, including FUSCA3 (At3 g26790, FUS3), are associated with embryo maturation and oil biosynthesis in seeds. However, the ability of FUS3 to increase TAG biosynthesis in other tissues has not been quantitatively examined. Here, we evaluated the ability of FUS3 to activate TAG accumulation in non-seed tissues. Overexpression of FUS3 driven by an estradiol-inducible promoter increased oil contents in Arabidopsis seedlings up to 6% of dry weight; more than 50-fold over controls. Eicosenoic acid, a characteristic fatty acid of Arabidopsis seed oil, accumulated to over 20% of fatty acids in cotyledons and leaves. These large increases depended on added sucrose, although without sucrose TAG increased three- to four-fold. Inducing the expression of FUS3 in tobacco BY2 cells also increased TAG accumulation, and co-expression of FUS3 and diacylglycerol acyltransferase 1 (DGAT1) further increased TAG levels to 4% of dry weight. BY2 cell growth was not altered by FUS3 expression, although Arabidopsis seedling development was impaired, consistent with the ability of FUS3 to induce embryo characteristics in non-seed tissues. Microarrays of Arabidopsis seedlingsmore »
- Authors:
-
- Northwest A&F University, Yangling, Shaanxi (China). College of Agronomy; Michigan State Univ., East Lansing, MI (United States). Department of Plant Biology and Great Lakes Bioenergy Research Center
- Michigan State Univ., East Lansing, MI (United States). Department of Plant Biology and Great Lakes Bioenergy Research Center
- Northwest A&F University, Yangling, Shaanxi (China). College of Agronomy
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1427683
- Grant/Contract Number:
- FC02-07ER64494
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The Plant Journal
- Additional Journal Information:
- Journal Volume: 88; Journal Issue: 1; Journal ID: ISSN 0960-7412
- Publisher:
- Society for Experimental Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 09 BIOMASS FUELS; FUSCA3; triacylglycerol; vegetative tissue; microarray; arabidopsis; tobacco
Citation Formats
Zhang, Meng, Cao, Xia, Jia, Qingli, and Ohlrogge, John. FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells. United States: N. p., 2016.
Web. doi:10.1111/tpj.13233.
Zhang, Meng, Cao, Xia, Jia, Qingli, & Ohlrogge, John. FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells. United States. https://doi.org/10.1111/tpj.13233
Zhang, Meng, Cao, Xia, Jia, Qingli, and Ohlrogge, John. Sat .
"FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells". United States. https://doi.org/10.1111/tpj.13233. https://www.osti.gov/servlets/purl/1427683.
@article{osti_1427683,
title = {FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells},
author = {Zhang, Meng and Cao, Xia and Jia, Qingli and Ohlrogge, John},
abstractNote = {Triacylglycerol (TAG) is the main storage lipid in plant seeds and the major form of plant oil used for food and, increasingly, for industrial and biofuel applications. Several transcription factors, including FUSCA3 (At3 g26790, FUS3), are associated with embryo maturation and oil biosynthesis in seeds. However, the ability of FUS3 to increase TAG biosynthesis in other tissues has not been quantitatively examined. Here, we evaluated the ability of FUS3 to activate TAG accumulation in non-seed tissues. Overexpression of FUS3 driven by an estradiol-inducible promoter increased oil contents in Arabidopsis seedlings up to 6% of dry weight; more than 50-fold over controls. Eicosenoic acid, a characteristic fatty acid of Arabidopsis seed oil, accumulated to over 20% of fatty acids in cotyledons and leaves. These large increases depended on added sucrose, although without sucrose TAG increased three- to four-fold. Inducing the expression of FUS3 in tobacco BY2 cells also increased TAG accumulation, and co-expression of FUS3 and diacylglycerol acyltransferase 1 (DGAT1) further increased TAG levels to 4% of dry weight. BY2 cell growth was not altered by FUS3 expression, although Arabidopsis seedling development was impaired, consistent with the ability of FUS3 to induce embryo characteristics in non-seed tissues. Microarrays of Arabidopsis seedlings revealed that FUS3 overexpression increased the expression of a higher proportion of genes involved in TAG biosynthesis than genes involved in fatty acid biosynthesis or other lipid pathways. Together these results provide additional insights into FUS3 functions in TAG metabolism and suggest complementary strategies for engineering vegetative oil accumulation.},
doi = {10.1111/tpj.13233},
journal = {The Plant Journal},
number = 1,
volume = 88,
place = {United States},
year = {Sat Jun 11 00:00:00 EDT 2016},
month = {Sat Jun 11 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product
journal, March 2000
- Reidt, Wim; Wohlfarth, Thomas; Ellerstrom, Mats
- The Plant Journal, Vol. 21, Issue 5
The Transcription Factor FUSCA3 Controls Developmental Timing in Arabidopsis through the Hormones Gibberellin and Abscisic Acid
journal, September 2004
- Gazzarrini, Sonia; Tsuchiya, Yuichiro; Lumba, Shelley
- Developmental Cell, Vol. 7, Issue 3
Plant triacylglycerols as feedstocks for the production of biofuels
journal, May 2008
- Durrett, Timothy P.; Benning, Christoph; Ohlrogge, John
- The Plant Journal, Vol. 54, Issue 4, p. 593-607
Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis
journal, February 2011
- Sanjaya, ; Durrett, Timothy P.; Weise, Sean E.
- Plant Biotechnology Journal, Vol. 9, Issue 8, p. 874-883
fusca3: A Heterochronic Mutation Affecting Late Embryo Development in Arabidopsis.
journal, May 1994
- Keith, K.; Kraml, M.; Dengler, N. G.
- The Plant Cell
Oleaginous crops as integrated production platforms for food, feed, fuel and renewable industrial feedstock: Manipulation of plant lipid composition via metabolic engineering and new opportunities from association genetics for crop improvement and valorisation of co-products
journal, November 2014
- Beaudoin, Frédéric; Sayanova, Olga; Haslam, Richard P.
- OCL, Vol. 21, Issue 6
Increasing the flow of carbon into seed oil
journal, November 2009
- Weselake, Randall J.; Taylor, David C.; Rahman, M. Habibur
- Biotechnology Advances, Vol. 27, Issue 6
Complementation of Seed Maturation Phenotypes by Ectopic Expression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis
journal, April 2015
- Roscoe, Thomas T.; Guilleminot, Jocelyne; Bessoule, Jean-Jacques
- Plant and Cell Physiology, Vol. 56, Issue 6
Phospholipid:diacylglycerol acyltransferase: An enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants
journal, May 2000
- Dahlqvist, A.; Stahl, U.; Lenman, M.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6487-6492
Changes in gene expression in the leafy cotyledon1 (lec1) and fusca3 (fus3) mutants of Arabidopsis thaliana L.
journal, June 2000
- Vicient, C. M.
- Journal of Experimental Botany, Vol. 51, Issue 347
Regulatory Networks in Seeds Integrating Developmental, Abscisic Acid, Sugar, and Light Signaling
journal, January 2003
- Brocard-Gifford, Inès M.; Lynch, Tim J.; Finkelstein, Ruth R.
- Plant Physiology, Vol. 131, Issue 1
LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves
journal, August 2005
- Santos Mendoza, Monica; Dubreucq, Bertrand; Miquel, Martine
- FEBS Letters, Vol. 579, Issue 21
Two B3 domain transcriptional repressors prevent sugar-inducible expression of seed maturation genes in Arabidopsis seedlings
journal, January 2007
- Tsukagoshi, H.; Morikami, A.; Nakamura, K.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 7
Arabidopsis Mutants Deficient in Diacylglycerol Acyltransferase Display Increased Sensitivity to Abscisic Acid, Sugars, and Osmotic Stress during Germination and Seedling Development
journal, June 2002
- Lu, Chaofu; Hills, Matthew J.
- Plant Physiology, Vol. 129, Issue 3
The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyltransferase gene
journal, September 1999
- Zou, Jitao; Wei, Yangdou; Jako, Colette
- The Plant Journal, Vol. 19, Issue 6
WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis
journal, September 2004
- Cernac, Alex; Benning, Christoph
- The Plant Journal, Vol. 40, Issue 4, p. 575-585
Enhanced Seed Oil Production in Canola by Conditional Expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in Developing Seeds
journal, May 2011
- Tan, Helin; Yang, Xiaohui; Zhang, Fengxia
- Plant Physiology, Vol. 156, Issue 3
The turnip Mutant of Arabidopsis Reveals That LEAFY COTYLEDON1 Expression Mediates the Effects of Auxin and Sugars to Promote Embryonic Cell Identity
journal, August 2006
- Casson, Stuart A.; Lindsey, Keith
- Plant Physiology, Vol. 142, Issue 2
Identification of Direct Targets of FUSCA3, a Key Regulator of Arabidopsis Seed Development
journal, January 2013
- Wang, Fangfang; Perry, Sharyn E.
- Plant Physiology, Vol. 161, Issue 3
Expression of ZmLEC1 and ZmWRI1 Increases Seed Oil Production in Maize
journal, May 2010
- Shen, Bo; Allen, William B.; Zheng, Peizhong
- Plant Physiology, Vol. 153, Issue 3
TRANSPARENT TESTA GLABRA1 Regulates the Accumulation of Seed Storage Reserves in Arabidopsis
journal, July 2015
- Chen, Mingxun; Zhang, Bin; Li, Chengxiang
- Plant Physiology, Vol. 169, Issue 1
Seed-Specific Over-Expression of an Arabidopsis cDNA Encoding a Diacylglycerol Acyltransferase Enhances Seed Oil Content and Seed Weight
journal, June 2001
- Jako, Colette; Kumar, Arvind; Wei, Yangdou
- Plant Physiology, Vol. 126, Issue 2
Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: Implications for somatic embryogenesis
journal, February 2008
- Stone, S. L.; Braybrook, S. A.; Paula, S. L.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 8
TRANSPARENT TESTA2 regulates embryonic fatty acid biosynthesis by targeting FUSCA3 during the early developmental stage of Arabidopsis seeds
journal, February 2014
- Wang, Zhong; Chen, Mingxun; Chen, Tianlong
- The Plant Journal, Vol. 77, Issue 5
Molecular modification of triacylglycerol accumulation by over-expression of DGAT1 to produce canola with increased seed oil content under field conditionsThis paper is one of a selection of papers published in a Special Issue from the National Research Council of Canada – Plant Biotechnology Institute.
journal, June 2009
- Taylor, David C.; Zhang, Yan; Kumar, Arvind
- Botany, Vol. 87, Issue 6
Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass
journal, June 2015
- Zale, Janice; Jung, Je Hyeong; Kim, Jae Yoon
- Plant Biotechnology Journal, Vol. 14, Issue 2
Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves
journal, October 2013
- Vanhercke, Thomas; El Tahchy, Anna; Liu, Qing
- Plant Biotechnology Journal, Vol. 12, Issue 2
TRANSPARENT TESTA8 Inhibits Seed Fatty Acid Accumulation by Targeting Several Seed Development Regulators in Arabidopsis
journal, April 2014
- Chen, Mingxun; Xuan, Lijie; Wang, Zhong
- Plant Physiology, Vol. 165, Issue 2
LECs go crazy in embryo development
journal, December 2008
- Braybrook, S.; Harada, J.
- Trends in Plant Science, Vol. 13, Issue 12
WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis: Oil synthesis regulatory network in seeds
journal, April 2007
- Baud, Sébastien; Mendoza, Monica Santos; To, Alexandra
- The Plant Journal, Vol. 50, Issue 5
AtGA3ox2, a Key Gene Responsible for Bioactive Gibberellin Biosynthesis, Is Regulated during Embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis
journal, October 2004
- Curaba, Julien; Moritz, Thomas; Blervaque, Renaud
- Plant Physiology, Vol. 136, Issue 3
An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants
journal, October 2000
- Zuo, Jianru; Niu, Qi-Wen; Chua, Nam-Hai
- The Plant Journal, Vol. 24, Issue 2
WRINKLED Transcription Factors Orchestrate Tissue-Specific Regulation of Fatty Acid Biosynthesis in Arabidopsis
journal, December 2012
- To, Alexandra; Joubès, Jérôme; Barthole, Guillaume
- The Plant Cell, Vol. 24, Issue 12
Biochemical pathways in seed oil synthesis
journal, June 2013
- Bates, Philip D.; Stymne, Sten; Ohlrogge, John
- Current Opinion in Plant Biology, Vol. 16, Issue 3
ACTIVATOR of Spomin::LUC1/WRINKLED1 of Arabidopsis thaliana Transactivates Sugar-inducible Promoters
journal, April 2005
- Masaki, Takeshi; Mitsui, Naoko; Tsukagoshi, Hironaka
- Plant and Cell Physiology, Vol. 46, Issue 4
Metabolic engineering of plant oils and waxes for use as industrial feedstocks
journal, November 2012
- Vanhercke, Thomas; Wood, Craig C.; Stymne, Sten
- Plant Biotechnology Journal, Vol. 11, Issue 2
Analysis of Acyl Fluxes through Multiple Pathways of Triacylglycerol Synthesis in Developing Soybean Embryos
journal, March 2009
- Bates, Philip D.; Durrett, Timothy P.; Ohlrogge, John B.
- Plant Physiology, Vol. 150, Issue 1
Dissection of a complex seed phenotype: Novel insights of FUSCA3 regulated developmental processes
journal, May 2008
- Tiedemann, Jens; Rutten, Twan; Mönke, Gudrun
- Developmental Biology, Vol. 317, Issue 1
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
journal, June 2003
- Beisson, Frédéric; Koo, Abraham J. K.; Ruuska, Sari
- Plant Physiology, Vol. 132, Issue 2
Lipid extraction of tissues with a low-toxicity solvent
journal, October 1978
- Hara, Atsushi; Radin, Norman S.
- Analytical Biochemistry, Vol. 90, Issue 1
Triacylglycerol Metabolism, Function, and Accumulation in Plant Vegetative Tissues
journal, April 2016
- Xu, Changcheng; Shanklin, John
- Annual Review of Plant Biology, Vol. 67, Issue 1
Dual Role for Phospholipid:Diacylglycerol Acyltransferase: Enhancing Fatty Acid Synthesis and Diverting Fatty Acids from Membrane Lipids to Triacylglycerol in Arabidopsis Leaves
journal, September 2013
- Fan, J.; Yan, C.; Zhang, X.
- The Plant Cell, Vol. 25, Issue 9, p. 3506-3518
Driving on Biomass
journal, May 2009
- Ohlrogge, J.; Allen, D.; Berguson, B.
- Science, Vol. 324, Issue 5930
DGAT1 and PDAT1 Acyltransferases Have Overlapping Functions in Arabidopsis Triacylglycerol Biosynthesis and Are Essential for Normal Pollen and Seed Development
journal, December 2009
- Zhang, Meng; Fan, Jilian; Taylor, David C.
- The Plant Cell, Vol. 21, Issue 12
Tobacco BY-2 Cell Line as the “HeLa” Cell in the Cell Biology of Higher Plants
book, January 1992
- Nagata, Toshiyuki; Nemoto, Yasuyuki; Hasezawa, Seiichiro
- International Review of Cytology
Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning
journal, June 2011
- Bourgis, F.; Kilaru, A.; Cao, X.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 30
LEAFY COTYLEDON1 Controls Seed Storage Protein Genes through Its Regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3
journal, March 2005
- Kagaya, Yasuaki; Toyoshima, Ryoko; Okuda, Rie
- Plant and Cell Physiology, Vol. 46, Issue 3
Cellular Differentiation Regulated by Gibberellin in the Arabidopsis thaliana pickle Mutant
journal, July 1997
- Ogas, Joe; Cheng, Jin-Chen; Sung, Z. Renee
- Science, Vol. 277, Issue 5322
Tobacco as a production platform for biofuel overexpression of Arabidopsis DGAT and LEC2 genes increases accumulation and shifts the composition of lipids in green biomass
journal, April 2010
- Andrianov, Vyacheslav; Borisjuk, Nikolai; Pogrebnyak, Natalia
- Plant Biotechnology Journal, Vol. 8, Issue 3, p. 277-287
Diverse Roles and Mechanisms of Gene Regulation by the Arabidopsis Seed Maturation Master Regulator FUS3 Revealed by Microarray Analysis
journal, November 2010
- Yamamoto, Akiko; Kagaya, Yasuaki; Usui, Haruko
- Plant and Cell Physiology, Vol. 51, Issue 12
LEAFY COTYLEDON1 Is a Key Regulator of Fatty Acid Biosynthesis in Arabidopsis
journal, August 2008
- Mu, Jinye; Tan, Helin; Zheng, Qi
- Plant Physiology, Vol. 148, Issue 2
Efficient Lipid Staining in Plant Material with Sudan Red 7B or Fluoral Yellow 088 in Polyethylene Glycol-Glycerol
journal, January 1991
- Brundrett, Mark C.; Kendrick, Bryce; Peterson, Carol A.
- Biotechnic & Histochemistry, Vol. 66, Issue 3
wrinkled1 : A Novel, Low-Seed-Oil Mutant of Arabidopsis with a Deficiency in the Seed-Specific Regulation of Carbohydrate Metabolism
journal, September 1998
- Focks, Nicole; Benning, Christoph
- Plant Physiology, Vol. 118, Issue 1
The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development.
journal, August 1997
- Parcy, F.; Valon, C.; Kohara, A.
- The Plant Cell, Vol. 9, Issue 8
Two Arabidopsis cyclin promoters mediate distinctive transcriptional oscillation in synchronized tobacco BY-2 cells.
journal, May 1996
- Shaul, O.; Mironov, V.; Burssens, S.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 10
Misexpression of FATTY ACID ELONGATION1 in the Arabidopsis Epidermis Induces Cell Death and Suggests a Critical Role for Phospholipase A2 in This Process
journal, April 2009
- Reina-Pinto, José J.; Voisin, Derry; Kurdyukov, Sergey
- The Plant Cell, Vol. 21, Issue 4
Leafy Cotyledon Mutants of Arabidopsis.
journal, August 1994
- Meinke, D. W.; Franzmann, L. H.; Nickle, T. C.
- The Plant Cell
Developmental control of Arabidopsis seed oil biosynthesis
journal, May 2007
- Wang, Hongyun; Guo, Jinhua; Lambert, Kris N.
- Planta, Vol. 226, Issue 3
Acyl-Lipid Metabolism
journal, January 2010
- Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred
- The Arabidopsis Book, Vol. 8
Acyl-Lipid Metabolism
journal, January 2013
- Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred
- The Arabidopsis Book, Vol. 11
Leafy Cotyledon Mutants of Arabidopsis
journal, August 1994
- Meinke, David W.; Franzmann, Linda H.; Nickle, Todd C.
- The Plant Cell, Vol. 6, Issue 8
State-of-the-Art in CRISPR Technology and Engineering Drought, Salinity, and Thermo-tolerant crop plants
journal, March 2021
- Chennakesavulu, Kunchapu; Singh, Harshita; Trivedi, Prabodh Kumar
- Plant Cell Reports
fusca3: A Heterochronic Mutation Affecting Late Embryo Development in Arabidopsis
journal, May 1994
- Keith, Kallie; Kraml, Marlene; Dengler, Nancy G.
- The Plant Cell, Vol. 6, Issue 5
The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 Loci Act in Concert to Control Multiple Aspects of Arabidopsis Seed Development
journal, August 1997
- Parcy, Francois; Valon, Christiane; Kohara, Atuko
- The Plant Cell, Vol. 9, Issue 8
Works referencing / citing this record:
Genome-wide analysis reveals the evolution and structural features of WRINKLED1 in plants
journal, November 2018
- Tang, Tong; Du, Chang; Song, Huan
- Molecular Genetics and Genomics, Vol. 294, Issue 2
Enhancing micro RNA 167A expression in seed decreases the α‐linolenic acid content and increases seed size in Camelina sativa
journal, February 2019
- Na, GunNam; Mu, Xiaopeng; Grabowski, Paul
- The Plant Journal, Vol. 98, Issue 2
Unconditional and conditional QTL analyses of seed fatty acid composition in Brassica napus L.
journal, March 2018
- Chen, Feng; Zhang, Wei; Yu, Kunjiang
- BMC Plant Biology, Vol. 18, Issue 1
Deciphering the transcriptional regulatory networks that control size, color, and oil content in Brassica rapa seeds
journal, May 2020
- Niu, Yue; Wu, Limin; Li, Yanhua
- Biotechnology for Biofuels, Vol. 13, Issue 1
Transcriptome analysis of pecan seeds at different developing stages and identification of key genes involved in lipid metabolism
journal, April 2018
- Xu, Zheng; Ni, Jun; Shah, Faheem Afzal
- PLOS ONE, Vol. 13, Issue 4
WRINKLED1, a “Master Regulator” in Transcriptional Control of Plant Oil Biosynthesis
journal, July 2019
- Kong, Que; Yuan, Ling; Ma, Wei
- Plants, Vol. 8, Issue 7
Deciphering the transcriptional regulatory networks that control size, color, and oil content in Brassica rapa seeds
journal, May 2020
- Niu, Yue; Wu, Limin; Li, Yanhua
- Biotechnology for Biofuels and Bioproducts
Deciphering the transcriptional regulatory networks that control size, color, and oil content in Brassica rapa seeds
journal, May 2020
- Niu, Yue; Wu, Limin; Li, Yanhua
- Biotechnology for Biofuels and Bioproducts
Transcriptome analysis of pecan seeds at different developing stages and identification of key genes involved in lipid metabolism
journal, April 2018
- Xu, Zheng; Ni, Jun; Shah, Faheem Afzal
- PLOS ONE, Vol. 13, Issue 4