Expression of a Bacterial Trehalose-6-phosphate Synthase otsA Increases Oil Accumulation in Plant Seeds and Vegetative Tissues
Abstract
We previously demonstrated that exogenous trehalose 6-phosphate (T6P) treatment stabilized WRINKLED1 (WRI1), a master transcriptional regulator of fatty acid (FA) synthesis and increased total FA content in Brassica napus ( B. napus ) embryo suspension cell culture. Here, we explore Arabidopsis lines heterologously expressing the Escherichia coli T6P synthase (otsA) or T6P phosphatase (otsB) to refine our understanding regarding the role of T6P in regulating fatty acid synthesis both in seeds and vegetative tissues. Arabidopsis 35S: otsA transgenic seeds showed an increase of 13% in fatty acid content compared to those of wild type (WT), while seeds of 35: otsB transgenic seeds showed a reduction of 12% in fatty acid content compared to WT. Expression of otsB significantly reduced the level of WRI1 and expression of its target genes in developing seeds. Like Arabidopsis seeds constitutively expressing otsA, transient expression of otsA in Nicotiana benthamiana leaves resulted in strongly elevated levels of T6P. This was accompanied by an increase of 29% in de novo fatty acid synthesis rate, a 2.3-fold increase in triacylglycerol (TAG) and a 20% increase in total fatty acid content relative to empty vector (EV) controls. Taken together, these data support the heterologous expression of otsA asmore »
- Authors:
- Publication Date:
- Research Org.:
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1770223
- Alternate Identifier(s):
- OSTI ID: 1777435
- Report Number(s):
- BNL-221260-2021-JAAM
Journal ID: ISSN 1664-462X; 656962
- Grant/Contract Number:
- SC0012704
- Resource Type:
- Published Article
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Name: Frontiers in Plant Science Journal Volume: 12; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Media SA
- Country of Publication:
- Switzerland
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; rehalose; 6 phosphate; triacylglycerol; fatty; acid; synthesis; oil accumulation; sugar signaling
Citation Formats
Zhai, Zhiyang, Keereetaweep, Jantana, Liu, Hui, Feil, Regina, Lunn, John E., and Shanklin, John. Expression of a Bacterial Trehalose-6-phosphate Synthase otsA Increases Oil Accumulation in Plant Seeds and Vegetative Tissues. Switzerland: N. p., 2021.
Web. doi:10.3389/fpls.2021.656962.
Zhai, Zhiyang, Keereetaweep, Jantana, Liu, Hui, Feil, Regina, Lunn, John E., & Shanklin, John. Expression of a Bacterial Trehalose-6-phosphate Synthase otsA Increases Oil Accumulation in Plant Seeds and Vegetative Tissues. Switzerland. https://doi.org/10.3389/fpls.2021.656962
Zhai, Zhiyang, Keereetaweep, Jantana, Liu, Hui, Feil, Regina, Lunn, John E., and Shanklin, John. Wed .
"Expression of a Bacterial Trehalose-6-phosphate Synthase otsA Increases Oil Accumulation in Plant Seeds and Vegetative Tissues". Switzerland. https://doi.org/10.3389/fpls.2021.656962.
@article{osti_1770223,
title = {Expression of a Bacterial Trehalose-6-phosphate Synthase otsA Increases Oil Accumulation in Plant Seeds and Vegetative Tissues},
author = {Zhai, Zhiyang and Keereetaweep, Jantana and Liu, Hui and Feil, Regina and Lunn, John E. and Shanklin, John},
abstractNote = {We previously demonstrated that exogenous trehalose 6-phosphate (T6P) treatment stabilized WRINKLED1 (WRI1), a master transcriptional regulator of fatty acid (FA) synthesis and increased total FA content in Brassica napus ( B. napus ) embryo suspension cell culture. Here, we explore Arabidopsis lines heterologously expressing the Escherichia coli T6P synthase (otsA) or T6P phosphatase (otsB) to refine our understanding regarding the role of T6P in regulating fatty acid synthesis both in seeds and vegetative tissues. Arabidopsis 35S: otsA transgenic seeds showed an increase of 13% in fatty acid content compared to those of wild type (WT), while seeds of 35: otsB transgenic seeds showed a reduction of 12% in fatty acid content compared to WT. Expression of otsB significantly reduced the level of WRI1 and expression of its target genes in developing seeds. Like Arabidopsis seeds constitutively expressing otsA, transient expression of otsA in Nicotiana benthamiana leaves resulted in strongly elevated levels of T6P. This was accompanied by an increase of 29% in de novo fatty acid synthesis rate, a 2.3-fold increase in triacylglycerol (TAG) and a 20% increase in total fatty acid content relative to empty vector (EV) controls. Taken together, these data support the heterologous expression of otsA as an approach to increasing TAG accumulation in plant seeds and vegetative tissues.},
doi = {10.3389/fpls.2021.656962},
journal = {Frontiers in Plant Science},
number = ,
volume = 12,
place = {Switzerland},
year = {Wed Mar 10 00:00:00 EST 2021},
month = {Wed Mar 10 00:00:00 EST 2021}
}
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Works referenced in this record:
The sucrose–trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P
journal, January 2014
- Yadav, Umesh Prasad; Ivakov, Alexander; Feil, Regina
- Journal of Experimental Botany, Vol. 65, Issue 4
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
Improved Gateway Binary Vectors: High-Performance Vectors for Creation of Fusion Constructs in Transgenic Analysis of Plants
journal, August 2007
- Nakagawa, Tsuyoshi; Suzuki, Takamasa; Murata, Satoko
- Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 8
Wheat Grain Development Is Characterized by Remarkable Trehalose 6-Phosphate Accumulation Pregrain Filling: Tissue Distribution and Relationship to SNF1-Related Protein Kinase1 Activity
journal, March 2011
- Martínez-Barajas, Eleazar; Delatte, Thierry; Schluepmann, Henriette
- Plant Physiology, Vol. 156, Issue 1
The SUGAR-DEPENDENT1 Lipase Limits Triacylglycerol Accumulation in Vegetative Tissues of Arabidopsis
journal, May 2013
- Kelly, A. A.; van Erp, H.; Quettier, A.-L.
- PLANT PHYSIOLOGY, Vol. 162, Issue 3, p. 1282-1289
An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis
journal, November 2009
- Maeo, Kenichiro; Tokuda, Tsuyoshi; Ayame, Atsuko
- The Plant Journal, Vol. 60, Issue 3
Expression of the genes coding for plastidic acetyl-CoA carboxylase subunits is regulated by a location-sensitive transcription factor binding site
journal, June 2013
- Fukuda, Natsumi; Ikawa, Yuki; Aoyagi, Toshihiro
- Plant Molecular Biology, Vol. 82, Issue 4-5
Regulation of shoot branching in arabidopsis by trehalose 6‐phosphate
journal, November 2020
- Fichtner, Franziska; Barbier, Francois F.; Annunziata, Maria G.
- New Phytologist, Vol. 229, Issue 4
Arabidopsis plants harbouring a mutation in AtSUC2, encoding the predominant sucrose/proton symporter necessary for efficient phloem transport, are able to complete their life cycle and produce viable seed
journal, September 2009
- Srivastava, Avinash C.; Dasgupta, Kasturi; Ajieren, Eric
- Annals of Botany, Vol. 104, Issue 6
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
Contrapuntal Networks of Gene Expression during Arabidopsis Seed Filling
journal, June 2002
- Ruuska, Sari A.; Girke, Thomas; Benning, Christoph
- The Plant Cell, Vol. 14, Issue 6
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
The impact of Arabidopsis thaliana SNF 1‐related‐kinase 1 (Sn RK 1)‐activating kinase 1 (Sn AK 1) and Sn AK 2 on Sn RK 1 phosphorylation status: characterization of a Sn AK double mutant
journal, February 2017
- Glab, Nathalie; Oury, Céline; Guérinier, Thomas
- The Plant Journal, Vol. 89, Issue 5
Wrinkled1 Accelerates Flowering and Regulates Lipid Homeostasis between Oil Accumulation and Membrane Lipid Anabolism in Brassica napus
journal, November 2015
- Li, Qing; Shao, Jianhua; Tang, Shaohua
- Frontiers in Plant Science, Vol. 6
Towards oilcane: Engineering hyperaccumulation of triacylglycerol into sugarcane stems
journal, May 2020
- Parajuli, Saroj; Kannan, Baskaran; Karan, Ratna
- GCB Bioenergy, Vol. 12, Issue 7
Trehalose 6-Phosphate Is Required for the Onset of Leaf Senescence Associated with High Carbon Availability
journal, January 2012
- Wingler, Astrid; Delatte, Thierry L.; O’Hara, Liam E.
- Plant Physiology, Vol. 158, Issue 3
14-3-3 protein mediates plant seed oil biosynthesis through interaction with AtWRI1
journal, August 2016
- Ma, Wei; Kong, Que; Mantyla, Jenny J.
- The Plant Journal, Vol. 88, Issue 2
Metabolic engineering for enhanced oil in biomass
journal, April 2019
- Vanhercke, Thomas; Dyer, John M.; Mullen, Robert T.
- Progress in Lipid Research, Vol. 74
The Role of Trehalose 6-Phosphate (Tre6P) in Plant Metabolism and Development
journal, January 2021
- Fichtner, Franziska; Lunn, John Edward
- Annual Review of Plant Biology, Vol. 72, Issue 1
Arabidopsis Protein Kinases GRIK1 and GRIK2 Specifically Activate SnRK1 by Phosphorylating Its Activation Loop
journal, April 2009
- Shen, Wei; Reyes, Maria Ines; Hanley-Bowdoin, Linda
- Plant Physiology, Vol. 150, Issue 2
WRINKLED1 Regulates BIOTIN ATTACHMENT DOMAIN-CONTAINING Proteins that Inhibit Fatty Acid Synthesis
journal, June 2019
- Liu, Hui; Zhai, Zhiyang; Kuczynski, Kate
- Plant Physiology, Vol. 181, Issue 1
Inhibition of SNF1-Related Protein Kinase1 Activity and Regulation of Metabolic Pathways by Trehalose-6-Phosphate
journal, February 2009
- Zhang, Yuhua; Primavesi, Lucia F.; Jhurreea, Deveraj
- Plant Physiology, Vol. 149, Issue 4
Carbon flux and fatty acid synthesis in plants
journal, March 2002
- Rawsthorne, Stephen
- Progress in Lipid Research, Vol. 41, Issue 2
A central integrator of transcription networks in plant stress and energy signalling
journal, August 2007
- Baena-González, Elena; Rolland, Filip; Thevelein, Johan M.
- Nature, Vol. 448, Issue 7156
Sugar Potentiation of Fatty Acid and Triacylglycerol Accumulation
journal, August 2017
- Zhai, Zhiyang; Liu, Hui; Xu, Changcheng
- Plant Physiology, Vol. 175, Issue 2
The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function
journal, November 2016
- Broeckx, Tom; Hulsmans, Sander; Rolland, Filip
- Journal of Experimental Botany, Vol. 67, Issue 22
A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose
journal, August 2016
- Figueroa, Carlos M.; Lunn, John E.
- Plant Physiology, Vol. 172, Issue 1
Chemical intervention in plant sugar signalling increases yield and resilience
journal, December 2016
- Griffiths, Cara A.; Sagar, Ram; Geng, Yiqun
- Nature, Vol. 540, Issue 7634
Lipid Biosynthesis
journal, July 1995
- Ohlrogge, J.; Browse, J.
- THE PLANT CELL ONLINE, Vol. 7, Issue 7, p. 957-970
The Biosynthesis of Trehalose Phosphate
journal, March 1958
- Cabib, E.; Leloir, Luis F.
- Journal of Biological Chemistry, Vol. 231, Issue 1
Step changes in leaf oil accumulation via iterative metabolic engineering
journal, January 2017
- Vanhercke, Thomas; Divi, Uday K.; El Tahchy, Anna
- Metabolic Engineering, Vol. 39
SnRK1 and trehalose 6-phosphate – two ancient pathways converge to regulate plant metabolism and growth
journal, June 2020
- Baena-González, Elena; Lunn, John Edward
- Current Opinion in Plant Biology, Vol. 55
Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana
journal, June 2006
- Lunn, John E.; Feil, Regina; Hendriks, Janneke H. M.
- Biochemical Journal, Vol. 397, 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
Chloroplast acetyl-CoA carboxylase activity is 2-oxoglutarate-regulated by interaction of PII with the biotin carboxyl carrier subunit
journal, December 2009
- Feria Bourrellier, A. B.; Valot, B.; Guillot, A.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 1
Transcriptional transitions in Nicotiana benthamiana leaves upon induction of oil synthesis by WRINKLED1 homologs from diverse species and tissues
journal, August 2015
- Grimberg, Åsa; Carlsson, Anders S.; Marttila, Salla
- BMC Plant Biology, Vol. 15, Issue 1
Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana
journal, May 2003
- Schluepmann, H.; Pellny, T.; van Dijken, A.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 11
Trehalose 6-phosphate coordinates organic and amino acid metabolism with carbon availability
journal, January 2016
- Figueroa, Carlos M.; Feil, Regina; Ishihara, Hirofumi
- The Plant Journal, Vol. 85, Issue 3
On the Export of Fatty Acids from the Chloroplast
journal, February 2004
- Koo, Abraham J. K.; Ohlrogge, John B.; Pollard, Mike
- Journal of Biological Chemistry, Vol. 279, Issue 16
Phosphorylation of WRINKLED1 by KIN10 Results in Its Proteasomal Degradation, Providing a Link between Energy Homeostasis and Lipid Biosynthesis
journal, March 2017
- Zhai, Zhiyang; Liu, Hui; Shanklin, John
- The Plant Cell, Vol. 29, Issue 4
A leaf-based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways
journal, December 2009
- Wood, Craig C.; Petrie, James R.; Shrestha, Pushkar
- Plant Biotechnology Journal, Vol. 7, Issue 9
Acyl-Lipid Metabolism
journal, January 2013
- Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred
- The Arabidopsis Book, Vol. 11
Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR
journal, May 2002
- Pfaffl, M. W.
- Nucleic Acids Research, Vol. 30, Issue 9
Trehalose 6-Phosphate Positively Regulates Fatty Acid Synthesis by Stabilizing WRINKLED1
journal, September 2018
- Zhai, Zhiyang; Keereetaweep, Jantana; Liu, Hui
- The Plant Cell, Vol. 30, Issue 10