Diversion of Carbon Flux from Sugars to Lipids Improves the Growth of an Arabidopsis Starchless Mutant
Abstract
Inactivation of ADP-glucose pyrophosphorylase1 (ADG1) causes a starchless phenotype in Arabidopsis. Mutants defective in ADG1 show severe growth retardation in day/night conditions but exhibit similar growth to the wild type under continuous light, implying an important role of starch in supporting respiration, metabolism and growth at night. In addition to carbohydrates, lipids and proteins can serve as alternative respiratory substrates for energy production in mature plants. To test the role of lipids in diurnal growth, we generated transgenic plants overexpressing phospholipid:diacylglycerol acyltransferase1 (PDAT1) in adg1. We found that PDAT1 overexpression caused an increase in both fatty acid synthesis and turnover and increased accumulation of triacylglycerol (TAG) at the expense of sugars, and improved the diurnal growth of adg1. We demonstrated that unlike sugars, which were metabolized within a few hours of darkness, TAG breakdown was slow, occurring throughout the entire dark period. The slow pace of TAG hydrolysis enabled a sustained supply of fatty acids for energy production, thereby alleviating energy deficiency at night and hence improving growth of the starchless mutants. We conclude that lipids can contribute to diurnal plant growth by providing a constant supply of fatty acids as an alternative energy source in mature starchless mutant plants.
- Authors:
- Publication Date:
- Research Org.:
- Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
- OSTI Identifier:
- 1543017
- Alternate Identifier(s):
- OSTI ID: 1546074; OSTI ID: 1556883
- Report Number(s):
- BNL-211945-2019-JAAM
Journal ID: ISSN 2223-7747; PLANCD; PII: plants8070229
- Grant/Contract Number:
- SC0018420 and DE-SC0012704; SC0018420; SC0012704
- Resource Type:
- Published Article
- Journal Name:
- Plants
- Additional Journal Information:
- Journal Name: Plants Journal Volume: 8 Journal Issue: 7; Journal ID: ISSN 2223-7747
- Publisher:
- MDPI AG
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; starch; sugars; lipids; triacylglycerol; phospholipid:diacylglycerol acyltransferase1; phospholipid; diacylglycerol acyltransferase1
Citation Formats
Fan, Jilian, Zhou, Chao, Yu, Linhui, Li, Ping, Shanklin, John, and Xu, Changcheng. Diversion of Carbon Flux from Sugars to Lipids Improves the Growth of an Arabidopsis Starchless Mutant. Netherlands: N. p., 2019.
Web. doi:10.3390/plants8070229.
Fan, Jilian, Zhou, Chao, Yu, Linhui, Li, Ping, Shanklin, John, & Xu, Changcheng. Diversion of Carbon Flux from Sugars to Lipids Improves the Growth of an Arabidopsis Starchless Mutant. Netherlands. https://doi.org/10.3390/plants8070229
Fan, Jilian, Zhou, Chao, Yu, Linhui, Li, Ping, Shanklin, John, and Xu, Changcheng. Wed .
"Diversion of Carbon Flux from Sugars to Lipids Improves the Growth of an Arabidopsis Starchless Mutant". Netherlands. https://doi.org/10.3390/plants8070229.
@article{osti_1543017,
title = {Diversion of Carbon Flux from Sugars to Lipids Improves the Growth of an Arabidopsis Starchless Mutant},
author = {Fan, Jilian and Zhou, Chao and Yu, Linhui and Li, Ping and Shanklin, John and Xu, Changcheng},
abstractNote = {Inactivation of ADP-glucose pyrophosphorylase1 (ADG1) causes a starchless phenotype in Arabidopsis. Mutants defective in ADG1 show severe growth retardation in day/night conditions but exhibit similar growth to the wild type under continuous light, implying an important role of starch in supporting respiration, metabolism and growth at night. In addition to carbohydrates, lipids and proteins can serve as alternative respiratory substrates for energy production in mature plants. To test the role of lipids in diurnal growth, we generated transgenic plants overexpressing phospholipid:diacylglycerol acyltransferase1 (PDAT1) in adg1. We found that PDAT1 overexpression caused an increase in both fatty acid synthesis and turnover and increased accumulation of triacylglycerol (TAG) at the expense of sugars, and improved the diurnal growth of adg1. We demonstrated that unlike sugars, which were metabolized within a few hours of darkness, TAG breakdown was slow, occurring throughout the entire dark period. The slow pace of TAG hydrolysis enabled a sustained supply of fatty acids for energy production, thereby alleviating energy deficiency at night and hence improving growth of the starchless mutants. We conclude that lipids can contribute to diurnal plant growth by providing a constant supply of fatty acids as an alternative energy source in mature starchless mutant plants.},
doi = {10.3390/plants8070229},
journal = {Plants},
number = 7,
volume = 8,
place = {Netherlands},
year = {2019},
month = {7}
}
https://doi.org/10.3390/plants8070229
Web of Science
Works referenced in this record:
Starch turnover: pathways, regulation and role in growth
journal, June 2012
- Stitt, Mark; Zeeman, Samuel C.
- Current Opinion in Plant Biology, Vol. 15, Issue 3
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
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
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana
journal, August 2003
- Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J.
- Science, Vol. 301, Issue 5633, p. 653-657
Isolation and Characterization of a Starchless Mutant of Arabidopsis thaliana (L.) Heynh Lacking ADPglucose Pyrophosphorylase Activity
journal, April 1988
- Lin, Tsan-Piao; Caspar, Timothy; Somerville, Chris
- Plant Physiology, Vol. 86, Issue 4
Sink regulation of photosynthesis
journal, July 2001
- Paul, Matthew J.; Foyer, Christine H.
- Journal of Experimental Botany, Vol. 52, Issue 360
The Arabidopsis sex1 Mutant Is Defective in the R1 Protein, a General Regulator of Starch Degradation in Plants, and Not in the Chloroplast Hexose Transporter
journal, August 2001
- Yu, Tien-Shin; Kofler, Heike; Häusler, Rainer E.
- The Plant Cell, Vol. 13, Issue 8
Exaggerated root respiration accounts for growth retardation in a starchless mutant of Arabidopsis thaliana
journal, June 2014
- Brauner, Katrin; Hörmiller, Imke; Nägele, Thomas
- The Plant Journal, Vol. 79, Issue 1
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures
journal, July 1962
- Murashige, Toshio; Skoog, Folke
- Physiologia Plantarum, Vol. 15, Issue 3, p. 473-497
STARCH-EXCESS4 Is a Laforin-Like Phosphoglucan Phosphatase Required for Starch Degradation in Arabidopsis thaliana
journal, January 2009
- Kötting, Oliver; Santelia, Diana; Edner, Christoph
- The Plant Cell, Vol. 21, Issue 1
Starch Deficiency Enhances Lipid Biosynthesis and Turnover in Leaves
journal, August 2018
- Yu, Linhui; Fan, Jilian; Yan, Chengshi
- Plant Physiology, Vol. 178, Issue 1
Starch and the clock: the dark side of plant productivity
journal, March 2011
- Graf, Alexander; Smith, Alison M.
- Trends in Plant Science, Vol. 16, Issue 3
Identification of a plastid acyl-acyl carrier protein synthetase in Arabidopsis and its role in the activation and elongation of exogenous fatty acids
journal, October 2005
- Koo, Abraham J. K.; Fulda, Martin; Browse, John
- The Plant Journal, Vol. 44, Issue 4, p. 620-632
Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period
journal, September 2004
- Gibon, Yves; Bläsing, Oliver E.; Palacios-Rojas, Natalia
- The Plant Journal, Vol. 39, Issue 6
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998
- Clough, Steven J.; Bent, Andrew F.
- The Plant Journal, Vol. 16, Issue 6, p. 735-743
SUGAR-DEPENDENT1 Encodes a Patatin Domain Triacylglycerol Lipase That Initiates Storage Oil Breakdown in Germinating Arabidopsis Seeds
journal, March 2006
- Eastmond, P. J.
- The Plant Cell Online, Vol. 18, Issue 3, p. 665-675
Regulation of Starch Biosynthesis in Response to a Fluctuating Environment
journal, March 2011
- Geigenberger, Peter
- Plant Physiology, Vol. 155, Issue 4
Modification of Carbon Partitioning, Photosynthetic Capacity, and O 2 Sensitivity in Arabidopsis Plants with Low ADP-Glucose Pyrophosphorylase Activity
journal, January 1999
- Sun, Jindong; Okita, Thomas W.; Edwards, Gerald E.
- Plant Physiology, Vol. 119, Issue 1
Understanding in vivo carbon precursor supply for fatty acid synthesis in leaf tissue
journal, April 2000
- Bao, Xiaoming; Focke, Manfred; Pollard, Mike
- The Plant Journal, Vol. 22, Issue 1, p. 39-50
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
Metabolic regulation of photosynthesis
journal, March 2018
- Heyneke, Elmien; Fernie, Alisdair R.
- Biochemical Society Transactions, Vol. 46, Issue 2
Regulation of Fatty Acid Synthesis
journal, June 1997
- Ohlrogge, John B.; Jaworski, Jan G.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 48, Issue 1, p. 109-136
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
Glycerolipid Synthesis: Biochemistry and Regulation
journal, June 1991
- Browse, J.; Somerville, C.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 42, Issue 1
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo
journal, June 2008
- Baker, Neil R.
- Annual Review of Plant Biology, Vol. 59, Issue 1
Coordination of carbon supply and plant growth
journal, September 2007
- Smith, Alison M.; Stitt, Mark
- Plant, Cell & Environment, Vol. 30, Issue 9
Seed Storage Oil Mobilization
journal, June 2008
- Graham, Ian A.
- Annual Review of Plant Biology, Vol. 59, Issue 1, p. 115-142
Alterations in Growth, Photosynthesis, and Respiration in a Starchless Mutant of Arabidopsis thaliana (L.) Deficient in Chloroplast Phosphoglucomutase Activity
journal, September 1985
- Caspar, Timothy; Huber, Steven C.; Somerville, Chris
- Plant Physiology, Vol. 79, Issue 1
Acyl-Lipid Metabolism
journal, January 2013
- Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred
- The Arabidopsis Book, Vol. 11
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence
journal, January 1989
- Genty, Bernard; Briantais, Jean-Marie; Baker, Neil R.
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 990, Issue 1
Turnover of Fatty Acids during Natural Senescence of Arabidopsis, Brachypodium , and Switchgrass and in Arabidopsis β- Oxidation Mutants
journal, June 2009
- Yang, Zhenle; Ohlrogge, John B.
- Plant Physiology, Vol. 150, Issue 4
Regulation of Fatty Acid Synthesis
journal, February 1969
- Zakim, David; Herman, Robert H.
- The American Journal of Clinical Nutrition, Vol. 22, Issue 2
The Arabidopsis sex1 Mutant Is Defective in the R1 Protein, a General Regulator of Starch Degradation in Plants, and Not in the Chloroplast Hexose Transporter
journal, August 2001
- Yu, Tien-Shin; Kofler, Heike; Hausler, Rainer E.
- The Plant Cell, Vol. 13, Issue 8