Diversion of Carbon Flux from Sugars to Lipids Improves the Growth of an Arabidopsis Starchless Mutant

Fan, Jilian; Zhou, Chao; Yu, Linhui; Li, Ping; Shanklin, John; Xu, Changcheng

doi:10.3390/plants8070229

Title: 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:

Fan, Jilian;

;

; Li, Ping; Shanklin, John;

Publication Date:: 2019-07-17

Research Org.:: Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Brookhaven National Lab. (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.  https://doi.org/10.3390/plants8070229.

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                    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

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                    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.

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@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}

}

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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
DOI: 10.1016/j.pbi.2012.03.016

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
DOI: 10.1104/pp.113.219840

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
DOI: 10.1111/j.1365-313X.2008.03442.x

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
DOI: 10.1126/science.1086391

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
DOI: 10.1104/pp.86.4.1131

Sink regulation of photosynthesis
journal, July 2001

Paul, Matthew J.; Foyer, Christine H.
Journal of Experimental Botany, Vol. 52, Issue 360
DOI: 10.1093/jexbot/52.360.1383

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
DOI: 10.1105/TPC.010091

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
DOI: 10.1111/tpj.12555

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
DOI: 10.1111/j.1399-3054.1962.tb08052.x

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
DOI: 10.1105/tpc.108.064360

Starch Deficiency Enhances Lipid Biosynthesis and Turnover in Leaves
journal, August 2018

Yu, Linhui; Fan, Jilian; Yan, Chengshi
Plant Physiology, Vol. 178, Issue 1
DOI: 10.1104/pp.18.00539

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
DOI: 10.1073/pnas.120067297

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
DOI: 10.1016/j.tplants.2010.12.003

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
DOI: 10.1111/j.1365-313X.2005.02553.x

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
DOI: 10.1111/j.1365-313X.2004.02173.x

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
DOI: 10.1046/j.1365-313x.1998.00343.x

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
DOI: 10.1105/tpc.105.040543

Regulation of Starch Biosynthesis in Response to a Fluctuating Environment
journal, March 2011

Geigenberger, Peter
Plant Physiology, Vol. 155, Issue 4
DOI: 10.1104/pp.110.170399

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
DOI: 10.1104/pp.119.1.267

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
DOI: 10.1046/j.1365-313x.2000.00712.x

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
DOI: 10.1146/annurev-arplant-043015-111641

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
DOI: 10.1105/tpc.113.117358

Metabolic regulation of photosynthesis
journal, March 2018

Heyneke, Elmien; Fernie, Alisdair R.
Biochemical Society Transactions, Vol. 46, Issue 2
DOI: 10.1042/BST20170296

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
DOI: 10.1146/annurev.arplant.48.1.109

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
DOI: 10.1105/tpc.109.071795

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
DOI: 10.1146/annurev.pp.42.060191.002343

Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo
journal, June 2008

Baker, Neil R.
Annual Review of Plant Biology, Vol. 59, Issue 1
DOI: 10.1146/annurev.arplant.59.032607.092759

Coordination of carbon supply and plant growth
journal, September 2007

Smith, Alison M.; Stitt, Mark
Plant, Cell & Environment, Vol. 30, Issue 9
DOI: 10.1111/j.1365-3040.2007.01708.x

Seed Storage Oil Mobilization
journal, June 2008

Graham, Ian A.
Annual Review of Plant Biology, Vol. 59, Issue 1, p. 115-142
DOI: 10.1146/annurev.arplant.59.032607.092938

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
DOI: 10.1104/pp.79.1.11

Acyl-Lipid Metabolism
journal, January 2013

Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred
The Arabidopsis Book, Vol. 11
DOI: 10.1199/tab.0161

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
DOI: 10.1016/S0304-4165(89)80016-9

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
DOI: 10.1104/pp.109.140491

Regulation of Fatty Acid Synthesis
journal, February 1969

Zakim, David; Herman, Robert H.
The American Journal of Clinical Nutrition, Vol. 22, Issue 2
DOI: 10.1093/ajcn/22.2.200

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
DOI: 10.2307/3871327

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Title: Diversion of Carbon Flux from Sugars to Lipids Improves the Growth of an Arabidopsis Starchless Mutant

Abstract

Citation Formats

Starch turnover: pathways, regulation and role in growth journal, June 2012

The SUGAR-DEPENDENT1 Lipase Limits Triacylglycerol Accumulation in Vegetative Tissues of Arabidopsis journal, May 2013

Plant triacylglycerols as feedstocks for the production of biofuels journal, May 2008

Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana journal, August 2003

Isolation and Characterization of a Starchless Mutant of Arabidopsis thaliana (L.) Heynh Lacking ADPglucose Pyrophosphorylase Activity journal, April 1988

Sink regulation of photosynthesis journal, July 2001

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

Exaggerated root respiration accounts for growth retardation in a starchless mutant of Arabidopsis thaliana journal, June 2014

A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures journal, July 1962

STARCH-EXCESS4 Is a Laforin-Like Phosphoglucan Phosphatase Required for Starch Degradation in Arabidopsis thaliana journal, January 2009

Starch Deficiency Enhances Lipid Biosynthesis and Turnover in Leaves journal, August 2018

Phospholipid:diacylglycerol acyltransferase: An enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants journal, May 2000

Starch and the clock: the dark side of plant productivity journal, March 2011

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

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

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana journal, December 1998

SUGAR-DEPENDENT1 Encodes a Patatin Domain Triacylglycerol Lipase That Initiates Storage Oil Breakdown in Germinating Arabidopsis Seeds journal, March 2006

Regulation of Starch Biosynthesis in Response to a Fluctuating Environment journal, March 2011

Modification of Carbon Partitioning, Photosynthetic Capacity, and O 2 Sensitivity in Arabidopsis Plants with Low ADP-Glucose Pyrophosphorylase Activity journal, January 1999

Understanding in vivo carbon precursor supply for fatty acid synthesis in leaf tissue journal, April 2000

Triacylglycerol Metabolism, Function, and Accumulation in Plant Vegetative Tissues journal, April 2016

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

Metabolic regulation of photosynthesis journal, March 2018

Regulation of Fatty Acid Synthesis journal, June 1997

DGAT1 and PDAT1 Acyltransferases Have Overlapping Functions in Arabidopsis Triacylglycerol Biosynthesis and Are Essential for Normal Pollen and Seed Development journal, December 2009

Glycerolipid Synthesis: Biochemistry and Regulation journal, June 1991

Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo journal, June 2008

Coordination of carbon supply and plant growth journal, September 2007

Seed Storage Oil Mobilization journal, June 2008

Alterations in Growth, Photosynthesis, and Respiration in a Starchless Mutant of Arabidopsis thaliana (L.) Deficient in Chloroplast Phosphoglucomutase Activity journal, September 1985

Acyl-Lipid Metabolism journal, January 2013

The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence journal, January 1989

Turnover of Fatty Acids during Natural Senescence of Arabidopsis, Brachypodium , and Switchgrass and in Arabidopsis β- Oxidation Mutants journal, June 2009

Regulation of Fatty Acid Synthesis journal, February 1969

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

Starch turnover: pathways, regulation and role in growth
journal, June 2012

The SUGAR-DEPENDENT1 Lipase Limits Triacylglycerol Accumulation in Vegetative Tissues of Arabidopsis
journal, May 2013

Plant triacylglycerols as feedstocks for the production of biofuels
journal, May 2008

Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana
journal, August 2003

Isolation and Characterization of a Starchless Mutant of Arabidopsis thaliana (L.) Heynh Lacking ADPglucose Pyrophosphorylase Activity
journal, April 1988

Sink regulation of photosynthesis
journal, July 2001

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

Exaggerated root respiration accounts for growth retardation in a starchless mutant of Arabidopsis thaliana
journal, June 2014

A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures
journal, July 1962

STARCH-EXCESS4 Is a Laforin-Like Phosphoglucan Phosphatase Required for Starch Degradation in Arabidopsis thaliana
journal, January 2009

Starch Deficiency Enhances Lipid Biosynthesis and Turnover in Leaves
journal, August 2018

Phospholipid:diacylglycerol acyltransferase: An enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants
journal, May 2000

Starch and the clock: the dark side of plant productivity
journal, March 2011

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

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

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998

SUGAR-DEPENDENT1 Encodes a Patatin Domain Triacylglycerol Lipase That Initiates Storage Oil Breakdown in Germinating Arabidopsis Seeds
journal, March 2006

Regulation of Starch Biosynthesis in Response to a Fluctuating Environment
journal, March 2011

Modification of Carbon Partitioning, Photosynthetic Capacity, and O ₂ Sensitivity in Arabidopsis Plants with Low ADP-Glucose Pyrophosphorylase Activity
journal, January 1999

Understanding in vivo carbon precursor supply for fatty acid synthesis in leaf tissue
journal, April 2000

Triacylglycerol Metabolism, Function, and Accumulation in Plant Vegetative Tissues
journal, April 2016

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

Metabolic regulation of photosynthesis
journal, March 2018

Regulation of Fatty Acid Synthesis
journal, June 1997

DGAT1 and PDAT1 Acyltransferases Have Overlapping Functions in Arabidopsis Triacylglycerol Biosynthesis and Are Essential for Normal Pollen and Seed Development
journal, December 2009

Glycerolipid Synthesis: Biochemistry and Regulation
journal, June 1991

Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo
journal, June 2008

Coordination of carbon supply and plant growth
journal, September 2007

Seed Storage Oil Mobilization
journal, June 2008

Alterations in Growth, Photosynthesis, and Respiration in a Starchless Mutant of Arabidopsis thaliana (L.) Deficient in Chloroplast Phosphoglucomutase Activity
journal, September 1985

Acyl-Lipid Metabolism
journal, January 2013

The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence
journal, January 1989

Turnover of Fatty Acids during Natural Senescence of Arabidopsis, Brachypodium , and Switchgrass and in Arabidopsis β- Oxidation Mutants
journal, June 2009

Regulation of Fatty Acid Synthesis
journal, February 1969

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