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Genetically-determined variations in photosynthesis indicate roles for specific fatty acid species in chilling responses

Journal Article · · Plant, Cell and Environment
DOI:https://doi.org/10.1111/pce.14313· OSTI ID:1980643

Using a population of recombinant inbred lines (RILs) cowpea (Vigna unguiculata. L. Walp), we tested for co-linkages between lipid contents and chilling responses of photosynthesis. Under low-temperature conditions (19°C/13°C, day/night), we observed co-linkages between quantitative trait loci intervals for photosynthetic light reactions and specific fatty acids, most strikingly, the thylakoid-specific fatty acid 16:1Δ3trans found exclusively in phosphatidylglycerol (PG 16:1t). By contrast, we did not observe co-associations with bulk polyunsaturated fatty acids or high-melting-point-PG (sum of PG 16:0, PG 18:0 and PG 16:1t) previously thought to be involved in chilling sensitivity. These results suggest that in cowpea, chilling sensitivity is modulated by specific lipid interactions rather than bulk properties. We were able to recapitulate the predicted impact of PG 16:1t levels on photosynthetic responses at low temperature using mutants and transgenic Arabidopsis lines. Because PG 16:1t synthesis requires the activity of peroxiredoxin-Q, which is activated by H2O2 and known to be involved in redox signalling, here we hypothesise that the accumulation of PG 16:1t occurs as a result of upstream effects on photosynthesis that alter redox status and production of reactive oxygen species.

Research Organization:
Michigan State University, East Lansing, MI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); Michigan State University
Grant/Contract Number:
FG02-91ER20021; SC0007101
OSTI ID:
1980643
Alternate ID(s):
OSTI ID: 1859148
Journal Information:
Plant, Cell and Environment, Journal Name: Plant, Cell and Environment Journal Issue: 6 Vol. 45; ISSN 0140-7791
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (72)

Chilling sensitivity of Arabidopsis thaliana with genetically engineered membrane lipids. journal December 1992
The action of lipases on chloroplast membranes. III. The effect of lipid hydrolysis on chlorophyll-protein complexes in thylakoid membranes journal January 1984
Chloroplast biogenesis at cold-hardening temperatures. Kinetics of trans-?3-hexadecenoic acid accumulation and the assembly of LHCII journal February 1988
Thioredoxin and germinating barley: targets and protein redox changes journal January 2003
Where do the electrons go? How numerous redox processes drive phytochemical diversity: Redox processes in phytochemistry journal January 2021
The role of phospholipids in the molecular organisation of pea chloroplast membranes. Effect of phospholipid depletion on photosynthetic activities journal October 1983
The possible role of transhexadecenoic acid and phosphatidylglycerol in light reactions of photosynthesis: The photochemistry and fluorescence properties of young pea leaf chloroplasts treated by phospholipase A 2 journal October 1979
The role of phospholipids in regulating photosynthetic electron transport activities: Treatment of chloroplasts with phospholipase A2 journal August 1989
The C16:3\C18:3 fatty acid balance in photosynthetic tissues from 468 plant species journal October 1998
Prior Accumulation of Phosphatidylglycerol high in Trans-03Hexadecenoic Acid Enhances the in vitro Stability of Oligomeric Light Harvesting Complex II journal August 1989
Energy balance and acclimation to light and cold journal June 1998
Monogalactosyldiacylglycerol deficiency in tobacco inhibits the cytochrome b6f-mediated intersystem electron transport process and affects the photostability of the photosystem II apparatus journal June 2013
Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes journal June 2016
Decreased stability of photosystem I in dgd1 mutant of Arabidopsis thaliana journal June 2005
Critical regulation of galactolipid synthesis controls membrane differentiation and remodeling in distinct plant organs and following environmental changes journal July 2011
Investigations on the Reaction Pattern of Photosystem II in Leaves from Arabidopsis thaliana Wild Type Plants and Mutants with Genetically Modified Lipid Content journal March 2005
Modification of the Water Oxidizing Complex in Leaves of the dgd1 Mutant of Arabidopsis thaliana Deficient in the Galactolipid Digalactosyldiacylglycerol journal September 1997
Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution journal May 2016
The membrane-localized protein kinase MAP4K4/TOT3 regulates thermomorphogenesis journal May 2021
Structural insight into light harvesting for photosystem II in green algae journal November 2019
Plastic and adaptive gene expression patterns associated with temperature stress in Arabidopsis thaliana journal May 2007
Cy5 maleimide labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms journal March 2004
Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function : Arabidopsis journal February 2003
Anionic lipids are required for chloroplast structure and function in Arabidopsis journal December 2003
Functional differences between galactolipids and glucolipids revealed in photosynthesis of higher plants journal April 2006
Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis journal October 2007
A consensus genetic map of cowpea [Vigna unguiculata (L) Walp.] and synteny based on EST-derived SNPs journal October 2009
Arabidopsis requires polyunsaturated lipids for low-temperature survival. journal July 1993
Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. journal July 1995
A proteoliposome-based system reveals how lipids control photosynthetic light harvesting journal February 2020
Structure and dynamics of thylakoids in land plants journal March 2014
Low Temperature Treatments Induce an Increase in the Relative Content of Both Linolenic and  3-Hexadecenoic Acids in Thylakoid Membrane Phosphatidylglycerol of Squash Cotyledons journal January 1997
Molecular Species Composition of Phosphatidylglycerols from Chilling-Sensitive and Chilling-Resistant Plants journal January 1983
Phosphatidylglycerol is Essential for the Development of Thylakoid Membranes in Arabidopsis thaliana journal December 2002
Digalactosyl-Diacylglycerol Deficiency Impairs the Capacity for Photosynthetic Intersystem Electron Transport and State Transitions in Arabidopsis thaliana Due to Photosystem I Acceptor-Side Limitations journal August 2006
The pgp1 Mutant Locus of Arabidopsis Encodes a Phosphatidylglycerolphosphate Synthase with Impaired Activity journal May 2002
Expression and Characterization of the Thylakoid Lumen Protease DegP1 from Arabidopsis journal October 2002
Isolation and Characterization of a New Peroxiredoxin from Poplar Sieve Tubes That Uses Either Glutaredoxin or Thioredoxin as a Proton Donor journal November 2001
A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta journal September 2003
A Suppressor of fab1 Challenges Hypotheses on the Role of Thylakoid Unsaturation in Photosynthetic Function journal May 2006
Monogalactosyldiacylglycerol Deficiency in Arabidopsis Affects Pigment Composition in the Prolamellar Body and Impairs Thylakoid Membrane Energization and Photoprotection in Leaves journal July 2008
The Role of Diglycosyl Lipids in Photosynthesis and Membrane Lipid Homeostasis in Arabidopsis journal April 2009
Low-Temperature Damage and Subsequent Recovery of fab1 Mutant Arabidopsis Exposed to 2[deg]C journal February 1997
Inducible Knockdown of MONOGALACTOSYLDIACYLGLYCEROL SYNTHASE1 Reveals Roles of Galactolipids in Organelle Differentiation in Arabidopsis Cotyledons     journal September 2014
Changes in the Composition of the Photosynthetic Apparatus in the Galactolipid-Deficient dgd1 Mutant of Arabidopsis thaliana journal November 1997
Trienoic Fatty Acids Are Required to Maintain Chloroplast Function at Low Temperatures journal December 2000
Temperature-Dependent Phase Behavior of Phosphatidylglycerols from Chilling-Sensitive and Chilling-Resistant Plants journal April 1984
Phosphatidylglycerol and Chilling Sensitivity in Plants journal March 1985
Analysis of Photosynthetic Antenna Function in a Mutant of Arabidopsis thaliana (L.) Lacking trans -Hexadecenoic Acid journal August 1985
Low Temperature Development Induces a Specific Decrease in trans3 -Hexadecenoic Acid Content which Influences LHCII Organization journal May 1987
Low Temperature-Induced Decrease in trans3 -Hexadecenoic Acid Content Is Correlated with Freezing Tolerance in Cereals journal January 1989
A Mutant of Arabidopsis Deficient in Desaturation of Palmitic Acid in Leaf Lipids journal July 1989
A Role for Membrane Lipid Polyunsaturation in Chloroplast Biogenesis at Low Temperature journal May 1992
The Thylakoid Lumen Protease Deg1 Is Involved in the Repair of Photosystem II from Photoinhibition in Arabidopsis journal March 2007
Elevated Levels of High-Melting-Point Phosphatidylglycerols Do Not Induce Chilling Sensitivity in an Arabidopsis Mutant. journal January 1995
FATTY ACID DESATURASE4 of Arabidopsis encodes a protein distinct from characterized fatty acid desaturases: FATTY ACID DESATURASE4 of Arabidopsis encodes a distinct protein journal December 2009
NPQ (T) : a chlorophyll fluorescence parameter for rapid estimation and imaging of non-photochemical quenching of excitons in photosystem-II-associated antenna complexes : New, rapid probe of non-photochemical quenching journal July 2017
Role of galactolipid biosynthesis in coordinated development of photosynthetic complexes and thylakoid membranes during chloroplast biogenesis in Arabidopsis journal November 2012
A multi‐parent advanced generation inter‐cross ( MAGIC ) population for genetic analysis and improvement of cowpea ( Vigna unguiculata L. Walp.) journal February 2018
The genome of cowpea ( Vigna unguiculata [L.] Walp.) journal March 2019
PEROXIREDOXIN Q stimulates the activity of the chloroplast 16:1 Δ3trans FATTY ACID DESATURASE4 journal January 2020
Mechanisms and functions of membrane lipid remodeling in plants journal May 2021
Lipid Trafficking in Plant Cells journal July 2014
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana journal August 2003
Freezing Tolerance in Plants Requires Lipid Remodeling at the Outer Chloroplast Membrane journal August 2010
Chilling Injury in Plants journal June 1973
Photoregulation of the Composition, Function, and Structure of Thylakoid Membranes journal June 1986
Phosphatidylglycerol and ß-Carotene Bound onto the D 1-Core Peptide of Photosystem II in the Filamentous Cyanobacterium: Oscillatoria chalybea journal February 1994
The Role of Phosphatidylglycerol as a Functional Effector and Membrane Anchor of the D1-Core Peptide from Photosystem II-Particles of the Cyanobacterium Oscillatoria chalybea journal June 1995
Elevated Levels of High-Melting-Point Phosphatidylglycerols Do Not Induce Chilling Sensitivity in an Arabidopsis Mutant journal January 1995
Kinetic analysis of the interactions between plant thioredoxin and target proteins journal January 2013
The Role of Chloroplast Membrane Lipid Metabolism in Plant Environmental Responses journal March 2021