PEROXIREDOXIN Q stimulates the activity of the chloroplast 16:1 Δ3trans FATTY ACID DESATURASE4
Abstract
Summary Thylakoid membrane lipids, comprised of glycolipids and the phospholipid phosphatidylglycerol (PG), are essential for normal plant growth and development. Unlike other lipid classes, chloroplast PG in nearly all plants contains a substantial fraction of the unusual trans fatty acid 16:1 Δ3trans or 16:1t. We determined that, in Arabidopsis thaliana , 16:1t biosynthesis requires both FATTY ACID DESATURASE4 (FAD4) and a thylakoid‐associated redox protein, PEROXIREDOXIN Q (PRXQ), to produce wild‐type levels of 16:1t. The FAD4–PRXQ biochemical relationship appears to be very specific in planta , as other fatty acids (FA) desaturases do not require peroxiredoxins for their activity, nor does FAD4 require other chloroplast peroxiredoxins under standard growth conditions. Although most of chloroplast PG assembly occurs at the inner envelope membrane, FAD4 was primarily associated with the thylakoid membranes facing the stroma. Furthermore, co‐production of PRXQ with FAD4 was required to produce Δ3‐desaturated FAs in yeast. Alteration of the redox state of FAD4 or PRXQ through site‐directed mutagenesis of conserved cysteine residues impaired Δ3 FA production. However, these mutations did not appear to directly alter disulfide status of FAD4. These results collectively demonstrate that the production of 16:1t is linked to the redox status of the chloroplast through PRXQ associatedmore »
- Authors:
-
- Department of Energy‐Plant Research Laboratory Michigan State University East Lansing MI 48824 USA
- Department of Energy‐Plant Research Laboratory Michigan State University East Lansing MI 48824 USA, Department of Chemical Engineering and Materials Science Michigan State University East Lansing MI 48824 USA
- Department of Energy‐Plant Research Laboratory Michigan State University East Lansing MI 48824 USA, Department of Biochemistry and Molecular Biology Michigan State University East Lansing MI 48824 USA
- Department of Energy‐Plant Research Laboratory Michigan State University East Lansing MI 48824 USA, Department of Biochemistry and Molecular Biology Michigan State University East Lansing MI 48824 USA, Department of Plant Biology Michigan State University East Lansing MI 48824 USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1596397
- Grant/Contract Number:
- DE‐FG02‐91ER20021; DE‐FG02‐98ER20305
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- The Plant Journal
- Additional Journal Information:
- Journal Name: The Plant Journal Journal Volume: 102 Journal Issue: 4; Journal ID: ISSN 0960-7412
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Horn, Patrick J., Smith, Montgomery D., Clark, Tessa R., Froehlich, John E., and Benning, Christoph. PEROXIREDOXIN Q stimulates the activity of the chloroplast 16:1 Δ3trans FATTY ACID DESATURASE4. United Kingdom: N. p., 2020.
Web. doi:10.1111/tpj.14657.
Horn, Patrick J., Smith, Montgomery D., Clark, Tessa R., Froehlich, John E., & Benning, Christoph. PEROXIREDOXIN Q stimulates the activity of the chloroplast 16:1 Δ3trans FATTY ACID DESATURASE4. United Kingdom. https://doi.org/10.1111/tpj.14657
Horn, Patrick J., Smith, Montgomery D., Clark, Tessa R., Froehlich, John E., and Benning, Christoph. Fri .
"PEROXIREDOXIN Q stimulates the activity of the chloroplast 16:1 Δ3trans FATTY ACID DESATURASE4". United Kingdom. https://doi.org/10.1111/tpj.14657.
@article{osti_1596397,
title = {PEROXIREDOXIN Q stimulates the activity of the chloroplast 16:1 Δ3trans FATTY ACID DESATURASE4},
author = {Horn, Patrick J. and Smith, Montgomery D. and Clark, Tessa R. and Froehlich, John E. and Benning, Christoph},
abstractNote = {Summary Thylakoid membrane lipids, comprised of glycolipids and the phospholipid phosphatidylglycerol (PG), are essential for normal plant growth and development. Unlike other lipid classes, chloroplast PG in nearly all plants contains a substantial fraction of the unusual trans fatty acid 16:1 Δ3trans or 16:1t. We determined that, in Arabidopsis thaliana , 16:1t biosynthesis requires both FATTY ACID DESATURASE4 (FAD4) and a thylakoid‐associated redox protein, PEROXIREDOXIN Q (PRXQ), to produce wild‐type levels of 16:1t. The FAD4–PRXQ biochemical relationship appears to be very specific in planta , as other fatty acids (FA) desaturases do not require peroxiredoxins for their activity, nor does FAD4 require other chloroplast peroxiredoxins under standard growth conditions. Although most of chloroplast PG assembly occurs at the inner envelope membrane, FAD4 was primarily associated with the thylakoid membranes facing the stroma. Furthermore, co‐production of PRXQ with FAD4 was required to produce Δ3‐desaturated FAs in yeast. Alteration of the redox state of FAD4 or PRXQ through site‐directed mutagenesis of conserved cysteine residues impaired Δ3 FA production. However, these mutations did not appear to directly alter disulfide status of FAD4. These results collectively demonstrate that the production of 16:1t is linked to the redox status of the chloroplast through PRXQ associated with the thylakoids.},
doi = {10.1111/tpj.14657},
journal = {The Plant Journal},
number = 4,
volume = 102,
place = {United Kingdom},
year = {Fri Jan 31 00:00:00 EST 2020},
month = {Fri Jan 31 00:00:00 EST 2020}
}
https://doi.org/10.1111/tpj.14657
Web of Science
Works referenced in this record:
The essential role of phosphatidylglycerol in photosynthesis
journal, July 2007
- Wada, Hajime; Murata, Norio
- Photosynthesis Research, Vol. 92, Issue 2
Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis †
journal, March 2006
- Lamkemeyer, Petra; Laxa, Miriam; Collin, Valérie
- The Plant Journal, Vol. 45, Issue 6
Peroxiredoxins in Plants and Cyanobacteria
journal, August 2011
- Dietz, Karl-Josef
- Antioxidants & Redox Signaling, Vol. 15, Issue 4
Purification and characterization of the stearoyl-acyl carrier protein desaturase and the acyl-acyl carrier protein thioesterase from maturing seeds of safflower.
journal, October 1982
- McKeon, T. A.; Stumpf, P. K.
- Journal of Biological Chemistry, Vol. 257, Issue 20
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
The evolution of desaturases
journal, February 2003
- Sperling, P.; Ternes, P.; Zank, T. K.
- Prostaglandins, Leukotrienes and Essential Fatty Acids, Vol. 68, Issue 2
Analysis of Photosynthetic Antenna Function in a Mutant of Arabidopsis thaliana (L.) Lacking trans -Hexadecenoic Acid
journal, August 1985
- McCourt, Peter; Browse, John; Watson, Jan
- Plant Physiology, Vol. 78, Issue 4
A Mutant of Arabidopsis Lacking a Chloroplast-Specific Lipid
journal, February 1985
- Browse, J.; Mccourt, P.; Somerville, C. R.
- Science, Vol. 227, Issue 4688
Yeast lipid metabolism at a glance
journal, March 2014
- Klug, Lisa; Daum, Günther
- FEMS Yeast Research, Vol. 14, Issue 3
Production of Disulfide‐Bonded Proteins in Escherichia coli
journal, October 2014
- Ke, Na; Berkmen, Mehmet
- Current Protocols in Molecular Biology, Vol. 108, Issue 1
Glycerolipids in photosynthesis: Composition, synthesis and trafficking
journal, April 2014
- Boudière, Laurence; Michaud, Morgane; Petroutsos, Dimitris
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 4
Separation of polyunsaturated fatty acids by argentation thin layer chromatography
journal, February 1975
- Dudley, Peter A.; Anderson, Robert E.
- Lipids, Vol. 10, Issue 2
Rapid and reliable protein extraction from yeast
journal, January 2000
- Kushnirov, Vitaly V.
- Yeast, Vol. 16, Issue 9
Lipid Composition of Pea and Bean Leaves during Chloroplast Development
journal, July 1972
- Roughan, P. G.; Boardman, N. K.
- Plant Physiology, Vol. 50, Issue 1
Yeast Pgc1p ( YPL206c ) Controls the Amount of Phosphatidylglycerol via a Phospholipase C-type Degradation Mechanism
journal, April 2008
- S̆imoc̆ková, Mária; Holic̆, Roman; Tahotná, Dana
- Journal of Biological Chemistry, Vol. 283, Issue 25
REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction
journal, June 2004
- Apel, Klaus; Hirt, Heribert
- Annual Review of Plant Biology, Vol. 55, Issue 1
Fatty acids, part 16. Thin layer and gas—liquid chromatographic properties of the cis and trans methyl octadecenoates and of some acetylenic esters
journal, August 1967
- Gunstone, F. D.; Ismail, I. A.; Lie ken jie, M.
- Chemistry and Physics of Lipids, Vol. 1, Issue 4
The biosynthesis of trans-Δ3-hexadecenoic acid by Chlorella vulgaris
journal, December 1965
- Nichols, B. W.; Harris, P.; James, A. T.
- Biochemical and Biophysical Research Communications, Vol. 21, Issue 5
Metabolic engineering of Saccharomyces cerevisiae for production of novel lipid compounds
journal, July 2002
- J., Dyer; D., Chapital; J., Kuan
- Applied Microbiology and Biotechnology, Vol. 59, Issue 2-3
Channeling of Eukaryotic Diacylglycerol into the Biosynthesis of Plastidial Phosphatidylglycerol
journal, December 2006
- Fritz, Markus; Lokstein, Heiko; Hackenberg, Dieter
- Journal of Biological Chemistry, Vol. 282, Issue 7
PEST sequences and regulation by proteolysis
journal, July 1996
- Rechsteiner, Martin; Rogers, Scott W.
- Trends in Biochemical Sciences, Vol. 21, Issue 7
A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta
journal, September 2003
- Curtis, Mark D.; Grossniklaus, Ueli
- Plant Physiology, Vol. 133, Issue 2, p. 462-469
Structure and function of glycoglycerolipids in plants and bacteria
journal, September 2007
- Hölzl, Georg; Dörmann, Peter
- Progress in Lipid Research, Vol. 46, Issue 5
Acyl-Lipid Metabolism
journal, January 2013
- Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred
- The Arabidopsis Book, Vol. 11
In vivo lipid ‘tag and track’ approach shows acyl editing of plastid lipids and chloroplast import of phosphatidylglycerol precursors in Arabidopsis thaliana
journal, July 2018
- Hurlock, Anna K.; Wang, Kun; Takeuchi, Tomomi
- The Plant Journal, Vol. 95, Issue 6
Functional analysis of desaturases from the myxobacterium Myxococcus xanthus
journal, July 2009
- Ring, Michael W.; Bode, Edna; Schwär, Gertrud
- FEMS Microbiology Letters, Vol. 296, Issue 1
NADPH Thioredoxin Reductase C Controls the Redox Status of Chloroplast 2-Cys Peroxiredoxins in Arabidopsis thaliana
journal, March 2009
- Kirchsteiger, Kerstin; Pulido, Pablo; González, Maricruz
- Molecular Plant, Vol. 2, Issue 2
CarF Mediates Signaling by Singlet Oxygen, Generated via Photoexcited Protoporphyrin IX, in Myxococcus xanthus Light-Induced Carotenogenesis
journal, January 2012
- Galbis-Martinez, M.; Padmanabhan, S.; Murillo, F. J.
- Journal of Bacteriology, Vol. 194, Issue 6
Tracking synthesis and turnover of triacylglycerol in leaves
journal, January 2015
- Tjellström, Henrik; Strawsine, Merissa; Ohlrogge, John B.
- Journal of Experimental Botany, Vol. 66, Issue 5
A simplified isolation of phosphatidylglycerol
journal, January 1986
- Roughan, Grattan
- Plant Science, Vol. 43, Issue 1
Desaturation of oleoyl groups in envelope membranes from spinach chloroplasts.
journal, December 1990
- Schmidt, H.; Heinz, E.
- Proceedings of the National Academy of Sciences, Vol. 87, Issue 23
A bacterial light response reveals an orphan desaturase for human plasmalogen synthesis
journal, October 2019
- Gallego-García, Aránzazu; Monera-Girona, Antonio J.; Pajares-Martínez, Elena
- Science, Vol. 366, Issue 6461
Peroxiredoxins and Redox Signaling in Plants
journal, March 2018
- Liebthal, Michael; Maynard, Daniel; Dietz, Karl-Josef
- Antioxidants & Redox Signaling, Vol. 28, Issue 7
A Plastid Phosphatidylglycerol Lipase Contributes to the Export of Acyl Groups from Plastids for Seed Oil Biosynthesis
journal, July 2017
- Wang, Kun; Froehlich, John E.; Zienkiewicz, Agnieszka
- The Plant Cell, Vol. 29, Issue 7
NADH- and NADPH-dependent desaturation of linoleic acid in the extracted microsomal fraction of rat liver, and related effects of catalase and hydrogen peroxide
journal, March 1979
- Larsson, Orla M.; Brimer, Leon
- Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 572, Issue 3
The PMR analysis of non-conjugated alkenoic and alkynoic acids and esters
journal, September 1975
- Frost, D. J.; Gunstone, F. D.
- Chemistry and Physics of Lipids, Vol. 15, Issue 1
Identification and Characterization of DegP, a Serine Protease Associated with the Luminal Side of the Thylakoid Membrane
journal, March 1998
- Itzhaki, Hanan; Naveh, Leah; Lindahl, Marika
- Journal of Biological Chemistry, Vol. 273, Issue 12
Studying Arabidopsis Envelope Protein Localization and Topology Using Thermolysin and Trypsin Proteases
book, January 2011
- Froehlich, John
- Chloroplast Research in Arabidopsis
Proteome Map of the Chloroplast Lumen of Arabidopsis thaliana
journal, November 2001
- Schubert, Maria; Petersson, Ulrika A.; Haas, Brian J.
- Journal of Biological Chemistry, Vol. 277, Issue 10
The Roles of Mitochondrial Reactive Oxygen Species in Cellular Signaling and Stress Response in Plants
journal, March 2016
- Huang, Shaobai; Van Aken, Olivier; Schwarzländer, Markus
- Plant Physiology, Vol. 171, Issue 3
The chloroplast 2-cysteine peroxiredoxin functions as thioredoxin oxidase in redox regulation of chloroplast metabolism
journal, October 2018
- Vaseghi, Mohamad-Javad; Chibani, Kamel; Telman, Wilena
- eLife, Vol. 7
Poplar Peroxiredoxin Q. A Thioredoxin-Linked Chloroplast Antioxidant Functional in Pathogen Defense
journal, February 2004
- Rouhier, Nicolas; Gelhaye, Eric; Gualberto, Jose M.
- Plant Physiology, Vol. 134, Issue 3
Comprehensive survey of proteins targeted by chloroplast thioredoxin
journal, September 2001
- Motohashi, K.; Kondoh, A.; Stumpp, M. T.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 20
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
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011
- Sievers, Fabian; Wilm, Andreas; Dineen, David
- Molecular Systems Biology, Vol. 7, Issue 1
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
- Gao, Jinpeng; Ajjawi, Imad; Manoli, Arthur
- The Plant Journal, Vol. 60, Issue 5
NTRC and Chloroplast-Generated Reactive Oxygen Species Regulate Pseudomonas syringae pv. tomato Disease Development in Tomato and Arabidopsis
journal, March 2012
- Ishiga, Yasuhiro; Ishiga, Takako; Wangdi, Tamding
- Molecular Plant-Microbe Interactions, Vol. 25, Issue 3
Constructs and methods for high-throughput gene silencing in plants
journal, August 2003
- Helliwell, C.
- Methods, Vol. 30, Issue 4
Sequences Required for the Activity of PTOX (IMMUTANS), a Plastid Terminal Oxidase: IN VITRO AND IN PLANTA MUTAGENESIS OF IRON-BINDING SITES AND A CONSERVED SEQUENCE THAT CORRESPONDS TO EXON 8
journal, October 2005
- Fu, Aigen; Park, Sungsoon; Rodermel, Steven
- Journal of Biological Chemistry, Vol. 280, Issue 52
Midpoint redox potentials of plant and algal ferredoxins
journal, November 1977
- Cammack, R.; Rao, K. K.; Bargeron, C. P.
- Biochemical Journal, Vol. 168, Issue 2
Desaturation and Related Modifications of Fatty Acids
journal, June 1998
- Shanklin, John; Cahoon, Edgar B.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 49, Issue 1
ARAMEMNON, a Novel Database for Arabidopsis Integral Membrane Proteins
journal, January 2003
- Schwacke, Rainer; Schneider, Anja; van der Graaff, Eric
- Plant Physiology, Vol. 131, Issue 1
Chloroplast 2010: A Database for Large-Scale Phenotypic Screening of Arabidopsis Mutants
journal, January 2011
- Lu, Yan; Savage, Linda J.; Larson, Matthew D.
- Plant Physiology, Vol. 155, Issue 4
Identification of the Arabidopsis Palmitoyl-Monogalactosyldiacylglycerol Δ7-Desaturase Gene FAD5 , and Effects of Plastidial Retargeting of Arabidopsis Desaturases on the fad5 Mutant Phenotype
journal, December 2004
- Heilmann, Ingo; Mekhedov, Sergei; King, Barbara
- Plant Physiology, Vol. 136, Issue 4
The Prx Q protein of Arabidopsis thaliana is a member of the luminal chloroplast proteome
journal, October 2006
- Petersson, Ulrika A.; Kieselbach, Thomas; García-Cerdán, José G.
- FEBS Letters, Vol. 580, Issue 26
Switching desaturase enzyme specificity by alternate subcellular targeting
journal, July 2004
- Heilmann, I.; Pidkowich, M. S.; Girke, T.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 28
Evidence for the different responses of Δ9-, Δ6-and Δ5-fatty acyl-CoA desaturases to cytoplasmic proteins
journal, January 1978
- Jeffcoat, R.; Dunton, A. P.; James, A. T.
- Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 528, Issue 1