Arabidopsis ACYL CARRIER PROTEIN4 and RHOMBOID LIKE10 act independently in chloroplast phosphatidate synthesis

Xu, Yang; Kambhampati, Shrikaar; Morley, Stewart A.; Cook, Ron; Froehlich, John; Allen, Doug K.; Benning, Christoph

doi:10.1093/plphys/kiad483

Title: Arabidopsis ACYL CARRIER PROTEIN4 and RHOMBOID LIKE10 act independently in chloroplast phosphatidate synthesis

Journal Article · Sat Sep 02 00:00:00 EDT 2023 · Plant Physiology (Bethesda)

DOI:https://doi.org/10.1093/plphys/kiad483· OSTI ID:2217573

;

Abstract ACYL CARRIER PROTEIN4 (ACP4) is the most abundant ACP isoform in Arabidopsis (Arabidopsis thaliana) leaves and acts as a scaffold for de novo fatty acid biosynthesis and as a substrate for acyl-ACP-utilizing enzymes. Recently, ACP4 was found to interact with a protein-designated plastid RHOMBOID LIKE10 (RBL10) that affects chloroplast monogalactosyldiacylglycerol (MGDG) biosynthesis, but the cellular function of this interaction remains to be explored. Here, we generated and characterized acp4 rbl10 double mutants to explore whether ACP4 and RBL10 directly interact in influencing chloroplast lipid metabolism. Alterations in the content and molecular species of chloroplast lipids such as MGDG and phosphatidylglycerol were observed in the acp4 and rbl10 mutants, which are likely associated with the changes in the size and profiles of diacylglycerol (DAG), phosphatidic acid (PA), and acyl-ACP precursor pools. ACP4 contributed to the size and profile of the acyl-ACP pool and interacted with acyl-ACP-utilizing enzymes, as expected for its role in fatty acid biosynthesis and chloroplast lipid assembly. RBL10 appeared to be involved in the conversion of PA to DAG precursors for MGDG biosynthesis as evidenced by the increased 34:x PA and decreased 34:x DAG in the rbl10 mutant and the slow turnover of radiolabeled PA in isolated chloroplasts fed with [14C] acetate. Interestingly, the impaired PA turnover in rbl10 was partially reversed in the acp4 rbl10 double mutant. Collectively, this study shows that ACP4 and RBL10 affect chloroplast lipid biosynthesis by modulating substrate precursor pools and appear to act independently.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0022207

OSTI ID:: 2217573

Alternate ID(s):: OSTI ID: 1999685

Journal Information:: Plant Physiology (Bethesda), Journal Name: Plant Physiology (Bethesda) Vol. 193 Journal Issue: 4; ISSN 0032-0889

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (46)

Ultra Performance Liquid Chromatography and High Resolution Mass Spectrometry for the Analysis of Plant Lipids Hummel, Jan; Segu, Shruthi; Li, Yan Frontiers in Plant Science, Vol. 2 https://doi.org/10.3389/fpls.2011.00054	journal	January 2011
Fatty Acid and Lipid Transport in Plant Cells Li, Nannan; Xu, Changcheng; Li-Beisson, Yonghua Trends in Plant Science, Vol. 21, Issue 2 https://doi.org/10.1016/j.tplants.2015.10.011	journal	February 2016
Acyl-Carrier Protein. II. Intermediary Reactions of Fatty Acid Synthesis Alberts, Alfred W.; Majerus, Philip W.; Talamo, Barbara Biochemistry, Vol. 3, Issue 10 https://doi.org/10.1021/bi00898a030	journal	October 1964
Better together: Protein partnerships for lineage-specific oil accumulation Busta, Lucas; Chapman, Kent D.; Cahoon, Edgar B. Current Opinion in Plant Biology, Vol. 66 https://doi.org/10.1016/j.pbi.2022.102191	journal	April 2022
A General Method for Quantification and Discovery of Acyl Groups Attached to Acyl Carrier Proteins in Fatty Acid Metabolism Using LC-MS/MS Nam, Jeong-Won; Jenkins, Lauren M.; Li, Jia The Plant Cell, Vol. 32, Issue 4 https://doi.org/10.1105/tpc.19.00954	journal	February 2020
Manipulating Fatty Acid Biosynthesis in Microalgae for Biofuel through Protein-Protein Interactions Blatti, Jillian L.; Beld, Joris; Behnke, Craig A. PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0042949	journal	September 2012
Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the ‘16:3’ plant Arabidopsis thaliana Browse, J.; Warwick, N.; Somerville, C. R. Biochemical Journal, Vol. 235, Issue 1 https://doi.org/10.1042/bj2350025	journal	April 1986
Genes of ACYL CARRIER PROTEIN Family Show Different Expression Profiles and Overexpression of ACYL CARRIER PROTEIN 5 Modulates Fatty Acid Composition and Enhances Salt Stress Tolerance in Arabidopsis Huang, Jiexue; Xue, Caiwen; Wang, Han Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00987	journal	June 2017
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J. Science, Vol. 301, Issue 5633, p. 653-657 https://doi.org/10.1126/science.1086391	journal	August 2003
K+ channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions Obrdlik, P.; El-Bakkoury, M.; Hamacher, T. Proceedings of the National Academy of Sciences, Vol. 101, Issue 33 https://doi.org/10.1073/pnas.0404467101	journal	August 2004
Role of plastidial acyl-acyl carrier protein: Glycerol 3-phosphate acyltransferase and acyl-acyl carrier protein hydrolase in channelling the acyl flux through the prokaryotic and eukaryotic pathway L�hden, Imma; Frentzen, Margrit Planta, Vol. 176, Issue 4 https://doi.org/10.1007/BF00397657	journal	January 1988
Subcellular localization of acyl carrier protein in leaf protoplasts of Spinacia oleracea. Ohlrogge, J. B.; Kuhn, D. N.; Stumpf, P. K. Proceedings of the National Academy of Sciences, Vol. 76, Issue 3 https://doi.org/10.1073/pnas.76.3.1194	journal	March 1979
Metabolic and functional connections between cytoplasmic and chloroplast triacylglycerol storage Xu, Changcheng; Fan, Jilian; Shanklin, John Progress in Lipid Research, Vol. 80 https://doi.org/10.1016/j.plipres.2020.101069	journal	November 2020
Structural and functional roles of non-bilayer lipid phases of chloroplast thylakoid membranes and mitochondrial inner membranes Garab, Győző; Yaguzhinsky, Lev S.; Dlouhý, Ondřej Progress in Lipid Research, Vol. 86 https://doi.org/10.1016/j.plipres.2022.101163	journal	April 2022
A predicted plastid rhomboid protease affects phosphatidic acid metabolism in Arabidopsis thaliana Lavell, Anastasiya; Froehlich, John E.; Baylis, Olivia The Plant Journal https://doi.org/10.1111/tpj.14377	journal	June 2019
Re-evaluation of the solution structure of acyl carrier protein. Rock, C. O.; Cronan, J. E. Journal of Biological Chemistry, Vol. 254, Issue 19 https://doi.org/10.1016/S0021-9258(19)83584-6	journal	October 1979
Tracking the metabolic pulse of plant lipid production with isotopic labeling and flux analyses: Past, present and future Allen, Doug K.; Bates, Philip D.; Tjellström, Henrik Progress in Lipid Research, Vol. 58 https://doi.org/10.1016/j.plipres.2015.02.002	journal	April 2015
Multiple mechanisms contribute to increased neutral lipid accumulation in yeast producing recombinant variants of plant diacylglycerol acyltransferase 1 Xu, Yang; Chen, Guanqun; Greer, Michael S. Journal of Biological Chemistry, Vol. 292, Issue 43 https://doi.org/10.1074/jbc.M117.811489	journal	October 2017
Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method Zhang, Xiuren; Henriques, Rossana; Lin, Shih-Shun Nature Protocols, Vol. 1, Issue 2 https://doi.org/10.1038/nprot.2006.97	journal	June 2006
Importance of phosphatidylcholine on the chloroplast surface Botella, César; Jouhet, Juliette; Block, Maryse A. Progress in Lipid Research, Vol. 65 https://doi.org/10.1016/j.plipres.2016.11.001	journal	January 2017
Expression of Antisense Acyl Carrier Protein-4 Reduces Lipid Content in Arabidopsis Leaf Tissue Branen, Jill K.; Shintani, David K.; Engeseth, Nicki J. Plant Physiology, Vol. 132, Issue 2 https://doi.org/10.1104/pp.102.018622	journal	April 2003
Assessing compartmentalized flux in lipid metabolism with isotopes Allen, Doug K. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1861, Issue 9 https://doi.org/10.1016/j.bbalip.2016.03.017	journal	September 2016
Compartmentation of Triacylglycerol Accumulation in Plants Chapman, Kent D.; Ohlrogge, John B. Journal of Biological Chemistry, Vol. 287, Issue 4, p. 2288-2294 https://doi.org/10.1074/jbc.R111.290072	journal	November 2011
Protein interactomes for plant lipid biosynthesis and their biotechnological applications Xu, Yang; Singer, Stacy D.; Chen, Guanqun Plant Biotechnology Journal, Vol. 21, Issue 9 https://doi.org/10.1111/pbi.14027	journal	March 2023
The C16:3\C18:3 fatty acid balance in photosynthetic tissues from 468 plant species Mongrand, Sébastien; Bessoule, Jean-Jacques; Cabantous, Francis Phytochemistry, Vol. 49, Issue 4 https://doi.org/10.1016/S0031-9422(98)00243-X	journal	October 1998
Energetic Manipulation of Chloroplast Protein Import and the Use of Chemical Cross-Linkers to Map Protein–Protein Interactions Inoue, Hitoshi; Wang, Fei; Inaba, Takehito Chloroplast Research in Arabidopsis https://doi.org/10.1007/978-1-61779-234-2_18	book	January 2011
Overexpression of Acyl Carrier Protein-1 Alters Fatty Acid Composition of Leaf Tissue in Arabidopsis Branen, Jill K.; Chiou, Tzyy-Jen; Engeseth, Nicki J. Plant Physiology, Vol. 127, Issue 1 https://doi.org/10.1104/pp.127.1.222	journal	September 2001
Activation of the Chloroplast Monogalactosyldiacylglycerol Synthase MGD1 by Phosphatidic Acid and Phosphatidylglycerol Dubots, Emmanuelle; Audry, Magali; Yamaryo, Yoshiki Journal of Biological Chemistry, Vol. 285, Issue 9 https://doi.org/10.1074/jbc.M109.071928	journal	December 2009
Quantification of Acyl-Acyl Carrier Proteins for Fatty Acid Synthesis Using LC-MS/MS Jenkins, Lauren M.; Nam, Jeong-Won; Evans, Bradley S. Methods in Molecular Biology https://doi.org/10.1007/978-1-0716-1362-7_13	book	January 2021
The pgp1 Mutant Locus of Arabidopsis Encodes a Phosphatidylglycerolphosphate Synthase with Impaired Activity Xu, Changcheng; Härtel, Heiko; Wada, Hajime Plant Physiology, Vol. 129, Issue 2 https://doi.org/10.1104/pp.002725	journal	May 2002
Specificities and Selectivities of Glycerol-3-Phosphate Acyltransferase and Monoacylglycerol-3-Phosphate Acyltransferase from Pea and Spinach Chloroplasts Frentzen, Margrit; Heinz, Ernst; McKEON, Thomas A. European Journal of Biochemistry, Vol. 129, Issue 3 https://doi.org/10.1111/j.1432-1033.1983.tb07096.x	journal	January 1983
Activity of Acyl Carrier Protein Isoforms in Reactions of Plant Fatty Acid Metabolism Guerra, Daniel J.; Ohlrogge, John B.; Frentzen, Margrit Plant Physiology, Vol. 82, Issue 2 https://doi.org/10.1104/pp.82.2.448	journal	October 1986
Revisiting the expression and purification of MGD1, the major galactolipid synthase in Arabidopsis to establish a novel standard for biochemical and structural studies Rocha, Joana; Audry, Magali; Pesce, Gaelle Biochimie, Vol. 95, Issue 4 https://doi.org/10.1016/j.biochi.2012.11.011	journal	April 2013
Elucidation of transient protein-protein interactions within carrier protein-dependent biosynthesis Bartholow, Thomas G.; Sztain, Terra; Patel, Ashay Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-01838-3	journal	March 2021
Proteins associated with the Arabidopsis thaliana plastid rhomboid‐like protein RBL10 Lavell, Anastasiya; Smith, Montgomery; Xu, Yang The Plant Journal, Vol. 108, Issue 5 https://doi.org/10.1111/tpj.15514	journal	October 2021
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy Porra, R. J.; Thompson, W. A.; Kriedemann, P. E. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 975, Issue 3 https://doi.org/10.1016/S0005-2728(89)80347-0	journal	August 1989
Decoding allosteric regulation by the acyl carrier protein Sztain, Terra; Bartholow, Thomas G.; Lee, D. John Proceedings of the National Academy of Sciences, Vol. 118, Issue 16 https://doi.org/10.1073/pnas.2025597118	journal	April 2021
Improved prediction of protein-protein interactions using AlphaFold2 Bryant, Patrick; Pozzati, Gabriele; Elofsson, Arne Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28865-w	journal	March 2022
Two Closely Related Genes of Arabidopsis Encode Plastidial Cytidinediphosphate Diacylglycerol Synthases Essential for Photoautotrophic Growth Haselier, André; Akbari, Hana; Weth, Agnes Plant Physiology, Vol. 153, Issue 3 https://doi.org/10.1104/pp.110.156422	journal	May 2010
Oil-Producing Metabolons Containing DGAT1 Use Separate Substrate Pools from those Containing DGAT2 or PDAT Regmi, Anushobha; Shockey, Jay; Kotapati, Hari Kiran Plant Physiology, Vol. 184, Issue 2 https://doi.org/10.1104/pp.20.00461	journal	July 2020
A transferase interactome that may facilitate channeling of polyunsaturated fatty acid moieties from phosphatidylcholine to triacylglycerol Xu, Yang; Caldo, Kristian Mark P.; Jayawardhane, Kethmi Journal of Biological Chemistry, Vol. 294, Issue 41 https://doi.org/10.1074/jbc.AC119.010601	journal	September 2019
High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method Gietz, R. Daniel; Schiestl, Robert H. Nature Protocols, Vol. 2, Issue 1 https://doi.org/10.1038/nprot.2007.13	journal	January 2007
Similarities and Differences in Lipid Metabolism of Chloroplasts Isolated from 18:3 and 16:3 Plants Heinz, Ernst; Roughan, P. Grattan Plant Physiology, Vol. 72, Issue 2 https://doi.org/10.1104/pp.72.2.273	journal	June 1983
An efficient modified method for plant leaf lipid extraction results in improved recovery of phosphatidic acid Shiva, Sunitha; Enninful, Regina; Roth, Mary R. Plant Methods, Vol. 14, Issue 1 https://doi.org/10.1186/s13007-018-0282-y	journal	February 2018
Cellular Organization and Regulation of Plant Glycerolipid Metabolism Lavell, A. A.; Benning, C. Plant and Cell Physiology, Vol. 60, Issue 6 https://doi.org/10.1093/pcp/pcz016	journal	January 2019
Phosphatidylglycerol biosynthesis in chloroplasts of Arabidopsis mutants deficient in acyl-ACP glycerol-3- phosphate acyltransferase Xu, Changcheng; Yu, Bin; Cornish, Adam J. The Plant Journal, Vol. 47, Issue 2 https://doi.org/10.1111/j.1365-313X.2006.02790.x	journal	July 2006

Similar Records

A predicted plastid rhomboid protease affects phosphatidic acid metabolism in Arabidopsis thaliana

Journal Article · Tue May 07 00:00:00 EDT 2019 · The Plant Journal · OSTI ID:2217573

Lavell, Anastasiya; Froehlich, John E.; Baylis, Olivia; +2 more

Proteins associated with the Arabidopsis thaliana plastid rhomboid-like protein RBL10

Journal Article · Tue Sep 28 00:00:00 EDT 2021 · The Plant Journal · OSTI ID:2217573

Lavell, Anastasiya; Smith, Montgomery; Xu, Yang; +3 more

Tracking synthesis and turnover of triacylglycerol in leaves

Journal Article · Wed Jan 21 00:00:00 EST 2015 · Journal of Experimental Botany · OSTI ID:2217573

Tjellstrom, Henrik; Strawsine, Merissa; Ohlrogge, John B.

Title: Arabidopsis ACYL CARRIER PROTEIN4 and RHOMBOID LIKE10 act independently in chloroplast phosphatidate synthesis

Citation Formats

References (46)

Similar Records

Related Subjects