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

Lavell, Anastasiya; Froehlich, John E.; Baylis, Olivia; Rotondo, Anthony D.; Benning, Christoph

doi:10.1111/tpj.14377

Title: 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

DOI:https://doi.org/10.1111/tpj.14377· OSTI ID:1608419

Lavell, Anastasiya ^[1]; Froehlich, John E. ^[1]; Baylis, Olivia ^[1]; Rotondo, Anthony D. ^[1];

^[1]

Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory

The thylakoid membranes of the chloroplast harbor the photosynthetic machinery that converts light into chemical energy. Chloroplast membranes are unique in their lipid makeup, which is dominated by the galactolipids mono- and digalactosyldiacylglycerol (MGDG and DGDG). Additionally, the most abundant galactolipid, MGDG, is assembled through both plastid and endoplasmic reticulum (ER) pathways in Arabidopsis, resulting in distinguishable molecular lipid species. Phosphatidic acid (PA) is the first glycerolipid formed by the plastid galactolipid biosynthetic pathway. It is converted to substrate diacylglycerol (DAG) for MGDG Synthase (MGD1) which adds to it a galactose from UDP-Gal. The enzymatic reactions yielding these galactolipids have been well established. However, auxiliary or regulatory factors are largely unknown. We identified a predicted rhomboid-like protease 10 (RBL10), located in plastids of Arabidopsis thaliana, that affects galactolipid biosynthesis likely through intramembrane proteolysis. Plants with T-DNA disruptions in RBL10 have greatly decreased 16:3 (acyl carbons:double bonds) and increased 18:3 acyl chain abundance in MGDG of leaves. Additionally, rbl10-1 mutants show reduced [¹⁴C]-acetate incorporation into MGDG during pulse-chase labeling, indicating a reduced flux through the plastid galactolipid biosynthesis pathway. While plastid MGDG biosynthesis is blocked in rbl10-1 mutants, they are capable of synthesizing PA, as well as producing normal amounts of MGDG by compensating with ER-derived lipid precursors. In conclusion, these findings link this predicted protease to the utilization of PA for plastid galactolipid biosynthesis potentially revealing a regulatory mechanism in chloroplasts.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Institutes of Health (NIH)

Grant/Contract Number:: FG02-91ER20021; T32‐GM110523

OSTI ID:: 1608419

Journal Information:: The Plant Journal, Vol. 99, Issue 5; ISSN 0960-7412

Publisher:: Society for Experimental BiologyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 7 works

Citation information provided by
Web of Science

References (50)

Large-Scale Reverse Genetics in Arabidopsis: Case Studies from the Chloroplast 2010 Project Ajjawi, Imad; Lu, Yan; Savage, Linda J. Plant Physiology, Vol. 152, Issue 2 https://doi.org/10.1104/pp.109.148494	journal	November 2009
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
Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana Awai, K.; Marechal, E.; Block, M. A. Proceedings of the National Academy of Sciences, Vol. 98, Issue 19 https://doi.org/10.1073/pnas.181331498	journal	September 2001
A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking Awai, K.; Xu, C.; Tamot, B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 28, p. 10817-10822 https://doi.org/10.1073/pnas.0602754103	journal	July 2006
Structural basis for intramembrane proteolysis by rhomboid serine proteases Ben-Shem, A.; Fass, D.; Bibi, E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 2 https://doi.org/10.1073/pnas.0609773104	journal	December 2006
SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information Biasini, Marco; Bienert, Stefan; Waterhouse, Andrew Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/nar/gku340	journal	April 2014
rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Bier, E.; Jan, L. Y.; Jan, Y. N. Genes & Development, Vol. 4, Issue 2 https://doi.org/10.1101/gad.4.2.190	journal	February 1990
The phosphatidic acid phosphatase of the chloroplast envelope is located on the inner envelope membrane Block, Maryse A.; Dorne, Albert-Jean; Joyard, Jacques FEBS Letters, Vol. 164, Issue 1 https://doi.org/10.1016/0014-5793(83)80030-1	journal	November 1983
ALA10, a Phospholipid Flippase, Controls FAD2/FAD3 Desaturation of Phosphatidylcholine in the ER and Affects Chloroplast Lipid Composition in Arabidopsis thaliana Botella, César; Sautron, Emeline; Boudiere, Laurence Plant Physiology, Vol. 170, Issue 3 https://doi.org/10.1104/pp.15.01557	journal	November 2015
A Mutant of Arabidopsis Deficient in C _18:3 and C _16:3 Leaf Lipids Browse, John; McCourt, Peter; Somerville, Chris Plant Physiology, Vol. 81, Issue 3 https://doi.org/10.1104/pp.81.3.859	journal	July 1986
Galactosyltransferases Involved in Galactolipid Biosynthesis Are Located in the Outer Membrane of Pea Chloroplast Envelopes Cline, Kenneth; Keegstra, Kenneth Plant Physiology, Vol. 71, Issue 2 https://doi.org/10.1104/pp.71.2.366	journal	February 1983
Proteolysis inside the Membrane Is a Rate-Governed Reaction Not Driven by Substrate Affinity Dickey, Seth W.; Baker, Rosanna P.; Cho, Sangwoo Cell, Vol. 155, Issue 6 https://doi.org/10.1016/j.cell.2013.10.053	journal	December 2013
Steric trapping reveals a cooperativity network in the intramembrane protease GlpG Guo, Ruiqiong; Gaffney, Kristen; Yang, Zhongyu Nature Chemical Biology, Vol. 12, Issue 5 https://doi.org/10.1038/nchembio.2048	journal	March 2016
Lipid Trafficking in Plant Cells Hurlock, Anna K.; Roston, Rebecca L.; Wang, Kun Traffic, Vol. 15, Issue 9 https://doi.org/10.1111/tra.12187	journal	July 2014
Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant Jarvis, P.; Dormann, P.; Peto, C. A. Proceedings of the National Academy of Sciences, Vol. 97, Issue 14 https://doi.org/10.1073/pnas.100132197	journal	June 2000
An Arabidopsis Rhomboid homolog is an intramembrane protease in plants Kanaoka, Masahiro M.; Urban, Sinisa; Freeman, Matthew FEBS Letters, Vol. 579, Issue 25 https://doi.org/10.1016/j.febslet.2005.09.049	journal	October 2005
Rhomboid proteases in plants - still in square one? Knopf, Ronit Rimon; Adam, Zach Physiologia Plantarum, Vol. 145, Issue 1 https://doi.org/10.1111/j.1399-3054.2011.01532.x	journal	November 2011
Rhomboid proteins in the chloroplast envelope affect the level of allene oxide synthase in Arabidopsis thaliana: Chloroplast rhomboids affect allene oxide synthase Knopf, Ronit Rimon; Feder, Ari; Mayer, Kristin The Plant Journal, Vol. 72, Issue 4 https://doi.org/10.1111/j.1365-313X.2012.05090.x	journal	September 2012
Rhomboid distorts lipids to break the viscosity-imposed speed limit of membrane diffusion Kreutzberger, Alex J. B.; Ji, Ming; Aaron, Jesse Science, Vol. 363, Issue 6426 https://doi.org/10.1126/science.aao0076	journal	January 2019
Altered regulation of lipid biosynthesis in a mutant of Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity Kunst, L.; Browse, J.; Somerville, C. Proceedings of the National Academy of Sciences, Vol. 85, Issue 12, p. 4143-4147 https://doi.org/10.1073/pnas.85.12.4143	journal	June 1988
Regulated Intracellular Ligand Transport and Proteolysis Control EGF Signal Activation in Drosophila Lee, Jeffrey R.; Urban, Sinisa; Garvey, Clare F. Cell, Vol. 107, Issue 2 https://doi.org/10.1016/S0092-8674(01)00526-8	journal	October 2001
Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases Lemberg, M. K.; Freeman, M. Genome Research, Vol. 17, Issue 11 https://doi.org/10.1101/gr.6425307	journal	November 2007
Identification of Putative Substrates of SEC2, a Chloroplast Inner Envelope Translocase Li, Yubing; Martin, Jonathan R.; Aldama, Giovanni A. Plant Physiology, Vol. 173, Issue 4 https://doi.org/10.1104/pp.17.00012	journal	February 2017
Acyl-Lipid Metabolism Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred The Arabidopsis Book, Vol. 11 https://doi.org/10.1199/tab.0161	journal	January 2013
Reduced Biosynthesis of Digalactosyldiacylglycerol, a Major Chloroplast Membrane Lipid, Leads to Oxylipin Overproduction and Phloem Cap Lignification in Arabidopsis Lin, Yang-Tsung; Chen, Lih-Jen; Herrfurth, Cornelia The Plant Cell, Vol. 28, Issue 1 https://doi.org/10.1105/tpc.15.01002	journal	December 2015
An improved method for preparing Agrobacterium cells that simplifies the Arabidopsis transformation protocol Logemann, Elke; Birkenbihl, Rainer P.; Ülker, Bekir Plant Methods, Vol. 2, Issue 1 https://doi.org/10.1186/1746-4811-2-16	journal	October 2006
A 25-Amino Acid Sequence of the Arabidopsis TGD2 Protein Is Sufficient for Specific Binding of Phosphatidic Acid Lu, Binbin; Benning, Christoph Journal of Biological Chemistry, Vol. 284, Issue 26 https://doi.org/10.1074/jbc.M109.016014	journal	May 2009
The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking: Rhomboid protease PARL cleaves human Pink1 Meissner, Cathrin; Lorenz, Holger; Weihofen, Andreas Journal of Neurochemistry, Vol. 117, Issue 5 https://doi.org/10.1111/j.1471-4159.2011.07253.x	journal	April 2011
Intramembrane protease PARL defines a negative regulator of PINK1- and PARK2/Parkin-dependent mitophagy Meissner, Cathrin; Lorenz, Holger; Hehn, Beate Autophagy, Vol. 11, Issue 9 https://doi.org/10.1080/15548627.2015.1063763	journal	September 2015
Membrane immersion allows rhomboid proteases to achieve specificity by reading transmembrane segment dynamics Moin, Syed M.; Urban, Sinisa eLife, Vol. 1 https://doi.org/10.7554/eLife.00173	journal	November 2012
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
Plastidic Phosphatidic Acid Phosphatases Identified in a Distinct Subfamily of Lipid Phosphate Phosphatases with Prokaryotic Origin Nakamura, Yuki; Tsuchiya, Mami; Ohta, Hiroyuki Journal of Biological Chemistry, Vol. 282, Issue 39 https://doi.org/10.1074/jbc.M704385200	journal	July 2007
The gene and the RNA for the precursor to the plastid-located glycerol-3-phosphate acyltransferase of Arabidopsis thaliana Nishida, Ikuo; Tasaka, Yasushi; Shiraishi, Hideaki Plant Molecular Biology, Vol. 21, Issue 2 https://doi.org/10.1007/BF00019943	journal	January 1993
Serine peptidases: Classification, structure and function Page, M. J.; Di Cera, E. Cellular and Molecular Life Sciences, Vol. 65, Issue 7-8 https://doi.org/10.1007/s00018-008-7565-9	journal	February 2008
Structural insights and membrane binding properties of MGD1, the major galactolipid synthase in plants Rocha, Joana; Sarkis, Joe; Thomas, Aline The Plant Journal, Vol. 85, Issue 5 https://doi.org/10.1111/tpj.13129	journal	February 2016
Arabidopsis chloroplast lipid transport protein TGD2 disrupts membranes and is part of a large complex: TGD2 involved in chloroplast lipid transport Roston, Rebecca; Gao, Jinpeng; Xu, Changcheng The Plant Journal, Vol. 66, Issue 5 https://doi.org/10.1111/j.1365-313X.2011.04536.x	journal	March 2011
TGD1, -2, and -3 Proteins Involved in Lipid Trafficking Form ATP-binding Cassette (ABC) Transporter with Multiple Substrate-binding Proteins Roston, Rebecca L.; Gao, Jinpeng; Murcha, Monika W. Journal of Biological Chemistry, Vol. 287, Issue 25 https://doi.org/10.1074/jbc.M112.370213	journal	April 2012
Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase Stevenson, Lindsay G.; Strisovsky, Kvido; Clemmer, Katy M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 3 https://doi.org/10.1073/pnas.0608140104	journal	January 2007
An Arabidopsis rhomboid protease has roles in the chloroplast and in flower development Thompson, Elinor P.; Llewellyn Smith, Stefan G.; Glover, Beverley J. Journal of Experimental Botany, Vol. 63, Issue 10 https://doi.org/10.1093/jxb/ers012	journal	March 2012
A novel serine/proline-rich domain in combination with a transmembrane domain is required for the insertion of AtTic40 into the inner envelope membrane of chloroplasts Tripp, Joanna; Inoue, Kentaro; Keegstra, Kenneth The Plant Journal, Vol. 52, Issue 5 https://doi.org/10.1111/j.1365-313X.2007.03279.x	journal	December 2007
Substrate Specificity of Rhomboid Intramembrane Proteases Is Governed by Helix-Breaking Residues in the Substrate Transmembrane Domain Urban, Sinisa; Freeman, Matthew Molecular Cell, Vol. 11, Issue 6 https://doi.org/10.1016/S1097-2765(03)00181-3	journal	June 2003
Drosophila Rhomboid-1 Defines a Family of Putative Intramembrane Serine Proteases Urban, Sinisa; Lee, Jeffrey R.; Freeman, Matthew Cell, Vol. 107, Issue 2 https://doi.org/10.1016/S0092-8674(01)00525-6	journal	October 2001
Crystal structure of a rhomboid family intramembrane protease Wang, Yongcheng; Zhang, Yingjiu; Ha, Ya Nature, Vol. 444, Issue 7116 https://doi.org/10.1038/nature05255	journal	October 2006
The Phosphatidic Acid Binding Site of the Arabidopsis Trigalactosyldiacylglycerol 4 (TGD4) Protein Required for Lipid Import into Chloroplasts Wang, Zhen; Anderson, Nicholas Scott; Benning, Christoph Journal of Biological Chemistry, Vol. 288, Issue 7 https://doi.org/10.1074/jbc.M112.438986	journal	January 2013
Two Abscisic Acid-Responsive Plastid Lipase Genes Involved in Jasmonic Acid Biosynthesis in Arabidopsis thaliana Wang, Kun; Guo, Qiang; Froehlich, John E. The Plant Cell, Vol. 30, Issue 5 https://doi.org/10.1105/tpc.18.00250	journal	April 2018
Mutation of the TGD1 Chloroplast Envelope Protein Affects Phosphatidate Metabolism in Arabidopsis Xu, Changcheng; Fan, Jilian; Froehlich, John E. The Plant Cell, Vol. 17, Issue 11, p. 3094-3110 https://doi.org/10.1105/tpc.105.035592	journal	November 2005
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
Coevolution of Domain Interactions in the Chloroplast TGD1, 2, 3 Lipid Transfer Complex Specific to Brassicaceae and Poaceae Plants Yang, Yang; Zienkiewicz, Agnieszka; Lavell, Anastasiya The Plant Cell, Vol. 29, Issue 6 https://doi.org/10.1105/tpc.17.00182	journal	May 2017
Loss of Plastidic Lysophosphatidic Acid Acyltransferase Causes Embryo-Lethality in Arabidopsis Yu, Bin; Wakao, Setsuko; Fan, Jilian Plant and Cell Physiology, Vol. 45, Issue 5 https://doi.org/10.1093/pcp/pch064	journal	May 2004
SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information Biasini, Marco; Bienert, Stefan; Waterhouse, Andrew Oxford University Press https://doi.org/10.5451/unibas-ep34396	text	January 2014

Similar Records

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) · OSTI ID:1608419

Xu, Yang; Kambhampati, Shrikaar; Morley, Stewart A.; +4 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:1608419

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

Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana

Journal Article · Tue Sep 06 00:00:00 EDT 2016 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1608419

Kelly, Amélie A.; Kalisch, Barbara; Hölzl, Georg; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
chloroplast
galactolipid
lipid transport
phosphatidic acid
rhomboid protease
enzyme biochemistry
membrane transport

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

Citation Formats

References (50)

Similar Records

Related Subjects