A predicted plastid rhomboid protease affects phosphatidic acid metabolism in Arabidopsis thaliana
Abstract
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 ofmore »
- Authors:
-
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Institutes of Health (NIH)
- OSTI Identifier:
- 1608419
- Grant/Contract Number:
- FG02-91ER20021; T32‐GM110523
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The Plant Journal
- Additional Journal Information:
- Journal Volume: 99; Journal Issue: 5; Journal ID: ISSN 0960-7412
- Publisher:
- Society for Experimental Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; chloroplast; galactolipid; lipid transport; phosphatidic acid; rhomboid protease; enzyme biochemistry; membrane transport
Citation Formats
Lavell, Anastasiya, Froehlich, John E., Baylis, Olivia, Rotondo, Anthony D., and Benning, Christoph. A predicted plastid rhomboid protease affects phosphatidic acid metabolism in Arabidopsis thaliana. United States: N. p., 2019.
Web. doi:10.1111/tpj.14377.
Lavell, Anastasiya, Froehlich, John E., Baylis, Olivia, Rotondo, Anthony D., & Benning, Christoph. A predicted plastid rhomboid protease affects phosphatidic acid metabolism in Arabidopsis thaliana. United States. https://doi.org/10.1111/tpj.14377
Lavell, Anastasiya, Froehlich, John E., Baylis, Olivia, Rotondo, Anthony D., and Benning, Christoph. Tue .
"A predicted plastid rhomboid protease affects phosphatidic acid metabolism in Arabidopsis thaliana". United States. https://doi.org/10.1111/tpj.14377. https://www.osti.gov/servlets/purl/1608419.
@article{osti_1608419,
title = {A predicted plastid rhomboid protease affects phosphatidic acid metabolism in Arabidopsis thaliana},
author = {Lavell, Anastasiya and Froehlich, John E. and Baylis, Olivia and Rotondo, Anthony D. and Benning, Christoph},
abstractNote = {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.},
doi = {10.1111/tpj.14377},
journal = {The Plant Journal},
number = 5,
volume = 99,
place = {United States},
year = {Tue May 07 00:00:00 EDT 2019},
month = {Tue May 07 00:00:00 EDT 2019}
}
Web of Science
Works referenced in this record:
Large-Scale Reverse Genetics in Arabidopsis: Case Studies from the Chloroplast 2010 Project
journal, November 2009
- Ajjawi, Imad; Lu, Yan; Savage, Linda J.
- Plant Physiology, Vol. 152, Issue 2
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
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
journal, September 2001
- Awai, K.; Marechal, E.; Block, M. A.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 19
A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking
journal, July 2006
- Awai, K.; Xu, C.; Tamot, B.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 28, p. 10817-10822
Structural basis for intramembrane proteolysis by rhomboid serine proteases
journal, December 2006
- Ben-Shem, A.; Fass, D.; Bibi, E.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 2
SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information
journal, April 2014
- Biasini, Marco; Bienert, Stefan; Waterhouse, Andrew
- Nucleic Acids Research, Vol. 42, Issue W1
rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster.
journal, February 1990
- Bier, E.; Jan, L. Y.; Jan, Y. N.
- Genes & Development, Vol. 4, Issue 2
The phosphatidic acid phosphatase of the chloroplast envelope is located on the inner envelope membrane
journal, November 1983
- Block, Maryse A.; Dorne, Albert-Jean; Joyard, Jacques
- FEBS Letters, Vol. 164, Issue 1
ALA10, a Phospholipid Flippase, Controls FAD2/FAD3 Desaturation of Phosphatidylcholine in the ER and Affects Chloroplast Lipid Composition in Arabidopsis thaliana
journal, November 2015
- Botella, César; Sautron, Emeline; Boudiere, Laurence
- Plant Physiology, Vol. 170, Issue 3
A Mutant of Arabidopsis Deficient in C 18:3 and C 16:3 Leaf Lipids
journal, July 1986
- Browse, John; McCourt, Peter; Somerville, Chris
- Plant Physiology, Vol. 81, Issue 3
Galactosyltransferases Involved in Galactolipid Biosynthesis Are Located in the Outer Membrane of Pea Chloroplast Envelopes
journal, February 1983
- Cline, Kenneth; Keegstra, Kenneth
- Plant Physiology, Vol. 71, Issue 2
Proteolysis inside the Membrane Is a Rate-Governed Reaction Not Driven by Substrate Affinity
journal, December 2013
- Dickey, Seth W.; Baker, Rosanna P.; Cho, Sangwoo
- Cell, Vol. 155, Issue 6
Steric trapping reveals a cooperativity network in the intramembrane protease GlpG
journal, March 2016
- Guo, Ruiqiong; Gaffney, Kristen; Yang, Zhongyu
- Nature Chemical Biology, Vol. 12, Issue 5
Lipid Trafficking in Plant Cells
journal, July 2014
- Hurlock, Anna K.; Roston, Rebecca L.; Wang, Kun
- Traffic, Vol. 15, Issue 9
Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant
journal, June 2000
- Jarvis, P.; Dormann, P.; Peto, C. A.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 14
An Arabidopsis Rhomboid homolog is an intramembrane protease in plants
journal, October 2005
- Kanaoka, Masahiro M.; Urban, Sinisa; Freeman, Matthew
- FEBS Letters, Vol. 579, Issue 25
Rhomboid proteases in plants - still in square one?
journal, November 2011
- Knopf, Ronit Rimon; Adam, Zach
- Physiologia Plantarum, Vol. 145, Issue 1
Rhomboid proteins in the chloroplast envelope affect the level of allene oxide synthase in Arabidopsis thaliana: Chloroplast rhomboids affect allene oxide synthase
journal, September 2012
- Knopf, Ronit Rimon; Feder, Ari; Mayer, Kristin
- The Plant Journal, Vol. 72, Issue 4
Rhomboid distorts lipids to break the viscosity-imposed speed limit of membrane diffusion
journal, January 2019
- Kreutzberger, Alex J. B.; Ji, Ming; Aaron, Jesse
- Science, Vol. 363, Issue 6426
Altered regulation of lipid biosynthesis in a mutant of Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity
journal, June 1988
- Kunst, L.; Browse, J.; Somerville, C.
- Proceedings of the National Academy of Sciences, Vol. 85, Issue 12, p. 4143-4147
Regulated Intracellular Ligand Transport and Proteolysis Control EGF Signal Activation in Drosophila
journal, October 2001
- Lee, Jeffrey R.; Urban, Sinisa; Garvey, Clare F.
- Cell, Vol. 107, Issue 2
Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases
journal, November 2007
- Lemberg, M. K.; Freeman, M.
- Genome Research, Vol. 17, Issue 11
Identification of Putative Substrates of SEC2, a Chloroplast Inner Envelope Translocase
journal, February 2017
- Li, Yubing; Martin, Jonathan R.; Aldama, Giovanni A.
- Plant Physiology, Vol. 173, Issue 4
Acyl-Lipid Metabolism
journal, January 2013
- Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred
- The Arabidopsis Book, Vol. 11
Reduced Biosynthesis of Digalactosyldiacylglycerol, a Major Chloroplast Membrane Lipid, Leads to Oxylipin Overproduction and Phloem Cap Lignification in Arabidopsis
journal, December 2015
- Lin, Yang-Tsung; Chen, Lih-Jen; Herrfurth, Cornelia
- The Plant Cell, Vol. 28, Issue 1
An improved method for preparing Agrobacterium cells that simplifies the Arabidopsis transformation protocol
journal, October 2006
- Logemann, Elke; Birkenbihl, Rainer P.; Ülker, Bekir
- Plant Methods, Vol. 2, Issue 1
A 25-Amino Acid Sequence of the Arabidopsis TGD2 Protein Is Sufficient for Specific Binding of Phosphatidic Acid
journal, May 2009
- Lu, Binbin; Benning, Christoph
- Journal of Biological Chemistry, Vol. 284, Issue 26
The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking: Rhomboid protease PARL cleaves human Pink1
journal, April 2011
- Meissner, Cathrin; Lorenz, Holger; Weihofen, Andreas
- Journal of Neurochemistry, Vol. 117, Issue 5
Intramembrane protease PARL defines a negative regulator of PINK1- and PARK2/Parkin-dependent mitophagy
journal, September 2015
- Meissner, Cathrin; Lorenz, Holger; Hehn, Beate
- Autophagy, Vol. 11, Issue 9
Membrane immersion allows rhomboid proteases to achieve specificity by reading transmembrane segment dynamics
journal, November 2012
- Moin, Syed M.; Urban, Sinisa
- eLife, Vol. 1
The C16:3\C18:3 fatty acid balance in photosynthetic tissues from 468 plant species
journal, October 1998
- Mongrand, Sébastien; Bessoule, Jean-Jacques; Cabantous, Francis
- Phytochemistry, Vol. 49, Issue 4
Plastidic Phosphatidic Acid Phosphatases Identified in a Distinct Subfamily of Lipid Phosphate Phosphatases with Prokaryotic Origin
journal, July 2007
- Nakamura, Yuki; Tsuchiya, Mami; Ohta, Hiroyuki
- Journal of Biological Chemistry, Vol. 282, Issue 39
The gene and the RNA for the precursor to the plastid-located glycerol-3-phosphate acyltransferase of Arabidopsis thaliana
journal, January 1993
- Nishida, Ikuo; Tasaka, Yasushi; Shiraishi, Hideaki
- Plant Molecular Biology, Vol. 21, Issue 2
Serine peptidases: Classification, structure and function
journal, February 2008
- Page, M. J.; Di Cera, E.
- Cellular and Molecular Life Sciences, Vol. 65, Issue 7-8
Structural insights and membrane binding properties of MGD1, the major galactolipid synthase in plants
journal, February 2016
- Rocha, Joana; Sarkis, Joe; Thomas, Aline
- The Plant Journal, Vol. 85, Issue 5
Arabidopsis chloroplast lipid transport protein TGD2 disrupts membranes and is part of a large complex: TGD2 involved in chloroplast lipid transport
journal, March 2011
- Roston, Rebecca; Gao, Jinpeng; Xu, Changcheng
- The Plant Journal, Vol. 66, Issue 5
TGD1, -2, and -3 Proteins Involved in Lipid Trafficking Form ATP-binding Cassette (ABC) Transporter with Multiple Substrate-binding Proteins
journal, April 2012
- Roston, Rebecca L.; Gao, Jinpeng; Murcha, Monika W.
- Journal of Biological Chemistry, Vol. 287, Issue 25
Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase
journal, January 2007
- Stevenson, Lindsay G.; Strisovsky, Kvido; Clemmer, Katy M.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 3
An Arabidopsis rhomboid protease has roles in the chloroplast and in flower development
journal, March 2012
- Thompson, Elinor P.; Llewellyn Smith, Stefan G.; Glover, Beverley J.
- Journal of Experimental Botany, Vol. 63, Issue 10
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
journal, December 2007
- Tripp, Joanna; Inoue, Kentaro; Keegstra, Kenneth
- The Plant Journal, Vol. 52, Issue 5
Substrate Specificity of Rhomboid Intramembrane Proteases Is Governed by Helix-Breaking Residues in the Substrate Transmembrane Domain
journal, June 2003
- Urban, Sinisa; Freeman, Matthew
- Molecular Cell, Vol. 11, Issue 6
Drosophila Rhomboid-1 Defines a Family of Putative Intramembrane Serine Proteases
journal, October 2001
- Urban, Sinisa; Lee, Jeffrey R.; Freeman, Matthew
- Cell, Vol. 107, Issue 2
Crystal structure of a rhomboid family intramembrane protease
journal, October 2006
- Wang, Yongcheng; Zhang, Yingjiu; Ha, Ya
- Nature, Vol. 444, Issue 7116
The Phosphatidic Acid Binding Site of the Arabidopsis Trigalactosyldiacylglycerol 4 (TGD4) Protein Required for Lipid Import into Chloroplasts
journal, January 2013
- Wang, Zhen; Anderson, Nicholas Scott; Benning, Christoph
- Journal of Biological Chemistry, Vol. 288, Issue 7
Two Abscisic Acid-Responsive Plastid Lipase Genes Involved in Jasmonic Acid Biosynthesis in Arabidopsis thaliana
journal, April 2018
- Wang, Kun; Guo, Qiang; Froehlich, John E.
- The Plant Cell, Vol. 30, Issue 5
Mutation of the TGD1 Chloroplast Envelope Protein Affects Phosphatidate Metabolism in Arabidopsis
journal, November 2005
- Xu, Changcheng; Fan, Jilian; Froehlich, John E.
- The Plant Cell, Vol. 17, Issue 11, p. 3094-3110
Phosphatidylglycerol biosynthesis in chloroplasts of Arabidopsis mutants deficient in acyl-ACP glycerol-3- phosphate acyltransferase
journal, July 2006
- Xu, Changcheng; Yu, Bin; Cornish, Adam J.
- The Plant Journal, Vol. 47, Issue 2
Coevolution of Domain Interactions in the Chloroplast TGD1, 2, 3 Lipid Transfer Complex Specific to Brassicaceae and Poaceae Plants
journal, May 2017
- Yang, Yang; Zienkiewicz, Agnieszka; Lavell, Anastasiya
- The Plant Cell, Vol. 29, Issue 6
Loss of Plastidic Lysophosphatidic Acid Acyltransferase Causes Embryo-Lethality in Arabidopsis
journal, May 2004
- Yu, Bin; Wakao, Setsuko; Fan, Jilian
- Plant and Cell Physiology, Vol. 45, Issue 5
SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information
text, January 2014
- Biasini, Marco; Bienert, Stefan; Waterhouse, Andrew
- Oxford University Press