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Title: 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 » 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.« less

Authors:
 [1];  [1];  [1];  [1]; ORCiD logo [1]
  1. 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}
}

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