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The Role of Chloroplast Membrane Lipid Metabolism in Plant Environmental Responses

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The Role of Chloroplast Membrane Lipid Metabolism in Plant Environmental Responses cells Review The Role of Chloroplast Membrane Lipid Metabolism in Plant Environmental Responses Ron Cook 1,2,†, Josselin Lupette 1,†,‡ and Christoph Benning 1,2,3,* 1 MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI 48824-1319, USA; [email protected] (R.C.); [email protected] (J.L.) 2 Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824-1319, USA 3 Department of Plant Biology, Michigan State University, East Lansing, MI 48824-1319, USA * Correspondence: [email protected] † These authors contributed equally to this work. ‡ Present address: Laboratoire de Biogenèse Membranaire, Université de Bordeaux, CNRS, UMR 5200, F-33140 Villenave d’Ornon, France. Abstract: Plants are nonmotile life forms that are constantly exposed to changing environmental conditions during the course of their life cycle. Fluctuations in environmental conditions can be drastic during both day–night and seasonal cycles, as well as in the long term as the climate changes. Plants are naturally adapted to face these environmental challenges, and it has become increasingly apparent that membranes and their lipid composition are an important component of this adaptive response. Plants can remodel their membranes to change the abundance of different lipid classes, and they can release fatty acids that give rise to signaling compounds in response to environmental cues. Chloroplasts harbor the photosynthetic apparatus of plants embedded into one of the most extensive membrane systems found in nature. In part one of this review, we focus on changes in chloroplast membrane lipid class composition in response to environmental changes, and in part two, we will detail chloroplast lipid-derived signals. Citation: Cook, R.; Lupette, J.; Benning, C. The Role of Chloroplast Membrane Keywords: fatty acids; glycerolipids; galactolipids; jasmonate; oxylipin; phospholipids; plant stress Lipid Metabolism in Plant Environmental Responses. Cells 2021, 10, 706. https://doi.org/10.3390/cells10030706 Academic Editor: Viktor Žárský 1. Introduction The chloroplast is the organelle in plants that synthesizes the bulk of fatty acids (FAs) Received: 19 February 2021 for the assembly of glycerolipids at the chloroplast envelope membranes and the endo- Accepted: 19 March 2021 plasmic reticulum (ER). Both compartments extensively interact in the biogenesis of the Published: 23 March 2021 photosynthetic membranes, necessitating the exchange of lipid precursors across multiple membranes. Phosphatidic acid (PA) is a central metabolite of glycerolipid metabolism, Publisher’s Note: MDPI stays neutral and its synthesis, transport, and conversion are complex and not yet fully understood. In with regard to jurisdictional claims in addition, PA affects the activity of multiple enzymes of lipid metabolism, making it often published maps and institutional affil- difficult to distinguish its metabolic functions from its signaling functions. As we discuss iations. general aspects of chloroplast lipid metabolism during the first part of this review, a focus is placed on the potential roles of PA and its different molecular species in chloroplast lipid metabolism. Chloroplast membranes have evolved to accommodate an extensive photosynthetic Copyright: © 2021 by the authors. apparatus while maintaining a minimal dependence on limiting nutrients. While phos- Licensee MDPI, Basel, Switzerland. phate is a component of most lipids in virtually all other biological membranes, within This article is an open access article chloroplasts, it exists in less than half of envelope membrane lipids and less than 15% distributed under the terms and of thylakoid membrane lipids [1–5]. Instead, these membranes are primarily composed conditions of the Creative Commons of galactolipids, which are directly derived from photosynthetic products. In addition, Attribution (CC BY) license (https:// sulfolipids are present as an alternative to phosphate-based anionic membrane lipids. This creativecommons.org/licenses/by/ unique membrane system is more than just an economical scaffold for the photosynthetic 4.0/). Cells 2021, 10, 706. https://doi.org/10.3390/cells10030706 https://www.mdpi.com/journal/cells Cells 2021, 10, x FOR PEER REVIEW 2 of 21 unique membrane system is more than just an economical scaffold for the photosynthetic machinery, it is also mobilized by plant signaling and metabolic networks in response to biotic and abiotic stimuli. In addition to providing background on chloroplast lipid me- tabolism, the first part of this review describes changes in the lipid classes as a response to stress. During the second part of this review, we discuss the interconnectivity of chlo- Cells 2021, 10, 706 roplast lipid metabolism and lipid-based signaling by oxylipins as one aspect of the2 of dy- 20 namic response of chloroplast lipid metabolism to environmental cues. machinery,2. Chloroplast it is Lipid also mobilized Metabolism by plant signaling and metabolic networks in response to2.1. biotic Biosynthesis and abiotic of Lipid stimuli. Precursors In addition to providing background on chloroplast lipid metabolism,Nearly theall firstplant part lipid of thisbiosynthesis review describes begins changeswith FA in biosynthesis the lipid classes in the as achloroplast response tostroma stress. [6] During, by a theType second II FA part synthase of this similar review, to we that discuss of prokaryotes the interconnectivity [7] (Figure of 1). chloro- In the plastplastid lipid pathway metabolism of lipid and biosynthesis, lipid-based signalingthe acyltransferase by oxylipins ATS1 as one transfers aspect 18:1 of the acyl dynamic groups responsefrom acyl of-acyl chloroplast carrier protein lipid metabolism (acyl-ACP) to the environmental sn-1 position cues. of glycerol 3-phosphate [8,9]. Then, ATS2 transfers an additional acyl group from ACP to the sn-2 position, producing 2. Chloroplast Lipid Metabolism PA at the inner leaflet of the chloroplast inner envelope membrane (IEM) [10]. Since ATS2 2.1. Biosynthesis of Lipid Precursors is specific to 16:0 acyl-ACP, lipids with a 16-carbon moiety at the sn-2 position can be identifiedNearly as all originating plant lipid from biosynthesis plastid-synthesized begins with PA FA [11] biosynthesis. The plastid inpathway the chloroplast for mem- stromabrane lipid [6], by biosynthesis a Type II FA is also synthase referred similar to as tothe that “prokaryotic” of prokaryotes pathway, [7] (Figure although1). In its the en- plastidzyme components pathway of lipidactually biosynthesis, have eukaryotic the acyltransferase origins [12]. ATS1 transfers 18:1 acyl groups from acyl-acylFAs destined carrier for proteinthe ER are (acyl-ACP) released thefromsn ACP-1 position in the ofstroma glycerol by IEM 3-phosphate-associated [8 ,thi-9]. Then,oesterases, ATS2 exported, transfers anand additional activated acylby acyl group-CoA from synthetases ACP to the associatedsn-2 position, with the producing outer en- PAvelope at the membrane inner leaflet (OEM) of the[13,14] chloroplast. Acyl-CoAs inner are envelope used for membranePA biosynthesis (IEM) in [ 10the]. ER Since just ATS2 is specific to 16:0 acyl-ACP, lipids with a 16-carbon moiety at the sn-2 position can as acyl-ACPs are used in the plastid, with one key difference in substrate specificity: the be identified as originating from plastid-synthesized PA [11]. The plastid pathway for ER acyltransferase that acylates the sn-2 position prefers 18-carbon substrates, not 16-car- membrane lipid biosynthesis is also referred to as the “prokaryotic” pathway, although its bon substrates [15]. This allows for lipids with 18-carbon chains at the sn-2 position to be enzyme components actually have eukaryotic origins [12]. identified as derivatives of ER-synthesized PA, or the “eukaryotic” pathway in plants. FigureFigure 1.1. Roles of of phosphatidic phosphatidic acid acid (PA) (PA) in inchloroplast chloroplast lipid lipid metabolism. metabolism. Proteins Proteins colored colored in green in greenhave specific have specific interactions interactions with PA, with which PA, whichmay serve may as serve a regulator, as a regulator, substrate, substrate, or both.or The both. potential The potentialrole of PA role as ofthe PA substrate as the substrate for lipid import for lipid into import the chloroplast into the chloroplast is represented is represented by a dotted by arrow a dotted and arrowa question and a mark, question as this mark, remains as this uncertain. remains uncertain. List of abbr Listeviations of abbreviations in alphabetical in alphabetical order: CPSFL1, order: CPSFL1,CHLOROPLAST CHLOROPLAST SEC14-LIKE1 SEC14-LIKE1 protein; protein; DAG, diacylglycerol; DAG, diacylglycerol; DGD1, DGD1, UDP-galactose:MGDG UDP-galactose:MGDG galac- tosyltransferase; DGDG, digalactosyldiacylglycerol; ER, endoplasmic reticulum; FAS, Fatty acid galactosyltransferase; DGDG, digalactosyldiacylglycerol; ER, endoplasmic reticulum; FAS, Fatty synthase; MGD1,monogalactosyldiacylglycerol synthase; MGDG, monogalactosyldiacylglycerol; acid synthase; MGD1,monogalactosyldiacylglycerol synthase; MGDG, monogalactosyldiacylglycerol; PA, phosphatidic acid; PAP, phosphatidic acid phosphatase; PLAM, plastid associated microsomes; PA, phosphatidic acid; PAP, phosphatidic acid phosphatase; PLAM, plastid associated microsomes; TGD complex, trigalactosyldiacylglycerol complex; UDP-Gal, uridine diphosphate-galactose. The numbers refer to the TGD1-5 proteins forming the TGD complex. FAs destined for the ER are released from
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