Transport Proteins Enabling Plant Photorespiratory Metabolism

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Transport Proteins Enabling Plant Photorespiratory Metabolism plants Review Transport Proteins Enabling Plant Photorespiratory Metabolism Franziska Kuhnert, Urte Schlüter, Nicole Linka and Marion Eisenhut * Institute of Plant Biochemistry, Cluster of Excellence on Plant Science (CEPLAS), Heinrich Heine University Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf, Germany; [email protected] (F.K.); [email protected] (U.S.); [email protected] (N.L.) * Correspondence: [email protected]; Tel.: +49-211-8110467 Abstract: Photorespiration (PR) is a metabolic repair pathway that acts in oxygenic photosynthetic organisms to degrade a toxic product of oxygen fixation generated by the enzyme ribulose 1,5- bisphosphate carboxylase/oxygenase. Within the metabolic pathway, energy is consumed and carbon dioxide released. Consequently, PR is seen as a wasteful process making it a promising target for engineering to enhance plant productivity. Transport and channel proteins connect the organelles accomplishing the PR pathway—chloroplast, peroxisome, and mitochondrion—and thus enable efficient flux of PR metabolites. Although the pathway and the enzymes catalyzing the biochemical reactions have been the focus of research for the last several decades, the knowledge about transport proteins involved in PR is still limited. This review presents a timely state of knowledge with regard to metabolite channeling in PR and the participating proteins. The significance of transporters for implementation of synthetic bypasses to PR is highlighted. As an excursion, the physiological contribution of transport proteins that are involved in C4 metabolism is discussed. Keywords: photorespiration; photosynthesis; transport protein; plant; Rubisco; metabolite; synthetic bypass; C4 photosynthesis Citation: Kuhnert, F.; Schlüter, U.; Linka, N.; Eisenhut, M. Transport Proteins Enabling Plant Photorespiratory Metabolism. Plants 1. Introduction—The Photorespiratory Metabolism 2021, 10, 880. https://doi.org/ Oxygenic photosynthesis builds the foundation of life on earth. By the action of the 10.3390/plants10050880 photosynthesis apparatus, energy from the sun is harvested and converted into chemical energy, with oxygen (O2) as a byproduct. The chemical energy drives the Calvin–Benson Academic Editor: Pavel Kerchev cycle to fix atmospheric carbon dioxide (CO2) and produce sugars. Central to CO2 fix- ation is the enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco). This Received: 26 March 2021 world’s most abundant protein accomplishes assimilation of ca. 250 billion tons of CO2 Accepted: 20 April 2021 into biomass per year [1]. As a biochemical reaction, Rubisco catalyzes the condensation Published: 27 April 2021 of one molecule of ribulose 1,5-bisphosphate with one molecule of CO2 to produce two molecules of 3-phosphoglycerate (3-PGA). However, the enzyme also accepts O2 as a Publisher’s Note: MDPI stays neutral substrate. In the case of oxygenation activity, Rubisco forms one molecule of 3-PGA and with regard to jurisdictional claims in one molecule of 2-phosphoglycolate (2-PG) [2]. 2-PG acts as an inhibitor of enzymes of published maps and institutional affil- the central carbon metabolism. These are phosphofructokinase [3], sedoheptulose 1,7- iations. bisphosphatase [4], and triose phosphate isomerase [5]. Confronted with the challenge to perform oxygenic photosynthesis and to thrive, cyanobacteria have evolved the pho- torespiratory (PR) metabolism to degrade 2-PG rapidly [6,7]. Oxygenic photosynthetic eukaryotes, including algae and land plants, inherited the indispensable ability to perform Copyright: © 2021 by the authors. PR metabolism (reviewed in [8]). The vital necessity of PR is indicated by the typical PR Licensee MDPI, Basel, Switzerland. phenotype: mutants with defects in PR metabolism grow only in an atmosphere with This article is an open access article elevated CO2 concentrations. When cultivated under ambient CO2 conditions (currently distributed under the terms and 0.041% CO2 in air) growth is impaired or even fully inhibited (reviewed in [9]). By the conditions of the Creative Commons concerted action of nine enzymatic steps (Figure1), the metabolic repair pathway leads to Attribution (CC BY) license (https:// the detoxification of 2-PG and recycles 75% of the carbon contained in 2-PG to regenerate creativecommons.org/licenses/by/ 4.0/). 3-PGA, which is resupplied to the Calvin–Benson (CB) cycle for the regeneration of the Plants 2021, 10, 880. https://doi.org/10.3390/plants10050880 https://www.mdpi.com/journal/plants Plants 2021, 10, x FOR PEER REVIEW 2 of 15 (reviewed in [9]). By the concerted action of nine enzymatic steps (Figure 1), the metabolic Plants 2021, 10, 880 repair pathway leads to the detoxification of 2-PG and recycles 75% of the carbon2 of 15 contained in 2-PG to regenerate 3-PGA, which is resupplied to the Calvin–Benson (CB) cycle for the regeneration of the acceptor molecule ribulose 1,5-bisphosphate and productionacceptor molecule of triose ribulose phosphates. 1,5-bisphosphate The remaining and 25% production are lost in of the triose form phosphates. of CO2 during The the glycine decarboxylation reaction (reviewed in [8,10]). Reduction in photosynthetic remaining 25% are lost in the form of CO2 during the glycine decarboxylation reaction efficiency(reviewed inand [8 ,10yield]). Reductionis estimated in photosynthetic to reach about efficiency 20% of andthe yieldCO2 previously is estimated fixed to reach by photosynthesis in C3 plants under temperate climate conditions and can be even higher about 20% of the CO2 previously fixed by photosynthesis in C3 plants under temperate underclimate hot conditions and dry and canconditions be even higher[10]. Consequently, under hot and dryPR—“respiration conditions [10]. Consequently,in light”—is consideredPR—“respiration as a wasteful in light”—is process. considered However, as besides a wasteful the detoxification process. However, of 2-PG, besides there theare additionaldetoxification beneficial of 2-PG, traits there of arethe additionalpathway: Fi beneficialrstly, since traits PR metabolism of the pathway: dissipates Firstly, energy since andPR metabolismreducing power dissipates its action energy lowers and the reducing potential power of photoinhibition its action lowers [11]. the Secondly, potential PR of metabolismphotoinhibition is not [11 ].an Secondly, isolated PRpathway metabolism but is nothighly an isolatedmetabolically pathway interconnected but is highly (reviewedmetabolically in [12–14]). interconnected Besides (reviewed the carbon in [recycling,12–14]). Besides it is also the intertwined carbon recycling, with nitrogen it is also [15]intertwined and sulphur with nitrogenmetabolism [15] and[16], sulphur and serves metabolism the production [16], and of serves amino the acids production (glycine, of serine,amino acidsglutamate, (glycine, cysteine) serine, and glutamate, activated cysteine) one-carbon and units activated [10,17]. one-carbon units [10,17]. glutamate + 2-OG NH4 malate DiT1 malate DiT2.1 ? ? glycine glycine + 2-OG glutamate NH4 glutamate ? ? BOU GGAT1 ? 2-OG FdGOGAT BASS6 glyoxylate CAT ? glutamine glutamate GOX1/2 H2O2 H2O GDC GS2 CO ½ O2 SHMT1 2 glycolate glycolate glycolate ? NH3 PGLP NADH O 2-PG 2 PXN Rubisco PLGG1 ? NAD+ CO glycerate glycerate glycerate 2 3-PGA OAA NAD+ GLYK HPR1 NADH hydroxy- 3-PGA pyruvate malate glyoxylate CB cycle SGAT1 glycine ? ? serine serine Chloroplast Peroxisome Mitochondrion Figure 1. Simplified presentation of the plant PR metabolism. Oxygenation activity of Rubisco within the chloroplast Figure 1. Simplified presentation of the plant PR metabolism. Oxygenation activity of Rubisco within the chloroplast results results in the generation of one molecule of 3-PGA and 2-PG each. While 3-PGA is metabolized in the CB cycle, 2-PG is in the generation of one molecule of 3-PGA and 2-PG each. While 3-PGA is metabolized in the CB cycle, 2-PG is degraded degraded by the PR metabolism. Within the chloroplast, 2-PG is dephosphorylated by 2-PG phosphatase (PGLP). Formed byglycolate the PR is metabolism. exported from Within the the chloroplast chloroplast, by 2-PGPLGG1 is dephosphorylated and BASS6 and enters by 2-PG the phosphatase peroxisome (PGLP).by a yet Formed unidentified glycolate (?) istranslocator. exported from Glycolate the chloroplast oxidase (G byOX1/2) PLGG1 generates and BASS6 glyoxylate and enters and theH2O peroxisome2. The latter by one a yet is converted unidentified by (?)catalase translocator. (CAT) Glycolateactivity into oxidase O2 and (GOX1/2) H2O. The generates PR intermediate glyoxylate glyoxylate and H2 Ois2 aminated. The latter by one glutamate:glyoxylate is converted by catalase aminotransferase (CAT) activity (GGAT1) into O2 andto yield H2O. glycine. The PR Glutamate intermediate serves glyoxylate as a donor is aminated for the amino by glutamate:glyoxylate group. The peroxisomal aminotransferase importer for (GGAT1) this amino to yieldacid but glycine. also Glutamateglycine is to serves date unknown. as a donor Glycine for the needs amino to group. be imported The peroxisomal by an unknown importer translocator for this into amino theacid mitochondrion. but also glycine Here, is the to dateconcerted unknown. action Glycine of the multienzyme needs to be importedsystem glycine by an decarb unknownoxylase translocator (GDC) and into serine the mitochondrion. hydroxymethyltransferase Here, the concerted (SHMT) actionresults ofin therelease multienzyme of CO2 and system NH3 from glycine one decarboxylase molecule of glycine (GDC) but and also serine
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