PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters

Pick TR, Bräutigam A, Schulz MA, Obata T, Fernie AR, Weber APM (2013)
Proceedings of the National Academy of Sciences of the United States of America 110(8): 3185-3190.

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Abstract
Photorespiratory carbon flux reaches up to a third of photosynthetic flux, thus contributes massively to the global carbon cycle. The pathway recycles glycolate-2-phosphate, the most abundant byproduct of RubisCO reactions. This oxygenation reaction of RubisCO and subsequent photorespiration significantly limit the biomass gains of many crop plants. Although photorespiration is a compartmentalized process with enzymatic reactions in the chloroplast, the peroxisomes, the mitochondria, and the cytosol, no transporter required for the core photorespiratory cycle has been identified at the molecular level to date. Using transcript coexpression analyses, we identified Plastidal glycolate glycerate translocator 1 (PLGG1) as a candidate core photorespiratory transporter. Related genes are encoded in the genomes of archaea, bacteria, fungi, and all Archaeplastida and have previously been associated with a function in programmed cell-death. A mutant deficient in PLGG1 shows WT-like growth only in an elevated carbon dioxide atmosphere. The mutant accumulates glycolate and glycerate, leading to the hypothesis that PLGG1 is a glycolate/glycerate transporter. This hypothesis was tested and supported by in vivo and in vitro transport assays and O-18(2)-metabolic flux profiling. Our results indicate that PLGG1 is the chloroplastidic glycolate/glycerate transporter, which is required for the function of the photorespiratory cycle. Identification of the PLGG1 transport function will facilitate unraveling the role of similar proteins in bacteria, archaea, and fungi in the future.
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Pick TR, Bräutigam A, Schulz MA, Obata T, Fernie AR, Weber APM. PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(8):3185-3190.
Pick, T. R., Bräutigam, A., Schulz, M. A., Obata, T., Fernie, A. R., & Weber, A. P. M. (2013). PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters. Proceedings of the National Academy of Sciences of the United States of America, 110(8), 3185-3190. doi:10.1073/pnas.1215142110
Pick, T. R., Bräutigam, A., Schulz, M. A., Obata, T., Fernie, A. R., and Weber, A. P. M. (2013). PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters. Proceedings of the National Academy of Sciences of the United States of America 110, 3185-3190.
Pick, T.R., et al., 2013. PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters. Proceedings of the National Academy of Sciences of the United States of America, 110(8), p 3185-3190.
T.R. Pick, et al., “PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters”, Proceedings of the National Academy of Sciences of the United States of America, vol. 110, 2013, pp. 3185-3190.
Pick, T.R., Bräutigam, A., Schulz, M.A., Obata, T., Fernie, A.R., Weber, A.P.M.: PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters. Proceedings of the National Academy of Sciences of the United States of America. 110, 3185-3190 (2013).
Pick, Thea R., Bräutigam, Andrea, Schulz, Matthias A., Obata, Toshihiro, Fernie, Alisdair R., and Weber, Andreas P. M. “PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters”. Proceedings of the National Academy of Sciences of the United States of America 110.8 (2013): 3185-3190.
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PMID: 29212086
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Charbonnier T, Le Coq D, McGovern S, Calabre M, Delumeau O, Aymerich S, Jules M., MBio 8(5), 2017
PMID: 28974613
The Genetics of Plant Metabolism.
Fernie AR, Tohge T., Annu. Rev. Genet. 51(), 2017
PMID: 28876980
Citrulline metabolism in plants.
Joshi V, Fernie AR., Amino Acids (), 2017
PMID: 28741223
Clarification of Photorespiratory Processes and the Role of Malic Enzyme in Diatoms.
Davis A, Abbriano R, Smith SR, Hildebrand M., Protist 168(1), 2017
PMID: 28104538
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Eisenhut M, Brautigam A, Timm S, Florian A, Tohge T, Fernie AR, Bauwe H, Weber APM., Mol Plant 10(1), 2017
PMID: 27702693
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Zhang X, Zheng X, Ke S, Zhu H, Liu F, Zhang Z, Peng X, Guo L, Zeng R, Hou P, Liu Z, Wu S, Song M, Yang J, Zhang G., Plant Mol. Biol. 92(6), 2016
PMID: 27614468
Can stable isotope mass spectrometry replace ‎radiolabelled approaches in metabolic studies?
Batista Silva W, Daloso DM, Fernie AR, Nunes-Nesi A, Araujo WL., Plant Sci. 249(), 2016
PMID: 27297990
The LysR-type transcriptional regulator, CidR, regulates stationary phase cell death in Staphylococcus aureus.
Chaudhari SS, Thomas VC, Sadykov MR, Bose JL, Ahn DJ, Zimmerman MC, Bayles KW., Mol. Microbiol. 101(6), 2016
PMID: 27253847
Photorespiration: origins and metabolic integration in interacting compartments.
Hagemann M, Weber AP, Eisenhut M., J. Exp. Bot. 67(10), 2016
PMID: PMC4867902
Perspectives for a better understanding of the metabolic integration of photorespiration within a complex plant primary metabolism network.
Hodges M, Dellero Y, Keech O, Betti M, Raghavendra AS, Sage R, Zhu XG, Allen DK, Weber AP., J. Exp. Bot. 67(10), 2016
PMID: 27053720
Photorespiratory glycolate-glyoxylate metabolism.
Dellero Y, Jossier M, Schmitz J, Maurino VG, Hodges M., J. Exp. Bot. 67(10), 2016
PMID: 26994478
Intracellular and cell-to-apoplast compartmentation of carbohydrate metabolism.
Fettke J, Fernie AR., Trends Plant Sci. 20(8), 2015
PMID: 26008154
Bending of protonema cells in a plastid glycolate/glycerate transporter knockout line of Physcomitrella patens.
Nakahara J, Takechi K, Myouga F, Moriyama Y, Sato H, Takio S, Takano H., PLoS ONE 10(3), 2015
PMID: 25793376
Unknown components of the plastidial permeome.
Pick TR, Weber AP., Front Plant Sci 5(), 2014
PMID: 25191333

46 References

Data provided by Europe PubMed Central.

Inhibition of photosynthesis in Arabidopsis mutants lacking leaf glutamate synthase activity
Somerville CR, Ogren WL., 1980
D-GLYCERATE 3-KINASE, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family.
Boldt R, Edner C, Kolukisaoglu U, Hagemann M, Weckwerth W, Wienkoop S, Morgenthal K, Bauwe H., Plant Cell 17(8), 2005
PMID: 15980259
Identification of photorespiratory glutamate:glyoxylate aminotransferase (GGAT) gene in Arabidopsis.
Igarashi D, Miwa T, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Ohsumi C., Plant J. 33(6), 2003
PMID: 12631323
Kinetic characteristics of the chloroplast envelope glycolate transporter
Howitz KT, McCarty RE., 1985
Substrate-specificity of the pea chloroplast glycolate transporter
Howitz KT, McCarty RE., 1985
Genome-wide insertional mutagenesis of Arabidopsis thaliana.
Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR., Science 301(5633), 2003
PMID: 12893945
Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition.
Lagarde D, Basset M, Lepetit M, Conejero G, Gaymard F, Astruc S, Grignon C., Plant J. 9(2), 1996
PMID: 8820606
Metabolite profiling for plant functional genomics
Fiehn O., 2001
High quality metabolomic data for Chlamydomonas reinhardtii.
Lee DY, Fiehn O., Plant Methods 4(), 2008
PMID: 18442406
A gateway cloning vector set for high-throughput functional analysis of genes in planta.
Curtis MD, Grossniklaus U., Plant Physiol. 133(2), 2003
PMID: 14555774
The promoter of Tl-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of agrobacterium binary vector
Koncz C, Schell J., 1986
The Rx gene from potato controls separate virus resistance and cell death responses.
Bendahmane A, Kanyuka K, Baulcombe DC., Plant Cell 11(5), 1999
PMID: 10330465
A simple method for isolating import-competent Arabidopsis chloroplasts.
Aronsson H, Jarvis P., FEBS Lett. 529(2-3), 2002
PMID: 12372603

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