The interplay of post-translational protein modifications in Arabidopsis leaves during photosynthesis induction.
Arabidopsis
acetylation
carbon assimilation
dark light transition
iodoTMT
metabolomics
phosphorylation
photosynthesis
proteomics
quantitative mass spectrometry
redox regulation
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
10
07
2023
received:
10
05
2023
accepted:
19
07
2023
medline:
10
11
2023
pubmed:
31
7
2023
entrez:
31
7
2023
Statut:
ppublish
Résumé
Diurnal dark to light transition causes profound physiological changes in plant metabolism. These changes require distinct modes of regulation as a unique feature of photosynthetic lifestyle. The activities of several key metabolic enzymes are regulated by light-dependent post-translational modifications (PTM) and have been studied at depth at the level of individual proteins. In contrast, a global picture of the light-dependent PTMome dynamics is lacking, leaving the response of a large proportion of cellular function undefined. Here, we investigated the light-dependent metabolome and proteome changes in Arabidopsis rosettes in a time resolved manner to dissect their kinetic interplay, focusing on phosphorylation, lysine acetylation, and cysteine-based redox switches. Of over 24 000 PTM sites that were detected, more than 1700 were changed during the transition from dark to light. While the first changes, as measured 5 min after onset of illumination, occurred mainly in the chloroplasts, PTM changes at proteins in other compartments coincided with the full activation of the Calvin-Benson cycle and the synthesis of sugars at later timepoints. Our data reveal connections between metabolism and PTM-based regulation throughout the cell. The comprehensive multiome profiling analysis provides unique insight into the extent by which photosynthesis reprograms global cell function and adds a powerful resource for the dissection of diverse cellular processes in the context of photosynthetic function.
Substances chimiques
Arabidopsis Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1172-1193Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : IF1655/3-1
Organisme : Deutsche Forschungsgemeinschaft
ID : MA2379/14-1
Organisme : Deutsche Forschungsgemeinschaft
ID : SCHW1719/5-1
Organisme : Deutsche Forschungsgemeinschaft
ID : IF1655/3-3
Organisme : European Union Horizon 2020
Organisme : Max-Planck-Gesellschaft
Informations de copyright
© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Anderson, L.B., Maderia, M., Ouellette, A.J.A., Putnam-Evans, C., Higgins, L.A., Krick, T. et al. (2002) Posttranslational modifications in the CP43 subunit of photosystem II. Proceedings. National Academy of Sciences. United States of America, 99, 14676-14681.
Balmer, Y., Koller, A., Del Val, G., Manieri, W., Schürmann, P. & Buchanan, B.B. (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proceedings of the National Academy of Sciences, 100, 370-375.
Balmer, Y., Vensel, W.H., Cai, N., Manieri, W., Schürmann, P., Hurkman, W.J. et al. (2006) A complete ferredoxin/thioredoxin system regulates fundamental processes in amyloplasts. Proceedings of the National Academy of Sciences, 103, 2988-2993.
Balparda, M., Bouzid, M., Martinez, P., Del, M., Zheng, K., Schwarzländer, M. et al. (2023) Regulation of plant carbon assimilation metabolism by post-translational modifications. The Plant Journal, 114, 1059-1079.
Balparda, M., Elsässer, M., Badia, M.B., Giese, J., Bovdilova, A., Hüdig, M. et al. (2021) Acetylation of conserved lysines fine-tunes mitochondrial malate dehydrogenase activity in land plants. The Plant Journal, 109, 92-111.
Barrero-Gil, J. & Salinas, J. (2013) Post-translational regulation of cold acclimation response. Plant Science, 205-206, 48-54.
Batth, T.S., Francavilla, C. & Olsen, J.V. (2014) Off-line high-pH reversed-phase fractionation for In-depth phosphoproteomics. Journal of Proteome Research, 13, 6176-6186.
Bellafiore, S., Barneche, F., Peltier, G. & Rochaix, J.-D. (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature, 433, 892-895.
Bensimon, A., Heck, A.J.R. & Aebersold, R. (2012) Mass spectrometry-based proteomics and network biology. Annual Review of Biochemistry, 81, 379-405.
Berardini, T.Z., Reiser, L., Li, D., Mezheritsky, Y., Muller, R., Strait, E. et al. (2015) The arabidopsis information resource: making and mining the “gold standard” annotated reference plant genome: Tair: making and mining the “gold standard” Plant Genome. Genesis, 53, 474-485.
Bläsing, O.E., Gibon, Y., Günther, M., Höhne, M., Morcuende, R., Osuna, D. et al. (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell, 17, 3257-3281.
Boersema, P.J., Raijmakers, R., Lemeer, S., Mohammed, S. & Heck, A.J.R. (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nature Protocols, 4, 484-494.
Buchanan, B.B. (1980) Role of light in the regulation of chloroplast enzymes. Annual Review of Plant Physiology, 31, 341-374.
Buchanan, B.B. (2016) The path to thioredoxin and redox regulation in chloroplasts. Annual Review of Plant Biology, 67, 1-24.
Bunney, T.D., Van Walraven, H.S. & De Boer, A.H. (2001) 14-3-3 protein is a regulator of the mitochondrial and chloroplast ATP synthase. Proceedings of the National Academy of Sciences of the United States of America, 98, 4249-4254.
Caldana, C., Martins, M.C.M., Mubeen, U. & Urrea-Castellanos, R. (2019) The magic ‘hammer’ of TOR: the multiple faces of a single pathway in the metabolic regulation of plant growth and development. Journal of Experimental Botany, 70, 2217-2225.
Carrillo, L.R., Froehlich, J.E., Cruz, J.A., Savage, L.J. & Kramer, D.M. (2016) Multi-level regulation of the chloroplast ATP synthase: the chloroplast NADPH thioredoxin reductase C (NTRC) is required for redox modulation specifically under low irradiance. The Plant Journal, 87, 654-663.
Chen, G.-H., Liu, M.-J., Xiong, Y., Sheen, J. & Wu, S.-H. (2018) TOR and RPS6 transmit light signals to enhance protein translation in deetiolating Arabidopsis seedlings. Proceedings. National Academy of Sciences. United States of America, 115, 12823-12828.
Chen, Q., Xiao, Y., Ming, Y., Peng, R., Hu, J., Wang, H. et al. (2022) Quantitative proteomics reveals redox-based functional regulation of photosynthesis under fluctuating light in plants. Journal of Integrative Plant Biology, 64, 2168-2186.
Choudhary, M.K., Nomura, Y., Wang, L., Nakagami, H. & Somers, D.E. (2015) Quantitative circadian phosphoproteomic analysis of Arabidopsis reveals extensive clock control of key components in physiological, metabolic, and signaling pathways*. Molecular & Cellular Proteomics, 14, 2243-2260.
Deutsch, E.W., Csordas, A., Sun, Z., Jarnuczak, A., Perez-Riverol, Y., Ternent, T. et al. (2017) The ProteomeXchange consortium in 2017: supporting the cultural change in proteomics public data deposition. Nucleic Acids Research, 45, D1100-D1106.
Dietz, K.-J. (2015) Efficient high light acclimation involves rapid processes at multiple mechanistic levels. Journal of Experimental Botany, 66, 2401-2414.
Dogra, V., Li, M., Singh, S., Li, M. & Kim, C. (2019) Oxidative post-translational modification of EXECUTER1 is required for singlet oxygen sensing in plastids. Nature Communications, 10, 2834.
Doncheva, N.T., Morris, J.H., Gorodkin, J. & Jensen, L.J. (2019) Cytoscape StringApp: network analysis and visualization of proteomics data. Journal of Proteome Research, 18, 623-632.
Dreaden Kasson, T.M., Rexroth, S. & Barry, B.A. (2012) Light-induced oxidative stress, N-formylkynurenine, and oxygenic photosynthesis R. Subramanyam, ed. PLoS One, 7, e42220.
Dunford, R.P., Durrant, M.C., Catley, M.A. & Dyer, T.A. (1998) Location of the redox-active cysteines in chloroplast sedoheptulose-1,7-bisphosphatase indicates that its allosteric regulation is similar but not identical to that of fructose-1,6-bisphosphatase. Photosynthesis Research, 58, 221-230.
Elsässer, M., Feitosa-Araujo, E., Lichtenauer, S. et al. (2020) Photosynthetic activity triggers pH and NAD redox signatures across different plant cell compartments, Plant Biology. Available from: https://doi.org/10.1101/2020.10.31.363051
Enganti, R., Cho, S.K., Toperzer, J.D., Urquidi-Camacho, R.A., Cakir, O.S., Ray, A.P. et al. (2018) Phosphorylation of ribosomal protein RPS6 integrates light signals and circadian clock signals. Frontiers in Plant Science, 8, 2210.
Fan, J., Shan, C., Kang, H.-B., Elf, S., Xie, J., Tucker, M. et al. (2014) Tyr phosphorylation of PDP1 toggles recruitment between ACAT1 and SIRT3 to regulate the pyruvate dehydrogenase complex. Molecular Cell, 53, 534-548.
Farinas, B. & Mas, P. (2011) Functional implication of the MYB transcription factor RVE8/LCL5 in the circadian control of histone acetylation. The Plant Journal, 66, 318-329.
Finkemeier, I., Goodman, M., Lamkemeyer, P., Kandlbinder, A., Sweetlove, L.J. & Dietz, K.-J. (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. Journal of Biological Chemistry, 280, 12168-12180.
Finkemeier, I., Laxa, M., Miguet, L., Howden, A.J.M. & Sweetlove, L.J. (2011) Proteins of diverse function and subcellular location are lysine acetylated in Arabidopsis. Plant Physiology, 155, 1779-1790.
Flis, A., Fernández, A.P., Zielinski, T., Mengin, V., Sulpice, R., Stratford, K. et al. (2015) Defining the robust behaviour of the plant clock gene circuit with absolute RNA timeseries and open infrastructure. Open Biology, 5, 150042.
Füßl, M., König, A., Eirich, J. et al. (2022) Dynamic light- and acetate-dependent regulation of the proteome and lysine acetylome of Chlamydomonas. The Plant Journal, 109, 261-277.
Gao, X., Hong, H., Li, W.-C., Yang, L., Huang, J., Xiao, Y.-L. et al. (2016) Downregulation of Rubisco activity by non-enzymatic acetylation of RbcL. Molecular Plant, 9, 1018-1027.
Giese, J., Eirich, J., Post, F., Schwarzländer, M. & Finkemeier, I. (2022) Mass Spectrometry-Based Quantitative Cysteine Proteome Profiling of Isolated Using Differential iodoTMT Labeling. In: Van Aken, O. & Rasmusson, A.G. (Eds.) Plant mitochondria. Methods in molecular biology. New York, NY: Springer US, pp. 215-234. Available from: https://doi.org/10.1007/978-1-0716-1653-6_16
Göhre, V. (2015) Immune responses: photosynthetic defence. Nature Plants, 1, 1-2.
Göhre, V., Jones, A.M.E., Sklenář, J., Robatzek, S. & Weber, A.P.M. (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Molecular Plant-Microbe Interactions, 25, 1083-1092.
Graf, A., Coman, D., Uhrig, R.G., Walsh, S., Flis, A., Stitt, M. et al. (2017) Parallel analysis of Arabidopsis circadian clock mutants reveals different scales of transcriptome and proteome regulation. Open Biology, 7, 160333.
Gurrieri, L., Fermani, S., Zaffagnini, M., Sparla, F. & Trost, P. (2021) Calvin-Benson cycle regulation is getting complex. Trends in Plant Science, 26, 898-912.
Hahn, A., Vonck, J., Mills, D.J., Meier, T. & Kühlbrandt, W. (2018) Structure, mechanism, and regulation of the chloroplast ATP synthase. Science, 360, eaat4318.
Hartl, M., Füßl, M., Boersema, P.J., Jost, J.O., Kramer, K., Bakirbas, A. et al. (2017) Lysine acetylome profiling uncovers novel histone deacetylase substrate proteins in Arabidopsis. Molecular Systems Biology, 13, 949.
Heber, U.W. & Santarius, K.A. (1965) Compartmentation and reduction of pyridine nucleotides in relation to photosynthesis. Biochimica et Biophysica Acta (BBA) - Biophysics including Photosynthesis, 109, 390-408.
Hosp, F., Lassowskat, I., Santoro, V., de Vleesschauwer, D., Fliegner, D., Redestig, H. et al. (2017) Lysine acetylation in mitochondria: from inventory to function. Mitochondrion, 33, 58-71.
Huber, J.L., Huber, S.C., Campbell, W.H. & Redinbaugh, M.G. (1992) Reversible light/dark modulation of spinach leaf nitrate reductase activity involves protein phosphorylation. Archives of Biochemistry and Biophysics, 296, 58-65.
Huber, J.L.A., Huber, S.C. & Nielsen, T.H. (1989) Protein phosphorylation as a mechanism for regulation of spinach leaf sucrose-phosphate synthase activity. Archives of Biochemistry and Biophysics, 270, 681-690.
Huber, S.C., Bachmann, M. & Huber, J.L. (1996) Post-translational regulation of nitrate reductase activity: a role for Ca2+ and 14-3-3 proteins. Trends in Plant Science, 1, 432-438.
Huber, S.C. & Huber, J.L. (1991) In vitro phosphorylation and inactivation of spinach leaf sucrose-phosphate synthase by an endogenous protein kinase. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1091, 393-400.
Inoue, S., Kinoshita, T., Matsumoto, M., Nakayama, K.I., Doi, M. & Shimazaki, K. (2008) Blue light-induced autophosphorylation of phototropin is a primary step for signaling. Proceedings of the National Academy of Sciences, 105, 5626-5631.
Kanekatsu, M., Saito, H., Motohashi, K. & Hisabori, T. (1998) The β subunit of chloroplast ATP synthase (CF0CF1-ATPase) is phosphorylated by casein kinase II. IUBMB Life, 46, 99-105.
Kelley, L.A., Mezulis, S., Yates, C.M., Wass, M.N. & Sternberg, M.J.E. (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10, 845-858.
Kim, S.Y., Harvey, C.M., Giese, J., Lassowskat, I., Singh, V., Cavanagh, A.P. et al. (2019) In vivo evidence for a regulatory role of phosphorylation of Arabidopsis Rubisco activase at the Thr78 site. Proceedings of the National Academy of Sciences, 116, 18723-18731.
König, A.-C., Hartl, M., Boersema, P.J., Mann, M. & Finkemeier, I. (2014) The mitochondrial lysine acetylome of Arabidopsis. Mitochondrion, 19, 252-260.
König, A.-C., Pham, P.A., Laxa, M. et al. (2014) The Arabidopsis class II Sirtuin is a lysine deacetylase and interacts with mitochondrial energy metabolism. Plant Physiology, 164, 1401-1414.
Kopka, J., Schauer, N., Krueger, S., Birkemeyer, C., Usadel, B., Bergmuller, E. et al. (2005) GMD@CSB.DB: the Golm metabolome database. Bioinformatics, 21, 1635-1638.
Kosová, K., Vítámvás, P., Urban, M.O., Prášil, I.T. & Renaut, J. (2018) Plant abiotic stress proteomics: the major factors determining alterations in cellular proteome. Frontiers in Plant Science, 9, 122. Available from: https://doi.org/10.3389/fpls.2018.00122/full
Lassowskat, I., Hartl, M., Hosp, F., Boersema, P.J., Mann, M. & Finkemeier, I. (2017) Dimethyl-labeling-based quantification of the lysine acetylome and proteome of plants. In: Fernie, A.R., Bauwe, H. & Weber, A.P.M. (Eds.) Photorespiration: methods and protocols. Methods in molecular biology. New York, NY: Springer, pp. 65-81. Available from: https://doi.org/10.1007/978-1-4939-7225-8_5
Lee, C.P., Eubel, H. & Millar, A.H. (2010) Diurnal changes in mitochondrial function reveal daily optimization of light and dark respiratory metabolism in Arabidopsis. Molecular & Cellular Proteomics, 9, 2125-2139.
Lemaire, S.D., Michelet, L., Zaffagnini, M., Massot, V. & Issakidis-Bourguet, E. (2007) Thioredoxins in chloroplasts. Current Genetics, 51, 343-365.
Lemeille, S., Turkina, M.V., Vener, A.V. & Rochaix, J.-D. (2010) Stt7-dependent phosphorylation during state transitions in the green alga Chlamydomonas reinhardtii*. Molecular & Cellular Proteomics, 9, 1281-1295.
Lendzian, K.J. (1980) Modulation of glucose-6-phosphate dehydrogenase by NADPH, NADP+ and dithiothreitol at variable NADPH/NADP+ ratios in an illuminated reconstituted Spinach (Spinacia oleracea L.) chloroplast system. Planta, 148, 1-6.
Leoni, C., Pietrzykowska, M., Kiss, A.Z., Suorsa, M., Ceci, L.R., Aro, E.-M. et al. (2013) Very rapid phosphorylation kinetics suggest a unique role for Lhcb2 during state transitions in Arabidopsis. The Plant Journal, 76, 236-246.
Li, L., Aro, E.-M. & Millar, A.H. (2018) Mechanisms of photodamage and protein turnover in photoinhibition. Trends in Plant Science, 23, 667-676.
Lindahl, M. & Kieselbach, T. (2009) Disulphide proteomes and interactions with thioredoxin on the track towards understanding redox regulation in chloroplasts and cyanobacteria. Journal of Proteomics, 72, 416-438.
Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. & Fernie, A.R. (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols, 1, 387-396.
Liu, J. & Last, R.L. (2015) A land plant-specific thylakoid membrane protein contributes to photosystem II maintenance in Arabidopsis thaliana. The Plant Journal, 82, 731-743.
Liu, S., Yu, F., Yang, Z., Wang, T., Xiong, H., Chang, C. et al. (2018) Establishment of dimethyl labeling-based quantitative acetylproteomics in Arabidopsis. Molecular & Cellular Proteomics, 17, 1010-1027.
Luedemann, A., von Malotky, L., Erban, A. & Kopka, J. (2012) TagFinder: preprocessing software for the fingerprinting and the profiling of gas chromatography-mass spectrometry based metabolome analyses. In: Hardy, N.W. & Hall, R.D. (Eds.) Plant metabolomics: methods and protocols. Methods in molecular biology. Totowa, NJ: Humana Press, pp. 255-286. Available from: https://doi.org/10.1007/978-1-61779-594-7_16
Mahfouz, M.M., Kim, S., Delauney, A.J. & Verma, D.P.S. (2006) Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell, 18, 477-490.
Mann, M. & Jensen, O.N. (2003) Proteomic analysis of post-translational modifications. Nature Biotechnology, 21, 255-261.
Margalha, L., Confraria, A. & Baena-González, E. (2019) SnRK1 and TOR: modulating growth-defense trade-offs in plant stress responses. Journal of Experimental Botany, 70, 2261-2274.
Marri, L., Zaffagnini, M., Collin, V., Issakidis-Bourguet, E., Lemaire, S.D., Pupillo, P. et al. (2009) Prompt and easy activation by specific thioredoxins of Calvin cycle enzymes of Arabidopsis thaliana associated in the GAPDH/CP12/PRK supramolecular complex. Molecular Plant, 2, 259-269.
Mcmichael, R.W., Klein, R.R., Salvucci, M.E. & Huber, S.C. (1993) Identification of the major regulatory phosphorylation site in sucrose-phosphate synthase. Archives of Biochemistry and Biophysics, 307, 248-252.
Menger, K.E., James, A.M., Cochemé, H.M., Harbour, M.E., Chouchani, E.T., Ding, S. et al. (2015) Fasting, but not aging, dramatically alters the redox status of cysteine residues on proteins in Drosophila melanogaster. Cell Reports, 11, 1856-1865.
Mergner, J., Frejno, M., List, M., Papacek, M., Chen, X., Chaudhary, A. et al. (2020) Mass-spectrometry-based draft of the Arabidopsis proteome. Nature, 579, 409-414.
Mertins, P., Qiao, J.W., Patel, J., Udeshi, N.D., Clauser, K.R., Mani, D.R. et al. (2013) Integrated proteomic analysis of post-translational modifications by serial enrichment. Nature Methods, 10, 634-637.
Meyer, Y., Buchanan, B.B., Vignols, F. & Reichheld, J.-P. (2009) Thioredoxins and glutaredoxins: unifying elements in redox biology. Annual Review of Genetics, 43, 335-367.
Michelet, L., Zaffagnini, M., Morisse, S., Sparla, F., Pérez-Pérez, M.E., Francia, F. et al. (2013) Redox regulation of the Calvin-Benson cycle: something old, something new. Frontiers in Plant Science, 4, 470. Available from: https://doi.org/10.3389/fpls.2013.00470/abstract
Møller, I.M. & Kristensen, B.K. (2006) Protein oxidation in plant mitochondria detected as oxidized tryptophan. Free Radical Biology and Medicine, 40, 430-435.
Nakagami, H. (2014) StageTip-based HAMMOC, an efficient and inexpensive phosphopeptide enrichment method for plant shotgun phosphoproteomics. In: Jorrin-Novo, J.V., Komatsu, S., Weckwerth, W. & Wienkoop, S. (Eds.) Plant proteomics: methods and protocols. Methods in molecular biology. Totowa, NJ: Humana Press, pp. 595-607. Available from: https://doi.org/10.1007/978-1-62703-631-3_40
Nelson, C.J. & Millar, A.H. (2015) Protein turnover in plant biology. Nature Plants, 1, 1-7.
Nietzel, T., Mostertz, J., Ruberti, C., Née, G., Fuchs, P., Wagner, S. et al. (2020) Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination. Proceedings National Academy of Sciences United States of America, 117, 741-751.
Nomura, H., Komori, T., Uemura, S., Kanda, Y., Shimotani, K., Nakai, K. et al. (2012) Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nature Communications, 3, 926.
Okuda, S., Watanabe, Y., Moriya, Y., Kawano, S., Yamamoto, T., Matsumoto, M. et al. (2017) jPOSTrepo: an international standard data repository for proteomes. Nucleic Acids Research, 45, D1107-D1111.
O'Leary, B.M., Scafaro, A.P., Fenske, R., Duncan, O., Ströher, E., Petereit, J. et al. (2020) Rubisco lysine acetylation occurs at very low stoichiometry in mature Arabidopsis leaves: implications for regulation of enzyme function. Biochemical Journal, 477, 3885-3896.
Plaxton, W.C. & Shane, M.W. (2018) The role of post-translational enzyme modifications in the metabolic adaptations of phosphorus-deprived Plants. In: Annual Plant Reviews online. Chichester, UK: John Wiley & Sons, Ltd, pp. 99-123. Available from: https://doi.org/10.1002/9781119312994.apr0519
Porter, M.A. & Hartman, F.C. (1990) Exploration of the function of a regulatory sulfhydryl of phosphoribulokinase from spinach. Archives of Biochemistry and Biophysics, 281, 330-334.
Portis, A.R., Li, C., Wang, D. & Salvucci, M.E. (2007) Regulation of Rubisco activase and its interaction with Rubisco. Journal of Experimental Botany, 59, 1597-1604.
Preiser, A.L., Fisher, N., Banerjee, A. & Sharkey, T.D. (2019) Plastidic glucose-6-phosphate dehydrogenases are regulated to maintain activity in the light. Biochemical Journal, 476, 1539-1551. Available from: https://www.osti.gov/pages/biblio/1607897
Ramazi, S. & Zahiri, J. (2021) Post-translational modifications in proteins: resources, tools and prediction methods. Database: The Journal of Biological Databases and Curation, 2021, baab012. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8040245/
Reiland, S., Messerli, G., Baerenfaller, K., Gerrits, B., Endler, A., Grossmann, J. et al. (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiology, 150, 889-903.
Rocha, A.G., Mehlmer, N., Stael, S., Mair, A., Parvin, N., Chigri, F. et al. (2014) Phosphorylation of Arabidopsis transketolase at Ser428 provides a potential paradigm for the metabolic control of chloroplast carbon metabolism. Biochemical Journal, 458, 313-322.
Román, Á., Li, X., Deng, D., Davey, J.W., James, S., Graham, I.A. et al. (2021) Superoxide is promoted by sucrose and affects amplitude of circadian rhythms in the evening. Proceedings of the National Academy of Sciences, 118, e2020646118. Available from: https://www.pnas.org/content/118/10/e2020646118
Rubin, P.M. & Randall, D.D. (1977) Regulation of plant pyruvate dehydrogenase complex by phosphorylation. Plant Physiology, 60, 34-39.
Rugen, N., Schaarschmidt, F., Braun, H.-P. & Eubel, H. (2020) Protein interaction patterns in Arabidopsis thaliana leaf mitochondria change in response to illumination, Plant Biology. Available from: https://doi.org/10.1101/2020.07.30.222745
Salvucci, M.E., Portis, A.R. & Ogren, W.L. (1985) A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase/oxygenase activation in vivo. Photosynthesis Research, 7, 193-201.
Santarius, K.A. & Heber, U. (1965) Changes in the intracellular levels of ATP, ADP, AMP and Pi and regulatory function of the adenylate system in leaf cells during photosynthesis. Biochimica et Biophysica Acta (BBA) - Biophysics including Photosynthesis, 102, 39-54.
Scheibe, R. & Anderson, L.E. (1981) Dark modulation of NADP-dependent malate dehydrogenase and glucose-6-phosphate dehydrogenase in the chloroplast. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 636, 58-64.
Scheibe, R., Geissler, A. & Fickenscher, K. (1989) Chloroplast glucose-6-phosphate dehydrogenase: Km shift upon light modulation and reduction. Archives of Biochemistry and Biophysics, 274, 290-297.
Schuller, K.A. & Randall, D.D. (1990) Mechanism of pyruvate inhibition of plant pyruvate dehydrogenase kinase and synergism with ADP. Archives of Biochemistry and Biophysics, 278, 211-216.
Schürmann, P. & Buchanan, B.B. (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxidants & Redox Signaling, 10, 1235-1274.
Shannon, P. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research, 13, 2498-2504.
Shapiguzov, A., Ingelsson, B., Samol, I., Andres, C., Kessler, F., Rochaix, J.-D. et al. (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proceedings of the National Academy of Sciences, 107, 4782-4787.
Smith, E.L. (1937) The induction period in photosynthesis. Journal of General Physiology, 21, 151-163.
Sparla, F., Pupillo, P. & Trost, P. (2002) The C-terminal extension of Glyceraldehyde-3-phosphate dehydrogenase subunit B acts as an autoinhibitory domain regulated by thioredoxins and nicotinamide adenine dinucleotide. Journal of Biological Chemistry, 277, 44946-44952.
Staiger, D., Shin, J., Johansson, M. & Davis, S.J. (2013) The circadian clock goes genomic. Genome Biology, 14, 208.
Su, W., Huber, S.C. & Crawford, N.M. (1996) Identification in vitro of a post-translational regulatory site in the hinge 1 region of Arabidopsis nitrate reductase. Plant Cell, 8, 519-527.
Suetsugu, N., Kagawa, T. & Wada, M. (2005) An Auxilin-like J-domain protein, JAC1, regulates phototropin-mediated chloroplast movement in Arabidopsis. Plant Physiology, 139, 151-162.
Sweetlove, L.J., Beard, K.F.M., Nunes-Nesi, A., Fernie, A.R. & Ratcliffe, R.G. (2010) Not just a circle: flux modes in the plant TCA cycle. Trends in Plant Science, 15, 462-470.
Szklarczyk, D., Gable, A.L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J. et al. (2019) STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research, 47, D607-D613.
Tovar-Mendez, A., Miernyk, J.A. & Randall, D.D. (2003) Regulation of pyruvate dehydrogenase complex activity in plant cells. European Journal of Biochemistry, 270, 1043-1049.
Tyanova, S., Temu, T. & Cox, J. (2016) The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nature Protocols, 11, 2301-2319.
Tyanova, S., Temu, T., Sinitcyn, P., Carlson, A., Hein, M.Y., Geiger, T. et al. (2016) The Perseus computational platform for comprehensive analysis of (prote)omics data. Nature Methods, 13, 731-740.
Uhrig, R.G., Echevarría-Zomeño, S., Schlapfer, P., Grossmann, J., Roschitzki, B., Koerber, N. et al. (2021) Diurnal dynamics of the Arabidopsis rosette proteome and phosphoproteome. Plant, Cell & Environment, 44, 821-841.
Uhrig, R.G., Schläpfer, P., Roschitzki, B., Hirsch-Hoffmann, M. & Gruissem, W. (2019) Diurnal changes in concerted plant protein phosphorylation and acetylation in Arabidopsis organs and seedlings. The Plant Journal, 99, 176-194.
Usadel, B., Poree, F., Nagel, A., Lohse, M., Czedik-Eysenberg, A. & Stitt, M. (2009) A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant, Cell & Environment, 32, 1211-1229.
Vu, L.D., Gevaert, K. & De Smet, I. (2018) Protein language: post-translational modifications talking to each other. Trends in Plant Science, 23, 1068-1080.
Wang, P., Zhao, Y., Li, Z., Hsu, C.C., Liu, X., Fu, L. et al. (2018) Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Molecular Cell, 69, 100-112.e6.
Werdan, K., Heldt, H.W. & Milovancev, M. (1975) The role of pH in the regulation of carbon fixation in the chloroplast stroma. Studies on CO2 fixation in the light and dark. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 396, 276-292.
Willems, P., Horne, A., Van Parys, T., Goormachtig, S., De Smet, I., Botzki, A. et al. (2019) The plant PTM viewer, a central resource for exploring plant protein modifications. The Plant Journal, 99, 752-762.
Willig, A., Shapiguzov, A., Goldschmidt-Clermont, M. & Rochaix, J.-D. (2011) The phosphorylation status of the chloroplast protein kinase STN7 of Arabidopsis affects its turnover. Plant Physiology, 157, 2102-2107.
Wirtz, W., Stitt, M. & Heldt, H.W. (1982) Light activation of Calvin cycle enzymes as measured in pea leaves. FEBS Letters, 142, 223-226.
Witze, E.S., Old, W.M., Resing, K.A. & Ahn, N.G. (2007) Mapping protein post-translational modifications with mass spectrometry. Nature Methods, 4, 798-806.
Wolosiuk, R.A. & Buchanan, B.B. (1977) Thioredoxin and glutathione regulate photosynthesis in chloroplasts. Nature, 266, 565-567.
Wu, G. & Ort, D.R. (2008) Mutation in the cysteine bridge domain of the γ-subunit affects light regulation of the ATP synthase but not photosynthesis or growth in Arabidopsis. Photosynthesis Research, 97, 185-193.
Wunder, T., Liu, Q., Aseeva, E., Bonardi, V., Leister, D. & Pribil, M. (2013) Control of STN7 transcript abundance and transient STN7 dimerisation are involved in the regulation of STN7 activity. Planta, 237, 541-558.
Yin, Z.-H., Neimanis, S., Wagner, U. & Heber, U. (1990) Light-dependent pH changes in leaves of C3 plants: I. Recording pH changes in various cellular compartments by fluorescent probes. Planta, 182, 244-252.
Zabala, T., De, M., Littlejohn, G., Jayaraman, S. et al. (2015) Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nature Plants, 1, 1-10.
Zhang, N., Meng, Y., Li, X., Zhou, Y., Ma, L., Fu, L. et al. (2019) Metabolite-mediated TOR signaling regulates the circadian clock in Arabidopsis. Proceedings National Academy of Sciences United States of America, 116, 25395-25397.
Zhang, N. & Portis, A.R. (1999) Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proceedings of the National Academy of Sciences, 96, 9438-9443.
Zhang, Y., Giese, J., Kerbler, S.M., Siemiatkowska, B., Perez de Souza, L., Alpers, J. et al. (2021) Two mitochondrial phosphatases, PP2c63 and Sal2, are required for posttranslational regulation of the TCA cycle in Arabidopsis. Molecular Plant, 14, 1104-1118.
Zhang, Y., Krahnert, I., Bolze, A., Gibon, Y. & Fernie, A.R. (2020) Adenine nucleotide and nicotinamide adenine dinucleotide measurements in plants. Current Protocols in Plant Biology, 5, e20115. Available from: https://doi.org/10.1002/cppb.20115
Zimmer, D., Swart, C., Graf, A., Arrivault, S., Tillich, M., Proost, S. et al. (2021) Topology of the redox network during induction of photosynthesis as revealed by time-resolved proteomics in tobacco. Science Advances, 7, eabi8307.