Photorespiration in plant adaptation to environmental changes

Abstract

Photorespiration begins with the oxygenation reaction catalyzed by 1,5-bisphosphate carboxylase/oxygenase (Rubisco) and serves as a repair pathway for carbon retrieval by converting 2-phosphoglycolate to 3-phosphogly-cerate allowing plants to thrive in an oxygen-rich environment. Photorespiration metabolism is intimately linked to plant primary metabolism, particularly carbon and nitrogen assimilation, and cellular redox equilibrium, and such interactions are dynamically regulated by environmental changes. Although the basic genetics and biochemistry of photorespiration have been well characterized, it is still essential to further improve our understanding of the regulatory mechanisms of photorespiration and the roles in responding to changing environments, which are required for the future genetic manipulation of photorespiration. Here, we summarize recent progress regarding the evolutionary aspects of photorespiration and its multifaceted regulation, highlighting its intricate interactions with environmental CO₂, light, and nitrogen nutrition. This review provides a comprehensive perspective on the functional implications of photorespiration for plants to adapt to the environment and opens new avenues for our in-depth exploration of photorespiration to develop better strategies to enhance plant productivity and adaptability in the face of changing environmental conditions.

Keywords

Carbon dioxide / Environmental change / Fluctuating light / Nitrogen assimilation / Photorespiration

Abbreviations

2-PG: 2-phosphoglycolate

C_a: ambient CO₂

C_c: CO₂ inside the chloroplast

DCT: dicarboxylate transporter

GDC: glycine decarboxylase complex

GGAT: glutamate:glyoxylate aminotransferase

GLO: glycolate oxidase

GLYK: glycerate 3-kinase

g_m: mesophyll conductance

GOGAT: ferredoxindependent glutamate synthase

GS: glutamine synthetase

g_s: stomatal conductance

HPR: hydroxypyruvate reductase

MDH: malate dehydrogenase

OMT: 2-OG/malate transporter (or malate/OAA transporter)

PGLP: 2-PG phosphatase

PTMs: post-translational modifications

r_m: mesophyll resistance

Rubisco: ribulose 1,5-bisphosphate (RuBP) carboxylase/oxygenase

S_c/o: specificity factor value

SGAT: serine:glyoxylate aminotransferase

TCA: tricarboxylic acid cycle

V_c: rate of Rubisco carboxylation

V_o: rate of Rubisco oxygenation

Availability of data and materials

Not applicable.

Authors’ contributions

Z.Z., G.Z., and X.P.: writing manuscript; Z.Z. and G.Z.: funding acquisition; Z.Z. and X.P.: writing, reviewing, and editing; X.P.: supervision.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We are thankful for the funding provided by the Double First-Class Discipline Promotion Project (2023B10564004) and National Natural Science Foundation of China (32070265, 32270252).

References

[1] Andrews, M., Condron, L.M., Kemp, P.D., Topping, J.F., Lindsey, K., Hodge, S., Raven, J.A., 2019. Elevated CO₂ effects on nitrogen assimilation and growth of C₃ vascular plants are similar regardless of N-form assimilated. J. Exp. Bot. 70, 683-690.

[2] Aranjuelo, I., Cabrerizo, P.M., Arrese-Igor, C., Aparicio-Tejo, P.M., 2013. Pea plant responsiveness under elevated [CO₂] is conditioned by the N source (N2 fixation versus NO₃ fertilization). Environ. Exp. Bot. 95, 34-40.

[3] Aroca, A., García-Díaz, I., García-Caldero, n, M., Gotor, C., M, arquez, A.J., Betti, M., 2023. Photorespiration: regulation and new insights on the potential role of persulfidation. J. Exp. Bot. 74, 6023-6039.

[4] Ashida, H., Danchin, A., Yokota, A., 2005. Was photosynthetic RuBisCO recruited by acquisitive evolution from RuBisCO-like proteins involved in sulfur metabolism? Res. Microbiol. 156, 611-618.

[5] Badger, M.R., Bek, E.J., 2008. Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO₂ acquisition by the CBB cycle. J. Exp. Bot. 59, 1525-1541.

[6] Bartsch, O., Mikkat, S., Hagemann, M., Bauwe, H., 2010. An autoinhibitory domain confers redox regulation to maize glycerate kinase. Plant Physiol. 153, 832-840.

[7] Bauwe, H., 2023. Photorespiration - Rubisco’s repair crew. J. Plant Physiol. 280, 153899.

[8] Bauwe, H., Hagemann, M., Fernie, A.R., 2010. Photorespiration: players, partners and origin. Trends Plant Sci. 15, 330-336.

[9] Bauwe, H., Hagemann, M., Kern, R., Timm, S., 2012. Photorespiration has a dual origin and manifold links to central metabolism. Curr. Opin. Plant Biol. 15, 269-275.

[10] Bloom, A.J., 2015. Photorespiration and nitrate assimilation: a major intersection between plant carbon and nitrogen. Photosynth. Res. 123, 117-128.

[11] Bloom, A.J., Burger, M., Asensio, J.S.R., Cousins, A.B., 2010. Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328, 899-903.

[12] Bloom, A.J., Smart, D.R., Nguyen, D.T., Searles, P.S., 2002. Nitrogen assimilation and growth of wheat under elevated carbon dioxide. Proc. Natl. Acad. Sci. U. S. A. 99, 1730-1735.

[13] Buchanan, B.B., 2016. The path to thioredoxin and redox regulation in chloroplasts. Annu. Rev. Plant Biol. 67, 1-24.

[14] Buckley, T.N., 2019. How do stomata respond to water status? New Phytol. 224, 21-36.

[15] Buckley, T.N., Mott, K.A., Farquhar, G.D., 2003. A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ. 26, 1767-1785.

[16] Buick, R., 2008. When did oxygenic photosynthesis evolve? Philos. Trans. R. Soc. B 363, 2731-2743.

[17] Bunce, J.A., 1988. Effects of boundary layer conductance on substomatal pressures of carbon dioxide. Plant Cell Environ. 11, 205-208.

[18] Busch, F.A., 2014. Opinion: the red-light response of stomatal movement is sensed by the redox state of the photosynthetic electron transport chain. Photosynth. Res. 119, 131-140.

[19] Busch, F.A., 2020. Photorespiration in the context of Rubisco biochemistry, CO₂ diffusion and metabolism. Plant J. 101, 919-939.

[20] Busch, F.A., Sage, R.F., Farquhar, G.D., 2018. Plants increase CO₂ uptake by assimilating nitrogen via the photorespiratory pathway. Nat. Plants 4, 46-54.

[21] Caemmerer, S.V., Evans, J.R., 1991. Determination of the average partial pressure of CO₂ in chloroplasts from leaves of several C₃ plants. Funct. Plant Biol. 18, 287-305.

[22] Campbell, W.J., Ogren, W.L., 1990. Glyoxylate inhibition of ribulosebisphosphate carboxylase/oxygenase activation in intact, lysed, and reconstituted chloroplasts. Photosynth. Res. 23, 257-268.

[23] Collatz, G.J., Ball, J.T., Grivet, C., Berry, J.A., 1991. Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer. Agric. For. Meteorol. 54, 107-136.

[24] Cui, L., Lu, Y., Li, Y., Yang, C., Peng, X., 2016. Overexpression of glycolate oxidase confers improved photosynthesis under high light and high temperature in rice. Front. Plant Sci. 7, 1165.

[25] da Fonseca-Pereira, P., Souza, P.V.L., Fernie, A.R., Timm, S., Daloso, D.M., Araújo, W.L., 2021. Thioredoxin-mediated regulation of (photo)respiration and central metabolism. J. Exp. Bot. 72, 5987-6002.

[26] da Fonseca-Pereira, P., Souza, P.V.L., Hou, L., Schwab, S., Geigenberger, P., Nunes- Nesi, A., Timm, S., Fernie, A.R., Thorm€ahlen, I., Araújo, W.L., Daloso, D.M., 2020. Thioredoxin h2contributes to the redox regulation of mitochondrial photorespiratory metabolism. Plant Cell Environ. 43, 188-208.

[27] Dao, O., Kuhnert, F., Weber, A.P.M., Peltier, G., Li-Beisson, Y., 2022. Physiological functions of malate shuttles in plants and algae. Trends Plant Sci. 27, 488-501.

[28] Douce, R., Neuburger, M., 1999. Biochemical dissection of photorespiration. Curr. Opin. Plant Biol. 2, 214-222.

[29] Ehlers, I., Augusti, A., Betson, T.R., Nilsson, M.B., Marshall, J.D., Schleucher, J., 2015. Detecting long-term metabolic shifts using isotopomers:CO₂-driven suppression of photorespiration in C₃ plants over the 20th century. Proc. Natl. Acad. Sci. U. S. A. 112, 15585-15590.

[30] Eisenhut, M., Ruth, W., Haimovich, M., Bauwe, H., Kaplan, A., Hagemann, M., 2008. The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proc. Natl. Acad. Sci. U. S. A. 105, 17199-17204.

[31] Fair, P., Tew, J., Cresswell, C.F., 1973. Enzyme activities associated with carbon dioxide exchange in illuminated leaves of Hordeum vulgare L. II. Effects of external concentrations of carbon dioxide and oxygen. Ann. Bot. 37, 1035-1039.

[32] Fair, P., Tew, J., Cresswell, C.F., 1974. Enzyme activities associated with carbon dioxide exchange in illuminated leaves of Hordeum vulgare L. IV. The effect of light intensity on the carbon dioxide compensation point. Ann. Bot. 38, 45-52.

[33] Fischer, R.A., Rees, D., Sayre, K.D., Lu, Z.M., Condon, A.G., Saavedra, A.L., 1998. Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Sci. 38, 1467-1475.

[34] Flexas, J., Ribas-Carbó, M., Diaz-Espejo, A., Galmés, J., Medrano, H., 2008. Mesophyll conductance to CO₂: current knowledge and future prospects. Plant Cell Environ. 31, 602-621.

[35] Flügel, F., Timm, S., Arrivault, S., Florian, A., Stitt, M., Fernie, A.R., Bauwe, H., 2017. The photorespiratory metabolite 2-phosphoglycolate regulates photosynthesis and starch accumulation in arabidopsis. Plant Cell 29, 2537-2551.

[36] Foyer, C.H., Bloom, A.J., Queval, G., Noctor, G., 2009. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu. Rev. Plant Biol. 60, 455-484.

[37] Fu, X., Walker, B.J., 2023. Dynamic response of photorespiration in fluctuating light environments. J. Exp. Bot. 74, 600-611.

[38] Fu, Z., Ding, F., Zhang, B., Liu, W., Huang, Z., Fan, S., Feng, Y., Lu, Y., Hua, W., 2024. Hydrogen peroxide sulfenylates and inhibits the photorespiratory enzyme PGLP1 to modulate plant thermotolerance. Plant Commun. 5, 100852.

[39] Geigenberger, P., Thorm€ahlen, I., Daloso, D.M., Fernie, A.R., 2017. The unprecedented versatility of the plant thioredoxin system. Trends Plant Sci. 22, 249-262.

[40] Giordano, M., Beardall, J., Raven, J.A., 2005. CO₂ concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56, 99-131.

[41] Hagemann, M., Bauwe, H., 2016. Photorespiration and the potential to improve photosynthesis. Curr. Opin. Chem. Biol. 35, 109-116.

[42] Hagemann, M., Fernie, A.R., Espie, G.S., Kern, R., Eisenhut, M., Reumann, S., Bauwe, H., Weber, A.P.M., Rennenberg, H., 2013. Evolution of the biochemistry of the photorespiratory C₂ cycle. Plant Biol. 15, 639-647.

[43] Hagemann, M., Kern, R., Maurino, V.G., Hanson, D.T., Weber, A.P.M., Sage, R.F., Bauwe, H., 2016. Evolution of photorespiration from cyanobacteria to land plants, considering protein phylogenies and acquisition of carbon concentrating mechanisms. J. Exp. Bot. 67, 2963-2976.

[44] Hodges, M., 2022. Photorespiration and improving photosynthesis. In: Lüttge, U., C,anovas, F.M., Risueño, M.C., Leuschner, C., Pretzsch, H. (Eds.), Progress in Botany, Vol. 84. Springer, Cham, Switzerland, pp. 171-219.

[45] Hodges, M., Dellero, Y., Keech, O., Betti, M., Raghavendra, A.S., Sage, R., Zhu, X., Allen, D.K., Weber, A.P.M., 2016. Perspectives for a better understanding of the metabolic integration of photorespiration within a complex plant primary metabolism network. J. Exp. Bot. 67, 3015-3026.

[46] Huang, W., Hu, H., Zhang, S., 2015. Photorespiration plays an important role in the regulation of photosynthetic electron flow under fluctuating light in tobacco plants grown under full sunlight. Front. Plant Sci. 6, 621.

[47] Huang, W., Yang, Y., Wang, J., Hu, H., 2019. Photorespiration is the major alternative electron sink under high light in alpine evergreen sclerophyllous rhododendron species. Plant Sci. 289, 110275.

[48] Igamberdiev, A.U., Bykova, N.V., Lea, P.J., Gardestro€m, P., 2001. The role of photorespiration in redox and energy balance of photosynthetic plant cells: A study with a barley mutant deficient in glycine decarboxylase. Physiol. Plant. 111, 427-438.

[49] Igamberdiev, A.U., Lea, P.J., 2002. The role of peroxisomes in the integration of metabolism and evolutionary diversity of photosynthetic organisms. Phytochemistry 60, 651-674.

[50] Igamberdiev, A.U., Lea, P.J., 2006. Land plants equilibrate O2 and CO₂ concentrations in the atmosphere. Photosynth. Res. 87, 177-194.

[51] James, D.B., Smith, S.M., 1979. Glycollate as a reductant source for nitrate reductase activity. In: Hewitt, E.J., Cutting, C.V. (Eds.), Nitrogen Assimilation of Plants. Academic Press, New York, U.S.A., pp.579-581

[52] Kebeish, R., Niessen, M., Thiruveedhi, K., Bari, R., Hirsch, H.J., Rosenkranz, R., St€abler, N., Scho€nfeld, B., Kreuzaler, F., Peterh€ansel, C., 2007. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat. Biotechnol. 25, 593-599.

[53] Keech, O., Gardestro€m, P., Kleczkowski, L.A., Rouhier, N., 2017. The redox control of photorespiration: from biochemical and physiological aspects to biotechnological considerations. Plant Cell Environ. 40, 553-569.

[54] Kern, R., Bauwe, H., Hagemann, M., 2011. Evolution of enzymes involved in the photorespiratory 2-phosphoglycolate cycle from cyanobacteria via algae toward plants. Photosynth. Res. 109, 103-114.

[55] Kimura, H., Hashimoto-Sugimoto, M., Iba, K., Terashima, I., Yamori, W., 2020. Improved stomatal opening enhances photosynthetic rate and biomass production in fluctuating light. J. Exp. Bot. 71, 2339-2350.

[56] Kinoshita, H., Nagasaki, J., Yoshikawa, N., Yamamoto, A., Takito, S., Kawasaki, M., Sugiyama, T., Miyake, H., Weber, A.P.M., Taniguchi, M., 2011. The chloroplastic 2- oxoglutarate/malate transporter has dual function as the malate valve and in carbon/ nitrogen metabolism. Plant J. 65, 15-26.

[57] Kleczkowski, L.A., Randall, D.D., 1985. Light and thiol activation of maize leaf glycerate kinase: the stimulating effect of reduced thioredoxins and ATP. Plant Physiol. 79, 274-277.

[58] Krämer, K., Kepp, G., Brock, J., Stutz, S., Heyer, A.G., 2022. Acclimation to elevated CO₂ affects the C/N balance by reducing de novo N-assimilation. Physiol. Plant. 174, e13615.

[59] Laxa, M., Fromm, S., 2018. Co-expression and regulation of photorespiratory genes in Arabidopsis thaliana: A bioinformatic approach. Curr. Plant Biol. 14, 2-18.

[60] Li, J., Weraduwage, S.M., Preiser, A.L., Tietz, S., Weise, S.E., Strand, D.D., Froehlich, J.E., Kramer, D.M., Hu, J., Sharkey, T.D., 2019. A cytosolic bypass and G6P shunt in plants lacking peroxisomal hydroxypyruvate reductase. Plant Physiol. 180, 783-792.

[61] Li, M., 1988. Relationship between the photorespiration and nitrate reduction. Acta Phytopathol. Sin. 14, 98-102.

[62] Liang, Y., Wang, J., Zeng, F., Wang, Q., Zhu, L., Li, H., Guo, N., Chen, H., 2021. Photorespiration regulates carbon-nitrogen metabolism by magnesium chelatase D subunit in rice. J. Agric. Food Chem. 69, 112-125.

[63] Lim, S.L., Voon, C.P., Guan, X., Yang, Y., Gardestrom, P., Lim, B.L., 2020. In planta study of photosynthesis and photorespiration using NADPH and NADH/NADþ fluorescent protein sensors. Nat. Commun. 11, 3238.

[64] Liu, X., Hu, B., Chu, C., 2022. Nitrogen assimilation in plants: current status and future prospects. J. Genet. Genomics 49, 394-404.

[65] Lu, Y., Li, Y., Yang, Q., Zhang, Z., Chen, Y., Zhang, S., Peng, X., 2014. Suppression of glycolate oxidase causes glyoxylate accumulation that inhibits photosynthesis through deactivating Rubisco in rice. Physiol. Plant. 150, 463-476.

[66] Mano, S., Hayashi, M., Nishimura, M., 1999. Light regulates alternative splicing of hydroxypyruvate reductase in pumpkin. Plant J. 17, 309-320.

[67] Maurino, V.G., Peterhansel, C., 2010. Photorespiration: current status and approaches for metabolic engineering. Curr. Opin. Plant Biol. 13, 248-255.

[68] McAusland, L., Vialet-Chabrand, S., Davey, P., Baker, N.R., Brendel, O., Lawson, T., 2016. Effects of kinetics of light-induced stomatal responses on photosynthesis and water- use efficiency. New Phytol. 211, 1209-1220.

[69] Michelet, L., Zaffagnini, M., Morisse, S., Sparla, F., P, erez-P, erez, M.E., Francia, F., Danon, A., Marchand, C.H., Fermani, S., Trost, P., Lemaire, S.D., 2013. Redox regulation of the Calvin-Benson cycle: something old, something new. Front. Plant Sci. 4, 470.

[70] Mooney, B.P., Miernyk, J.A., Randall, D.D., 2002. The complex fate of alpha-ketoacids. Annu. Rev. Plant Biol. 53, 357-375.

[71] Muller, M., Munne-Bosch, S., 2021. Hormonal impact on photosynthesis and photoprotection in plants. Plant Physiol. 185, 1500-1522.

[72] Nakamura, T., Osaki, M., Shinano, T., Tadano, T., 1997. Difference in system of current photosynthesized carbon distribution to carbon and nitrogen compounds between rice and soybean. Soil Sci. Plant Nutr. 43, 777-788.

[73] Niedermaier, S., Schneider, T., Bahl, M., Matsubara, S., Huesgen, P.F., 2020. Photoprotective acclimation of the arabidopsis thaliana leaf proteome to fluctuating light. Front. Genet. 11, 154.

[74] Okuda, A., Ida, S., 1966. Assimilation of ammonia, nitrate, and urea by chlorella ellipsoidea. Soil Sci. Plant Nutr. 12, 23-30.

[75] Oliver, D.J., Neuburger, M., Bourguignon, J., Douce, R., 1990. Interaction between the component enzymes of the glycine decarboxylase multienzyme complex. Plant Physiol. 94, 833-839.

[76] Orea, A., Pajuelo, P., Pajuelo, E., Quidiello, C., Romero, J.M., M, arquez, A.J., 2002. Isolation of photorespiratory mutants from lotus japonicus deficient in glutamine synthetase. Physiol. Plant 115, 352-361.

[77] Pachauri, R.K., Allen, M.R., Barros, V.R., Broome, J., Cramer, W., Christ, R., Church, J.A., Clarke, L., Dahe, Q., Dasgupta, P., 2014. Climate Change 2014:Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC.

[78] Pérez-Delgado, C.M., García-Caldero, n, M., S, anchez, D.H., Udvardi, M.K., Kopka, J., M, arquez, A.J., Betti, M., 2013. Transcriptomic and metabolic changes associated with photorespiratory ammonium accumulation in the model legume lotus japonicus. Plant Physiol. 162, 1834-1848.

[79] Peterhansel, C., Horst, I., Niessen, M., Blume, C., Kebeish, R., Kürkcüoglu, S., Kreuzaler, F., 2010. Photorespiration. Arabidopsis Book 8, e130.

[80] Plaut, Z., Littan, A., 1974. Interaction between photosynthetic CO₂ fixation products and nitrate reduction in spinach and wheat leaves. In: Avron, M. (Ed.), Proceedings of the 3rd International Congress on Photosynthesis. Elsevier, Amsterdam, pp. 1507-1516.

[81] Rachmilevitch, S., Cousins, A.B., Bloom, A.J., 2004. Nitrate assimilation in plant shoots depends on photorespiration. Proc. Natl. Acad. Sci. U. S. A. 101, 11506-11510.

[82] Reich, P.B., Hobbie, S.E., Lee, T., Ellsworth, D.S., West, J.B., Tilman, D., Knops, J.M.H., Naeem, S., Trost, J., 2006. Nitrogen limitation constrains sustainability of ecosystem response to CO₂. Nature 440, 922-925.

[83] Reinholdt, O., Schwab, S., Zhang, Y., Reichheld, J., Fernie, A.R., Hagemann, M., Timm, S., 2019. Redox-regulation of photorespiration through mitochondrial thioredoxin o1. Plant Physiol. 181, 442-457.

[84] Renne, P., Dressen, U., Hebbeker, U., Hille, D., Flugge, U.I., Westhoff, P., Weber, A.P., 2003. The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator dit2. Plant J. 35, 316-331.

[85] Rosa-T, ellez, S., Alc, antara-Enguídanos, A., Martínez-Seidel, F., Casatejada-Anchel, R., Saeheng, S., Bailes, C.L., Erban, A., Barbosa-Medeiros, D., Alepúz, P., Matus, J.T., Kopka, J., Munoz-Bertomeu, J., Krueger, S., Roje, S., Fernie, A.R., Ros, R., 2024. The serine-glycine-one-carbon metabolic network orchestrates changes in nitrogen and sulfur metabolism and shapes plant development. Plant Cell 36, 404-426.

[86] Rubio-Asensio, J.S., Bloom, A.J., 2017. Inorganic nitrogen form: a major player in wheat and Arabidopsis responses to elevated CO₂. J. Exp. Bot. 68, 2611-2625.

[87] Schneider, T., Bolger, A., Zeier, J., Preiskowski, S., Benes, V., Trenkamp, S., Usadel, B., Farre, E.M., Matsubara, S., 2019. Fluctuating light interacts with time of day and leaf development stage to reprogram gene expression. Plant Physiol. 179, 1632-1657.

[88] Schneidereit, J., H€ausler, R.E., Fiene, G., Kaiser, W.M., Weber, A.P.M., 2006. Antisense repression reveals a crucial role of the plastidic 2-oxoglutarate/malate translocator dit 1 at the interface between carbon and nitrogen metabolism. Plant J. 45, 206-224.

[89] Shen, B., Wang, L., Lin, X., Yao, Z., Xu, H., Zhu, C., Teng, H., Cui, L., Liu, E, Zhang, J., He, Z., Peng, X., 2019. Engineering a new chloroplastic photorespiratory bypass to increase photosynthetic efficiency and productivity in rice. Mol. Plant 12, 199-214.

[90] Shi, Q., Sun, H., Timm, S., Zhang, S., Huang, W., 2022. Photorespiration alleviates photoinhibition of photosystem I under fluctuating light in tomato. Plants 11, 195.

[91] Shih, P.M., Occhialini, A., Cameron, J.C., Andralojc, P.J., Parry, M.A.J., Kerfeld, C.A., 2016. Biochemical characterization of predicted Precambrian RuBisCO. Nat. Commun. 7, 10382.

[92] Slattery, R.A., Walker, B.J., Weber, A., Ort, D.R., 2018. The impacts of fluctuating light on crop performance. Plant Physiol. 176, 990-1003.

[93] South, P.F., Cavanagh, A.P., Liu, H.W., Ort, D.R., 2019. Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363, eaat9077.

[94] Stitt, M., Krapp, A., 1999. The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ. 22, 583-621.

[95] Sunil, B., Saini, D., Bapatla, R.B., Aswani, V., Raghavendra, A.S., 2019. Photorespiration is complemented by cyclic electron flow and the alternative oxidase pathway to optimize photosynthesis and protect against abiotic stress. Photosynth. Res. 139, 67-79.

[96] Sweetlove, L.J., Beard, K.F., Nunes-Nesi, A., Fernie, A.R., Ratcliffe, R.G., 2010. Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci. 15, 462-470.

[97] Tabita, F.R., Hanson, T.E., Li, H., Satagopan, S., Singh, J., Chan, S., 2007. Function, structure, and evolution of the rubisco-like proteins and their rubisco homologs. Microbiol. Mol. Biol. Rev. 71, 576-599.

[98] Takatani, N., Ito, T., Kiba, T., Mori, M., Miyamoto, T., Maeda, S., Omata, T., 2014. Effects of high CO₂ on growth and metabolism of Arabidopsis seedlings during growth with a constantly limited supply of nitrogen. Plant Cell Physiol. 55, 281-292.

[99] Tanaka, Y., Adachi, S., Yamori, W., 2019. Natural genetic variation of the photosynthetic induction response to fluctuating light environment. Curr. Opin. Plant Biol. 49, 52-59.

[100] Taniguchi, M., Miyake, H., 2012. Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism. Curr. Opin. Plant Biol. 15, 252-260.

[101] Taylor, S.H., Long, S.P., 2017. Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21% of productivity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372.

[102] Tcherkez, G.G., Farquhar, G.D., Andrews, T.J., 2006. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc. Natl. Acad. Sci. U. S. A. 103, 7246-7251.

[103] Tholen, D., Ethier, G., Genty, B., Pepin, S., Zhu, X.G., 2012. Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ. 35, 2087-2103.

[104] Timm, S., 2020. The impact of photorespiration on plant primary metabolism through metabolic and redox regulation. Biochem. Soc. Trans. 48, 2495-2504.

[105] Timm, S., Alexandra, F., Maria, W., Kathrin, J., Martin, H., Alisdair R, F., Hermann, B., 2013. Serine acts as a metabolic signal for the transcriptional control of photorespiration-related genes in Arabidopsis. Plant Physiol. 162, 379-389.

[106] Timm, S., Florian, A., Arrivault, S., Stitt, M., Fernie, A.R., Bauwe, H., 2012. Glycine decarboxylase controls photosynthesis and plant growth. FEBS Lett. 586, 3692-3697.

[107] Timm, S., Florian, A., Fernie, A.R., Bauwe, H., 2016. The regulatory interplay between photorespiration and photosynthesis. J. Exp. Bot. 67, 2923-2929.

[108] Timm, S., Hagemann, M., 2020. Photorespiration - how is it regulated and how does it regulate overall plant metabolism? J. Exp. Bot. 71, 3955-3965.

[109] Timm, S., Woitschach, F., Heise, C., Hagemann, M., Bauwe, H., 2019. Faster removal of 2- phosphoglycolate through photorespiration improves abiotic stress tolerance of Arabidopsis. Plants 8, 563.

[110] Ushijima, T., Hanada, K., Gotoh, E., Yamori, W., Kodama, Y., Tanaka, H., Kusano, M., Fukushima, A., Tokizawa, M., Yamamoto, Y.Y., Tada, Y., Suzuki, Y., Matsushita, T., 2017. Light controls protein localization through phytochrome-mediated alternative promoter selection. Cell 171, 1316-1325.

[111] Valentini, R., Epron, D., Angelis, P., Matteucci, G., Dreyer, E., 1995. In situ estimation of net CO₂ assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. Cerris L.) leaves: diurnal cycles under different levels of water supply. Plant Cell Environ. 18, 631-640.

[112] von Bismarck, T., Wendering, P., de Souza, L.P, Ruß, J., Strandberg, L., Heyneke, E., Walker, B.J., Scho€ttler, M.A., Fernie, A.R., Nikoloski, Z., Armbruster, U., 2023. Growth in fluctuating light buffers plants against photorespiratory perturbations. Nat. Commun. 14, 7052.

[113] Voss, I., Sunil, B., Scheibe, R., Raghavendra, A.S., 2013. Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biol. 15, 713-722.

[114] Walker, B.J., Strand, D.D., Kramer, D.M., Cousins, A.B., 2014. The response of cyclic electron flow around photosystem I to changes in photorespiration and nitrate assimilation. Plant Physiol. 165, 453-462.

[115] Walker, B.J., VanLoocke, A., Bernacchi, C.J., Ort, D.R., 2016. The costs of photorespiration to food production now and in the future. Annu. Rev. Plant Biol. 67, 107-129.

[116] Wallsgrove, R.M., Keys, A.J., Lea, P.J., Miflin, B.J., 1983. Photosynthesis, photorespiration and nitrogen metabolism. Plant Cell Environ. 6, 301-309.

[117] Wang, L., Shen, B., Li, B., Zhang, C., Lin, M., Tong, P., Cui, L., Zhang, Z., Peng, X., 2020. A synthetic photorespiratory shortcut enhances photosynthesis to boost biomass and grain yield in rice. Mol. Plant 13, 1802-1815.

[118] Wang, Y., Cheng, Y., Chen, K., Tsay, Y., 2018. Nitrate transport, signaling, and use efficiency. Annu. Rev. Plant Biol. 69, 85-122.

[119] Wang, Z., Wang, Y., Wang, Y., Li, H., Wen, Z., Hou, X., 2022. HPR1 is required for high light intensity induced photorespiration in Arabidopsis thaliana. Int. J. Mol. Sci. 23, 4444.

[120] Wong, S.C., Cowan, I.R., Farquhar, G.D., 1978. Leaf conductance in relation to assimilation in Eucalyptus pauciflora sieb. ex spreng: influence of irradiance and partial pressure of carbon dioxide. Plant Physiol. 62, 670-674.

[121] Woo, K.C., Jokinen, M., Canvin, D.T., 1980. Reduction of nitrate via a dicarboxylate shuttle in a reconstituted system of supernatant and mitochondria from spinach leaves. Plant Physiol. 65, 433-436.

[122] Xu, Z., Guo, W., Mo, B., Pan, Q., Lu, J., Wang, Z., Peng, X., Zhang, Z., 2023. Mitogen- activated protein kinase 2 specifically regulates photorespiration in rice. Plant Physiol. 193, 1381-1394.

[123] Yin, X., Busch, F.A., Struik, P.C., Sharkey, T.D., 2021. Evolution of a biochemical model of steady-state photosynthesis. Plant Cell Environ. 44, 2811-2837.

[124] Zamani-Nour, S., Lin, H., Walker, B.J., Mettler-Altmann, T., Khoshravesh, R., Karki, S., Bagunu, E., Sage, T.L., Quick, W.P., Weber, A.P.M., 2021. Overexpression of the chloroplastic 2-oxoglutarate/malate transporter disturbs carbon and nitrogen homeostasis in rice. J. Exp. Bot. 72, 137-152.

[125] Zhang, Z., Mao, X., Ou, J., Ye, N., Zhang, J., Peng, X., 2015. Distinct photorespiratory reactions are preferentially catalyzed by glutamate:glyoxylate and serine:glyoxylate aminotransferases in rice. J. Photochem. Photobiol. B 142, 110-117.

[126] Zhou, Z., Zhang, Z., van der Putten, P.E.L., Fabre, D., Dingkuhn, M., Struik, P.C., Yin, X., 2023. Triose phosphate utilisation in leaves is modulated by whole- plant sink-source ratios and nitrogen budgets in rice. J. Exp. Bot. 74, 6692-6707.