Effect of CO2 content in air on functioning of Arabidopsis thaliana photosynthetic electron transport chain
Boris N. Ivanov
A * , Marina A. Kozuleva A , Natalia N. Rudenko A , Lyudmila K. Ignatova A , Elena M. Nadeeva A , Ilya A. Naydov A , Daria V. Vetoshkina A , Daria V. Vilyanen A and Maria M. Borisova-Mubarakshina A
A
Abstract
The functioning of the photosynthetic electron transport chain and the proceeding of accompanying processes were studied in Arabidopsis thaliana plants acclimated during 2 weeks to reduced (150 ppm) or elevated (1000 ppm) CO2 concentrations in air. Measured at ambient CO2, the quantum yields of both photosystems were lower in plants acclimated to these CO2 concentrations as compared with control plants grown at ambient CO2. The difference was more pronounced at the beginning of the illumination. It is discussed that this difference resulted from the difference in Rubisco content, which at both reduced and elevated CO2 in air was lower than in control plants. The quantum yield of regulated non-photochemical energy loss in photosystem II under both reduced and elevated CO2 was lower than in control plants. This correlated with reduced expression of the PsbS protein gene. H2O2 content in the leaves increased during the first days of plant adaptation to 150 ppm CO2, but then decreased. The increase resulted from enhanced rates of both photorespiration and Mehler reaction, while the following decrease resulted from enhancing contents of ascorbate peroxidases in all cell compartments.
Keywords: adaptation to reduced and elevated air CO2 concentrations, Arabidopsis thaliana L., ascorbate peroxidases, hydrogen peroxide, non-photochemical chlorophyll a quenching, photosynthetic electron transport chain, proton-motive force, quantum yields of photosystems, Rubisco.
References
Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351-372.
| Crossref | Google Scholar | PubMed |
Anjum NA, Sharma P, Gill SS, Hasanuzzaman M, Khan EA, Kachhap K, Mohamed AA, Thangavel P, Devi GD, Vasudhevan P, Sofo A, Khan NA, Misra AN, Lukatkin AS, Singh HP, Pereira E, Tuteja N (2016) Catalase and ascorbate peroxidase—representative H2O2-detoxifying heme enzymes in plants. Environmental Science and Pollution Research 23, 19002-19029.
| Crossref | Google Scholar | PubMed |
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601-639.
| Crossref | Google Scholar | PubMed |
Askari N, Aliniaeifard S, Visser RGF (2022) Low CO2 levels are detrimental for in vitro plantlets through disturbance of photosynthetic functionality and accumulation of reactive oxygen species. Horticulturae 8, 44.
| Crossref | Google Scholar |
Balmer Y, Koller A, del Val G, Manieri W, Schürmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proceedings of the National Academy of Sciences 100, 370-375.
| Crossref | Google Scholar | PubMed |
Borisova-Mubarakshina MM, Vetoshkina DV, Ivanov BN (2019) Antioxidant and signaling functions of the plastoquinone pool in higher plants. Physiologia Plantarum 66, 181-198.
| Crossref | Google Scholar |
Bouges-Bocquet B (1981) Factors regulating the slow electrogenic phase in green algae and higher plants. Biochimica et Biophysica Acta (BBA) - Bioenergetics 635, 327-340.
| Crossref | Google Scholar | PubMed |
Chen G-Y, Yong Z-H, Liao Y, Zhang D-Y, Chen Y, Zhang H-B, Chen J, Zhu J-G, Xu D-Q (2005) Photosynthetic acclimation in rice leaves to free-air CO2 enrichment related to both ribulose-1,5-bisphosphate carboxylation limitation and ribulose-1,5-bisphosphate regeneration limitation. Plant and Cell Physiology 46, 1036-1045.
| Crossref | Google Scholar | PubMed |
Cheng S-H, Moore Bd, Seemann JR (1998) Effects of short- and long-term elevated CO2 on the expression of ribulose-1,5-bisphosphate carboxylase/oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L.) Heynh. Plant Physiology 116, 715-723.
| Crossref | Google Scholar | PubMed |
Cormier MJ, Prichard PM (1968) An investigation of the mechanism of the luminescent peroxidation of luminol by stopped flow techniques. Journal of Biological Chemistry 243, 4706-4714.
| Crossref | Google Scholar | PubMed |
Cruz JA, Sacksteder CA, Kanazawa A, Kramer DM (2001) Contribution of electric field (Δψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Δψ and ΔpH by ionic strength. Biochemistry 40, 1226-1237.
| Crossref | Google Scholar | PubMed |
Delucia EH, Sasek TW, Strain BR (1985) Photosynthetic inhibition after long-term exposure to elevated levels of atmospheric carbon dioxide. Photosynthesis Research 7, 175-184.
| Crossref | Google Scholar |
Durchan M, Vácha F, Krieger-Liszkay A (2001) Effects of severe CO2 starvation on the photosynthetic electron transport chain in tobacco plants. Photosynthesis Research 68, 203-213.
| Crossref | Google Scholar | PubMed |
Gerhart LM, Ward JK (2010) Plant responses to low [CO2] of the past. New Phytologist 188, 674-695.
| Crossref | Google Scholar | PubMed |
Hommel E, Liebers M, Offermann S, Pfannschmidt T (2022) Effectiveness of light-quality and dark-white growth light shifts in short-term light acclimation of photosynthesis in Arabidopsis. Frontiers in Plant Science 12, 615253.
| Crossref | Google Scholar |
Hope AB, Matthews DB (1987) The slow phase of the electrochromic shift in relation to the Q-cycle in thylakoids. Australian Journal Plant Physiology 14, 29-46.
| Crossref | Google Scholar |
Ivanov BN, Borisova-Mubarakshina MM, Kozuleva MA (2018) Formation mechanisms of superoxide radical and hydrogen peroxide in chloroplasts, and factors determining the signalling by hydrogen peroxide. Functional Plant Biology 45, 102-110.
| Crossref | Google Scholar | PubMed |
Ivanov B, Borisova-Mubarakshina M, Vilyanen D, Vetoshkina D, Kozuleva M (2022) Cooperative pathway of O2 reduction to H2O2 in chloroplast thylakoid membrane: new insight into the Mehler reaction. Biophysical Reviews 14, 857-869.
| Crossref | Google Scholar | PubMed |
Jang JC, Leon P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9, 5-19.
| Crossref | Google Scholar |
Klughammer C, Schreiber U (2008a) Saturation pulse method for assessment of energy conversion in PS I. PAM Application Notes 1, 11-14.
| Google Scholar |
Klughammer C, Schreiber U (2008b) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Application Notes 1, 27-35.
| Google Scholar |
Kozuleva M, Klenina I, Mysin I, Kirilyuk I, Opanasenko V, Proskuryakov I, Ivanov B (2015) Quantification of superoxide radical production in thylakoid membrane using cyclic hydroxylamines. Free Radical Biology and Medicine 89, 1014-1023.
| Crossref | Google Scholar | PubMed |
Kozuleva M, Petrova A, Milrad Y, Semenov A, Ivanov B, Redding KE, Iftach Y (2021) Phylloquinone is the principal Mehler reaction site within photosystem I in high light. Plant Physiology 186, 1848-1858.
| Crossref | Google Scholar | PubMed |
Laloi C, Przybyla D, Apel K (2006) A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. Journal of Experiential Botany 57, 1719-1724.
| Crossref | Google Scholar |
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350-382.
| Google Scholar |
Martínez-Carrasco R, Pérez P, Morcuende R (2005) Interactive effects of elevated CO2, temperature and nitrogen on photosynthesis of wheat grown under temperature gradient tunnels. Environmental and Experimental Botany 54, 49-59.
| Crossref | Google Scholar |
Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant and Cell Physiology 51, 190-200.
| Crossref | Google Scholar | PubMed |
Michelet L, Zaffagnini M, Morisse S, Sparla F, Pérez-Pérez ME, Francia F, Danon A, Marchand CH, Fermani S, Trost P, Lemaire SD (2013) Redox regulation of the Calvin–Benson cycle: something old, something new. Frontiers in Plant Science 4, 470.
| Crossref | Google Scholar | PubMed |
Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant and Cell Physiology 33, 541-553.
| Crossref | Google Scholar |
Mudrik VA, Romanova AK, Ivanov BN, Novichkova NS, Polyakova VA (1997) Effect of increased CO2 concentration on growth, photosynthesis, and biochemical composition of Pisum sativum L. plants. Russian Journal of Plant Physiology 44, 26-32.
| Google Scholar |
Neubauer C, Yamamoto HY (1994) Membrane barriers and Mehler-peroxidase reaction limit the ascorbate available for violaxanthin de-epoxidase activity in intact chloroplasts. Photosynthesis Research 39, 137-147.
| Crossref | Google Scholar |
Nilkens M, Kress E, Lambrev P, Miloslavina Y, Müller M, Holzwarth AR, Jahns P (2010) Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1797, 466-475.
| Crossref | Google Scholar | PubMed |
Pandurangam V, Sharma-Natu P, Sreekanth B, Ghildiyal MC (2006) Photosynthetic acclimation to elevated CO2 in relation to Rubisco gene expression in three C3 species. Indian Journal of Experimental Biology 44, 408-415.
| Google Scholar | PubMed |
Romanova AK (2005) Physiological and biochemical aspects and molecular mechanisms of plant adaptation to the elevated concentration of atmospheric CO2. Russian Journal of Plant Physiology 52, 112-126.
| Crossref | Google Scholar |
Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the Photosystem II antenna. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1817, 167-181.
| Crossref | Google Scholar |
Rudenko NN, Fedorchuk TP, Vetoshkina DV, Zhurikova EM, Ignatova LK, Ivanov BN (2018) Influence of knockout of At4g20990 gene encoding α-CA4 on photosystem II light-harvesting antenna in plants grown under different light intensities and day lengths. Protoplasma 255, 69-78.
| Crossref | Google Scholar | PubMed |
Rudenko NN, Ignatova LK, Naydov IA, Novichkova NS, Ivanov BN (2022) Effect of CO2 content in air on the activity of carbonic anhydrases in cytoplasm, chloroplasts, and mitochondria and the expression level of carbonic anhydrase genes of the α- and β-families in Arabidopsis thaliana leaves. Plants 11, 2113.
| Crossref | Google Scholar | PubMed |
Sagun JV, Badger MR, Chow WS, Ghannoum O. (2021) Mehler reaction plays a role in C3 and C4 photosynthesis under shade and low CO2. Photosynth Research 149, 171-185.
| Crossref | Google Scholar |
Sanz-Sáez A, Erice G, Aranjuelo I, Aroca R, Ruíz-Lozano JM, Aguirreolea J, Irigoyen JJ, Sanchez-Diaz M (2013) Photosynthetic and molecular markers of CO2 mediated photosynthetic down regulation in nodulated alfalfa. Journal of Integrative Plant Biology 55, 721-734.
| Google Scholar | PubMed |
Van Oosten JJ, Besford RT (1995) Some relationships between the gas exchange, biochemistry and molecular biology of photosynthesis during leaf development of tomato plants after transfer to different carbon dioxide concentrations. Plant Cell and Environment 18, 1253-1266.
| Crossref | Google Scholar |
Venkatesh J, Park SW (2014) Role of L-ascorbate in alleviating abiotic stresses in crop plants. Botanical Studies 55, 38.
| Crossref | Google Scholar | PubMed |
Urban O (2003) Physiological impacts of elevated CO2 concentrations ranging from molecular to whole plant response. Photosynthetica 41, 9-20.
| Crossref | Google Scholar |
Zavřel T, Szabó M, Tamburic B, Evenhuis C, Kuzhiumparambil U, Literáková P, Larkum AWD, Raven JA, Červený J, Ralph PJ (2018) Effect of carbon limitation on photosynthetic electron transport in Nannochloropsis oculata. Journal of Photochemistry and Photobiology B: Biology 181, 31-43.
| Crossref | Google Scholar | PubMed |
Zheng Y, Li F, Hao L, Yu J, Guo L, Zhou H, Ma C, Zhang X, Xu M (2019) Elevated CO2 concentration induces photosynthetic down-regulation with changes in leaf structure, non-structural carbohydrates and nitrogen content of soybean. BMC Plant Biology 19, 255.
| Crossref | Google Scholar | PubMed |
