Пластидна термінальна оксидаза (Plastid Terminal Oxidase — PTOX) залізовмістний фермент, переносник електронів у електронтранспортному ланцюзі хлоропластів, функції якого до кінця не вивчені донині. В огляді розглянуто будову та окремі відомості щодо функціонування РТОХ у нормальних фізіологічних умовах та за дії різних абіотичних стресів. Одна з відомих функцій РТОХ — участь у синтезі каротиноїдів. У нефотосинтезувальних тканинах або на ранніх стадіях розвитку рослини, коли фотосинтетичний транспорт електронів не повністю активний, РTOX є основним кофактором для фітоендесатурази і z-каротиндесатурази, які беруть участь у реакції десатурації каротиноїдів. Також РТОХ задіяна у хлорореспіраторному механізмі в зелених тканинах рослин за дії стресів. На рослинах дикого типу й різноманітних мутантних формах розглянуто участь РТОХ у протидії світловому, температурному, сольовому стресам та їх комбінаціям. Показано, що дуже висока експресія гена РТОХ у рослинах-мутантах не завжди приводить до очікуваного підвищення стійкості. У протилежність цьому наведено дані дослідників, які виявили підвищення стійкості різних видів рослин за дії стресів за рахунок посилення транспорту електронів крізь РТОХ. Це сприяло зменшенню продукування активних форм кисню і руйнування білка D1, а, відповідно, й збереженню активності фотосистеми II (ФС II). Представлено також результати щодо підвищеного вмісту РТОХ у контрольних рослин сортів озимої пшениці високої стійкості, отримані авторами. За дії посухи вміст РТОХ у цих сортів ще більше підвищувався, а квантовий вихід ФС II зберігався на високому рівні. Вважається, що PTOX працює як ініційований стресом запобіжний клапан, що підтримує окиснення акцепторної сторони ФС II, тим самим захищаючи ФС II від фотопошкодження. Таким чином, PTOX можна використовувати як один із потенційних кандидатів для генно-інженерного підвищення стресостійкості сільськогосподарських рослин.
Ключові слова: фотосинтез, фотодихання, пластидна термінальна оксидаза, абіотичний стрес
Повний текст та додаткові матеріали
У вільному доступі: PDFЦитована література
1. Bukhov, N.G. & Carpentier, N.G. (2004). Alternative photosystem I-driven electron transport routes: mechanisms and functions. Photosynthesis Research, No. 82, pp. 17-33. https://doi.org/10.1023/B:PRES.0000040442.59311.72
2. Wetzel, C.M., Jiang, C.-Z., Meehan, L.J., Voytas, D.F. & Rodermel, S.R. (1994). Nuclear-organelle interactions: the immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis. Plant J., No. 6, pp. 161-175. https://doi.org/10.1046/j.1365-313X.1994.6020161.x
3. Carol, P., Stevenson, D., Bisanz, C., Breitenbach, J., Sandmann, G., Mache, R., Coupland, G. & Kuntz, M. (1999). Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell, No. 11 (1), pp. 57-68. https://doi.org/10.1105/tpc.11.1.57
4. Lennon, A.M., Prommeenate, P. & Nixon, P.J. (2003). Location, expression and orientation of the putative chlororespiratory enzymes, Ndh and IMMUTANS, in higher-plant plastids. Planta, No. 218, pp. 254-260. https://doi.org/10.1007/s00425-003-1111-7
5. Quiles, M.J. (2006). Stimulation of chlororespiration by heat and high light intensity in oat plants. Plant Cell Environ., No. 29, pp. 1463-1470. https://doi.org/10.1111/j.1365-3040.2006.01510.x
6. Stepien, P. & Johnson, G.N. (2009). Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: Role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol., No. 149, pp. 1154-1165. https://doi.org/10.1104/pp.108.132407
7. Stepien, P. & Johnson, G.N. (2018). Plastid terminal oxidase requires translocation to the grana stacks to act as a sink for electron transport. Proc. Natl. Acad. Sci. U.S.A., No. 115, pp. 9634-9639. https://doi.org/10.1073/pnas.1719070115
8. Ivanov, A.G., Rosso, D., Savitch, L.V., Stachula, P., Rosembert, M., Oquist, G., Hurry, V. & Huner N.P.A. (2012). Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold acclimated Arabidopsis thaliana. Photosynthesis Research, No. 113, pp. 191-206. https://doi.org/10.1007/s11120-012-9769-y
9. Laureau, C., De Paepe, R., Latouche G., Moreno-Chacon, M., Finazzi, G., Kuntz, M., Cornic, G. & Streb, P. (2013). Plastid terminal oxidase (PTOX) has the potential to act as a safety valve for excess excitation energy in the alpine plant species Ranunculus glacialis L. Plant, Cell and Environ., No. 36, pp. 1296-1310. https://doi.org/10.1111/pce.12059
10. Trouillard, M., Shahbazi, M., Moyet, L., Rappaport, F., Joliot, P., Kuntz, M. & Finazzi, G. (2012). Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant. Biochim. Biophys. Acta, No. 1817, pp. 2140-2148. https://doi.org/10.1016/j.bbabio.2012.08.006
11. Nawrocki, W.J., Tourasse, N.J., Taly, A., Rappaport, F. & Wollman, F.-A. (2015). The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annu. Rev. Plant Biol., No. 66, pp. 49-74. https://doi.org/10.1146/annurev-arplant-043014-114744
12. Yu, Q., Feilke, K., Krieger-Liszkay, A. & Beyer, P. (2014). Functional and molecular characterization of plastid terminal oxidase from rice (Oryza sativa). Biochim. Biophys. Acta, No. 1837, pp. 1284-1292. https://doi.org/10.1016/j.bbabio.2014.04.007
13. Feilke, K., Streb, P., Cornic, G., Perreau, F., Kruk, J. & Krieger-Liszkay, A. (2016). Effect of Chlamydomonas plastid terminal oxidase 1 expressed in tobacco on photosynthetic electron transfer. Plant J., No. 85, pp. 219-228. https://doi.org/10.1111/tpj.13101
14. Krieger-Liszkay, A. & Feilke, K. (2016). The dual role of the plastid terminal oxidase PTOX: between a protective and a pro-oxidant function. Front. Plant Sci., No. 6, p. 1147. https://doi.org/10.3389/fpls.2015.01147
15. Bolte, S., Marcon, E., Jaunario, M., Moyet L., Paternostre, M., Kuntz, M. & Krieger-Liszkay, A. (2020). Dynamics of the localization of the plastid terminal oxidase inside the chloroplast. J. Exp. Botany, No. 9, pp. 2661-2669. https://doi.org/10.1093/jxb/
16. Kochubey, S.M., Bondarenko, O.Yu. & Shevchenko, V.V. (2014). Structural organization and functional features of the light phase of photosynthesis. Photosynthesis. Vol. 1. Kyiv: Logos [in Russian].
17. Pribil, M., Labs, M. & Leister, D. (2014). Structure and dynamics of thylakoids in land plants. J. Exp. Botany, No. 8, pp. 1955-1972. https://doi.org/10.1093/jxb/eru090
18. Kirchhoff, H. (2019). Chloroplast ultrastructure in plants. New Phytologist., pp. 565-574. https://doi.org/10.1111/nph.15730
19. Shevchenko, V.V., Bondarenko, O.Yu. & Kornyeyev, D.Yu. (2022). Short-term heating causes thylakoid restructuring in pea chloroplasts and modifies spectral properties of pigment-proteins. Plant physiology and genetics., No. 2, pp. 134-147. https://doi.org/10.15407/frg2022.02.134
20. Kirchhoff, H., Hall, C., Wood, M., Herbstova, M., Tsabari, O., Nevo, R., Charuvi, D., Shimoni & Reich, Z. (2011). Dynamic control of protein diffusion within the granal thylakoid lumen. Proc. Natl. Acad. Sci. USA, No. 108 (50), pp. 20248-20253. https://doi.org/10.1073/pnas.1104141109
21. Ruban, A. (2016). Nonphotochemical Chlorophyll Fluorescence Quenching: Mechanism and Effectiveness in Protecting Plants from Photodamage. Plant Physiol., No. 4, pp. 1903-1916. https://doi.org/10.1104/pp.15.01935
22. Jotham, A.R., Frost, E., Vidi, P.-A., Kessler, F. & Staehelin, L.A. (2006). Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell, No. 7, pp. 1693-703. https://doi.org/10.1105/tpc.105.039859
23. Shiba, T., Kido, Y., Sakamoto, K., Inaoka, D., Tsuge, C., Tatsumi, R., Takahashi, G., Balogun, E.O., Nara, T., Aoki, T., Honma, T., Inoue, M., Matsuoka, S., Saimoto, H., Moore, A.L., Harada, S. & Kita, K. (2013). Structure of the trypanosome cyanideinsensitive alternative oxidase. Proc. Natl. Acad. Sci. USA, No. 110, pp. 4580-4585. https://doi.org/10.1073/pnas.1218386110
24. Gemmecker, S., Schaub, P., Koschmieder, J., Brausemann, A., Drepper, F., Rodriguez-Franco, M., Ghisla, S., Wairsceid. B., Einsle, O. & Beyer, P. (2015). Phytoene Desaturase from Oryza sativa: Oligomeric Assembly, Membrane Association and Preliminary 3d-Analysis. PLoS One, No. 10, e0131717. https://doi.org/10.1371/journal.pone.0131717
25. Wu, D., Wright, D.A., Wetzel, C., Voytas, D.F. & Rodermel, S. (1999). The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell, No. 11 (1), pp. 43-55. https://doi.org/10.1105/tpc.11.1.43
26. Allison, E., McDonald, A., Ivanov, G., Bode, R., Maxwell, D.P., Rodermel, S.R. & Huner, N.P.A. (2011). Flexibility in photosynthetic electron transport: The physiological role of plastoquinol terminal oxidase (PTOX). Biochim. Biophys. Acta, No. 1807, pp. 954-967 https://doi.org/10.1016/j.bbabio.2010.10.024
27. Berthold, D.A., Andersson, M.E. & Nordlund, P. (2000). New insight into the structure and function of the alternative oxidase. Biochim. Biophys. Acta, No. 1460, pp. 241-254. https://doi.org/10.1016/S0005-2728(00)00149-3
28. Andersson, M.E. & Nordlund, P. (1999). A revised model of the active site of alternative oxidase, FEBS Lett., No. 449, pp. 17-22. https://doi.org/10.1016/S0014-5793(99)00376-2
29. Berthold, D.A., Voevodskaya, N., Stenmark, P., Graslund, A. & Nordlund, P. (2002). EPR studies of the mitochondrial alternative oxidase. Evidence for a diiron carboxylate center. J. Biol. Chem., No. 277, pp. 43608-43614. https://doi.org/10.1074/jbc.M206724200
30. Moore, A.L., Carre, J.E., Affourtit, C., Albury, M.S., Crichton, P.G., Kita, K. & Heathcote, P. (2008). Compelling EPR evidence that the alternative oxidase is a diiron carboxylate protein. Biochim. Biophys. Acta, No. 1777, pp. 327-330. https://doi.org/10.1016/j.bbabio.2008.01.004
31. Fu, A., Park, S. & Rodermel S. (2005). Sequences required for the activity of PTOX (IMMUTANS), a plastid terminal oxidase: in vitro and in planta mutagenesis of iron-binding sites and a conserved sequence that corresponds to Exon 8. J. Biol. Chem., No. 280, pp. 42489-42496. https://doi.org/10.1074/jbc.M508940200
32. Cournac, L., Josse, E.-M., Joet, T., Rumeau, D., Redding, K., Kuntz, M. & Peltier, G. (2000). Flexibility in photosynthetic electron transport: a newly identified chloroplast oxidase involved in chlororespiration. Phil. Trans. R. Soc. Lond. B., No. 355, pp. 1447-1454. https://doi.org/10.1098/rstb.2000.0705
33. Josse, E.-M., Alcaraz, J.-P., Laboure, A.-M. & Kuntz, M. (2003). In vitro characterization of a plastid terminal oxidase (PTOX). Eur. J. Biochem., No. 270, pp. 3787-3794. https://doi.org/10.1046/j.1432-1033.2003.03766.x
34. Fu, A., Aluru, M. & Rodermel, S.R. (2009). Conserved active site sequences in Arabidopsis plastid terminal oxidase (PTOX): in vitro and in planta mutagenesis studies, J. Biol. Chem., No. 284, pp. 22625-22632. https://doi.org/10.1074/jbc.M109.017905
35. Heber, U. & Walker, D. (1992). Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiol., No. 100, pp. 1621-1626. https://doi.org/10.1104/pp.100.4.1621
36. Ravenel, J., Peltier, G. & Havaux, M. (1994). The cyclic electron pathways around photosystem I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. Planta, No. 193, pp. 251-259. https://doi.org/10.1007/BF00192538
37. Bennoun, P. (1982). Evidence for a respiratory chain in the chloroplast. Proceedings of the National Academy of Sciences of the United States of America, 79, pp. 4352-4356. https://doi.org/10.1073/pnas.79.14.4352
38. Peltier, G., Ravenel, J. & Vermeglio, A. (1987). Inhibition of a respiratory activity by short saturating flashes in Chlamydomonas: Evidence for a chlororespiration. Biochim. Bioph. Acta (BBA) - Bioenergetics, No. 893, pp. 83-90. https://doi.org/10.1016/0005-2728(87)90151-4
39. Burrows, P.A., Sazanov, L.A., Svab, Z., Maliga, P. & Nixon, P.J. (1998). Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J., No. 17, pp. 868-876. https://doi.org/10.1093/emboj/17.4.868
40. Shikanai, T., Endo, T., Hashimoto, T., Yamada, Y., Asada, K. & Yokota, A. (1998). Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl. Acad. Sci., No. 95, pp. 9705-9709. https://doi.org/10.1073/pnas.95.16.9705
41. Kofer, W., Koop, H.-U., Wanner, G. & Steinmuller, K. (1998). Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation. Mol. Gen. Genet., No. 258, pp. 166-173. https://doi.org/10.1007/s004380050719
42. Cournac, L., Redding, K., Ravenel, J., Rumeau, D., Josse, E.-M., Kuntz, M. and Peltier, G. (2000). Electron flow between photosystem II and oxygen in chloroplasts of photosystem I deficient algae is mediated by a quinol oxidase involved in chlororespiration. J. Biol. Chem., No. 275, pp. 17256-17262. https://doi.org/10.1074/jbc.M908732199
43. Powles, S.B. (1984). Photoingibition of photosynthesis induced by visible light. Annu. Rev. Plant. Physiol., No. 35, pp. 15-44. https://doi.org/10.1146/annurev.pp.35.060184.000311
44. Shadchina, T.M. & Pryadkina, G.A. (2006). The effect of soil salinity and nitrogen deficiency on violaxanthin cycle activity and non-photochemical quenching of chlorophyll fluorescence in wheat leaves. Physiology and biochemistry of cultivated plants, No. 3, pp. 214-221.
45. Osmond, C.B. (1981). Photorespiration and photoingibition. Some implication for the energetics of photosintesis. Biochim. Biophys. Acta, No. 639, pp. 77-98. https://doi.org/10.1016/0304-4173(81)90006-9
46. Kirizy, D.A, Stasik, О.О., Pryadkina, G.O. & Shadchina, Т.М. (2014). Assimilation of CO2 and mechanisms of its regulation. Photosynthesis. Vol. 2. Кyiv: Logos [in Ukrainian].
47. Wu, J., Neimanis, S. & Heber, U. (1991). Photorespiration is more effective than the Mehler reaction in protecting the photosynthetic apparatus against photoinhibition. Bot. Acta. No. 104, pp. 283-291. https://doi.org/10.1071/PP99112
48. Flexas, J., Bota, J., Escalona, J.M., Sampol, B. & Medrano, H. (2002). Effects of drought on photosynthesis in grapevines under field conditions: An evaluation of stomatal and mesophyll limitations. Funct. Plant Biol., No. 29. https://doi.org/10.1071/PP01119
49. Medrano, H., Escalona, J.M., Bota, J., Gulias, J. & Flexas, J. (2002). Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Ann. Bot., No. 89, pp. 895-905. https://doi.org/10.1093/aob/mcf079
50. Rodermel, S. (2001) Pathways of plastid-to-nucleus signaling. Plant Sci., No. 6, pp. 471-478. https://doi.org/10.1016/S1360-1385(01)02085-4
51. Yu, F., Fu, A., Aluru, M., Park, S., Xu, Y., Liu, H., Liu, X., Foudree, A., Nambogga, M. & Rodermel, S. (2007). Variegation mutants and mechanisms of chloroplast biogenesis. Plant Cell Environ., No. 3, pp. 350-365. https://doi.org/10.1111/j.1365-3040.2006.01630.x
52. Fu, A., Liu, H., Yu, F., Kambakam, S., Luan, S. & Rodermel, S. (2012). Alternative oxidases (AOX1a and AOX2) can functionally substitute for plastid terminal oxidase in Arabidopsis chloroplasts. Plant Cell, No. 4, pp. 1579-1595. https://doi.org/10.1105/tpc.112.096701
53. Tilney-Bassett, R.A.E. (1974). The control of plastid inheritance in Pelargonium. III. Heredity, No. 3, pp. 353-360. https://doi.org/10.1038/hdy.1974.102
54. Luru, M.R. & Rodermel, S.R. (2004). Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol. Plant., No. 1, pp. 4-11. https://doi.org/10.1111/j.0031-9317.2004.0217.x
55. Redei, G.P. (1963). Somatic Instability Caused by a Cysteine-Sensitive Gene in Arabidopsis. Science, No. 3556, pp. 767-769. https://doi.org/10.1126/science.139.3556.767
56. Robbelen, G. (1968). Arabidopsis Research Science, No. 3700, pp. 1192. https://doi.org/10.1126/science.150.3700.1192
57. Rosso, D., Bode, R., Li, W., Krol, M., Saccon, D., Wang, S., Schillaci, L., Rodermel, S., Maxwell, D. & Huner, N. (2009). Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2. Plant Cell, No. 21, pp. 3473-3492. https://doi.org/10.1105/tpc.108.062752
58. Della Penna, D. & Pogson, B.J. (2006). Vitamin synthesis in plants: tocopherols and carotenoids. Annu. Rev. Plant Biol., No. 57, pp. 711-738. https://doi.org/10.1146/annurev.arplant.56.032604.144301
59. Oelmuller, R., Kendrick, R.E. & Briggs, W.R. (1989). Blue-light mediated accumulation of nuclear-encoded transcripts coding for proteins of the thylakoid membrane is absent in the phytochrome-deficient aurea mutant of tomato. Plant Mol. Biol., No. 2, pp. 223-232. https://doi.org/10.1007/BF00016140
60. Drickamer, K. & Taylor, M.E. (2005). Targeting diversity. Nat. Struct. Mol. Biol., No. 10, pp. 830-831. https://doi.org/10.1038/nsmb1005-830
61. Giraud, E. & Vermeglio, A. (2008). Bacteriophytochromes in anoxygenic photosynthetic bacteria. Photosynth. Res., No. 2, pp. 141-53. https://doi.org/10.1007/s11120-008-9323-0
62. McDonald, A.E., Ivanov, A.G., Bode, R., Maxwell, D.P., Rodermel, S.R. & Huner, N.P. (2011). Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminaloxidase (PTOX). Biochim. Biophys. Acta, No. 1807, pp. 954-967. https://doi.org/10.1016/j.bbabio.2010.10.024
63. Joet, T., Genty, B., Josse, E.-M., Kuntz, M., Cournac, L. & Peltier, G. (2002). Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J. Biol. Chem., No. 35, pp. 31623-31630. https://doi.org/10.1074/jbc.M203538200
64. Aluru, M.R. & Rodermel, S.R. (2004). Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol. Plant., No. 120, pp. 4-11. https://doi.org/10.1111/j.0031-9317.2004.0217.x
65. Baena-Gonzalez, E., Allahverdiyeva, Y., Svab, Z., Maliga, P., Josse, E.M., Kuntz, M., Maenpaa, P. & Aro, E.M. (2003). Deletion of the tobacco plastid psbA gene triggers an upregulation of the thylakoid-associated NAD(P)H dehydrogenase complex and the plastid terminal oxidase (PTOX). Plant J., No. 6, pp. 704-16. https://doi.org/10.1046/j.1365-313X.2003.01842.x
66. Shahbazi, M., Gilbert, M., Laboure, A. M. & Kuntz, M. (2007). Dual Role of the Plastid Terminal Oxidase in TomatoPlant Physiol., No. 3, pp. 691-702. https://doi.org/10.1104/pp.107.106336
67. Bjorkman, O. & Demmig, B. (1987). Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta, No. 4, pp. 489-504. https://doi.org/10.1007/BF00402983
68. Heyno, E., Gross, C. M., Laureau, C., Culcasi, M., Pietri, S. & Krieger-Liszkay, A. (2009). Plastid Alternative Oxidase (PTOX) Promotes Oxidative Stress When Overexpressed in Tobacco. J. Biol. Chem., No. 45, pp. 31174-31180. https://doi.org/10.1074/jbc.M109.021667
69. Niyogi, K.K. (2000). Safety valves for photosynthesis. Curr. Opin. Plant Biol., No. 6, pp. 455-460. https://doi.org/10.1016/S1369-5266(00)00113-8
70. Peltier, G. & Cournac, L. (2002). Chlororespiration. Annu. Rev. Plant Biol., No. 53, pp. 523-550. https://doi.org/10.1146/annurev.arplant.53.100301.135242
71. Streb, P., Josse, E.M., Gallouet, E., Baptist, F., Kuntz, M., & Cornic, G. (2005). Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant Cell Environ., No. 28, pp. 1123-1135. https://doi.org/10.1111/j.1365-3040.2005.01350.x
72. Diaz, M., De Haro, V., Munoz, R. & Quiles M.J. (2007). Chlororespiration is involved in the adaptation of Brassica plants to heat and high light intensity. Plant Cell Environ., No. 30, pp. 1578-1585. https://doi.org/10.1111/j.1365-3040.2007.01735.x
73. Rosso, D., Ivanov, A.G., Fu, A., Geisler-Lee, J., Hendrickson, L., Geisler, M., Stewart, G., Krol, M., Hurry, V., Rodermel, S.R., Maxwell, D.P. & Huner, N.P.A. (2006). IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol., No. 142, pp. 574-585. https://doi.org/10.1104/pp.106.085886
74. Rumeau, D., Peltier, G., & Cournac, L. (2007). Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ., No. 30, pp. 1041-1051. https://doi.org/10.1111/j.1365-3040.2007.01675.x
75. Wise, R.R. & Hoober, J.K. (2006). The structure and function of plastids. Netherlands: Springer. https://doi.org/10.1007/978-1-4020-4061-0
76. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chetrit, P., Foyer, C.H., & de Paepe, R. (2003). Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell, No. 5, pp. 1212-1226. https://doi.org/10.1105/tpc.009464
77. Streb, P., Josse , E.-M., Gallouet, E., Baptist, F., Kuntz, M., Cornic, G., Stepien, P. & Johnson, G.N. (2009). Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: Role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol., No. 149, pp. 1154-1165. https://doi.org/10.1104/pp.108.132407
78. Johnson, G.N. & Stepien, P. (2016). Plastid terminal oxidase as a route to improving plant stress tolerance: known knowns and known unknowns. Plant Cell Physiol., No. 57, pp. 1387-1396. https://doi.org/10.1093/pcp/pcw042
79. Ahmad, N., Khan, M.O., Islam, E., Wei, Z.-Y., McAusland, L., Lawson, T., Johnson, G.N. & Nixon, P.J. (2020). Contrasting responses to stress displayed by tobacco overexpressing an algal plastid terminal oxidase in the chloroplast. Front. Plant Sci., No. 11, pp. 501. https://doi.org/10.3389/fpls.2020.00501
80. Houille-Vernes, L., Rappaport, F., Wollman, F.-A., Alric, J. & Johnson, X. (2011). Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc. Natl. Acad. Sci. USA, No. 108, pp. 20820-20825. https://doi.org/10.1073/pnas.1110518109
81. Ahmad, N., Michoux, F. & Nixon, P.J. (2012). Investigating the production of foreign membrane proteins in tobacco chloroplasts: expression of an algal plastid terminal oxidase. PLoS One, No. 7 (7): e41722. https://doi.org/10.1371/journal.pone.0041722
82. Wingler, A., Lea, P.W., Quick, P.W. & Leegod, R.C. (2000). Photorespiration: metabolic pathweys and their role in stress protection. Phil. Trans. R. Soc. Lond. B., No. 355, pp. 1517-1529. https://doi.org/10.1098/rstb.2000.0712
83. Takeba, G. & Kozaki, A. (1998). Photorespiration is essential mechanism for the protection of C-3 plants from photooxydation. Stress Responses of Photosynthetic Organisms. Amsterdam: Elsevier Science. https://doi.org/10.1016/B978-0-444-82884-2.50005-4
84. Cornic, G. & Fresneau, C. (2002). Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystem II activity during a mild drought. Ann. Bot., No. 89, pp. 887-894. https://doi.org/10.1093/aob/mcf064
85. Gururani, M.A., Venkatesh, J. & Tran, L.-S.P. (2015). Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol. Plant, No. 8, pp. 1304-1320. https://doi.org/10.1016/j.molp.2015.05.005
86. Shevchenko, V.V. & Bondarenko, O.Yu. (2022). Changes in the parameters of chlorophyll fluorescence induction and content of low molecular weight protective proteins in modern varieties of winter wheat under drought. Science and Education a New Dimension, No. 34, pp. 7-10 [in Ukranian]. https://doi.org/10.31174/SEND-NT2022-268X34-01
87. Bondarenko, O.Yu. & Shevchenko, V.V. (2021). Changes in the content of pigments and structural proteins of chloroplast membranes in different varieties of winter wheat under the influence of drought. Science and Education a New Dimension, No. 32, pp. 7-10 [in Ukranian]. https://doi.org/10.31174/SEND-NT2021-255IX32-01
88. Zandalinas, S.I., Sengupta, S., Fritschi, F.B., Azad, R.K., Nechushtai, R. & Mittler, R. (2021). The impact of multifactorial stress combination on plant grouth and survival. New Phytologst., No. 230, pp. 1034-1048. https://doi.org/10.1111/nph.17232
89. Kiriziy, D.A. & Stasik, O.O. (2022). Effects of drought and high temperature on physiological and biochemical processes, and productivity of plants. Fiziol. rast. genet., No. 2, pp. 95-122 [in Ukranian]. https://doi.org/10.15407/frg2022.02.095
90. Zandalinas, S.I., Fritschi, F.B. & Mittler, R. (2021). Global Warming, Climate Chenge, and Environmental Pollution: Recipe for a Multifactorial Stress Combination Disaster. Trend in Plant Science, No. 6. https://doi.org/10.1016/j.tplants.2021.02.011
91. Moor, C.E., Meacham-Hensold, K., Lemonnier, P., Slattery, R.A., Benjamin, C., Bernacchi, C.J., Lawson, T. & Cavanagh, A.P. (2021). The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. J. Exp. Bot., 72, No. 8, pp. 2822-2844. https://doi.org/10.1093/jxb/erab090
92. Kedruk, A.C., Kirizy, D.A., Sokolovska-Sergienko, O.G. & Stasik, О.О. (2021). Response of the photosynthetic apparatus of winter wheat varieties to the combined action of drought and higt temperature. Fiziol. rast. genet., No. 53, pp. 387-405 [in Ukranian]. https://doi.org/10.15407/frg2021.05.387
93. Shevchenko, V.V. & Bondarenko, O.Yu. (2020). Structural and functional changes of photosystem II in different varieties of winter wheat under the combined action of drought and high temperature. Science and Education a New Dimension. Natur. Techn. Sci., No. 28, pp. 7-9 [in Ukranian]. https://doi.org/10.31174/SEND-NT2020-233VIII28-01
94. Beyer, W.F., Fridovich, I., Mullenbach, G.T. & Hallewell, R. (1987). Examination of the role of arginine-143 in the human copper and zinc superoxide dismutase by site-specific mutagenesis. J. Biol Chem., No. 23, pp. 11182-11187. https://doi.org/10.1016/S0021-9258(18)60942-1
95. Mayer, M.P., Hahn, F.M., Stillman, D.J. & Poulter, C.D. (1992). Disruption and mapping of IDI1, the gene for isopentenyl diphosphate isomerase in Saccharomyces cerevisiae. Yeast, No. 9, pp. 743-748. https://doi.org/10.1002/yea.320080907
96. Mayer, S.M. & Beale, S.I. (1990). Light regulation of d-aminolevulinic acid biosynthetic enzymes and tRNA in Euglena gracilis. Plant Physiol., No. 3, pp. 1365-1375. https://doi.org/10.1104/pp.94.3.1365
97. Hugueney, P., Romer, S., Kuntz, M. & Camara, B. (1992). Characterization and molecular cloning of a bifunctional flavoprotein catalyzing the synthesis of phytofluene and z-carotene in Capsicum chromoplasts. Eur. J. Biochem., No. 209, pp. 399-407. https://doi.org/10.1111/j.1432-1033.1992.tb17302.x
98. Schledz, M., Al-Babili, S., von Lintig, J., Kleinig, H., Rabbani, S. & Beyer, P. (1996). Phytoene synthase cloned from Narcissus pseudonarcissus and functionally expressed in insect cells to reveal its galactolipid requirement, differential topology in chromoplasts and expression during flower development. The Plant Journal, No. 10, pp. 781-792 https://doi.org/10.1046/j.1365-313X.1996.10050781.x
99. Al-Babili, S., von Lintig, J., Haubruck, H. & Beyer, P. (1996). A novel, soluble form of phytoene desaturase from Narcissus pseudonarcissus chromoplasts is Hsp70-complexed and competent for flavinylation, membrane association and enzymatic activation. Plant J., No. 5, pp. 601-612. https://doi.org/10.1046/j.1365-313X.1996.9050601.x
100. Okegawa, Y., Kobayashi, Y. & Shikanai, T. (2010). Physiological links amoung alternative electron transport pathways that reduce and oxidize plastoquinone in Arabidopsis. The Plant Journal, No. 63, pp. 458-468. https://doi.org/10.1111/j.1365-313X.2010.04252.x
101. Rochaix, J.D. (2011). Regulation of photosynthetic electron transport. Biochim. Biophys. Acta, No. 3, pp. 375-83. https://doi.org/10.1016/j.bbabio.2010.11.010
102. Josse, E.M., Simkin, A.J., Gaffe, J., Laboure, A.M., Kuntz, M. & Carol, P. (2000). A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol., No. 123, pp. 1427-1436. https://doi.org/10.1104/pp.123.4.1427
103. Pfannschmindt, T., Nilsson, A. & Allen, J.F. (1999). Photosyntetic control of chloroplast gene expression. Nature, No. 397, p. 625. https://doi.org/10.1038/17624
104. Paul, M.J. & Frigerio, L. (2007). Coated vesicles in plant cells. Semin. Cell Dev. Biol., No. 4, pp. 471-478. https://doi.org/10.1016/j.semcdb.2007.07.005
105. Brzezowski, P., Ksas, B., Havaux, M., Grimm, B., Chazaux, M., Peltier, G., Johnson, X. & Alric, J. (2019). The function of protoporphyrinogen ix oxidase in chlorophyll biosynthesis requires oxidised plastoquinone in Chlamydomonas reinhardtii. Commun. Biology, No. 2, p. 159. https://doi.org/10.1038/s42003-019-0395-5
106. Carol, P. & Kuntz, M. (2001). A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trends Plant Sci., No. 6, pp. 31-36. https://doi.org/10.1016/S1360-1385(00)01811-2
107. Kuntz, M. (2004). Plastid terminal oxidase and its biological significance. Planta, No. 218, pp. 896-899. https://doi.org/10.1007/s00425-004-1217-6
108. Ibanez, H., Ballester, A., Munoz, R. & Quiles, M.J. (2010). Chlororespiration and tolerance to drought, heat and high illumination. J. Plant Physiol., No. 167, pp. 732-738. https://doi.org/10.1016/j.jplph.2009.12.013