RAS BiologyБиохимия Biochemistry

  • ISSN (Print) 0320-9725
  • ISSN (Online) 3034-5294

FEATURES OF PHOTOSYNTHESIS IN Arabidopsis thaliana PLANTS WITH KNOCKED OUT GENES ENCODING CHLOROPLAST CARBONIC ANHYDRASES αCA1 AND βCA1

PII
S30345294S0320972525070078-1
DOI
10.7868/S3034529425070078
Publication type
Article
Status
Published
Authors
Volume/ Edition
Volume 90 / Issue number 7
Pages
974-992
Abstract
The knockout of either At3g01500 gene, or At3g52720 gene encoding Arabidopsis thaliana βCA1 and αCA1 carbonic anhydrases, respectively led to a lower CA activity of chloroplast stroma preparations from knockout mutant plants αCA1-KO and βCA1-KO compared with the activity of such preparations from wild-type (WT) plants. To identify differences in the photosynthetic characteristics of mutant and WT plants, they were grown in low light (LL, 50-70 µmol quanta·m·s, natural conditions) and high light (HL, 400 µmol quanta·m·s, stressful conditions). The rate of CO assimilation measured at 400 µmoles quanta·m·s in αCA1-KO and βCA1-KO plants grown in LL was lower than in WT plants; in the circumstances, the rate of photosynthetic electron transport in αCA1-KO plants was lower, while in βCA1-KO plants higher than in WT; the CO content in chloroplasts was lower in βCA1-KO than in both WT and αKA1-KO, where it differed little; the value of the proton motive force was higher in βCA1-KO, and in αKA1-KO it was lower than in WT due to changes in the ΔpH value. The obtained results suggested that βCA1 facilitates the intake of inorganic carbon into chloroplasts, while αCA1 facilitates the conversion of bicarbonate into CO in chloroplasts stroma for its use in the reaction catalyzed by Rubisco. In αKA1-KO and βCA1-KO, the expression levels of genes encoding other chloroplast CAs were markedly different from the expression levels of these genes in WT; the patterns of the changes depended on the light intensity during cultivation. The content of hydrogen peroxide in leaves of both αCA1-KO and βCA1-KO plants was higher in LL and lower in HL than in WT. The expression levels of stress marker genes changed similarly in both types of mutant plants. The possible involvement of the chloroplast stroma CAs in the transmission of stress signals in higher plants are discussed.
Keywords
фотосинтез Arabidopsis хлоропласты карбоангидраза интенсивность света
Date of publication
04.02.2026
Year of publication
2026
Number of purchasers
0
Views
94

References

  1. 1. Wu, W., and Berkowitz, G. A. (1992) Stromal pH and photosynthesis are affected by electroneutral K+ and H+ exchange through chloroplast envelope ion channels, Plant Physiol., 98, 666-672, https://doi.org/10.1104/pp.98.2.666.
  2. 2. Badger, M. R., and Price, G. D. (1994) The role of carbonic anhydrase in photosynthesis, Ann. Rev. Plant Physiol. Plant Mol. Biol., 45, 369-392, https://doi.org/10.1146/annurev.pp.45.060194.002101.
  3. 3. Reed, M. L., and Graham, D. (1981) Carbonic anhydrase in plants: distribution, properties and possible physiological roles, Progr. Phytochem., 7, 47-94.
  4. 4. Henry, R. P. (1996) Multiple roles of carbonic anhydrase in cellular transport and metabolism, Annu. Rev. Physiol., 58, 523-38, https://doi.org/10.1146/annurev.ph.58.030196.002515.
  5. 5. Moroney, J. V., Bartlett, S. G., and Samuelsson, G. (2001). Carbonic anhydrases in plants and algae, Plant Cell Environ., 24, 141-153, https://doi.org/10.1046/j.1365-3040.2001.00669.x.
  6. 6. Fabre, N., Reiter I., Becuwe-Linka, N., Genty, B., and Rumeau, D. (2007) Characterization and expression analysis of genes encoding alpha and beta carbonic anhydrases in Arabidopsis, Plant Cell Environ., 30, 617-629, https://doi.org/10.1111/j.1365-3040.2007.01651.x.
  7. 7. Fawcett, T. W., Browse, J. A., Volokita, M., and Bartlett, S. G. (1990) Spinach carbonic-anhydrase primary structure deduced from the sequence of a cDNA clone, J. Biol. Chem., 265, 5414-5417, https://doi.org/10.1016/S0021-9258 (19)39375-5.
  8. 8. Okabe, K., Yang, S. Y., Tsuzuki, M., and Miyachi, S. (1984) Carbonic anhydrase: its content in spinach leaves and its taxonomic diversity studied with antispinach leaf carbonic anhydrase antibody, Plant Sci. Lett., 33, 145-153, https://doi.org/10.1016/0304-4211 (84)90004-X.
  9. 9. Bird, I. F., Cornelius, M. J., and Keys, A. J. (1980) Effect of carbonic anhydrase on the activity of ribulose bisphosphate carboxylase, J. Exp. Bot., 31, 365-369, https://doi.org/10.1093/jxb/31.2.365.
  10. 10. Shen, J., Li, Z., Fu, Y., and Liang, J. (2021) Identification and molecular characterization of the alternative spliced variants of beta carbonic anhydrase 1 (βCA1) from Arabidopsis thaliana, PeerJ, 9, e12673, https://doi.org/10.7717/peerj.12673.
  11. 11. Villarejo, A., Buren, S., Larsson, S., Dejardin, A., Monne, M., Rudhe, C., Karlsson, J., Jansson, S., Lerouge, P., Rolland, N., Heijne, G., Grebe, M., Bako, L., and Samuelsson, G. (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast, Nature Cell Biol., 7, 1224-1231, https://doi.org/10.1038/ncb1330.
  12. 12. Hines, K. M., Chaudhari, V., Edgeworth, K. N., Owens, T. G., and Hanson, M. R. (2021) Absence of carbonic anhydrase in chloroplasts affects C3 plant development but not photosynthesis, Proc. Natl. Acad. Sci. USA, 118, e2107425118, https://doi.org/10.1073/pnas.2107425118.
  13. 13. He, Y., Duan, W., Xue, B., Cong, X., Sun, P., Hou, X., and Liang, Y. K. (2023) OsαCA1 affects photosynthesis, yield potential, and after use efficiency in rice, Int. J. Mol. Sci., 14, 5560, https://doi.org/10.3390/ijms24065560.
  14. 14. Sharma, N., Froehlich, J. E., Rillema, R., Raba, D. A., Chambers, T., Kerfeld, C., Kramer, D., Walker, B., and Brandizzi, F. (2023) Arabidopsis stromal carbonic anhydrases exhibit non-overlapping roles in photosynthetic efficiency and development, Plant J., 115, 386-397, https://doi.org/10.1111/tpj.16231.
  15. 15. Friso, G., Giacomelli, L., Ytterberg, A. J., Peltier, J. B., Rudella, A., Sun, Q., and Wijk, K. J. (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database, Plant Cell, 16, 478-99, https://doi.org/10.1105/tpc.017814.
  16. 16. Ignatova, L., Zhurikova, E., and Ivanov, B. (2019) The presence of the low molecular mass carbonic anhydrase in photosystem II of C3 higher plants, J. Plant Physiol., 232, 94-99, https://doi.org/10.1016/j.jplph. 2018.11.017.
  17. 17. Fedorchuk, T. P., Kireeva, I. A., Opanasenko, V. K., Terentyev, V. V., Rudenko, N. N., Borisova-Mubarakshina, M. M., and Ivanov, B. N. (2021) Alpha carbonic anhydrase 5 mediates stimulation of ATP synthesis by bicarbonate in isolated Arabidopsis thylakoids, Front. Plant Sci., 12, 662082, https://doi.org/10.3389/fpls.2021.662082.
  18. 18. Rudenko, N. N., Ignatova, L. K., and Ivanov, B. N. (2007) Multiple sources of carbonic anhydrase activity in pea thylakoids. Soluble and membrane-bound forms, Photosynth. Res., 91, 81-89, https://doi.org/10.1007/s11120007-9148-2.
  19. 19. Fedorchuk, T., Rudenko, N., Ignatova L., and Ivanov, B. (2014) The presence of soluble carbonic anhydrase in the thylakoid lumen of chloroplasts from Arabidopsis leaves, J. Plant Physiol., 171, 903-906, https://doi.org/10.1016/j.jplph.2014.02.009.
  20. 20. Журикова Е. М., Игнатова Л. К., Руденко Н. Н., Мудрик В. А., Ветошкина Д. В., Иванов Б. Н. (2016) Участие двух карбоангидраз альфа семейства в фотосинтетических реакциях Arabidopsis thaliana, Биохимия, 81, 1463-1470, https://doi.org/10.1134/S0006297916100151.
  21. 21. Nadeeva, E. M., Ignatova, L. K., Rudenko, N. N., Vetoshkina, D. V., Naydov, I. A., Kozuleva, M. A., and Ivanov, B. N. (2023) Features of photosynthesis in Arabidopsis thaliana plants with knocked out gene of alpha carbonic anhydrase 2, Plants, 12, 1763, https://doi.org/10.3390/plants12091763.
  22. 22. Price, G. D., von Caemmerer, S., Evans, J. R., Yu. J.-W., Lloyd, J., Oja, V., Kell, P., Harrison, K., Gallagher, A., and Badger, M. R. (1994) Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco has a minor effect on photosynthetic CO2 assimilation, Planta, 193, 331-340, https://doi.org/10.1007/BF00201810.
  23. 23. Ferreira, F., Guo, C., and Coleman, J. (2008) Reduction of plastid-localized carbonic anhydrase activity results in reduced Arabidopsis seedling survivorship, Plant Physiol., 147, 585-594, https://doi.org/10.1104/pp.108.118661.
  24. 24. Hu, H., Boisson-Dernier, A., Israelsson-Nordström, M., Böhmer, M., Xue, S., Ries, A., Godoski J., Kuhn, J. M., and Schroeder, J. I. (2010) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells, Nat. Cell Biol., 12(1), 87-93, https://doi.org/10.1038/ncb2009.
  25. 25. Chen, T., Wu, H., Wu, J., Fan, X., Li, X., and Lin, Y. (2017) Absence of OsbCA1 causes a CO2 deficit and affects leaf photosynthesis and the stomatal response to CO2 in rice, Plant J., 90, 344-357, https://doi.org/10.1111/tpj.13497.
  26. 26. DiMario, R. J., Quebedeaux, J. C., Longstreth, D. J., Dassanayake, M., Hartman, M. M., and Moroney, J. V. (2016) The cytoplasmic carbonic anhydrases βCA2 and βCA4 are required for optimal plant growth at low CO2, Plant Physiol., 171, 280-293, https://doi.org/10.1104/pp.15.01990.
  27. 27. Hoang, C., and Chapman, K. (2002) Biochemical and molecular inhibition of plastidial carbonic anhydrase reduces the incorporation of acetate into lipids in cotton embryos and tobacco cell suspensions and leaves, Plant Physiol., 128, 1417-1427, https://doi.org/10.1104/pp.010879.
  28. 28. Wasternack, C., and Feussner, I. (2018) The oxylipin pathways: biochemistry and function, Annu. Rev. Plant. Biol., 69, 363-386, https://doi.org/10.1146/annurev-arplant-042817-040440.
  29. 29. Slaymaker, D. H., Navarre, D. A., Clark, D., del Pozo, O., Martin, G. B., and Klessig, D. (2002) The tobacco salicylic acid binding protein 3 (SABP3) is the chloroplast carbonic anhydrase which exhibits antioxidant activity and plays a role in the hypersensitive defense response, Proc. Natl. Acad. Sci. USA, 99, 11640-11645, https://doi.org/10.1073/pnas.182427699.
  30. 30. Medina-Puche, L., Castelló, M., Canet, J., Lamilla J., Colombo, M., and Tornero, P. (2017) β-carbonic anhydrases play a role in salicylic acid perception in Arabidopsis, PLoS One, 12, e0181820, https://doi.org/10.1371/journal. pone.0181820.
  31. 31. Rudenko, N. N., Fedorchuk, T. P., Vetoshkina, D. V., Zhurikova, E. M., Ignatova, L. K., and Ivanov, B. N. (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, https://doi.org/10.1007/s00709017-1133-9.
  32. 32. Rudenko, N. N., Fedorchuk, T. P., Terentyev, V. V., Dymova, O. V., Naydov, I. A., Golovko, T. K., BorisovaMubarakshina, M. M., and Ivanov, B. N. (2020) The role of carbonic anhydrase α-CA4 in the adaptive reactions of photosynthetic apparatus. The study with α-CA4 knockout plants, Protoplasma, 257, 489-499, https://doi.org/10.1007/s00709-019-01456-1.
  33. 33. Restrepo, S., Myers, K., del Pozo, O., Martin, G., Hart, A., Buell, C. R., Fry, W. E., and Smart, C. D. (2005) Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase, Mol. Plant Micr. Interact. J., 18, 913-922, https://doi.org/10.1094/MPMI-18-0913.
  34. 34. Руденко Н. Н., Ветошкина Д. В., Федорчук Т. П., Иванов Б. Н. (2017) Влияние освещенности растений при разном фотопериоде на уровень экспрессии генов карбоангидраз αи β-семейств в листьях Arabidopsis thaliana, Биохимия, 82, 1318-1329.
  35. 35. Rudenko, N. N., Ignatova, L. K., Naydov, I. A., Novichkova, N. S., and Ivanov, B. N. (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 αand β-families in Arabidopsis thaliana leaves, Plants, 14, 2113, https://doi.org/10.3390/plants11162113.
  36. 36. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72, 248-254, https://doi.org/10.1016/00032697 (76)90527-3.
  37. 37. Khristin, M. S., Ignatova, L. K., Rudenko, N. N., Ivanov, B. N., and Klimov, V. V. (2004) Photosystem II associated carbonic anhydrase activity in higher plants is situated in core complex, FEBS Lett., 577, 305-308, https://doi.org/10.1016/j.febslet.2004.10.001.
  38. 38. Witt, H.T. (1979) Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field, Biochim. Biophys. Acta, 505, 355-427, https://doi.org/10.1016/0304-4173 (79)90008-9.
  39. 39. Cruz, J. A., Avenson, T. J., Kanazawa, A., Takizawa, K., Edwards, G. E., and Kramer, D. A. (2005) Plasticity in light reactions of photosynthesis for energy production and photo-protection, J. Exp. Botany, 56, 395-406, https://doi.org/10.1093/jxb/eri022.
  40. 40. Gilmore, A. M., and Yamamoto, H. Y. (1991) Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport, Plant Physiol., 96, 635-643, https://doi.org/10.1104/pp.96.2.635.
  41. 41. Klughammer, C., and Schreiber, U. (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method, PAM Appl. Notes, 1, 201-247.
  42. 42. Flexas, J., Ortuño, M. F., Ribas-Carbo, M., Diaz-Espejo, A., Flórez-Sarasa, I. D, and Medrano, H. (2007) Mesophyll conductance to CO2 in Arabidopsis thaliana, New Phytol., 175, 501-511, https://doi.org/10.1111/j.14698137.2007.02111.x.
  43. 43. Busch, F. A., Ainsworth, E. A., Amtmann, A., Cavanagh, A. P., Driever, S. M., Ferguson, J. N., Kromdijk, J., Lawson, T., Leakey, A. D. B., Matthews, J. S. A., Meacham-Hensold, K., Vath, R. L., Vialet-Chabrand, S., Walker, B. J., and Papanatsiou, M. A. (2024) A guide to photosynthetic gas exchange measurements: fundamental principles, best practice and potential pitfalls, Plant Cell Environ., 47, 3344-3364, https://doi.org/10.1111/pce.14815.
  44. 44. Kaplan, F., Zhao, W., Richard, J. T., Wheeler, R. M., Guy, C. L., and Levine, L. H. (2012) Transcription and metabolic insights into the differential physiological responses of Arabidopsis to optimal and supraoptimal atmospheric CO2, PLoS ONE, 7, e43583, https://doi.org/10.1371/journal.pone.0043583.
  45. 45. Lichtenthaler, H. K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes, Methods Enzymol., 148, 350-382, https://doi.org/10.1016/0076-6879 (87)48036-1.
  46. 46. Любимов В. Ю., Застрижная О. М. (1992) Роль перекиси водорода в фотодыхании C4-растений, Физиол. Раст., 39, 701-710, https://doi.org/10.31857/S0015330322010080.
  47. 47. Borisova-Mubarakshina, M. M., Vetoshkina, D. V., Naydov, I. A., Rudenko, N. N., Zhurikova, E. M., Balashov, N. V., Ignatova, L. K., Fedorchuk, T. P., and Ivanov, B. N. (2020) Regulation of the size of photosystem II light harvesting antenna represents a universal mechanism of higher plant acclimation to stress conditions, Funct. Plant Biol., 47, 959-969, https://doi.org/10.1071/FP19362.
  48. 48. Borisova-Mubarakshina, M. M., Naydov, I. A., Vetoshkina, D. V., Kozuleva, M. A, Rudenko, N. N., and Ivanov, B. N. (2022) Photosynthetic antenna size regulation as an essential mechanism of higher plants acclimation to biotic and abiotic factors: the role of the chloroplast plastoquinone pool and hydrogen peroxide, in: Vegetation Index and Dynamics, pp. 277-338, https://doi.org/10.5772/intechopen.97664.
  49. 49. Myers, R. J., Fichman, Y., Zandalinas, S. I., and Mittler, R. (2023) Jasmonic acid and salicylic acid modulate systemic reactive oxygen species signaling during stress responses, Plant Physiol., 191, 862-873, https://doi.org/10.1093/plphys/kiac449.
  50. 50. Devireddy, A. R., Arbogast, J., and Mittler, R. (2020) Coordinated and rapid whole-plant systemic stomatal responses, New Phytol., 225, 21-25, https://doi.org/10.1111/nph.16143.
  51. 51. Chini, A., Fonseca, S., Fernández, G., Adie, B., Chico, J. M., Lorenzo, O., García-Casado, G., López-Vidriero, I., Lozano, F. M., Ponce, M. R., Micol, J. L., and Solano, R. (2007) The JAZ family of repressors is the missing link in jasmonate signalling, Nature, 448, 666-671, https://doi.org/10.1038/nature06006.
  52. 52. Anderson, L., and Carol, A. (2004) Enzyme co-localization with rubisco in pea leaf chloroplasts, Photosynth. Res., 82, 49-58, https://doi.org/10.1023/B:PRES.0000040443.92346.37.
  53. 53. Wang, L., Jin, X., Li, Q., Wang, X., Li, Z., and Wu, X. (2016) Comparative proteomics reveals that phosphorylation of β carbonic anhydrase 1 might be important for adaptation to drought stress in Brassica napus, Sci. Rep., 6, 39024, https://doi.org/10.1038/srep39024.
  54. 54. Soto, D., Cordoba, J. P., Villarreal, F., Bartoli, C., Schmitz, J., Maurino, V. G., Braun, H. P., Pagnussat, G. C., and Zabaleta, E. (2015) Functional characterization of mutants affected in the carbonic anhydrase domain of the respiratory complex I in Arabidopsis thaliana, Plant J., 83, 831-844, doi: 10.1111/tpj.12930.
  55. 55. Yu, S., Zhang, X., Guan, Q., Takano, T., and Liu, S. (2007) Expression of a carbonic anhydrase gene is induced by environmental stresses in rice (Oryza sativa L.), Biotechnol. Lett., 29, 89-94, https://doi.org/10.1007/s10529006-9199-z.
  56. 56. Rudenko, N. N., Permyakova, N. V., Ignatova, L. K., Nadeeva, E. M., Zagorskaya, A. A., Deineko, E. V., and Ivanov, B. N. (2022) The role of carbonic anhydrase αCA4 in photosynthetic reactions in Arabidopsis thaliana studied, using the Cas9 and T-DNA induced mutations in its gene, Plants, 11, 3303, https://doi.org/10.3390/plants11233303.
  57. 57. Nagao, M., Minami, A., Arakawa, K., Fujikawa, S., and Takezawa, D. (2005) Rapid degradation of starch in chloroplasts and concomitant accumulation of soluble sugars associated with ABA-induced freezing tolerance in the moss Physcomitrella patens, J. Plant Physiol., 162, 169-180, https://doi.org/10.1016/j.jplph.2004.06.012.
  58. 58. Thalmann, M., Pazmino, D., Seung, D., Horrer, D., Nigro, A., Meier, T., Kölling, K., Pfeifhofer, H. W., Zeeman, S. C., and Santelia, D. (2016) Regulation of leaf starch degradation by abscisic acid is important for osmotic stress tolerance in plants, Plant Cell, 28, 1860-1878, https://doi.org/10.1105/tpc.16.00143.
  59. 59. Anderson, J. M. (1986) Photoregulation of the composition, function, and structure of thylakoid membranes, Ann. Rev. Plant Physiol. Plant Mol. Biol., 37, 93-136, https://doi.org/10.1146/annurev.pp.37.060186.000521.
  60. 60. Pieterse, C. M., Van Der Does, D., Zamioudis, C., Leon-Reyes, A., and Van Wees, S. C. (2012) Hormonal modulation of plant immunity, Ann. Rev. Cell Dev. Biol., 28, 489-521, https://doi.org/10.1146/annurev-cellbio092910-154055.
  61. 61. Ветошкина Д. В., Позднякова-Филатова И. Ю., Журикова Е. М., Фролова А. А., Найдов И. А., Иванов Б. Н., Борисова-Мубаракшина М. М. (2019) Возрастание потенциала адаптации к повышенной освещенности растений ячменя, колонизированных ризобактериями P. putida BS3701, Прикл. Биохим. Микробиол., 55, 181-190, https://doi.org/10.1134/S0555109919020132.
QR
Translate

Indexing

Scopus

Scopus

Scopus

Crossref

Scopus

Higher Attestation Commission

At the Ministry of Education and Science of the Russian Federation

Scopus

Scientific Electronic Library