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Effect of light intensity under different photoperiods on expression level of carbonic anhydrase genes of the α- and β-families in Arabidopsis thaliana leaves

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Abstract

Changes in expression levels of genes encoding carbonic anhydrases α-CA1, α-CA2, α-CA4, β-CA1, β-CA2, βCA3, β-CA4, β-CA5, and β-CA6 in Arabidopsis thaliana leaves after light increase from 80 to 400 μmol PAR quanta·m−2·s−1 were investigated under short day (8 h) and long day (16 h) photoperiods. The expression of two forms of the gene, At3g01500.2 and At3g01500.3, encoding the most abundant carbonic anhydrase of leaves, β-CA1, situated in chloroplast stroma, was found. The content of At3g01500.3 transcripts was higher by approximately an order of magnitude compared to the content of At3g01500.2 transcripts. When plants were adapted to high light intensity under short day photoperiod, the expression level of both forms increased, whereas under long day photoperiod, the content of At3g01500.3 transcripts increased, and the content of transcripts of At3g01500.2 decreased. The expression levels of the At3g01500.3 gene and of genes encoding chloroplast carbonic anhydrases α-CA1, α-CA4, α-CA2 and cytoplasmic carbonic anhydrase β-CA2 increased significantly in response to increase in light intensity under short day, and these of the first three genes increased under long day as well. The expression level of the gene encoding α-CA2 under long day photoperiod as well as of genes of chloroplast β-CA5 and β-CA4 from plasma membranes and mitochondrial β-CA6 under both photoperiods depended insignificantly on light intensity. Hypotheses about the roles in higher plant metabolism of the studied carbonic anhydrases are discussed considering the effects of light intensity on expression levels of the correspondent genes.

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Abbreviations

CA:

carbonic anhydrase

Chl:

chlorophyll

HL:

high light (light of high intensity)

LL:

low light (light of low intensity)

PAR:

photosynthetically active radiation

PSII:

photosystem II

Rubisco:

ribulose-bisphosphate-carboxylase/oxygenase

References

  1. Fabre, N., Reiter, I. M., Becuwe-Linkan, N., Genty, B., and Rumeau, D. (2007) Characterization and expression analysis of genes encoding α and β carbonic anhydrases in Arabidopsis, Plant Cell Environ., 30, 617–629.

    Article  CAS  PubMed  Google Scholar 

  2. Moroney, J. V., Ma, Y., Frey, W. D., Fusilier, K. A., Pham, T. T., Simms, T. A., Di Mario, R. J., Yang, J., and Mukherjee, B. (2011) The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles, Photosynth. Res., 109, 133–149.

    Article  CAS  PubMed  Google Scholar 

  3. 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.

    Article  CAS  PubMed  Google Scholar 

  4. Friso, G., Giacomelli, L., Ytterberg, A. J., Peltier, J.-B., Rudella, A., Sun, Q., and Van Wijka, 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, 478–499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Villarejo, A., Buren, S., Larsson, S., Dejardin, A., Monne, M., Rudhe, Ch., Karlsson, J., Jansson, S., Lerouge, P., Rolland, N., Von 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, Nat. Cell Biol., 7, 1224–1231.

    Article  PubMed  Google Scholar 

  6. Zhurikova, E. M., Ignatova, L. K., Rudenko, N. N., Mudrik, V. A., Vetoshkina, D. V., and Ivanov, B. N. (2016) Participation of two carbonic anhydrases of the alpha family in photosynthetic reactions in Arabidopsis thaliana, Biochemistry (Moscow), 81, 1463–1470.

    Article  Google Scholar 

  7. 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 anti-sense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation, Planta, 193, 331–340.

    Article  CAS  Google Scholar 

  8. Buren, S. (2010) Targeting and Function of CAH1Characterisation of a Novel Protein Pathway to the Plant Cell Chloroplast, PhD Thesis, Umea University, Sweden.

    Google Scholar 

  9. Rudenko, N. N., Ignatova, L. K., Fedorchuk, T. P., and Ivanov, B. N. (2015) Carbonic anhydrases in photosynthetic cells of higher plants, Biochemistry (Moscow), 80, 674–687.

    Article  CAS  Google Scholar 

  10. Restrepo, S., Myers, K. L., Del Pozo, O., Martin, G. B., Hart, A. L., 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 Microbe Interact., 18, 913–922.

    Article  CAS  PubMed  Google Scholar 

  11. Frick, U. B., and Schaller, A. (2002) cDNA microarray analysis of fusicoccin-induced changes in gene expression in tomato plants, Planta, 216, 83–94.

    Article  CAS  PubMed  Google Scholar 

  12. De la Torre, W. R., and Burkey, K. O. (1990) Acclimation of barley to changes in light intensity: chlorophyll organization, Photosynth. Res., 24, 117–125.

    Article  PubMed  Google Scholar 

  13. Stitt, M. (1986) Limitation of photosynthesis by carbon metabolism. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2, Plant Physiol., 81, 1115–1122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Maenpaa, P., and Andersson, B. (1989) Photosystem II heterogeneity and long-term acclimation of light-harvesting, Z. Naturforsch., 44, 403–406.

    CAS  Google Scholar 

  15. Blazquez, M. A. (2005) The right time and place for making flowers, Science, 309, 1024–1025.

    Article  PubMed  Google Scholar 

  16. Wellmer, F., and Riechmann, J. L. (2010) Gene networks controlling the initiation of flower development, Trends Genet., 26, 519–527.

    Article  CAS  PubMed  Google Scholar 

  17. Ignatova, L. K., Rudenko, N. N., Mudrik, V. A., Fedorchuk, T. P., and Ivanov, B. N. (2011) Carbonic anhydrase activity in Arabidopsis thaliana thylakoid membrane and fragments enriched with PSI or PSII, Photosynth. Res., 110, 89–98.

    Article  CAS  PubMed  Google Scholar 

  18. Schagger, H., and Von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa, Anal. Biochem., 166, 368–379.

    Article  CAS  PubMed  Google Scholar 

  19. Morosinotto, T., Bassi, R., Frigerio, S., Finazzi, G., Morris, E., and Barber, J. (2006) Biochemical and structural analyses of a higher plant photosystem II supercomplex of a photosystem I-less mutant of barley: consequences of a chronic overreduction of the plastoquinone pool, FEBS J., 273, 4616–4630.

    Article  CAS  PubMed  Google Scholar 

  20. Onda, Y., Matsumura, T., Kimata-Ariga, Y., Sakakibara, H., Sugiyama, T., and Hase, T. (2000) Differential interaction of maize root ferredoxin: NADP1 oxidoreductase with photosynthetic and non-photosynthetic ferredoxin isoproteins, Plant Physiol., 123, 1037–1045.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Weigel, D., and Glazebrook, J. (2002) Arabidopsis: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  22. Bailey, S., Walters, R. G., Jansson, S., and Horton, P. (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses, Planta, 213, 794–801.

    Article  CAS  PubMed  Google Scholar 

  23. Borisova-Mubarakshina, M. M., Vetoshkina, D. V., Rudenko, N. N., Shirshikova, G. N., Fedorchuk, T. P., Naydov, I. A., and Ivanov, B. N. (2014) The size of the lightharvesting antenna of higher plant photosystem II is regulated by illumination intensity through transcription of antenna protein genes, Biochemistry (Moscow), 79, 520–523.

    Article  CAS  Google Scholar 

  24. Ruban, A. V. (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage, Plant Physiol., 140, 1903–1916.

    Article  Google Scholar 

  25. Alekhina, N. D., Balnokhin, Yu. V., Gavrilenko, V. F., Zhigalova, T. V., Meichik, N. R., Nosov, A. M., Polesskaya, O. G., Kharitonashvili, E. V., and Chub, V. V. (2005) Plant Physiology (Ermakova, I. P., ed.) [in Russian], Akademiya, Moscow, pp. 416–419.

  26. Reed, M. L., and Graham, D. (1981) Carbonic anhydrase in plants: distribution, properties and possible physiological roles, Progr. Phytochem., 7, 47–94.

    CAS  Google Scholar 

  27. DiMario, R. J., Quebedeaux, J. C., Longstreth, D. J., Dassanayaki, M., Hartman, M. M., and Moroney, J. V. (2016) βCA2 and βCA4 are required for optimal plant growth in a low CO2 environment, Plant Physiol., 171, 280–293.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hu, H., Boisson-Dernier, A., Israelsson-Nordstrom, M., Bohmer, 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, 87–93.

    Article  CAS  PubMed  Google Scholar 

  29. Ignatova, L. K., Moskvin, O. V., and Ivanov, B. N. (2001) Effects of carbonic anhydrase inhibitors on proton exchange and photosynthesis in pea protoplasts, Russ. J. Plant Physiol., 48, 467–472.

    Article  CAS  Google Scholar 

  30. Zhurikova, E. M., Ignatova, L. K., Semenova, G. A., Rudenko, N. N., Mudrik, V. A., and Ivanov, B. N. (2015) Effect of knockout of α-carbonic anhydrase 4 gene on photosynthetic characteristics and starch accumulation in leaves of Arabidopsis thaliana, Russ. J. Plant Physiol., 62, 564–569.

    Article  CAS  Google Scholar 

  31. Fedorchuk, T. P., Rudenko, N. N., Ignatova, L. K., and Ivanov, B. N. (2014) The presence of soluble carbonic anhydrase in the thylakoid lumen of chloroplasts from Arabidopsis leaves, J. Plant Physiol., 171, 903–906.

    Article  CAS  PubMed  Google Scholar 

  32. Onoiko, E. B., Polishchuck, A. V., and Zolotareva, E. K. (2010) The stimulation of photophosphorylation in isolated spinach chloroplasts by exogenous bicarbonate: the role of carbonic anhydrase, Rep. Nat. Acad. Sci. Ukr., 10, 161165.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Basic Biological Problems, Russian Academy of Sciences, 142290, Pushchino, Moscow Region, Russia

    N. N. Rudenko, D. V. Vetoshkina, T. P. Fedorchuk & B. N. Ivanov

Authors
  1. N. N. Rudenko
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  2. D. V. Vetoshkina
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  3. T. P. Fedorchuk
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  4. B. N. Ivanov
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Corresponding author

Correspondence to B. N. Ivanov.

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Original Russian Text © N. N. Rudenko, D. V. Vetoshkina, T. P. Fedorchuk, B. N. Ivanov, 2017, published in Biokhimiya, 2017, Vol. 82, No. 9, pp. 1318-1329.

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Rudenko, N.N., Vetoshkina, D.V., Fedorchuk, T.P. et al. Effect of light intensity under different photoperiods on expression level of carbonic anhydrase genes of the α- and β-families in Arabidopsis thaliana leaves. Biochemistry Moscow 82, 1025–1035 (2017). https://doi.org/10.1134/S000629791709005X

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  • DOI: https://doi.org/10.1134/S000629791709005X

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