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Metabolic compensation in Arabidopsis thaliana catalase-deficient mutants

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Abstract

Multigenic families are widely represented in the genomes of higher plants, and are required for the reliability of cellular functions. Damage of individual genes can be compensated by diverse metabolic alterations, but the exact mechanisms of such compensations still remain not fully understood. Here we present novel data regarding the mechanisms of metabolic compensation in photorespiratory knock-out mutants cat2, cat3 and cat2cat3 of Arabidopsis thaliana, which are lacking activity of catalase isoforms CAT2 and CAT3. It was found that cultivation of the mutants under low light at optimal or increased temperature did not result in any morphological, physiological or biochemical signs of oxidative stress. Each of the mutant lines shows specific features of the compensatory mechanisms. Increased activity of CAT3 isoenzyme was found in the cat2 mutant, whereas cat3 and cat2cat3 demonstrate induction of CAT1, an isoform normally absent in young leaves, as well as activation of peroxidases, namely APX and POD. Comparison of these results and earlier published data revealed that the lack of CAT2 and CAT3 isoforms is compensated by preferential activation of non-enzymatic and enzymatic protection mechanisms, respectively.

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References

  1. Arabidopsis Genome Initiative, Analysis of the genome sequence of the flowering plant Arabidopsis thaliana, Nature, 2000, vol. 408, no. 6814, pp. 796–815.

    Google Scholar 

  2. Baird, W.V. and Meagher, R.B., A complex gene superfamily encodes actin in petunia, EMBO J., 1987, vol. 6, no. 11, pp. 3223–3231.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Ross, J., Li, Y., Lim, E., and Bowles, D.J., Higher plant glycosyltransferases, Genome Biol., 2001, vol. 2, no. 2, reviews 3004.

    Google Scholar 

  4. Tognolli, M., Penel, C., Greppin, H., and Simon, P., Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana, Gene, 2002, vol. 288, nos. 1–2, pp. 129–138.

    Article  PubMed  CAS  Google Scholar 

  5. Panchuk, I.I., Zentgraf, U., and Volkov, R.A., Expression of the Apx gene family during leaf senescence of Arabidopsis thaliana, Planta, 2005, vol. 222, no. 5, pp. 926–932.

    Article  PubMed  CAS  Google Scholar 

  6. Volkov, R.A., Panchuk, I.I., and Schoffl, F., Small heat shock proteins are differentially regulated during pollen development and following heat stress in tobacco, Plant. Mol. Biol., 2005, vol. 57, no. 4, pp. 487–502.

    Article  PubMed  CAS  Google Scholar 

  7. Zimmermann, P., Heinlein, C., Orendi, G., and Zentgraf, U., Senescence-specific regulation of catalases in Arabidopsis thaliana (L.) Heynh, Plant Cell Environ., 2006, vol. 29, no. 6, pp. 1049–1060.

    Article  PubMed  CAS  Google Scholar 

  8. Panchuk, I.I., Volkov, R.A., and Schoffl, F., Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis, Plant Physiol., 2002, vol. 129, no. 2, pp. 838–853.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Du, Y.Y., Wang, P.C., Chen, J., and Song, C.P., Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana, J. Integr. Plant Biol., 2008, vol. 50, no. 10, pp. 1318–1326.

    Article  PubMed  CAS  Google Scholar 

  10. Mhamdi, A., Queval, G., Chaouch, S., Vanderauwera, S., Van Breusegem, F., and Noctor, G., Catalase function in plants: a focus on Arabidopsis mutants as stressmimic models, J. Exp. Bot., 2010, vol. 61, no. 15, pp. 4197–4220.

    CAS  Google Scholar 

  11. Yoshida, T., Ohama, N., Nakajima, J., Kidokoro, S., Mizoi, J., Nakashima, K., Maruyama, K., Kim, J.-M., Seki, M., Todaka, D., Osakabe, Y., Sakuma, Y., Schoffl, F., Shinozaki, K., and Yamaguchi-Shinozaki, K., Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression, Mol. Genet. Genom., 2011, vol. 286, nos. 5–6, pp. 321–332.

    Article  CAS  Google Scholar 

  12. Kliebenstein, D.J., Monde, R.A., and Last, R.L., Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization, Plant Physiol., 1998, vol. 118, no. 2, pp. 637–650.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Agarwal, M., Katiyar-Agarwal, S., Sahi, C., Gallie, D.R., and Grover, A., Arabidopsis thaliana HSP100 proteins: kith and in, Cell Stress Chaperones, 2001, vol. 6, no. 3, pp. 219–224.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Lin, B.L., Wang, J.S., Liu, H.C., Chen, R.W., Meyer, Y., Barakat, A., and Delseny, M., Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana, Cell Stress Chaperones, 2001, vol. 6, no. 3, pp. 201–208.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Scharf, K.D., Siddique, M., and Vierling, E., The expanding family of arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains (Acd proteins), Cell Stress Chaperones, 2001, vol. 6, no. 3, pp. 225–237.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Yoshida, S., Tamaoki, M., Shikano, T., Nakajima, N., Ogawa, D., Ioki, M., Aono, M., Kubo, A., Kamada, H., Inoue, Y., and Saji, H., Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana, Plant Cell Physiol., 2006, vol. 47, no. 2, pp. 304–308.

    Article  PubMed  CAS  Google Scholar 

  17. Kubo, A., Sano, T., Saji, H., Tanaka, K., Kondo, N., and Tanaka, K., Primary structure and properties of glutathione reductase from Arabidopsis thaliana, Plant Cell Physiol., 1993, vol. 34, no. 8, pp. 1259–1266.

    CAS  Google Scholar 

  18. Frugoli, J.A., Zhong, H.H., Nuccio, M.L., McCourt, P., McPeek, M.A., Thomas, T.L., and McClung, C.R., Catalase is encoded by a multigene family in Arabidopsis thaliana (L.) Heynh, Plant Physiol., 1996, vol. 112, no. 1, pp. 327–336.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Kendall, A.C., Keys, A.J., Turner, J.C., Lea, P.J., and Miflin, B.J., The isolation and characterization of a catalase-deficient mutant of barley (Hordeum vulgare L.), Planta, 1983, vol. 159, no. 6, pp. 505–511.

    Article  PubMed  CAS  Google Scholar 

  20. Queval, G., Issakidis-Bourguet, E., Hoeberichts, F.A., Vandorpe, M., Gakiere, B., Vanacker, H., Miginiac-Maslow, M., Van Breusegem, F., and Noctor, G., Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death, Plant J., 2007, vol. 52, no. 4, pp. 640–657.

    Article  PubMed  CAS  Google Scholar 

  21. Gao, X., Yuan, H.M., Hu, Y.Q., Li, J., and Lu, Y.T., Mutation of Arabidopsis CATALASE2 results in hyponastic leaves by changes of auxin levels, Plant, Cell Environ., 2014, vol. 37, no. 1, pp. 175–188.

    Article  CAS  Google Scholar 

  22. Hu, Y.Q., Liu, S., Yuan, H.M., Li, J., Yan, D.W., Zhang, J.F., and Lu, Y.T., Functional comparison of catalase genes in the elimination of photorespiratory H2O2 using promoter- and 3'-untranslated region exchange experiments in the Arabidopsis cat2 photorespiratory mutant, Plant, Cell Environ., 2010, vol. 33, no. 10, pp. 1656–1670.

    Article  CAS  Google Scholar 

  23. Zhong, H.H. and McClung, C.R., The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases, Mol. Gen. Genet., 1996, vol. 251, no. 2, pp. 196–203.

    PubMed  CAS  Google Scholar 

  24. Michael, T.P. and McClung, C.R., Phase-specific circadian clock regulatory elements in Arabidopsis, Plant Physiol., 2002, vol. 130, no. 2, pp. 627–638.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Du, Z. and Bramlage, W., Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts, J. Agric. Food Chem., 1992, vol. 40, no. 9, pp. 1566–1570.

    Article  CAS  Google Scholar 

  26. Lushchak, V.I., Semchyshyn, H.M., and Lushchak, O.V., The classic methods to measure oxidative damage: lipid peroxides, thiobarbituric-acid reactive substances, and protein carbonyls, in Oxidative Stress in Aquatic Ecosystems, Abele, D., Vazquez-Medina, J.P., and Zenteno-Savin, T., Eds., Chichester, UK: Wiley, 2011, pp. 426–430.

    Google Scholar 

  27. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, nos. 1–2, pp. 248–254.

    Article  PubMed  CAS  Google Scholar 

  28. Doliba, I.M., Volkov, R.A., and Panchuk, I.I., Method of catalase activity determination in plants, Physiol. Biochem. Cult. Plants, 2010, vol. 42, no. 6, pp. 497–503.

    CAS  Google Scholar 

  29. Amako, K., Chen, G.X., and Asada, K., Separate assays for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants, Plant Cell Physiol., 1994, vol. 35, no. 3, pp. 497–504.

    CAS  Google Scholar 

  30. Budzhak, V.V., Biometrics, Chernivtsi: Ruta, 2013, p. 326.

    Google Scholar 

  31. Xing, Y., Jia, W., and Zhang, J., AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis, J. Exp. Bot., 2007, vol. 58, no. 11, pp. 2969–2981.

    Article  PubMed  CAS  Google Scholar 

  32. Xing, Y., Jia, W., and Zhang, J., AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis, Plant J., 2008, vol. 54, no. 3, pp. 440–451.

    Article  PubMed  CAS  Google Scholar 

  33. Volkov, R.A., Panchuk, I.I., Mullineaux, P.M., and Schoeffl, F., Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis, Plant. Mol. Biol., 2006, vol. 61, nos. 4–5, pp. 733–746.

    Article  PubMed  CAS  Google Scholar 

  34. Choudhury, F.K., Rivero, R.M., Blumwald, E., and Mittler, R., Reactive oxygen species, abiotic stress and stress combination, Plant J., 2016, vol. 90, no. 5, pp. 856–867.

    Article  PubMed  CAS  Google Scholar 

  35. Savoure, A., Thorin, D., Davey, M., Hua, X-J., Mauro, S., Van Montagu, M., Inzé, D., and Verbruggen, N., NaCl and CuSO4 treatments trigger distinct oxidative defense mechanisms in Nicotiana plumbaginifolia L., Plant, Cell Environ., 1999, vol. 22, no. 4, pp. 387–396.

    Article  CAS  Google Scholar 

  36. Ohama, N., Sato, H., Shinozaki, K., and Yamaguchi- Shinozaki, K., Transcriptional regulatory network of plant heat stress response, Trends Plant Sci., 2017, vol. 22, no. 1, pp. 53–65.

    Article  PubMed  CAS  Google Scholar 

  37. Pyrizhok, R.Yu., Volkov, R.A., and Panchuk, I.I., Peroxidase activity in maize seedlings upon heat stress, Physiol. Biochem. Cult. Plants, 2009, vol. 41, no. 1, pp. 44–49.

    CAS  Google Scholar 

  38. Pyrizhok, R.Yu. and Panchuk, I.I., Activity of Nicotiana tabacum L. peroxidase upon heat stress, Nauk. Wisnyk Chernivets. Univ.: Zb. Nauk. Prats, 2009, vol. 455, pp. 116–119.

    Google Scholar 

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Correspondence to I. I. Panchuk.

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Original Ukrainian Text © I.M. Buzduga, R.A. Volkov, I.I. Panchuk, 2018, published in Tsitologiya i Genetika, 2018, Vol. 52, No. 1, pp. 41–51.

The article was translated by the authors.

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Buzduga, I.M., Volkov, R.A. & Panchuk, I.I. Metabolic compensation in Arabidopsis thaliana catalase-deficient mutants. Cytol. Genet. 52, 31–39 (2018). https://doi.org/10.3103/S0095452718010036

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  • DOI: https://doi.org/10.3103/S0095452718010036

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