Photosynthetica 2016, 54(3):321-330 | DOI: 10.1007/s11099-016-0212-z

Response of the photosynthetic apparatus to UV-A and red light in the phytochrome B-deficient Arabidopsis thaliana L. hy3 mutant

V. D. Kreslavski1,2, F. J. Schmitt3, C. Keuer3, T. Friedrich3, G. N. Shirshikova1, S. K. Zharmukhamedov1, A. A. Kosobryukhov1, S. I. Allakhverdiev1,2,4,*
1 Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia
2 Controlled Photobiosynthesis Laboratory, Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia
3 Technical University of Berlin, Institute of Chemistry Sekr. PC 14, Max-Volmer-Laboratory of Biophysical Chemistry, Berlin, Germany
4 Department of Plant Physiology, Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia

The effect of UV-A radiation (365 nm) and the protective effect of preillumination with red light (RL, 664 nm, 10 min) or with a combination of red and far-red light (FRL, 727 nm, 10 min) on the activity of the PSII as well as the expression levels of selected genes, especially those encoding chloroplast proteins (sAPX, tAPX, CAB1, and D1), were studied in leaves of the 26-d-old hy3 mutant of Arabidopsis thaliana, which is deficient in the phytochrome B apoprotein. The effects were compared with corresponding effects observed in the hy2 mutant of A. thaliana, which is deficient in the phytochrome chromophore. Illumination with UV-A decreased the photosynthetic pigment content, the maximum photochemical quantum yield of PSII (Fv/Fm), and the effective quantum yield of PSII (ΦPSII). The reduction of the Fv/Fm ratio and ΦPSII was more pronounced in the mutants as compared to wild-type plants (WT). The preillumination of the leaves with RL caused a significant reduction in the inhibitory effect of UV-radiation on the PSII activity in the WT plants, but it caused only a small decrease in the hy3 mutant. The preillumination of leaves with RL and FRL combination compensated the protective effect of RL on the UV-induced decrease of the fluorescence parameters in the WT. Such reversibility is typical for involvement of red/far-red reversible phytochromes at low intensity light. The results suggest an important role of red/far-red reversible phytochromes (phytochrome B) in the resistance of PSII to UV-A radiation caused by changes in contents of either carotenoids or other UV-absorbing pigments probably through biosynthesis of these pigments. The data also demonstrated that phytochrome B and other phytochromes can affect the PSII stress resistance by the fast regulation of the expression of genes encoding antioxidant enzymes and transcription factors at the step of gene transcription.

Keywords: Arabidopsis thaliana; chlorophyll a fluorescence; photosystem II; phytochrome system; stress resistance; transcription; ultraviolet

Received: December 29, 2015; Accepted: February 19, 2016; Published: September 1, 2016Show citation

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Kreslavski, V.D., Schmitt, F.J., Keuer, C., Friedrich, T., Shirshikova, G.N., Zharmukhamedov, S.K., Kosobryukhov, A.A., & Allakhverdiev, S.I. (2016). Response of the photosynthetic apparatus to UV-A and red light in the phytochrome B-deficient Arabidopsis thaliana L. hy3 mutant. Photosynthetica, 54(3), 321-330. doi: 10.1007/s11099-016-0212-z.
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    References

    1. Aleksandrov V., Krasteva V., Paunov M. et al.: Deficiency of some nutrient elements in bean and maize plants analyzed by luminescent method.-Bulg. J. Agric. Sci. 20: 24-30, 2014.
    2. Allakhverdiev S.I., Kreslavski V.D., Klimov V.V. et al.: Heat stress: An overview of molecular responses in photosynthesis.-Photosynth. Res. 98: 541-550, 2008. Go to original source...
    3. Allakhverdiev S.I., Murata N.: Environmental stress inhibits the synthesis de novo of proteins involved in the photodamagerepair cycle of Photosystem II in Synechocystis sp. PCC 6803-Biochim. Biophys. Acta 1657: 23-32, 2004.
    4. Asada K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions.-Plant Physiol. 141: 391-396, 2006. Go to original source...
    5. Babu T.S., Jansen M.A.K., Greenberg B.M. et al.: Amplified degradation of photosystem II D1 and D2 proteins under a mixture of photosynthetically active radiation and UV-B radiation: dependence on redox status of photosystem II.-Photoch. Photobio. 69: 553-559, 1999. Go to original source...
    6. Boccalandro H.E., Ploschuk E.L., Yanovsky M.J. et al.: Increased phytochrome B alleviates density effects on tuber yield of field potato crops.-Plant Physiol. 133: 1539-1546, 2003. Go to original source...
    7. Boccalandro H.E., Rugnone M.L., Moreno J.E. et al.: Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis.-Plant Physiol. 150: 1083-1092, 2009. Go to original source...
    8. Breštic M., Živcák M., Kunderlíková K. et al.: Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines.-Photosynth. Res. 125: 151-166, 2015. Go to original source...
    9. Carvalho R.F., Campos M.L., Azevedo R.A.: The role of phytochrome in stress tolerance.-J. Integr. Plant Biol. 53: 920-929, 2011.
    10. Chory J., Peto C.A., Ashbaugh M. et al.: Different roles for phytochrome in etiolated and green plants deduced from characterization of Arabidopsis thaliana mutants.-Plant Cell 1: 867-880, 1989. Go to original source...
    11. Davletova S., Rizhsky L., Liang H. et al.: Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis.-Plant Cell 17: 268-281, 2005. Go to original source...
    12. Gutierrez L., Mauriat M., Guénin S. et al.: The lack of a systematic validation of reference genes: a serious pitfall undervalued in reverse transcription-polymerase chain reaction (RT-PCR) analysis in plant.-Plant Biotechnol. J. 6: 609-618, 2008. Go to original source...
    13. Hu W., Franklin K.A., Sharrock R.A. et al.: Unanticipated regulatory roles for Arabidopsis phytochromes revealed by null mutant analysis.-P. Natl. Acad. Sci. USA 110: 1542-1547, 2013. Go to original source...
    14. Jiao Y., Lau O.S., Deng X.W.: Light-regulated transcriptional networks in higher plants.-Nat. Rev. Genet. 8: 217-230, 2007. Go to original source...
    15. Joshi P.N., Biswal B., Biswal U.C.: Effect of UV-A on aging of wheat leaves and role of phytochrome.-Environ. Exp. Bot. 31: 267-276, 1991. Go to original source...
    16. Koussevitzky S., Suzuki N., Huntington S. et al.: Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress.-J. Biol. Chem. 283: 34197-34203, 2008. Go to original source...
    17. Kreslavski V.D., Kosobryukhov A.A., Shmarev A.N. et al.: Introduction of the Arabidopsis PHYB gene increases resistance of photosynthetic apparatus in transgenic Solanum tuberosum plants to UV-B radiation.-Russ. J. Plant Physl+ 62: 204-209, 2015. Go to original source...
    18. Kreslavski V.D., Carpentier R., Klimov V.V. et al.: Transduction mechanisms of photoreceptor signals in plant cells.-J. Photoch. Photobio. C 10: 63-80, 2009. Go to original source...
    19. Kreslavski V.D., Lyubimov V.Y., Shirshikova G.N. et al.: Preillumination of lettuce seedlings with red light enhances the resistance of photosynthetic apparatus to UV-A.-J. Photoch. Photobio. B 122: 1-6, 2013a. Go to original source...
    20. Kreslavski V.D., Shirshikova G.N., Lyubimov V.Y. et al.: Effect of pre-illumination with red light on photosynthetic parameters and oxidant-/antioxidant balance in Arabidopsis thaliana in response to UV-A.-J. Photoch. Photobio. B 127: 229-236, 2013b. Go to original source...
    21. Kreslavski V.D., Khristin M.S., Shabnova N.I. et al.: Preillumination of excised spinach leaves with red light increases the resistance of photosynthetic apparatus to UV radiation.-Russ. J. Plant Physl+ 59: 717-723, 2012.
    22. Lichtenthaler H.K., Wellburn A.R.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.-Methods Enzymol. 148: 350-382, 1987. Go to original source...
    23. Lingakumar K., Kulandaivelu G.: Regulatory role of phytochrome on ultraviolet-B (280-315 nm) induced changes in growth and photosynthetic activities of Vigna sinensis L.-Photosynthetica 29: 341-351, 1993.
    24. Maruta T., Tanouchi A., Tamoi M. et al.: Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress.-Plant Cell Physiol. 51: 190-200, 2010. Go to original source...
    25. Maxwell K., Johnson G.N.: Chlorophyll fluorescence-a practical guide.-J. Exp. Bot. 51: 659-68, 2000. Go to original source...
    26. Mirecki R.M., Teramura A.H.: Effect of ultraviolet B irradiance on soybean, V. The dependence of plant sensitivity on photosynthesis flux density during and after leaf expansion.-Plant Physiol. 74: 475-480, 1984. Go to original source...
    27. Murata N., Takahashi S., Nishiyama Y. et al.: Photoinhibition of photosystem II under environmental stress.-BBABioenergetics 1767: 414-421, 2007. Go to original source...
    28. Najafpour M.M., Pashaei B., Zand Z.: Photodamage of the manganese-calcium oxide: a model for UV-induced photodamage of the water oxidizing complex in photosystem II.-Dalton T. 42: 4772-4776, 2013. Go to original source...
    29. Nishiyama Y., Allakhverdiev S.I., Murata N.: A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II.-BBA-Bioenergetics 1757: 742-749, 2006. Go to original source...
    30. Oukarroum A., Bussotti F., Goltsev V. et al.: Correlation between reactive oxygen species production and photochemistry of photosystems I and II in Lemna gibba L. plants under salt stress.-Environ. Exp. Bot. 109: 80-88, 2015. Go to original source...
    31. Parks B.M., Quail P.H.: Phytochrome-deficient hy1 and hy2 long hypocotyl mutants of Arabidopsis are defective in phytochrome chromophore biosynthesis.-Plant Cell 3: 1177-1186, 1991. Go to original source...
    32. Pfaffl M.W.: A new mathematical model for relative quantification in real-time RT-PCR.-Nucleic Acids Res. 29: e45, 2001. Go to original source...
    33. Qi Z., Yue M., Han R. et al.: The damage repair role of He-Ne laser on plants exposed to different intensities of ultraviolet-B radiation.-Photoch. Photobio. 75: 680-686, 2002. Go to original source...
    34. Qi Z., Yue M., Wang X.L.: Laser pretreatment protects cells of broad bean from UV-B radiation damage.-J. Photoch. Photobio. B Biol. 59: 33-37, 2000. Go to original source...
    35. Quail P.H.: Phytochrome photosensory signaling networks.-Nat. Rev. Mol. Cell Biol. 3: 85-93, 2002.
    36. Ranjbarfordoei A., Samson R., Van Damme P.: Photosynthesis performance in sweet almond [Prunus dulcis (Mill) D. Webb] exposed to supplemental UV-B radiation.-Photosynthetica 49: 107-111, 2011. Go to original source...
    37. Rao A.Q., Irfan M., Saleem Z. et al.: Overexpression of the phytochrome B gene from Arabidopsis thaliana increases plant growth and yield of cotton (Gossypium hirsutum).-J. Zhejiang Univ. Sci. B 12: 326-334, 2011. Go to original source...
    38. Rusaczonek A., Czarnocka W., Kacprzak S. et al.: Role of phytochromes A and B in the regulation of cell death and acclimatory responses to UV stress in Arabidopsis thaliana.-J. Exp. Bot. 66: 6679-6695, 2015. Go to original source...
    39. Schmitt F.J., Renger G., Friedrich T. et al.: Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms.-BBABioenergetics 1837: 835-848, 2014.
    40. Shaw A.K., Ghosh S., Kalaji H.M. et al.: Nano-CuO stress induced modulation of antioxidative defense and photosynthetic performance of syrian barley (Hordeum vulgare L.).-Environ. Exp. Bot. 102: 37-47, 2014. Go to original source...
    41. Sicora C., Máté Z., Vass I.: The interaction of visible and UV-B light during photodamage and repair of photosystem II.-Photosynth. Res. 75: 127-137, 2003. Go to original source...
    42. Somers D.E., Sharrock R.A., Tepperman J.M. et al.: The hy3 long hypocotyl mutant of Arabidopsis is deficient in phytochrome B.-Plant Cell 3: 1263-1274, 1991. Go to original source...
    43. Strasser B., Sánchez-Lamas M., Yanovsky M.J. et al.: Arabidopsis thaliana life without phytochromes.-P. Natl. Acad. Sci. USA 107: 4776-4781, 2010. Go to original source...
    44. Strid A.W., Chow W.S., Anderson J.M.: UV-B damage and protection at the molecular level in plants.-Photosynth. Res. 39: 475-489, 1994. Go to original source...
    45. Szilárd A., Sass L., Deák Z., Vass I.: The sensitivity of photosystem II to damage by UV-B radiation depends on the oxidation state of the water-splitting complex.-BBABioenergetics 1767: 876-882, 2007. Go to original source...
    46. Thiele A., Herold M., Lenk I. et al.: Heterologous expression of Arabidopsis phytochrome B in transgenic potato influences photosynthetic performance and tuber.-Plant Physiol. 120: 73-82, 1999. Go to original source...
    47. Tuba Z., Saxena D.K., Srivastava K. et al.: Chlorophyll a fluorescence measurements for validating the tolerant bryophytes for heavy metal (Pb) biomapping.-Curr. Sci. 98: 1505-1508, 2010.
    48. Weisshaar B., Jenkins, G.I. Phenylpropanoid biosynthesis and its regulation.-Curr. Opin. Plant Biol. 1: 251-257, 1998. Go to original source...
    49. Zhao J., Zhou J.J., Wang Y.Y. et al.: Positive regulation of phytochrome B on chlorophyll biosynthesis and chloroplast development in rice.-Rice Sci. 20: 243-248, 2013. Go to original source...
    50. Živcák M., Kalaji M.H., Shao H. et al.: Photosynthetic proton and electron transport in wheat leaves under prolonged moderate drought stress.-J. Photoch. Photobio. B 137: 107-115, 2014a. Go to original source...
    51. Živcák M., Olšovská K., Slamka P. et al.: Measurements of chlorophyll fluorescence in different leaf positions may detect nitrogen deficiency in wheat.-Zemdirbyste 101: 437-444, 2014b.

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