Advertisement

Photosynthetica

, Volume 54, Issue 3, pp 321–330 | Cite as

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

  • V. D. Kreslavski
  • F.-J. Schmitt
  • C. Keuer
  • T. Friedrich
  • G. N. Shirshikova
  • S. K. Zharmukhamedov
  • A. A. Kosobryukhov
  • S. I. Allakhverdiev
Original papers

Abstract

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.

Additional key words

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

Abbreviations

APX1

cytosolic ascorbate peroxidase 1

CAB1

Chl a/b-binding protein

Chl

chlorophyll

CHS

chalcone synthase

Fv/Fm

maximum photochemical quantum yield of PSII

PA

photosynthetic apparatus

Phy

phytochrome

PIF

phytochrome interacting factor

qPCR

real-time quantitative polymerase chain reaction

RL

red light

ROS

reactive oxygen species

sAPX

stromal ascorbate peroxidase

tAPX

thylakoid ascorbate peroxidase

UAPs

UV-absorbing acidic methanol extractable pigments

WT

wild type

ΦPSII

actual photochemical efficiency of PSII.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

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.Google Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  4. Asada K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions.–Plant Physiol. 141: 391–396, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  14. Jiao Y., Lau O.S., Deng X.W.: Light-regulated transcriptional networks in higher plants.–Nat. Rev. Genet. 8: 217–230, 2007.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  22. Lichtenthaler H.K., Wellburn A.R.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.–Methods Enzymol. 148: 350–382, 1987.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefPubMedGoogle Scholar
  25. Maxwell K., Johnson G.N.: Chlorophyll fluorescence–a practical guide.–J. Exp. Bot. 51: 659–68, 2000.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Murata N., Takahashi S., Nishiyama Y. et al.: Photoinhibition of photosystem II under environmental stress.–BBABioenergetics 1767: 414–421, 2007.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Pfaffl M.W.: A new mathematical model for relative quantification in real-time RT-PCR.–Nucleic Acids Res. 29: e45, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  35. Quail P.H.: Phytochrome photosensory signaling networks.–Nat. Rev. Mol. Cell Biol. 3: 85–93, 2002.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.Google Scholar
  48. Weisshaar B., Jenkins, G.I. Phenylpropanoid biosynthesis and its regulation.–Curr. Opin. Plant Biol. 1: 251–257, 1998.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2016

Authors and Affiliations

  • V. D. Kreslavski
    • 1
    • 2
  • F.-J. Schmitt
    • 3
  • C. Keuer
    • 3
  • T. Friedrich
    • 3
  • G. N. Shirshikova
    • 1
  • S. K. Zharmukhamedov
    • 1
  • A. A. Kosobryukhov
    • 1
  • S. I. Allakhverdiev
    • 1
    • 2
    • 4
  1. 1.Institute of Basic Biological ProblemsRussian Academy of SciencesPushchino, Moscow RegionRussia
  2. 2.Controlled Photobiosynthesis Laboratory, Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  3. 3.Technical University of BerlinInstitute of Chemistry Sekr. PC 14, Max-Volmer-Laboratory of Biophysical ChemistryBerlinGermany
  4. 4.Department of Plant Physiology, Faculty of BiologyM.V. Lomonosov Moscow State UniversityMoscowRussia

Personalised recommendations