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Photochemical activity and the structure of chloroplasts in Arabidopsis thaliana L. mutants deficient in phytochrome A and B

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Abstract

The reduced content of photoreceptors, such as phytochromes, can decrease the efficiency of photosynthesis and activity of the photosystem II (PSII). For the confirmation of this hypothesis, the effect of deficiency in both phytochromes (Phy) A and B (double mutant, DM) in 7–27-day-old Arabidopsis thaliana plants on the photosynthetic activity was studied in absence and presence of UV-A radiation as a stress factor. The DM with reduced content of apoproteins of PhyA and PhyB and wild type (WT) plants with were grown in white and red light (WL and RL, respectively) of high (130 μmol quanta m−2 s−1) and low (40 μmol quanta m−2 s−1) intensity. For DM and WT grown in WL, no notable difference in the photochemical activity of PSII was observed. However, the resistance of the photosynthetic apparatus (PA) to UV-A and the rate of photosynthesis under light saturation were lower in the DM compared to those in the WT. Growth in RL, when the photoreceptors of blue light—cryptochromes—are inactive, resulted in the significant decrease of the photochemical activity of PSII in DM compared to that in WT including amounts of QB-non-reducing complexes of PSII and noticeable enhancement of thermal dissipation of absorbed light energy. In addition, marked distortion of the thylakoid membrane structure was observed for DM grown in RL. It is suggested that not only PhyA and PhyB but also cryptochromes are necessary for normal functioning of the PA and formation of the mechanisms of its resistance to UV-radiation.

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Abbreviations

Chl:

Chlorophyll

Phy:

Phytochrome

RL:

Red light

FRL:

Far-red light

PSII:

Photosystem II

PA:

Photosynthetic apparatus

WT:

Wild type

DM:

phytochrome A, phytochrome B mutant

References

  • Babu TS, Jansen MAK, Greenberg BM, Gaba V, Malkin S, Mattoo AK, Edelman M (1999) 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. Photochem Photobiol 69:553–559

    Article  CAS  Google Scholar 

  • Biswal UC, Biswal B, Raval MK (2003) Chloroplast biogenesis. From propastid to gerontoplast. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Boccalandro HE, Rugnone ML, Moreno JE, Ploschuk EL, Serna L, Yanovsky MJ, Casal JJ (2009) Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis. Plant Physiol 150:1083–1092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borisova-Mubarakshina MM, Vetoshkina DV, Rudenko NN, Shirshikova GN, Fedorchuk TP, Naydov IA, Ivanov BN (2014) The size of the light-harvesting antenna of higher plant photosystem II Is regulated by illumination intensity through transcription of antenna protein genes. Biochem Mosc 79:520–523

    Article  CAS  Google Scholar 

  • Carvalho RF, Campos ML, Azevedo RA (2011) The role of phytochrome in stress tolerance. J Integr Plant Biol 53:920–929

    Article  CAS  PubMed  Google Scholar 

  • Casal JJ (2000) Phytochromes, cryptochromes, phototropin: photoreceptor interactions in plants. Photochem Photobiol 71:1–11

    Article  CAS  PubMed  Google Scholar 

  • Casal JJ, Sánchez RA, Botto JF (1998) Modes of action of phytochromes. J Exp Bot 49:127–138

    CAS  Google Scholar 

  • Foreman J, Johansson H, Hornitschek P, Josse EM, Fankhauser C, Halliday KJ (2011) Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J 65:441–452

    Article  CAS  PubMed  Google Scholar 

  • Franklin KA (2008) Shade avoidance. New Phytol 179:901–1201

    Article  Google Scholar 

  • Gururani MA, Venkatesh J, Ganesan M, Strasser RJ, Han Y, Kim JI, Lee HY, Song PS (2015) In vivo assessment of cold tolerance through chlorophyll-a fluorescence in transgenic zoysiagrass expressing mutant phytochrome A. PLoS One 10(5):e0127200

    Article  PubMed  PubMed Central  Google Scholar 

  • Häder DP, Kumar HD, Smith RC, Worrest RC (2003) Aquatic ecosystems: effects of solar ultraviolet radiation and interactions with other climatic change factors. Photochem Photobiol Sci 2:39–50

    Article  PubMed  Google Scholar 

  • Han T, Sinha RP, Häder DP (2001) UV-A/blue light-induced reactivation of photosynthesis in UV-B irradiated cyanobacterium, Anabaena sp. J Plant Physiol 158:1403–1413

    Article  CAS  Google Scholar 

  • Hu W, Franklin KA, Sharrock RA, Jones MA, Harmer SL, Lagarias JC (2013) Unanticipated regulatory roles for Arabidopsis phytochromes revealed by null mutant analysis. Proc Natl Acad Sci U S A 110:1542–1547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi PN, Biswal B, Biswal VC (1991) Effect of UV-A on aging of wheat leaves and role of phytochrome. Environ Exp Bot 31:267–276

    Article  Google Scholar 

  • Kalaji HM, Golstev V, Bosa K, Allakhverdiev SI, Strasser RJ, Govindjee (2012) Experimental in vivo measurements of light emission in plants: a perspective dedicated to David Walker. Photosynth Res 114:69–96

    Article  CAS  PubMed  Google Scholar 

  • Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dąbrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, DorothyBelle P, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serodio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014a) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska I, Cetner MD, Goltsev V, Ladle RJ, Dąbrowski P, Ahmad P (2014b) The use of chlorophyll fluorescence kinetics analysis to study the performance of photosynthetic machinery in plants. In: Ahmad P (ed.) Emerging Technologies and Management of Crop Stress Tolerance (Elsevier), Vol. II, 347 – 384

  • Klinkovsky T, Naus J (1994) Sensitivity of the relative Fpl level of chlorophyll fluorescence induction in leaves to the heat stress. Photosynth Res 39:201–204

    Article  CAS  PubMed  Google Scholar 

  • Kolli BK, Tiwari S, Mohanty P (1998) Ultraviolet-B induced damage to photosystem II in intact filaments of Spirulina platensis. Z Naturforsch 53:369–377

    CAS  Google Scholar 

  • Konstantinova TN, Aksenova NP, Gukasyan IA, Golyanovskaya SA, Romanov GA (2004) An Improved tolerance of PHYB_transgenic potato plants to the middle_wave ultraviolet irradiation. Dokl Biol Sci 395:130–132

    Article  CAS  PubMed  Google Scholar 

  • Kouril R, Wientjes E, Bultema JB, Croce R, Boekema E (2013) High-light vs. low-light: effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochim Biophys Acta 1827:411–419

    Article  CAS  PubMed  Google Scholar 

  • Kreslavski VD, Shirshikova GN, Lyubimov VY, Shmarev AN, Boutanaev AM, Kosobryukhov AA, Schmitt FJ, Friedrich T, Allakhverdiev SI (2013a) Effect of preillumination with red light on photosynthetic parameters and oxidant-/antioxidant balance in Arabidopsis thaliana in response to UV-A. J Photochem Photobiol B Biol 127:229–236

    Article  CAS  Google Scholar 

  • Kreslavski VD, Lyubimov VY, Shirshikova GN, Shmarev AN, Kosobryukhov AA, Schmitt FJ, Friedrich T, Allakhverdiev SI (2013b) Preillumination of lettuce seedlings with red light enhances the resistance of photosynthetic apparatus to UV-A. J Photochem Photobiol B Biol 122:1–6

    Article  CAS  Google Scholar 

  • Kreslavski VD, Kosobryukhov AA, Shmarev AN, Aksenova NP, Konstantinova TN, Golyanovskaya SA, Romanov GA (2015) Introduction of the Arabidopsis PHYB gene increases resistance of photosynthetic apparatus in transgenic Solanum tuberosum plants to UV-B radiation. Russ J Plant Physiol 62:204–209

    Article  CAS  Google Scholar 

  • Kreslavski VD, Schmitt FJ, Keuer C, Friedrich T, Shirshikova GN, Zharmukhamedov SK, Kosobryukhov AA, Allakhverdiev SI (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

    Article  CAS  Google Scholar 

  • Lankin AV, Kreslavski VD, Khudyakova AY, Zharmukhamedov SK, Allakhverdiev SI (2014) Effect of naphthalene on photosystem 2 photochemical activity of pea plants. Biochem Mosc 79:1216–1225

    Article  CAS  Google Scholar 

  • Larocca N, Barbato R, Casadoro G, Rascio N (1996) Eearly degradation of photosynthetic membranes in carob and sunflower cotyledons. Physiologia Plant 96:513–518

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lingakumar K, Kulandaivelu G (1993) 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

    CAS  Google Scholar 

  • Martirosyan YT, Polyakova MN, Dilovarova TA, Kosobryukhov AA (2013) Photosynthesis and productivity of potato plants in the conditions of different spectral irradiation. Agric Biol №1:107–112

    Google Scholar 

  • Mirecki RM, Teramura AH (1984) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Priol JL, Chartier P (1977) Partitioning of transfer and carboxilation components of intracellular resistance to photosynthetic CO2 fixation: a critical analysis of the methods used. Ann Bot 41:789–800

    Article  Google Scholar 

  • Rusaczonek A, Czarnocka W, Kacprzak S, Witoń D, Ślesak I, Szechyńska-Hebda M, Gawroński P, Karpiński S (2015) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitt F-J, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reevaluation of reactive oxygen species: monitoring, generation and role in stress signaling of phototrophic organisms. Biochim Biophys Acta 1837:835–848

    Article  CAS  PubMed  Google Scholar 

  • Schmitt F-J, Kreslavski VD, Zharmukhamedov SK, Friedrich T, Renger G, Los DA, Kuznetsov VV, Allakhverdiev SI (2015) The multiple roles of various reactive oxygen species (ROS) in photosynthetic organisms. In: Allakhverdiev S.I. (ed.) Photosynthesis: New Approaches to the Molecular, Cellular, and Organismal Levels (Scrivener Publishing LLC), Willey, 4–82

  • Semenova GA, Romanova AK (2011) Crystals in sugar beet (Beta vulgaris L.) leaves. Cell and Tissue Biol 5:74–80

    Article  Google Scholar 

  • Semenova GA, Ladygin VG, Tageeva SV (1977) Ultrastructural organization of membrane system of Chlamydomonas reinhardtii mutants chloroplasts with inactive photosystems. Russian J Plant Physiol 24:18–22

    CAS  Google Scholar 

  • Solovchenko AE, Merzlyak MN (2008) Screening of visible and UV radiation as a photoprotective mechanism in plants. Russian J Plant Physiol 55:719–737

    Article  CAS  Google Scholar 

  • Somers DE, Sharrock RA, James M, Teppermaq JM, Quail PH (1991) The hy3 long hypocotyl mutant of Arabidopsis is deficient in phytochrome B. Plant Cell 3:1263–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B Biol 104:36–57

    Article  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor and Francis, London, pp 445–483

    Google Scholar 

  • Strasser B, Sánchez-Lamas M, Yanovsky MJ, Casal JJ, Cerdán PD (2010) Arabidopsis thaliana life without phytochromes. Proc Natl Acad Sci U S A 107:4776–4781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strid AW, Chow S, Anderson JM (1994) UV-B damage and protection at the molecular level in plants. Photosynth Res 39:475–489

    Article  CAS  PubMed  Google Scholar 

  • Thiele A, Herold M, Lenk I, Quail PH, Gatz C (1999) Heterologous expression of Arabidopsis phytochrome B in transgenic potato influences photosynthetic performance and tuber development. Plant Physiol 120:73–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhou JJ, Wang YY, Gu JW, Xie XZ (2013) Positive regulation of phytochrome B on chlorophyll biosynthesis and chloroplast development in rice. Rice Sci 20:243–248

    Article  Google Scholar 

  • Živčák M, Brestič M, Olšovská K, Slamka P (2008) Performance index as a sensitive indicator of water stress in Triticum aestivum L. Plant Soil Environ 54:133–139

    Article  Google Scholar 

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Acknowledgments

This work was supported by grants from the Russian Foundation for Basic Research (Nos: 15-04-01199 and 14-04-01549), and by the Molecular and Cell Biology Programs from the Russian Academy of Sciences. The authors acknowledge support by the German Research Foundation DFG (cluster of excellence “Unifying Concepts in Catalysis”) and the COST MP1205 framework.

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Correspondence to Vladimir D. Kreslavski or Suleyman I. Allakhverdiev.

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Kreslavski, V.D., Kosobryukhov, A.A., Schmitt, FJ. et al. Photochemical activity and the structure of chloroplasts in Arabidopsis thaliana L. mutants deficient in phytochrome A and B. Protoplasma 254, 1283–1293 (2017). https://doi.org/10.1007/s00709-016-1020-9

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