Abstract
We studied the developmental changes in photosynthetic and respiration rates and thermal dissipation processes connected with chloroplasts and mitochondria activity in etiolated wheat (Triticum aestivum L., var. Irgina) seedlings during the greening process. Etioplasts gradually developed into mature chloroplasts under continuous light [190 μmol(photon) m−2 s−1] for 48 h in 5-day-dark-grown seedlings. The net photosynthetic rate of irradiated leaves became positive after 6 h of illumination and increased further. The first two hours of de-etiolation were characterized by low values of maximum (Fv/Fm) and actual photochemical efficiency of photosystem II (PSII) and by a coefficient of photochemical quenching in leaves. Fv/Fm reached 0.8 by the end of 24 h-light period. During greening, energy-dependent component of nonphotochemical quenching of chlorophyll fluorescence, violaxanthin cycle (VXC) operation, and lipoperoxidation activity changed in a similar way. Values of these parameters were the highest at the later phase of de-etiolation (4–12 h of illumination). The respiration rate increased significantly after 2 h of greening and it was the highest after 4–6 h of illumination. It was caused by an increase in alternative respiration (AP) capacity. The strong, positive linear correlation was revealed between AP capacity and heat production in greening tissues. These results indicated that VXC in chloroplasts and AP in mitochondria were intensified as energy-dissipating systems at the later stage of greening (after 4 h), when most of prolamellar bodies converted into thylakoids, and they showed the greatest activity until the photosynthetic machinery was almost completely developed.
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Abbreviations
- AL:
-
actinic light
- AP:
-
alternative pathway of respiration
- Ax:
-
antheraxanthin
- Car:
-
carotenoids
- Ch:
-
chloroplast
- Chl:
-
chlorophyll
- Chlide:
-
chlorophyllide
- CP:
-
cytochrome pathway of respiration
- DM:
-
dry mass
- ETC:
-
electron transport chain
- Ft, Fo′, and Fm :
-
stationary, minimal, and maximal fluorescence in leaves adapted to the actinic light [190 μmol(photon) m−2 s−1, PAR]
- FM:
-
fresh mass
- Fv/Fm :
-
maximum photochemical efficiency of PSII
- lut:
-
lutein
- LPA:
-
lipoperoxidation activity
- M:
-
mitochondrion
- NPQ:
-
nonphotochemical quenching
- Nx:
-
neoxanthin
- PAR:
-
photosynthetically active radiation
- PLB:
-
prolamellar body
- P N :
-
net photosynthetic rate
- Pchlide:
-
protochlorophyllide
- PSII:
-
photosystem II
- q:
-
rate of heat production
- qE :
-
energy-dependent component of nonphotochemical fluorescence quenching
- qN and qP :
-
coefficients of nonphotochemical and photochemical quenching, respectively
- R D :
-
dark respiration measured as CO2 emission rate
- ROS:
-
reactive oxygen species
- SHAM:
-
salicylhydroxamic acid
- TBARS:
-
thiobarbituric acid-reactive-substances
- TCA:
-
tricarboxylic acid cycle
- Valt and Vcyt :
-
capacity of alternative and cytochrome pathway of respiration, respectively
- Vt :
-
total respiration measured as O2 uptake rate
- VDE:
-
violaxanthin de-epoxidase
- Vx:
-
violaxanthin
- VXC:
-
violaxanthin cycle
- ΦPSII :
-
actual photochemical efficiency of PSII
- Zx:
-
zeaxanthin
- β-Car:
-
β-carotene
References
Boiko, B.N., Malyshev, R.V., Ogorodnikova S.Yu. et al.: [Differential microcalorimeter for research of metabolic processes in living structures and its application in physiology of plants.] — Nauchnoe priborostroenie 19: 36–44, 2009. [In Russian]
Bonente, G., Howes, B.D., Caffarri, S. et al.: Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. — J. Biol. Chem. 283: 8434–8445, 2008.
Covey-Crump, E.M., Bykova, N.V., Affrourtit, C. et al.: Temperature-dependent changes in respiration rates and redox poise of the ubiquinon pool in protoplasts and isolated mitochondria of potato leaves. — Physiol. Plant. 129: 175–84, 2007.
Cuttriss, A.J., Chubb, A.C., Alawady, A. et al.: Regulation of lutein biosynthesis and prolamellar body formation in Arabidopsis. — Funct. Plant Biol. 34: 663–72, 2007.
Demmig-Adams, B.: Carotenoids and photoprotection: a role for the xanthophyll zeaxanthin. — Biochim. Biophys. Acta 1020: 1–24, 1990.
Demming-Adams, B., Adams, W.W.III: Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. — Planta 198: 460–70, 1996.
Dinakar, C., Raghavendra, A.S., Padmasree, K.: Importance of AOX pathway in optimizing photosynthesis under high light stress: Role of pyruvate and malate in activating of AOX. — Physiol. Plant. 139: 13–26, 2010.
Feng, H.Q., Li, H.Y., Zhou, G.M. et al.: Influence of irradiation on cyanide-resistant respiration and AOX1multi-gene family expression during greening of etiolated rice seedlings. — Photosynthetica 45: 272–279, 2007.
Foyer, C.H., Noctor, G.: Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria — Physiol. Plant. 119: 355–364, 2003.
Franck, F., Mathis, P.: A short-lived intermediate in the photoenzymatic reduction of protochlorophyll(ide) into chlorophyll(ide) at a physiological temperature. — Photochem. Photobiol. 32: 799–803, 1980.
Garmash, E.V., Golovko, T.K.: CO2 gas exchange and growth in Rhaponticum carthamoides under the conditions of middle taiga subzone of Northeastern Europe: 1. Dependence of photosynthesis and respiration on environmental factors. — Russ. J. Plant Physiol. 44: 737–745, 1997.
Garmash, E.V., Golovko, T.K.: Effect of cadmium on growth and respiration of barley plants grown under two temperature regimes. — Russ. J. Plant Physiol. 56: 343–347, 2009.
Gechev, T.S., Van Breusegem, F., Stone, J.M. et al.: Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. — BioEssays 28: 1091–1101, 2006.
Gilmore, A.M.: Mechanistic aspects of xanthophyll cycledependent photoprotection in higher plant chloroplasts and leaves. — Physiol. Plant. 99: 197–209, 1997.
Gilmore, A.M., Yamamoto, H.Y.: Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. — Plant Physiol. 96: 635–43, 1991.
Gruszecki, W.I., Gospodarek, M., Grudziński, W. et al.: Lightinduced change of configuration of the LHCII-bound xanthophyll (tentatively assigned to violaxanthin): A resonance Raman study. — J. Phys. Chem. B. 113: 2506–2512, 2009.
Hansen, L.D., Hopkin, M.S., Rank, D.R. et al.: The relation between plant growth and respiration: A thermodynamic model. — Planta 194: 77–85, 1994.
Heath, R.L., Packer, L.: Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acids peroxidation. — Arch. Biochem. Biophys. 125: 189–98, 1968.
Horton, P., Ruban, A.V., Walters, R.G.: Regulation of light harvesting in green plants. Indication by nonphotochemical quenching of chlorophyll fluorescence. — Plant Physiol. 106: 415–420, 1994.
Ignatov, N.V., Krasnovskii, A.A., Jr., Litvin, F.F. et al.: Lowtemperature (77 K) excitation spectra of fluorescence and phosphorescence of native forms of protochlorophyll(ide) in etiolated leaves of Phaseolus vulgaris and P. coccineus. — Photosynthetica 17: 352–360, 1983.
Juszczuk, I.M., Szal, B., Rychter, A.M.: Oxidation-reduction and reactive oxygen species homeostasis in mutant plants with respiratory chain complex I dysfunction. — Plant Cell Environ. 35: 296–307, 2012.
Kalituho, L. Beran, K.C., Jahns, B.: The transiently generated nonphotochemical quenching of excitation energy in Arabidopsis leaves is modulated by zeaxanthin. — Plant Physiol. 143: 1861–1870, 2007.
Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: the basics. — Annu. Rev. Plant Physiol. Plant Mo1. Biol. 42: 313–349, 1991.
Kumar, N., Vyas, D., Kumar S.: Plants at high altitude exhibit higher component of alternative respiration. — J. Plant Physiol. 164: 31–38, 2007.
Lambers, H.: Cyanide-resistant respiration: A non-phosphorylating electron transport pathway acting as an energy overflow. — Physiol. Plant. 55: 478–85, 1982.
Latowski, D., Grzyb, J., Strzalka, K. The xanthophylls cycle — molecular mechanism and physiological significance. — Acta Physiol. Plant. 26: 197–212, 2004.
Lichtenthaler, H.K.: Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. — Methods Enzymol. 148: 350–382, 1987.
Logan, D.C.: The mitochondrial compartment. — J. Exp. Bot. 57: 1225–1243, 2006.
Maxwell, D.P., Wang, Y., McIntosh, L.: The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. — Proc. Nat. Acad. Sci. USA 96: 8271–8276, 1999.
Millenaar, F.F., Lambers, H.: The alternative oxidase: In vivo regulation and function. — Plant Biol. 5: 2–15, 2003.
Mubarakshina, M.M., Ivanov, B.N., Naydov, I.A. et al.: Production and diffusion of chloroplastic H2O2 and its implication to signaling. — J. Exp. Bot. 61: 3577–3587, 2010.
Møller, I.M., Bérczi, A., van der Plas, L.H.W. et al.: Measurement of the activity and capacity of the alternative pathway in intact plant tissues: Identification of problems and possible solutions. — Physiol. Plant. 72: 642–649, 1988.
Møller, I.M., Sweetlove, L.J.: ROS signalling — specificity is required. — Trends Plant Sci. 15: 370–374, 2010.
Navrot, N., Rouhier, N., Gelhaye, E. et al.: Reactive species oxygen generation and antioxidant systems in plant mitochondria. — Physiol. Plant. 129: 185–195, 2007.
Niyogi, K.K., Grossman, A.R., Björkman, O.: Arabidopsis mutants define a central role for the xanthophylls cycle in the regulation of photosynthetic energy conversion. — Plant Cell 10: 1121–1134, 1998.
Noguchi, K., Yoshida, K.: Interaction between photosynthesis and respiration in illuminated leaves. — Mitochondrion 8: 887–899, 2008.
Nowicka, B., Strzalka, W., Strzalka, K.: New transgenic line of Arabidopsis thaliana with partly disabled zeaxanthin epozidase activity displays changed carotenoid composition, xanthopyll cycle activity and non-photochemical quenching kinetics. — J. Plant Physiol. 166: 1045–1056, 2009.
Padmasree, K., Raghavendra, A.S.: Response of photosynthetic carbon assimilation in mesophyll protoplasts to restriction on mitochondrial oxidative metabolism: Metabolites related to the redox status and sucrose biosynthesis. — Photosynth. Res. 62: 231–239, 1999.
Park, H., Kreunen, S.S., Cuttriss, A.J. et al.: Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. — Plant Cell 14: 321–332, 2002.
Pfündel, E., Strasser, R.J.: Violaxanthin de-epoxidase in etiolated leaves. — Photosynth. Res. 15: 67–73, 1988.
Polesskaya, O.G., Alekhina, N.D.: [Nitrogen starvation effect on wheat chloroplast photochemical activity and their resistance to high intensivity light.] — Vestnik Moskovskogo universiteta (Moscow Univ. Biol. Sci. Bull.) 16: 31–37, 1995. [In Russian]
Quick, W.P., Stitt, M.: An examination of factors contributing to non-photochemical quenching of chlorophyll fluorescence in barley leaves. — Biochim. Biophys. Acta 977: 287–296, 1989.
Rachmilevich, S., Xu, Y., Gonzalez-Meler, M.A. et al.: Cytochrome and alternative pathway in roots of thermal and non-thermal Agrostis species in response to high soil temperature. — Physiol. Plant. 129: 163–174, 2007.
Rasmusson, A.G., Escobar, M.A.: Light and diurnal regulation of plant respiratory gene expression. — Physiol. Plant. 129: 57–67, 2007.
Ribas-Carbo., M., Robinson, S.A., González-Meler, M.A. et al.: Effects of light on respiration and oxygen isotope fractionation in soybean cotyledons. — Plant Cell Environ. 23: 983–989, 2000.
Ruban, A.V., Berera, R., Ilioaia, C. et al.: Identification of a mechanism of photoprotective energy dissipation in higher plants. — Nature 450: 575–578, 2007.
Ruban, A.V., Wentworth, M., Horton, P.: Kinetic analysis of nonphotochemical quenching of chlorophyll fluorescence. 1. Isolated chloroplasts. — Biochemistry 40: 9896–9901, 2001.
Schoefs, B., Bertrand, M., Lemoine, Y.: Changes in the photosynthetic pigments in bean leaves during the first photoperiod of greening and the subsequent dark-phase. Comparison between old (10-d-old) leaves and young (2-dold) leaves. — Photosynth. Res. 57: 203–213, 1998.
Schoefs, B., Franck, F.: Photoreduction of protochlorophyllide to chlorophyllide in 2-d-old dark-grown bean (Phaseolus vulgaris cv. Commodore) leaves. Comparison with 10-d-old dark-grown (etiolated) leaves. — J. Exp. Bot. 44: 1053–1057, 1993.
Semikhatova, O.A.: [Energy of Plant Respiration under Normal Conditions and Ecological Stress. The 48th Timiryazev Lecture.] — Nauka, Leningrad 1990. [In Russ.]
Solymosi, K., Schoefs, B.: Etioplast and etio-chloroplast formation under natural conditions: the dark side of chlorophyll biosynthesis in angiosperms. — Photosynth. Res. 105: 143–166, 2010.
Sweetlove, L.J., Heazlewood, J.L., Herald, V. et al.: The impact of oxidative stress on Arabidopsis mitochondria. — Plant J. 32: 891–904, 2002.
Szabó, I., Bergantino, E., Giacometti, G.M.: Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. — EMBO Reports 6: 629–634, 2005.
Tooming, Kh.G.: [Ecological Principles of the Maximal Productivity of Plant Stands.] — Gidrometeoizdat, Leningrad 1984. [In Russian]
Umbach, A.L., Fiorani, F., Siedow, J.N.: Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. — Plant Physiol. 139: 1806–1820, 2005.
Vanlerberghe, G.C., Cvetkovska, M. Wang, J.: Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? — Physiol. Plant. 137: 392–406, 2009.
Vanlerberghe, G.C., McIntosh, L.: Alternative oxidase: From gene to function. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 703–734, 1997.
Waloszek, A., Więckowski, S., Planner, A. et al.: Photothermal spectra of thylakoides isolated from cucumber cotyledons at various stages of greening. — Photosynthetica 40: 279–288, 2002.
Wilhelm, C., Selmar, D.: Energy dissipation is an essential mechanism to sustain the viability of plants: The physiological limits of improved photosynthesis. — J. Plant Physiol. 168: 179–87, 2011.
Yoshida, K., Watanabe, C., Kato, Y. et al.: Influence of chloroplastic photo-oxidative stress on mitochondrial alternative oxidase capacity and respiratory properties: A case study with Arabidopsis yellow variegated 2. — Plant Cell Physiol. 49: 592–603, 2008.
Zhang, D.-W., Xu, F., Zhang, Z.-W. et al.: Effects of light on cyanide-resistant respiration and alternative oxidase function in Arabidopsis seedlings. — Plant Cell Environ. 33: 2121–2131, 2010.
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Acknowledgments: We are thankful to Prof. Kazimierz Strzałka and Prof. Anna Rychter for reading the manuscript and for useful comments. This work is supported by the grant from the Ural Branch of the Russian Academy of Sciences (No 12-Y-4-1008). In addition, we are grateful to the reviewers for their valuable comments.
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Garmash, E.V., Dymova, O.V., Malyshev, R.V. et al. Developmental changes in energy dissipation in etiolated wheat seedlings during the greening process. Photosynthetica 51, 497–508 (2013). https://doi.org/10.1007/s11099-013-0044-z
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DOI: https://doi.org/10.1007/s11099-013-0044-z