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Photoinhibition of Suaeda salsa to chilling stress is related to energy dissipation and water-water cycle

  • Original Papers
  • Published:
Photosynthetica

Abstract

To investigate the photoprotection of energy dissipation and water-water cycle, a C3 euhalophytic herb, Suaeda salsa L., was exposed either to chilling temperature (4°C) accompanied by moderate irradiance (600 μmol m−2 s−1) (CM) and/or to chilling temperature (4°C) accompanied by low irradiance (100 μmol m−2 s−1) (CL). During chilling stress, both the maximal photochemical efficiency of PSII (Fv/Fm) and the oxidizable P700 decreased in S. salsa leaves either under CM or CL, which indicated the severe photoinhibition. Relative to Fv/Fm, the oxidizable P700 decreased markedly under CL, which indicated that PSI was more sensitive to CL treatment than PSII. Initial fluorescence, number of closed PSII centers, and nonphotochemical quenching increased under CM, but more markedly under CL in S. salsa leaves. Activity of superoxide dismutase and ascorbate peroxidase was higher under CM than that under CL. The production of reactive oxygen species (ROS) decreased first and then increased under both treatments, but the content of O2·− and H2O2 was higher under CL than that under CM after 12 h of chilling stress. These results suggested that photoinhibition in S. salsa might be related to the accumulation of reactive oxygen species (ROS) induced by excess energy. The water-water cycle could not dissipate energy efficiently under CL, which caused the great accumulation of ROS.

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Abbreviations

APX:

ascorbate peroxidase

AsA:

ascorbic acid

Chl:

chlorophyll

CL:

chilling temperature (4°C) accompanied by low irradiance (100 μmol m−2 s−1)

CM:

chilling temperature (4°C) accompanied by moderate irradiance (600 μmol m−2 s−1)

F0 :

minimal fluorescence yield of the dark-adapted state

Fm :

maximal fluorescence yield of the dark-adapted state

Fm′:

maximal fluorescence yield of the light-adapted state

Fs :

steady-state fluorescence yield

Fv :

variable fluorescence

Fv/Fm :

maximal quantum yield of PSII photochemistry

NPQ:

nonphotochemical quenching

QA :

primary quinone electron acceptor of PSII

qp :

photochemical quenching

RC:

reaction centre

ROS:

reactive oxygen species

SOD:

superoxide dismutase

ΦPSII :

effective quantum yield of PSII photochemistry

References

  • Allen D.J., Ort D.R.: Impacts of chilling temperatures on photosynthesis in warm-climate plants. — Trends Plant Sci. 1: 36–42, 2001.

    Article  Google Scholar 

  • Airaki M., Leterrier M., Mateos R.M. et al.: Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. — Plant Cell Environ. 2: 281–295, 2012.

    Article  Google Scholar 

  • Apel K., Hirt H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. — Annu. Rev. Plant Biol. 55: 373–399, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Aro E., Virgin I., Andersson B.: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. — BBA-Bioenergetics 2: 113–134, 1993.

    Article  Google Scholar 

  • Asada K.: The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. — Annu. Rev. Plant Biol. 1: 601–639, 1999.

    Article  Google Scholar 

  • Asada K.: Ascorbate peroxidase — a hydrogen peroxidescavenging enzyme in plants. — Physiol. Plantarum 2: 235–241, 1992.

    Article  Google Scholar 

  • Baker N.R.: A possible role for photosystem II in environmental perturbations of photosynthesis. — Physiol. Plant. 4: 563–570, 1991.

    Article  Google Scholar 

  • Demmig-Adams B., Adams W.W.: The role of xanthophyll cycle carotenoids in the protection of photosynthesis. — Trends Plant Sci. 1: 21–26, 1996.

    Article  Google Scholar 

  • Foyer C.H., Halliwell B.: The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. — Planta 1: 21–25, 1976.

    Article  Google Scholar 

  • Foyer C.H., Lelandais M., Kunert K.J.: Photooxidative stress in plants. — Physiol. Plantarum 4: 696–717, 1994.

    Article  Google Scholar 

  • Giannopolitis C.N., Ries S.K.: Superoxide dismutases: I. Occurrence in higher plants. — Plant Physiol. 2: 309–314, 1977.

    Article  Google Scholar 

  • Havaux M., Davaud A.: Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of photosystem II activity: Preferential inactivation of photosystem I. — Photosynth. Res. 1: 75–92, 1994.

    Article  Google Scholar 

  • Havaux M., Strasser R.J., Greppin H.: A theoretical and experimental analysis of the qp and qn coefficients of chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events. — Photosynth. Res. 1: 41–55, 1991.

    Article  Google Scholar 

  • Horton P., Ruban A.V., Walters R.G.: Regulation of light harvesting in green plants (indication by nonphotochemical quenching of chlorophyll fluorescence). — Plant Physiol. 2: 415–420, 1994.

    Google Scholar 

  • Inoue K., Fujii T., Yokoyama E. et al.: The photoinhibition site of photosystem I in isolated chloroplasts under extremely reducing conditions. — Plant Cell Physiol. 1: 65–71, 1989.

    Article  Google Scholar 

  • Jimenez A., Hernandez J.A., Del Río L.A. et al.: Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. — Plant Physiol. 1: 275–284, 1997.

    Google Scholar 

  • Kratsch H.A., Wise R.R.: The ultrastructure of chilling stress. — Plant Cell Environ. 4: 337–350, 2000.

    Article  Google Scholar 

  • Li X., Duan W., Meng Q. et al.: The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. — Plant Cell Physiol. 1: 103–108, 2004a.

    Article  Google Scholar 

  • Li X., Meng Q., Jiang G. et al.: The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle. — Photosynthetica 2: 259–265, 2003.

    Article  Google Scholar 

  • Li X., Wang X., Meng Q. et al.: Factors limiting photosynthetic recovery in sweet pepper leaves after short-term chilling stress under low irradiance. — Photosynthetica 2: 257–262, 2004b.

    Article  Google Scholar 

  • Liu P., Meng Q., Zou Q. et al.: Effects of cold-hardening on chilling-induced photoinhibition of photosynthesis and on xanthophyll cycle pigments in sweet pepper. — Photosynthetica 3: 467–472, 2001.

    Article  Google Scholar 

  • Lu C., Qiu N., Lu Q. et al.: Does salt stress lead to increased susceptibility of photosystem II to photoinhibition and changes in photosynthetic pigment composition in halophyte Suaeda salsa grown outdoors? — Plant Sci. 5: 1063–1068, 2002.

    Article  Google Scholar 

  • Lyons J.M., Raison J.K.: A temperature-induced transition in mitochondrial oxidation: contrasts between cold and warmblooded animals. — Comp. Biochem. Physiol. 3: 405–411, 1970.

    Article  Google Scholar 

  • Murata N., Los D.A.: Membrane fluidity and temperature perception. — Plant Physiol. 3: 875–879, 1997.

    Google Scholar 

  • Nishida I., Murata N.: Chilling sensitivity in plants and Cyanobacteria: the crucial contribution of membrane lipids. — Annu. Rev. Plant Biol. 1: 541–568, 1996.

    Article  Google Scholar 

  • Niyogi K.K.: Photoprotection revisited: genetic and molecular approaches. — Annu. Rev. Plant Biol. 1: 333–359, 1999.

    Article  Google Scholar 

  • Noctor G., Foyer C.H.: Ascorbate and glutathione: keeping active oxygen under control. — Annu. Rev. Plant Biol. 1: 249–279, 1998.

    Article  Google Scholar 

  • Qin L.Q., Li L., Bi C. et al.: Damaging mechanisms of chilling- and salt stress to Arachis hypogaea L. leaves. — Photosynthetica 49: 37–22, 2011.

    Article  CAS  Google Scholar 

  • Ögren E., Öquist G.: Photoinhibition of photosynthesis in Lemna gibba as induced by the interaction between light and temperature. III. Chlorophyll fluorescence at 77 K. — Physiol. Plantarum 2: 193–200, 1984.

    Article  Google Scholar 

  • Osmond C.B., Grace S.C.: Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? — J. Exp. Bot. 46: 1351–1362, 1995.

    Article  CAS  Google Scholar 

  • Sairam R.K., Srivastava G.C.: Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. — Plant Sci. 6: 897–904, 2002.

    Article  Google Scholar 

  • Schansker G., Srivastava A., Strasser R.J.: Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. — Funct. Plant Biol. 7: 785–796, 2003.

    Article  Google Scholar 

  • Schreiber U., Bilger W., Neubauer C.: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. — Ecophysiol. Photosynth. 100: 49–70, 1994.

    CAS  Google Scholar 

  • Somerville C.: Direct tests of the role of membrane lipid composition in low-temperature-induced photoinhibition and chilling sensitivity in plants and Cyanobacteria. — P. Natl. Acad. Sci. 14: 6215–6218, 1995.

    Article  Google Scholar 

  • Song X.S., Hu W.H., Mao W.H. et al.: Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus L. — Plant Physiol. Biochem. 12: 1082–1088, 2005.

    Article  Google Scholar 

  • Sonoike K.: Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. — Plant Cell Physiol. 3: 239–247, 1996.

    Article  Google Scholar 

  • Sonoike K., Kamo M., Hihara Y. et al.: The mechanism of the degradation of psab gene product, one of the photosynthetic reaction center subunits of photosystem I, upon photoinhibition. — Photosynth. Res. 1: 55–63, 1997.

    Article  Google Scholar 

  • Sonoike K., Terashima I.: Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. — Planta 2: 287–293, 1994.

    Article  Google Scholar 

  • Sonoike K., Terashima I., Iwaki M. et al.: Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. — FEBS Letters 2: 235–238, 1995.

    Article  Google Scholar 

  • Sui N., Li M., Liu X. et al.: Response of xanthophyll cycle and chloroplastic antioxidant enzymes to chilling stress in tomato over-expressing glycerol-3-phosphate acyltransferase gene. — Photosynthetica 3: 447–454, 2007.

    Article  Google Scholar 

  • Takami T., Shibata M., Kobayashi Y. et al.: De novo biosynthesis of fatty acids is important for maintenance of photochemical activity under low temperature environments in Arabidopsis. — In: Kuang T., Lu C., Zhang L. (ed.): Photosynthesis Research for Food, Fuel and the Future. Pp. 625–627. Springer, Berlin, Heidelberg 2013.

    Chapter  Google Scholar 

  • Terashima I., Funayama S., Sonoike K.: The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. — Planta 2: 300–306, 1994.

    Google Scholar 

  • Tjus S.E., Møller B.L., Scheller H.V.: Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. — Plant Physiol. 2: 755–764, 1998.

    Article  Google Scholar 

  • Van Kooten O., Snel J.F.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. — Photosynth. Res. 3: 147–150, 1990.

    Article  Google Scholar 

  • Wang A., Luo G.: Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. — Plant Physiol. Commun. 55–57, 1990.

  • Xu C.C., Jeon Y.A., Lee C.H.: Relative contributions of photochemical and non-photochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature. — Physiol. Plantarum 4: 447–453, 1999.

    Article  Google Scholar 

  • Xu D., Wu S.: Three phases of dark-recovery course from photoinhibition resolved by the chlorophyll fluorescence analysis in soybean leaves under field conditions. — Photosynthetica 3: 417–423, 1996.

    Google Scholar 

  • Zhang Y.J., Yang J.S., Guo S.J. et al.: Over-expression of the Arabidopsis cbf1 gene improves resistance of tomato leaves to low temperature under low irradiance. — Plant Biol. 2: 362–367, 2011.

    Article  Google Scholar 

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Authors and Affiliations

  1. Key Laboratory of Plant Stress Research, College of Life Science, Shandong Normal University, Jinan, 250014, China

    N. Sui

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  1. N. Sui
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Correspondence to N. Sui.

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Acknowledgements: We are grateful for financial support from the NSFC (National Natural Science Research Foundation of China, project No. 31300205), Natural Science Research Foundation of Shandong (ZR2013CQ009) and the Program for Scientific Research Innovation Team in Colleges and Universities of Shandong Province.

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Sui, N. Photoinhibition of Suaeda salsa to chilling stress is related to energy dissipation and water-water cycle. Photosynthetica 53, 207–212 (2015). https://doi.org/10.1007/s11099-015-0080-y

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  • DOI: https://doi.org/10.1007/s11099-015-0080-y

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