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Comparative analysis of ultrastructure, antioxidant enzyme activities, and photosynthetic performance in rice mutant 812HS prone to photooxidation

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Photosynthetica

Abstract

Under optimal conditions, most of the light energy is used to drive electron transport. However, when the light energy exceeds the capacity of photosynthesis, the overall photosynthetic efficiency drops down. The present study investigated the effects of high light on rice photooxidation-prone mutant 812HS, characterized by a mutation of leaf photooxidation 1 gene, and its wild type 812S under field conditions. Our results showed no significant difference between 812HS and 812S before exposure to high sunlight. However, during exposure to high light, shoot tips of 812HS turned yellow and their chlorophyll (Chl) content decreased. Transmission electron microscopy showed that photooxidation resulted in significant damage of chloroplast ultrastructure. It was confirmed also by inhibited photophosphorylation and reduced ATP content. The decreased coupling factor of ATP, Ca2+-ATPase and Mg2+-ATPase activities also verified these results. Further, significantly enhanced activities of antioxidative enzymes were observed during photooxidation. Malondialdehyde, hydrogen peroxide, and the superoxide generation rates also increased. Chl a fluorescence analysis found that the performance index and maximum quantum yield of PSII declined on August 4, 20 days after high-light treatment. Net photosynthetic rate also decreased and substomatal CO2 concentration increased in 812HS at the same time. In conclusion, our findings indicated that excessive energy triggered the production of toxic reactive oxygen species and promoted lipid peroxidation in 812HS plants, causing severe damage to cell membranes, degradation of photosynthetic pigments and proteins, and ultimately inhibition of photosynthesis.

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Abbreviations

AA:

ascorbate

APX:

ascorbate peroxidase

BSA:

bovine serum albumin

CAT:

catalase

Chl:

chlorophyll

C i :

substomatal CO2 concentration

DAB:

3,3-diaminobenzidine

FM:

fresh mass

FV/FM :

maximal quantum yield of PSII

GR:

glutathione reductase

MDA:

malondialdehyde

NBT:

nitroblue tetrazolium

\({O_2}^{_.^ - }\) :

superoxide

OH:

hydroxyl radical

PIABS :

performance index

P N :

net photosynthetic rate

POD:

guaiacol peroxidase

RC:

reaction centers

ROS:

reactive oxygen species

SOD:

superoxide dismutase

TBA:

thiobarbituric acid

TEM:

transmission electron microscopy

References

  • Alcázar R., Altabella T., Marco F. et al.: Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. — Planta 231: 1237–1249, 2010.

    Article  PubMed  Google Scholar 

  • Bishehkolaei R., Fahimi H., Saadatmand S. et al.: Ultrastructural localisation of chromium in Ocimum basilicum. — Turk. J. Bot. 35: 261–268, 2011.

    CAS  Google Scholar 

  • Blokhina O., Virolainen E., Fagerstedt K.V.: Antioxidants, oxidative damage and oxygen deprivation stress: a review. — Ann. Bot.-London 91: 179–194, 2003.

    Article  CAS  Google Scholar 

  • Fang J., Chai C.L, Qian Q. et al.: Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. — Plant J. 54: 177–189, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer C.H., Lopez-Delgado H., Dat J.F. et al.: Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. — Physiol. Plantarum 100: 241–254, 1997.

    Article  CAS  Google Scholar 

  • Fu Y.Y., Li F.F., Xu T. et al.: Bioaccumulation, subcellular, and molecular localization and damage to physiology and ultrastructure in Nymphoides peltata (Gmel.) O. Kuntze exposed to yttrium. — Environ. Sci. Pollut. R. 21: 2935–2942, 2014.

    Article  CAS  Google Scholar 

  • Gratão P.L., Polle A., Lea P.J. et al.: Making the life of heavy metal stressed plants a little easier. — Funct. Plant Biol. 32: 481–494, 2005.

    Article  Google Scholar 

  • Guha A., Sengupta D., Reddy A.R.: Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. — J. Photoch. Photobio. B. 119: 71–83, 2013.

    Article  CAS  Google Scholar 

  • Hossain M.A., Hasanuzzaman M., Fujita M.: Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. — Physiol. Mol. Biol. Plants 16: 259–272, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen G.X., Liu S.H., Zhang C.J. et al.: Effects of drought on photosynthetic characteristics of flag leaves of a newlydeveloped super-high-yield rice hybrid. — Photosynthetica 42: 573–578, 2004.

    Article  CAS  Google Scholar 

  • Kang Z., Li G., Huang J. et al.: Photosynthetic and physiological analysis of the rice high-chlorophyll mutant (Gc). — Plant Physiol. Bioch. 60: 81–87, 2012.

    Article  CAS  Google Scholar 

  • Ketcham S.R., Davenport J.W., Warncke K. et al: Role of the gamma subunit of chloroplast coupling factor 1 in the lightdependent activation of photophosphorylation and ATPase activity by dithiothreitol. — J. Biol. Chem. 259: 7286–7293, 1984.

    CAS  PubMed  Google Scholar 

  • Ladygin V.G.: Photosystem damage and spatial architecture of thylakoids in chloroplasts of pea chlorophyll mutants. — Biol. Bull+ 31: 268–276, 2004.

    Article  CAS  Google Scholar 

  • Lai D., Xia S.J., Lv C.G. et al.: Mapping a leaf photo-oxidation gene LPO1(t) in rice. — Jiangsu Agric. Sci. 28: 1212–1217, 2012.

    Google Scholar 

  • Li G., Wan S., Zhou J. et al.: Leaf chlorophyll fluorescence, hyperspectral reflectance, pigments content, malondialdehyde and proline accumulation responses of castor bean (Ricinus communis L.) seedlings to salt stress levels. — Ind. Crop. Prod. 31: 13–19, 2010.

    Article  Google Scholar 

  • Long S.P., East T.M., Baker N.R.: Chilling damage to photosynthesis in young Zea mays: 1. effects of light and temperature variation on photosynthetic CO2 assimilation. — J. Exp. Bot. 34: 177–188, 1983.

    Article  Google Scholar 

  • Ma J., Lv C.F., Xu M.L. et al.: Photosynthesis performance, antioxidant enzymes, and ultrastructural analyses of rice seedlings under chromium stress. — Environ. Sci. Pollut. R. 23: 1768–1778, 2016.

    Article  CAS  Google Scholar 

  • Nakano Y., Asada K.: Purification of ascorbate peroxidase in spinach chloroplasts: its inactivation in ascorbate depleted medium and reactivation by monodehydro ascorbate radical. — Plant Cell Physiol. 28: 131–140, 1987.

    CAS  Google Scholar 

  • Phung T. H., Jung S.: Differential antioxidant defense and detoxification mechanisms in photodynamically stressed rice plants treated with the deregulators of porphyrin biosynthesis, 5-aminolevulinic acid and oxyfluorfen. — Biochem. Bioph. Res. Co. 459: 346–351, 2015.

    Article  CAS  Google Scholar 

  • Qiao X.Q., Shi G.X., Chen L. et al.: Lead-induced oxidative damage in steriled seedlings of Nymphoides peltatum. — Environ. Sci. Pollut. R. 20: 5047–5055, 2013.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Rao M.V., Paliyath G., Ormrod D.P.: Ultraviolet-B-and ozoneinduced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. — Plant Physiol. 110: 125–136, 1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rossel J.B., Wilson P.B., Hussain D. et al.: Systemic and intracellular responses to photooxidative stress in Arabidopsis. — Plant Cell 19: 4091–4110, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandalio L.M., Dalurzo H.C., Gómez M. et al.: Cadmiuminduced changes in the growth and oxidative metabolism of pea plants. — J. Exp. Bot. 52: 2115–2126, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Shah K., Kumar R.G., Verma S. et al.: Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. — Plant Sci. 161: 1135–1144, 2001.

    Article  CAS  Google Scholar 

  • Sharma P., Dubey R.S.: Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminium. — Plant Cell Rep. 26: 2027–2038, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Shen W.J., Chen G.X., Xu J.G., et al.: High light acclimation of Oryza sativa L. leaves involves specific photosyntheticsourced changes of NADPH/NADP+ in the midvein. — Protoplasma 252: 77–87, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Singh S., Eapen S., D’Souza S.F.: Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. — Chemosphere 62: 233–246, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Sivaci A., Elmas E., Gümüş F. et al.: Removal of cadmium by Myriophyllum heterophyllum Michx. and Potamogeton crispus L. and its effect on pigments and total phenolic compounds. — Arch. Environ. Con. Tox. 54: 612–618, 2008.

    Article  CAS  Google Scholar 

  • Stewart R.R.C., Bewley J.D.: Lipid peroxidation associated with accelerated aging of soybean axes. — Plant Physiol. 65: 245–248, 1980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strasser R.J., Srivastava A., Govindjee.: Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. — Photochem. Photobiol. 61: 32–42, 1995.

    Article  CAS  Google Scholar 

  • Szabó I., Bergantino E., Giacometti G.M.: Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. — EMBO Rep. 6: 629–634, 2005.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vallejos R.H., Arana J.L., Ravizzini R.A.: Changes in activity and structure of the chloroplast proton ATPase induced by illumination of spinach leaves. — J. Biol. Chem. 258: 7317–7321, 1983.

    CAS  PubMed  Google Scholar 

  • Van Heerden P.D.R., Strasser R.J., Krüger G.: Reduction of dark chilling stress in N2-fixing soybean by nitrate as indicated by chlorophyll a fluorescence kinetics. — Physiol. Plantarum 121: 239–249, 2004.

    Article  Google Scholar 

  • Vuleta A., Jovanović S. M., Tucić B.: Adaptive flexibility of enzymatic antioxidants SOD, APX and CAT to high light stress: The clonal perennial monocot Iris pumila as a study case. — Plant Physiol. Bioch. 100: 166–173, 2016.

    Article  CAS  Google Scholar 

  • Wang C., Wang X., Tian Y.: Oxidative stress and potential biomarkers in tomato seedlings subjected to soil lead contamination. — Ecotox. Environ. Safe. 71: 685–691, 2008.

    Article  Google Scholar 

  • Wang Y., Jiang X., Li K. et al: Photosynthetic responses of Oryza sativa L. seedlings to cadmium stress: physiological, biochemical and ultrastructural analyses. — BioMetals 27: 389–401, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Wu Z.M., Zhang X., He B. et al.: A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. — Plant Physiol. 145: 29–40, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Q.S., Hu J.Z., Xie K.B. et al.: Accumulation and acute toxicity of silver in Potamogeton crispus L. — J. Hazard Mater. 173: 186–193, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Yang Y.L., Zhang Y.Y., Wei X.L. et al.: Comparative antioxidative responses and proline metabolism in two wheat cultivars under short term lead stress. — Ecotox. Environ. Safe. 74: 733–740, 2011.

    Article  CAS  Google Scholar 

  • Zhang S.S., Zhang H.M., Qin R. et al.: Cadmium induction of lipid peroxidation and effects on root tip cells and antioxidant enzyme activities in Vicia faba L. — Ecotoxicology 18: 814–823, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Zhao H.X., Yan L., Duan B. et al.: Sex-related adaptive responses of Populus cathayana to photoperiod transitions. — Plant Cell Environ. 32: 1401–1411, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y., Gong Z., Yang Z. et al.: Mutation of the light-induced yellow leaf 1 gene, which encodes a geranylgeranyl reductase, affects chlorophyll biosynthesis and light sensitivity in rice. — PLoS One 8: e75299, 2013.

    Article  Google Scholar 

  • Zhu X.Y., Chen G.C., Zhang C.L.: Photosynthetic electron transport, photophosphorylation, and antioxidants in two ecotypes of reed (Phragmites communis Trin.) from different habitats. — Photosynthetica 39: 183–189, 2001.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. School of Life Sciences, Nanjing Normal University, Nanjing, 210023, China

    J. Ma, C. F. Lv, B. B. Zhang, F. Wang, W. J. Shen, G. X. Chen & Z. P. Gao

  2. Institute of Food and Crops, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China

    C. G. Lv

Authors
  1. J. Ma
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  2. C. F. Lv
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  3. B. B. Zhang
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  4. F. Wang
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  5. W. J. Shen
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  6. G. X. Chen
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  7. Z. P. Gao
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  8. C. G. Lv
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Corresponding authors

Correspondence to Z. P. Gao or C. G. Lv.

Additional information

Acknowledgments: Studies in the Chen Laboratory were supported by the National Natural Science Foundation of China (Grant. No. 31271621/C1302, and No. 31671663), Project BK20140916 supported by NSF of Jiangsu Province of China, Program of Natural Science Research of Jiangsu Higher Education Institutions of China (Grant. No.14KJB180011), and a Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions and Jiangsu Collaborative Innovation Center for Modern Crop Production.

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Ma, J., Lv, C.F., Zhang, B.B. et al. Comparative analysis of ultrastructure, antioxidant enzyme activities, and photosynthetic performance in rice mutant 812HS prone to photooxidation. Photosynthetica 55, 568–578 (2017). https://doi.org/10.1007/s11099-016-0669-9

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  • DOI: https://doi.org/10.1007/s11099-016-0669-9

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