Exogenous Calcium Alleviates Photoinhibition of PSII by Improving the Xanthophyll Cycle in Peanut (Arachis Hypogaea) Leaves during Heat Stress under High Irradiance

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Yang, Sha ^a,b   Wang, Fang ^a,c   Guo, Feng ^a,b   Meng, Jing Jing ^a,b   Li, Xin Guo ^a,b   Dong, Shu Ting ^c   Wan, Shu Bo ^b  

^a SHANDONG PEANUT RESEARCH INSTITUTE   (China)

^b Key Laboratory for Genetic Improvement of Crop   (China)

^c SHANDONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM ION; CALMODULIN; CHLORPROMAZINE; EGTAZIC ACID; HYDROGEN PEROXIDE; LANTHANUM CHLORIDE; PROTEIN D1; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; CALMODULIN GENE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EPOXIDATION; GENE EXPRESSION; HEAT STRESS; IRRADIATION; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; NUCLEOTIDE SEQUENCE; PEANUT; PHOTOCHEMICAL EFFICIENCY; PHOTOINHIBITION; PHOTOSYSTEM II; PLANT GENE; PLANT GENOME; PLANT LEAF; PLANT STRESS; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TEMPERATURE MEASUREMENT; VDE GENE; XANTHOPHYLL CYCLE;

EID: 84881334093     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071214     Document Type: Article

References (64)

1. Björkman O (1989) Some viewpoints on photosynthetic response and adaptation to environmental stress. In: Briggs WR (ed) Photosynthesis. Alan R Liss, New York, USA, 45-58.
2. Allakhverdiev SI, Murata N, (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657: 23-32.
3. Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N, (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongationn of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43: 1321-1330.
4. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI, (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767: 414-421.
5. Adir N, Shochat S, Inoue Y, Ohad I, (1990) Mechanism of the light dependent turnover of the D1 protein. J Biol Chem 265: 12563-12568.
6. Aro EM, Virgin I, Andersson B, (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134.
7. Horton P, Ruban AV, Walters RG, (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47: 655-684.
8. Niyogi KK, Grossman AR, Björkman O, (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134.
9. Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, et al. (2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth Res 67: 139-145.
10. Demmig-Adams B, Adams WW III, (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198: 460-470.
11. Li XG, Meng QW, Jiang GQ, Zou Q, (2003) The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle. Photosynthetica 41: 259-265.
12. Li XG, Bi YP, Zhao SJ, Meng QW, Zou Q, et al. (2005) Cooperation of xanthophyll cycle with water-water cycle in the protection of photosystems 1 and 2 against inactivation during chilling stress under low irradiance. Photosynthetica 43: 261-266.
13. Yamamoto HY, (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem 51: 639-648.
14. Niyogi KK, (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333-359.
15. Gilmore AM, Farley SJ, McCutachan JS, (2002) Light stress and photosynthesis. Funct Plant Biol 29: 1125-1215.
16. Müller P, Li XP, Niyogi KK, (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558-1566.
17. Baroli I, Do AD, Yamane T, Niyogi KK, (2003) Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardt II from photo-oxidative stress. Plant Cell 15: 992-1008.
18. Bush DS, (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46: 95-122.
19. Bowler C, Fluhr R, (2000) The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci 5: 241-246.
20. Cooke A, Cookson A, Ealnshaw MJ, (1986) The mechanism of action of calciumin in the inhibition of high temperature-induced leakage of belacyanin from beet root discs. New Phytol 102: 491-497.
21. Arora R, Palta JP, (1988) In vivo perturbation of membrane-associated calcium by freeze-thaw stress in onion bulb cells. Simulation of this perturbation in extracellular KC1 and alleviation by calcium. Plant Physiol 87: 622-628.
22. Melgar A, Pérez JF, Laget H, Horillo A, (2007) Thermochemical equilibrium modelling of a gasifying process. Energy Convers Manage 48: 59-67.
23. Kreimer G, Melkonian M, Holtum JAM, Latzko E, (1988) Stromal free calcium concentration and light-mediated activation of chloroplast fructose-1,6-bisphosphatase. Plant Physiol 86: 423-428.
24. Tan W, Meng QW, Brestic M, Olsovska K, Yang XH, (2011) Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. J Plant Physiol 168: 2063-2071.
25. Liang WJ, Wang ML, Ai XZ, (2009) The role of calcium in regulating photosynthesis and related physiological indexes of cucumber seedlings under low light intensity and suboptimal temperature stress. Sci Hortic 123: 34-38.
26. Zhao HJ, Tan JF, (2005) Role of calcium ion in protection against heat and high irradiance stress-induced oxidative damage to photosynthesis of wheat leaves. Photosynthetica 43: 473-476.
27. Noctor G, Foyer CH, (1998) Ascorbate and glutathione: keep active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49: 249-279.
28. Ai X, Wang X, Cui Z, Wang Z, (2006) Effect of calcium on photosynthesis of cucumber under low light intensity and suboptimal temperature. Scientia Agricultura Sinica 39(9): 1865-1871.
29. Horton P, Ruban AV, Walters RG, (1994) Regulation of light harvesting in green plants. Indication by nonphotochemical quenching of chlorophyll fluorescence. Plant Physiol 106: 415-420.
30. Liu P, Meng QW, Zou Q, Zhao SJ, Liu QZ, (2001) Effects of cold-hardening on chilling-induced photoinhibition of photosynthesis and on xanthophyll cycle pigments in sweet pepper. Photosynthetica 39: 467-472.
31. Li XG, Duan W, Meng QW, Zou Q, Zhao SJ, (2004) The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. Plant Cell Physiol 45(1): 103-108.
32. Chinnusamy V, Jagendorf A, Zhu JK, (2005) Understanding and improving salt tolerance in plants. Crop Sci 45: 437-448.
33. Ottow EA, Brinker M, Tehchmann T, Fritz E, Kaiser W, et al. (2005) Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiol 139: 1762-1772.
34. Wang ZH, Sun DY, (1997) Advances of the studies on plant calmodulin. Chin Bull Bot 14: 1-7 (in Chinese).
35. Van Kooten O, Snel JFH, (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25: 147-150.
36. Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In Ecophysiology of Photosynthesis. Edited by Schulze ED, Caldwell MM Springer-Verlag, Berlin, 49-70.
37. Quick WP, Stitt M, (1989) An examination of factors contribution to nonphotochemical quenching of chlorophyll fluorescence in barely leaves. Biochim Biophys Acta 977: 287-296.
38. Zhang LX, Paakkarinen V, van Wijk KJ, Aro EM, (1999) Cotranslational assembly of the D1 protein into photosystem II. J Biol Chem 274: 16062-16067.
39. Porra RJ, Thompson WA, Kriedemann PE, (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectrometry. Biochim Biophys Acta 975: 384-394.
40. Sui N, Li M, Liu XY, Wang N, Fang W, et al. (2007) Response of xanthophyll cycle and chloroplastic antioxidant enzymes to chilling stress in tomato over-expressing glycerol-3-phosphate acyltransferase gene. Photosynthetica 45: 447-454.
41. Wang AG, Luo GH, (1990) Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. Plant Physiol 6: 55-57.
42. Zhao SJ, Meng QW, Xu CC, Han HY, Zou Q, (1995) Analysis of xanthophyll cycle components in lant tissues by high performance liquid chromatography. Plant Physiol 31: 438-442.
43. Liu C, Pan BF, Cao WQ, Lu Y, Huang H, et al. (2008) Influences of calcium deficiency and cerium on growth of spinach plants. Biol Trace Elem Res 121: 266-275.
44. Asada K, (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141: 391-396.
45. Takahashi S, Murata N, (2006) Glycerate-3-phosphate, produced by CO2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. Biochim Biophys Acta 1757: 198-205.
46. Pospíšil P, (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta 1787: 1151-1160.
47. Jiang YW, Huang BR, (2001) Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J Exp Bot 52: 341-349.
48. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS, (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol-Cell Physiol 287: 817-833.
49. Farooq M, Aziz T, Basra SMA, Wahid A, Khaliq A, et al. (2008) Exploring the role of calcium to improve chilling tolerance in hybrid maize. J Agron Crop Sci 194: 350-359.
50. Yang T, Poovaiah BW, (2002) Hydrogen peroxide homeostasis: Activation of plant catalase by calcium/calmodulin. PNAS 99: 4097-4102.
51. Demmig-Adams B, Adams WW III, (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599-626.
52. Müller-Moulé P, Havaux M, Niyogi KK, (2003) Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis. Plant Physiol 133: 748-760.
53. Wang N, Fang W, Han H, Sui N, Li B, et al. (2008) Overexpression of zeaxanthin epoxidase gene enhances the sensitivity of tomato PSII photoinhibition to high light and chilling stress. Plant Physiol 132: 384-396.
54. Khamis S, Lamaze T, Lemoine Y, Foyer C, (1990) Adaptation of the photosynthetic apparatus in maize leaves as a result of nitrogen limitation: relationship between electron transport and carbon assimilation. Plant Physiol 94: 1436-1443.
55. Verhoeven AS, Demmig-Adams B, Adams III WW, (1997) Enhanced employment of the xanthophyll cycle and the thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiol 113: 817-824.
56. Chen Y, Murchie EH, Hubbart S, Horton P, Peng S, (2003) Effects of season-dependent irradiance levels and nitrogen-deficiency on photosynthesis and photoinhibition in field-grown rice. Physiologia Plantarum 117: 343-351.
57. Demmig-Adams B, (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1-24.
58. Wang LJ, Huang WD, Li JY, Liu YF, Shi YL, (2004) Peroxidation of membrane lipid and Ca2+ homeostasis in grape mesophyll cells during the process of cross-adaptation to temperature stresses. Plant Sci 167: 71-77.
59. Bhattacharjee S, (2008) Calcium-dependent signaling pathway in the heat-induced oxidative injury in Amaranthus lividus. Plant Bio 52(1): 137-140.
60. Rudd JJ, Franklin-Tong VE, (2001) Unravelling response-specificity in Ca2+ signalling pathways in plant cells. New Phytol 151: 7-33.
61. van Der Luit AH, Olivari C, Haley A, Knight MR, Trewavas AJ, (1999) Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco. Plant Physiol 121: 705-714.
62. Ma L, Xu X, Cui S, Sun D, (1999) The presence of a heterotrimeric G protein and its role in signal transduction of extracellular calmodulin in pollen germination and tube growth. Plant Cell 11: 1351-1364.
63. Szymanski DB, Liao B, Zielinski RE, (1996) Calmodulin isoforms differentially enhance the binding of cauliflower nuclear proteins and recombinant TGA3 to a region derived from the Arabidopsis Cam-3 promoter. Plant Cell 8: 1069-1077.
64. Yang T, Poovaiah BW, (2000) Molecular and biochemical evidence for the involvement of calcium/calmodulin in auxin action. J Biol Chem 275: 3137-3143.