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Brassinosteroids Alleviate Heat-Induced Inhibition of Photosynthesis by Increasing Carboxylation Efficiency and Enhancing Antioxidant Systems in Lycopersicon esculentum

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Abstract

To investigate the effects of exogenously applied brassinosteroids on the thermotolerance of plants, leaf CO2 assimilation, chlorophyll fluorescence parameters, and antioxidant enzyme metabolism were examined in tomato (Lycopersicon esculentum Mill. cv. 9021) plants with or without 24-epibrassinolide (EBR) application. Tomato plants were exposed to 40/30°C for 8 days and then returned to optimal conditions for 4 days. High temperature significantly decreased the net photosynthetic rate (P n), stomatal conductance (G s), and maximum carboxylation rate of Rubisco (V cmax), the maximum potential rate of electron transport contributed to ribulose-1,5-bisphosphate (RuBP), as well as the relative quantum efficiency of PSII photochemistry (ФPSII), photochemical quenching (q P), and increased nonphotochemical quenching (NPQ). However, only slight reversible photoinhibition occurred during heat stress. Interestingly, EBR pretreatment significantly alleviated high-temperature-induced inhibition of photosynthesis. The activities of antioxidant enzymes such as superoxide dismutase (SOD), ascorbate peroxidase (APX), guaiacol peroxidase (GPOD), and catalase (CAT) increased during heat treatments, and these increases proved to be more significant in EBR-treated plants. EBR application also reduced total hydrogen peroxide (H2O2) and malonaldehyde (MDA) contents, while significantly increasing shoot weight following heat stress. It was concluded that EBR could alleviate the detrimental effects of high temperatures on plant growth by increasing carboxylation efficiency and enhancing antioxidant enzyme systems in leaves.

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References

  • Allen DJ, Mckee IF, Farage PK, Baker NR (1997) Analysis of limitation to CO2 assimilation on exposure of leaves of two Brassica napus cultivars to UV-B. Plant Cell Environ 20:633–640

    Article  CAS  Google Scholar 

  • Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: Relationships in green cells. Physiol Plant 100:224–233

    Article  CAS  Google Scholar 

  • Anderson JA (2002) Catalase activity, hydrogen peroxide content and thermotolerance of pepper leaves. Sci Hort 95:277–284

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Baker NR, Nogués S, Allen DJ (1997) Plants and UV-B; response to environmental change. In: Lumsden PJ (ed) Photosynthesis and photoinhibition. Cambridge University Press, Cambridge pp 95–111

    Google Scholar 

  • Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature inhigher plants. Ann Rev Plant Physiol 31:491–543

    Article  Google Scholar 

  • Bilger W, Björkman O (1990) Role of the xanthophylls cycle in photo protection elucidated by measurements of light induced absorbance changes, fluorescence and photosynthesis in Hedera canariensis. Photosyn Res 25:173–185

    Article  CAS  Google Scholar 

  • Bishop GJ, Koncz C (2002) Brassinosteroids and plant steroid hormone signaling. PlantCell 14:S97–S110

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein - dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of super oxide dismutase ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227

    Article  PubMed  CAS  Google Scholar 

  • Cao S, Xu Q, Cao Y, Qian K, An K, Zhu Y, Binzeng H, Zhao H, Kuai B (2005) Loss of function mutations in DET2 gene lead to an enhanced resistance to oxidative stress in Arabidopsis. Physiol Plant 123:57–66

    Article  CAS  Google Scholar 

  • Clouse SD (1996) Molecular genetic studies confirm the role of brassinosteroids in plant growth and development. Plant J 10:1–8

    Article  PubMed  CAS  Google Scholar 

  • Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Ann Rev Plant Physiol Plant Mol Biol 49:427–451

    Article  CAS  Google Scholar 

  • Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Nat Acad Sci U S A 97:13430–13435

    Article  CAS  Google Scholar 

  • Crafts-Brandner SJ, Salvucci ME (2002) Sensitivity of photosynthesis in a C4 plant, maize to heat stress. Plant Physiol 129:73–1780

    Article  CAS  Google Scholar 

  • Dhaubhadel S, Chaundhary S, Dobinson KF, Krishna P (1999) Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Mol Biol 40:333–342

    Article  PubMed  CAS  Google Scholar 

  • Ershova A, Khripach V (1996) Effects of epibrassinolide on lipid peroxidation in Pisum sativum at normal aeration and under oxygen deficiency. Russ J Plant Physiol 43:750–752

    CAS  Google Scholar 

  • Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant Cell Environ 27:137–153

    Article  CAS  Google Scholar 

  • Garcia-Ferris C, Moreno J (1994) Oxidative modification and breakdown of ribulose 1,5-bisphosphate carboxylase/oxygenase induced in Euglena gracilis by nitrogen starvation. Planta 193:208–215

    Article  CAS  Google Scholar 

  • Genty B, Briatais JM, Baker NR (1989) The relationships between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase I. Occurrences in higher plants. Plant Physiol 59:309–414

    PubMed  CAS  Google Scholar 

  • Gilmore AM (1997) Mechanistic aspects of xanthophylls cycle dependent photoprotection in higher plant chloroplast and leaves. Physiol Plant 99:197–209

    Article  CAS  Google Scholar 

  • Haldimann P, Feller U (2005) Growth at moderately elevated temperature alters the physiological response of the photosynthetic apparatus to heat stress in pea (Pisum sativum L.) leaves. Plant Cell Environ 28:302–317

    Article  CAS  Google Scholar 

  • Haubrick LL, Assman SM (2006) Brassinosteroids and plant function: some clues, more puzzles. Plant Cell Environ 29:446–457

    Article  PubMed  CAS  Google Scholar 

  • Havaux M (1993) Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Sci 94:19–33

    Article  CAS  Google Scholar 

  • Heckathorn SA, Downs CA, Sharkey TD, Coleman JS (1998) The small, methionine-rich chloroplast heat shock proteins protect photosystem II electron transport during heat stress. Plant Physiol 116: 439–444

    Article  PubMed  CAS  Google Scholar 

  • Hirotsu N, Makino A, Ushio A, Mae T (2004) Changes in the thermal dissipation and the electron flow in the water–water cycle in rice grown under conditions of physiologically low temperature. Plant Cell Physiol 45:635–644

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996 Regulation of light harvesting in green plants. Ann Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  CAS  Google Scholar 

  • Irihimovitch V, Shapira M (2000) Glutathione redox potential modulated by reactive oxygen species regulates translation of Rubisco large subunit in the chloroplast. J Biol Chem 275:16289–16295

    Article  PubMed  CAS  Google Scholar 

  • Ishida H, Shimizu S, Makino A, Mae T (1998) Light dependent fragmentation of the large subunit of ribulose -5,1 bisphosphate carboxylase/oxygenase in chloroplast isolated from wheat leaves. Planta 204:305–309

    Article  PubMed  CAS  Google Scholar 

  • Khripach V, Zhabinskii V, De Groot A (2000) Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI century. Ann Bot 86:441–447

    Article  CAS  Google Scholar 

  • Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289–297

    Article  PubMed  CAS  Google Scholar 

  • Kulaeva ON, Burkhanova EA, Fedina AB, Khokhlova VA, Bokebayeva GA, Vorbrodt HM, Adam G (1991) Effects of brassinosteroids on protein synthesis and plant cell ultrastructure under stress conditions. In: Cutler HG, Yokota T, Adam G (eds), Brassinosteroids: Chemistry, Bioactivity, and Applications, Am Chem Soc Symp Ser 474. Washington, DC: American Chemical Society, pp 141–155

    Google Scholar 

  • Law RD, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1, 5-bisphosphate carboxylase/oxygenase. Plant Physiol 120:173–181

    Article  PubMed  CAS  Google Scholar 

  • Leakey ADB, Press MC, Scholes JD (2003) High temperature inhibition of photosynthesis is greater under sun flecks than uniform irradiance in a tropical rain forest tree seedling. Plant Cell Environ 26:1681–1690

    Article  Google Scholar 

  • Lefebvre S, Lawson T, Fryer M, Zalchleniuk OK, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138:451–460

    Article  PubMed  CAS  Google Scholar 

  • Mandava NB (1988) Plant growth-promoting brassinosteroids. Ann Rev Plant Physiol Plant Mol Biol 39:23–25

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Montoya T, Nomura T, Yokota T, Farrar K, Harrison K, Jones JGD, Kaneta T, Kamiya W, Szekeres M, Bishop GR (2005) Patterns of dwarf expression and brassinosteroid accumulation in tomato reveal the importance of brassinosteroid synthesis during fruit development. Plant J 42:262–269

    Article  PubMed  CAS  Google Scholar 

  • Mazzora LM, Núñez M, Hechararria M, Coll F, Sanchez-Blanco MJ (2002) Influence of brassinosteroids on antioxidant enzyme activity in tomato under different temperatures. Biol Plant 45:593–596

    Article  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast. Plant Cell Physiol 22:676–690

    Google Scholar 

  • Nakashita H, Yasuda M, Nitta T, Asami T, Fujikoa S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S (2003) Brassinosteroids functions in a broad range of disease resistance in tobacco and rice. Plant J 33:887–898

    Article  PubMed  CAS  Google Scholar 

  • Nogués S, Baker NR (2000) Effect of drought on photosynthesis in Mediterranean plants grown under enhanced UV-B radiation. J Exp Bot 51:1309–1317

    Article  PubMed  Google Scholar 

  • Núñez M, Mazzafera P, Mazzora LM, Sigueira WJ, Zullo MAT (2003) Influence of a brassinosteroid analogue on antioxidant enzymes in rice grown in culture medium with NaCl. Biol Plant 47:67–70

    Article  Google Scholar 

  • Ölcer H, Llyod JC, Raines CA (2001) Photosynthetic capacity is differentially affected by reduction in sedoheptulose-1,7-bisphosphatase activity during leaf development in transgenic tobacco plants. Plant Physiol 125:982–989

    Article  PubMed  Google Scholar 

  • Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis. Curr Opin Plant Biol 5:193–198

    Article  PubMed  CAS  Google Scholar 

  • Ozdemir F, Bor M, Demiral T, Turkan I (2004) Effects of 24-epibrassinolide on seed germination, seedling growth, lipid peroxidation, proline content and antioxidative system of rice (Oryza sativa L) under salinity stress. Plant Growth Regul 42:203–211

    Article  Google Scholar 

  • Patterson BD, Mackae EA, Mackae I (1984) Estimation of hydrogen peroxide in plants extracts using Titanium (ıv). Anal Biochem 139:487–492

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T (2003) Chloroplast redox signals how photosynthesis controls its own genes. Trends Plant Sci 8:33–41

    Article  PubMed  CAS  Google Scholar 

  • Quinn PJ, Williams WP (1985) Environmental induced changes in chloroplast membranes and their effects on photosynthetic function. In: Baker NR, Barberand J (eds), Photosynthetic mechanisms and the environment. Amsterdam: Elsevier, pp. 1–47

    Google Scholar 

  • Rivero RM, Ruiz JM, Romero L (2004) Oxidative metabolism in tomato plants subjected to heat stress. J Hort Sci Biotechnol 79:560–564

    CAS  Google Scholar 

  • Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiol 134:1460–1470

    Article  PubMed  CAS  Google Scholar 

  • Scandalios JG (2002) Oxidative stress responses—What have genome-scale studies taught us? Genome Biol 3:10191–10196

    Article  Google Scholar 

  • Sharkey TD (2006) Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Environ 29:1659–1670

    Article  CAS  Google Scholar 

  • Singh I, Shono M (2005) Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regul 47:111–119

    Article  CAS  Google Scholar 

  • Steber CM, McCourt P (2001) A role for brassinosteroid in germination in Arabidopsis. Plant Physiol 125:763–769

    Article  PubMed  CAS  Google Scholar 

  • Takahama U, Oniki T (1992) Regulation of peroxidase-dependent oxidation of phenolics in the apoplast of spinach leaves by ascorbate. Plant Cell Physiol 33:379–387

    CAS  Google Scholar 

  • van Kooten O, Snel J (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Res 25:147–150

    Article  Google Scholar 

  • Verhoeven AS, Demmig-Adams B, Adams WWIII (1997) Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiol 113:817–824

    PubMed  CAS  Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  Google Scholar 

  • Wilen RW, Sacco M, Gusta LV, Krishna P (1995) Effects of 24-epibrassinolide on freezing and thermotolerance of bromegrass (Bromus inermis) cell cultures. Physiol Plant 95:195–202

    Article  CAS  Google Scholar 

  • Willenkens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inze D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816

    Article  Google Scholar 

  • Yamori W, Suzuki K, Noguchi K, Nakai M, Terashima I (2006) Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Environ 29:1659–1670

    Article  PubMed  CAS  Google Scholar 

  • Yordanov I, Dilova S, Petkova R, Pangelova T, Goltsev VKH (1986) Mechanisms of the temperature damage and acclimation of the photosynthetic apparatus. Photobiochem Photobiophys 12:147–155

    Google Scholar 

  • Yu JQ, Matsui Y (1997) Effects of root exudates and allelochemicals on ion uptake by cucumber seedlings. J Chem Ecol 23:17–827

    Article  CAS  Google Scholar 

  • Yu JQ, Zhou YH, Ye SF, Huang LF (2002) 24-epibrassinolide and abscisic acid protect cucumber seedlings from chilling injury. J Hort Sci Biotechnol 77:430–473

    Google Scholar 

  • Yu JQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, Nogués S (2004) A role forbrassinosteroids in the regulation of photosynthesis in Cucumis sativus. J Exp Bot 55:1135–1143

    Article  PubMed  CAS  Google Scholar 

  • Zhou YH, Yu JQ, Huang LF, Nogués S (2004) The relationship between CO2 assimilation, photosynthetic electron transport and water-water cycle in chill-exposed cucumber leaves under low light and subsequent recovery. Plant Cell Environ 27:1503–1514

    Article  Google Scholar 

  • Zhou YH, Yu JQ, Mao WH, Huang LF, Song XS, Nogués S (2006) Genotypic variation on Rubisco expression, photosynthetic electron flow and antioxidant metabolism in the chloroplasts of chill-exposed cucumber plants. Plant Cell Physiol 47:192–199

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (3050344, 30671428) and the National Outstanding Youth Scientist Foundation (30235029).

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Authors and Affiliations

  1. Department of Horticulture, Huajiachi Campus, Zhejiang University, Kaixuan Road 268, Hangzhou, 310029, P.R. China

    Joshua Otieno Ogweno, Xing Shun Song, Kai Shi, Wen Hai Hu, Wei Hua Mao, Yan Hong Zhou & Jing Quan Yu

  2. Key Laboratory of Horticultural Plant Growth, Development and Biotechnology, Agricultural Ministry of China, Kaixuan Road 268, Hangzhou, 310029, P.R. China

    Jing Quan Yu

  3. Departament de Biologia Vegetal, Universitat de Barcelona, 645 Diagonal Av, E-08028, Barcelona, Spain

    Salvador Nogués

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  1. Joshua Otieno Ogweno
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Correspondence to Jing Quan Yu.

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Ogweno, J.O., Song, X.S., Shi, K. et al. Brassinosteroids Alleviate Heat-Induced Inhibition of Photosynthesis by Increasing Carboxylation Efficiency and Enhancing Antioxidant Systems in Lycopersicon esculentum . J Plant Growth Regul 27, 49–57 (2008). https://doi.org/10.1007/s00344-007-9030-7

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