Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants

Daymi Camejo A , Ana Jiménez B C , Juan José Alarcón B , Walfredo Torres A , Juana María Gómez B and Francisca Sevilla B
+ Author Affiliations
- Author Affiliations

A Instituto Nacional de Ciencias Agrícolas, INCA, Gaveta Postal 1, 23700, San José de las Lajas, La Habana, Cuba.

B Centro de Edafología y Biología Aplicada del Segura, CSIC, Apartado 164, E-30100 Murcia, Spain.

C Corresponding author. Email: ajimenez@cebas.csic.es

Functional Plant Biology 33(2) 177-187 https://doi.org/10.1071/FP05067
Submitted: 17 March 2005  Accepted: 15 September 2005   Published: 3 February 2006

Abstract

Seedlings of two tomato genotypes, Lycopersicon esculentum Mill. var. Amalia and the wild thermotolerant type Nagcarlang, were grown under a photoperiod of 16 h light at 25°C and 8 h dark at 20°C. At the fourth true leaf stage, a group of plants were exposed to a heat-shock temperature of 45°C for 3 h, and measurements of chlorophyll fluorescence, gas-exchange characteristics, dark respiration and oxidative and antioxidative parameters were made after releasing the stress. The heat shock induced severe alterations in the photosynthesis of Amalia that seem to mitigate the damaging impact of high temperatures by lowering the leaf temperature and maintaining stomatal conductance and more efficient maintenance of antioxidant capacity, including ascorbate and glutathione levels. These effects were not evident in Nagcarlang. In Amalia plants, a larger increase in dark respiration also occurred in response to heat shock and the rates of the oxidative processes were higher than in Nagcarlang. This suggests that heat injury in Amalia may involve chlorophyll photooxidation mediated by activated oxygen species (AOS) and more severe alterations in the photosynthetic apparatus. All these changes could be related to the more dramatic effect of heat shock seen in Amalia than in Nagcarlang plants.

Keywords: antioxidant activities, fluorescence, heat shock, photosynthesis, tomato.


Acknowledgments

This work was supported by grants from the ‘Convenio de Cooperación Científica Hispano-Cubano del CSIC/CITMA’ (2001CU0015), and the MCYT-FEDER, Ministry of Science and Technology (BFI 2002-03207).


References


Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
PubMed |
open url image1

Al-Khatib K, Paulsen GM (1989) Enhancement of thermal injury to photosynthesis in wheat plants and thylakoids by high light intensity. Plant Physiology 90, 1041–1048. open url image1

Álvarez M, Armas G, Martínez B (1997) Amalia y Mariela, dos variedades de tomate para consumo fresco. Cultivos Tropicales 1810, 83. open url image1

Anderson JA (2002) Catalase activity, hydrogen peroxide content and thermotolerance of pepper leaves. Scientia Horticulturae 95, 277–284.
Crossref | GoogleScholarGoogle Scholar | open url image1

Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15. open url image1

Asada K, Endo T, Mano J, Miyake C (1998) Molecular mechanism for relaxation of and protection from light stress. In ‘Stress responses of photosynthetic organisms’. (Eds K Saton, N Murata) pp. 37–52. (Elsevier: Amsterdam)

Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Annals of Biochemistry 44, 276–287.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Annals of Biochemistry 72, 248–254.
Crossref |
open url image1

Buege JA, Aust SD (1972) Microsomal lipid peroxidation. Methods in Enzymology 52, 302–310. open url image1

Camejo D, Rodríguez P, Morales MA, Dell’Amico J, Torrecillas A, Alarcón JJ (2005) High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. Journal of Plant Physiology 162, 281–289.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dat JF, Foyer CH, Scott MI (1998) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiology 118, 1455–1461.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. Journal of Experimental Botany 53, 1255–1272.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

De Biasi MG, Astolfi S, Acampora A, Zuchi S, Fonzo V, Santangelo E, Caccia R, Badiani M, Soressi GP (2003) A H2O2-forming peroxidase rather than a NAD(P)H-dependent O2·– synthase may be the major player in cell death responses controlled by the Pto–Fen complex following fenthion treatment. Functional Plant Biology 30, 409–417.
Crossref | GoogleScholarGoogle Scholar | open url image1

del Río LA, Sandalio LM, Altomare DA, Tilinskas BA (2003) Mitochondrial and peroxisomal manganese superoxide dismutase: differential expression during leaf senescence. Journal of Experimental Botany 54, 923–933.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Feller U, Crafts-Brandner SJ, Salvucci ME (1998) Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco) activase-mediated activation of Ribulose. Plant Physiology 116, 539–546.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Foyer CH, López-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signaling. Physiologia Plantarum 100, 241–254.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gómez JM, Hernández JA, Jiménez A, del Río LA, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plants. Free Radical Research 31, S11–S18.
PubMed |
open url image1

Gómez JM, Jiménez A, Olmos E, Sevilla F (2004) Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv. Puget) chloroplasts. Journal of Experimental Botany 55, 119–130.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gucci R, Xilyannis C, Flore JA (1991) Gas exchange parameters, water relations and carbohydrate partitioning in leaves of field-grown Prunus domestica following fruit removal. Physiologia Plantarum 83, 497–505.
Crossref | GoogleScholarGoogle Scholar | open url image1

Havaux M (1993) Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Science 94, 19–33.
Crossref | GoogleScholarGoogle Scholar | open url image1

Havaux M, Tardy F (1996) Temperature-dependent adjustment the thermal stability to photosystem II in vivo: possible involvement of xanthophylls-cycle pigments. Planta 198, 324–333.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hernández JA, Ferrer MA, Jiménez A, Ros Barceló A, Sevilla F (2001) Antioxidant systems and O2·– / H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiology 127, 817–831.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hoagland DR, Arnold DI (1950) The water-culture method for growing plants without soil. Californian Agriculture Experimental 347, 123–125. open url image1

Huang B, Liu X, Xu Q (2001) Supraoptimal soil temperatures induced oxidative stress in leaves of creeping bentgrass cultivars differing in heat tolerance. Crop Science 41, 430–435. open url image1

Jiao J, Grodzinski B (1996) The effect of leaf temperature and photorespiratory conditions on export of sugars during steady state photosynthesis in Salvia splendens. Plant Physiology 111, 169–173.
PubMed |
open url image1

Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate–glutathione cycle in mitochondria and peroxisomes of pea (Pisum sativum L.) leaves. Plant Physiology 114, 275–284.
PubMed |
open url image1

Jiménez A, Lundquist M, Olmos E, Gómez J, Sevilla F (2003) Response to ripening of the antioxidant system in purified mitochondria, chloroplasts and chromoplasts from pepper fruits. Free Radical Research 37, 31–32. open url image1

Kobza J, Edwards GE (1987) Influence of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiology 83, 69–74. open url image1

Kraus TE, Fletcher A (1994) Paclobutrazol protects wheat seedlings from heat and paraquat injury. Is detoxification of active oxygen species involved? Plant and Cell Physiology 35, 45–52. open url image1

Kwiatowski J, Kaniuga Z (1984) Evidence for iron-containing superoxide dismutase in leaves of Lycopersicon esculemtum and Phaseolus vulgaris. Acta Physiologiae Plantarum 6, 197–202. open url image1

Lafuente MT, Belver A, Guye MG, Salveit ME (1991) Effect of temperature conditioning on chilling injury of cucumber cotyledons: possible role of abscisic acid and heat-shock proteins. Plant Physiology 95, 443–449. open url image1

Lee BH, Won SH, Lee HS, Miyao M, Chung WI, Kim IJ, Jo J (2000) Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice. Gene 245, 283–290.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu X, Huang B (2000) Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Science 40, 503–510. open url image1

Li HY, Chang CS, Lu LS, Liu CA, Chan MT, Charng YY (2003) Over-expression of Arabidopsis thaliana heat shock factor gene (AtHsf1b) enhances chilling tolerance in transgenic tomato. Botanic Bulletin Academic Singapore 44, 129–154. open url image1

Loggini B, Scartazza A, Brugnoli E, Navari-Izzo F (1999) Antioxidant defense system, pigment composition and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiology 119, 1091–1099.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Makino A, Nakano H, Mae T (1994) Effects of growth temperature on the responses of ribulose-1,5-bisphosphate carboxylase, electron transport components, and sucrose synthesis enzymes to leaf nitrogen in rice, and their relationships to photosynthesis. Plant Physiology 105, 1231–1238.
PubMed |
open url image1

Mateos RM, León AM, Sandalio LM, Gómez M, del Río LA, Palma JM (2003) Peroxisomes from pepper fruits (Capsicum annuum L.): purification, characterization and antioxidant activity. Journal of Plant Physiology 160, 1507–1516.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McCain DC, Croxdale J, Markey JL (1989) Thermal damage to chloroplast envelope membrane. Plant Physiology 90, 606–609. open url image1

McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (henocuprein). Journal of Biological Chemistry 244, 6049–6055.
PubMed |
open url image1

Mishra NP, Mishra RK, Singhal GS (1993) Changes in the activity of anti-oxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in the presence of protein synthesis inhibitors. Plant Physiology 102, 903–910.
PubMed |
open url image1

Morgan RW, Christman MF, Jacobson FS, Stroz G, Ames BN (1986) Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proceedings of the National Academy of Sciences USA 83, 8059–8063. open url image1

Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mittova V, Volokita M, Buy M, Tal M (2000) Activities of SOD and the ascorbate–glutathione cycle enzymes in subcellular compartments in leaves and roots of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiologia Plantarum 110, 42–51.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mullineaux PM, Creissen GP (1997) Glutathione reductase: regulation and role in oxidative stress. In ‘Oxidative stress and the molecular biology of antioxidants defenses’. (Ed. JG Scandalios) pp. 667–713. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor)

Nieto-Sotelo J, Tuan-Hua H (1986) Effect of heat-shock on the metabolism of glutathione in maize roots. Plant Physiology 82, 1031–1035. open url image1

Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Panchuk II, Volkov RA, Schöffl F (2002) Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiology 129, 838–853.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Paolacci AR, Badiani M, Dannibale A, Fusar A, Matteucci G (1997) Antioxidants and photosynthesis in the leaves of Triticum durum Desf. seedlings acclimated to non-stressing high temperatures. Journal of Plant Physiology 150, 381–387. open url image1

Perl-Treves R, Galun E (1991) The tomato Cu, Zn superoxide dismutase genes are developmentally regulated and respond to light and stress. Plant Molecular Biology 17, 745–760.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Prasad TK (1996) Mechanism of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities. The Plant Journal 10, 1017–1026.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rainwater DT, Gossett DR, Millhollon EP, Hanna HY, Banks SW, Cran Lucas M (1996) The relationship between yield and the antioxidant defense system in tomatoes grown under heat stress. Free Radical Research 25, 421–435.
PubMed |
open url image1

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 Physiology 134, 1460–1470.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Santarius KA, Weis E (1988) Heat stress and membranes. In ‘Plant membranes — structure, assembly and function’. (Eds JL Harwood, TJ Walton) pp. 97–112. (Biochemical Society: London)

Sato Y, Murakami T, Funatsucki H, Matsuba S, Saruyama H, Tanida M (2001) Heat-shock-mediated APX gene expression and protection against chilling injury in rice seedlings. Journal of Experimental Botany 52, 145–151.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schaffer L, Feierabend J (2000) Photoinactivation and protection of glycolate oxidase in vitro and in leaves. Zitschrift fur Naturforschung C-A Journal of Biosciences 55, 361–372. open url image1

Scholander PF, Hammel HT, Bradstreet ED, Hemingsen EA (1965) Sap pressure in vascular plants. Science 148, 339–346. open url image1

Shi WM, Muratomoto Y, Ueda A, Takabet T (2001) Cloning of peroxisomal ascorbate preoxidase gene from barley. Horticultural Science 120, 1050–1056. open url image1

Starck Z, Wazynska Z, Kucewicz D (1993) Comparative effects of heat stress on photosynthesis and chloroplast ultrastructure in tomato plants with source–sink modulated by growth regulators. Physiologia Plantarum 15, 125–133. open url image1

Stefanov D, Yordanov I, Tsonev T (1996) Effect of thermal stress combined with different irradiance on some photosynthetic characteristics of barley (Hordeum vulgare L.) plants. Photosynthetica 32, 171–180. open url image1

Storozhenko S, De Pauw P, Van Montagu M, Inzé D, Kushnir S (1998) The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiology 118, 1005–1014.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. The Plant Cell 11, 1195–1206.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wardlaw IF, Wrigley CW (1994) Heat tolerance in temperature cereals: an overview. Australian Journal of Plant Physiology 21, 695–703. open url image1