Enhanced salt tolerance in maize plants induced by H2O2 leaf spraying is associated with improved gas exchange rather than with non-enzymatic antioxidant system

Gondim, Franklin Aragão; Miranda, Rafael de Souza; Gomes-Filho, Enéas; Prisco, José Tarquinio

Abstract

Hydrogen peroxide (H2O2) is an essential signaling molecule that mediates plant responses against several biotic and abiotic stresses. H2O2 pretreatment has emerged as a signaling way, inducing salt stress acclimation in plants. Here, we analyzed the effects of H2O2 leaf pretreatment on the non-enzymatic defense system (ascorbate and glutathione), plant growth, relative water content (RWC), relative chlorophyll content, H2O2 content, and gas exchange in maize plants under NaCl stress. The results showed that salinity reduced the leaf area and shoot and root dry mass as compared to control, and the leaf spraying with H2O2 significantly improved the growth of salt stressed plants. Photosynthesis and transpiration, stomatal conductance and intercellular CO2 concentration were strongly decreased by salinity after 7 and 14 days of salt exposure; however, the decrease was lower in plants sprayed with H2O2. The improved gas exchange in H2O2-sprayed stressed plants correlated positively with higher RWC and relative chlorophyll content and lower leaf H2O2 accumulation under NaCl stress conditions. Ascorbate and glutathione did not play any obvious effects as non-enzymatic antioxidants in the ROS scavenging. In conclusion, the salt tolerance induced by H2O2 leaf pretreatment is attributed to a reduction in the H2O2 content and maintenance of RWC and chlorophyll in maize leaves. These characteristics allow maize plants to maintain high rates of photosynthesis under salt stress and improve the growth.

ascorbate; glutathione; hydrogen peroxide; salinity; Zea mays

Asada K (1994) Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. In: Baker NR, Bower JR (eds.) Photoinhibition of photosynthesis, pp. 131-145. Bios Scientific Publishers, Oxford.
Azevedo Neto AD, Gomes Filho E, Prisco JT (2008) Salinity and oxidative Stress. In: Khan NA, Singh S (eds.) Abiotic stress and plant responses, pp. 58-82.. IK International, New Delhi.
Azevedo Neto AD, Prisco JT, Enéas-Filho J, Medeiros JR, Gomes Filho E (2005) Hydrogen peroxide pre-treatment induces salt-stress acclimation in maize plants. Journal of Plant Physiology 162:1114-1122.
Chakraborty K, Sairam RK, Bhattacharya RC (2012) Differential expression of salt overly sensitive pathway genes determines salinity stress tolerance in Brassica genotypes. Plant Physiology and Biochemistry 51:90-101.
Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. Journal of Experimental Botany 55:2365-2384.
Costa PHA, Silva JF, Bezerra MA, Enéas Filho J, Prisco JT, Gome-Filho E (2003) Crescimento e níveis de solutos orgânicos e inorgânicos de Vigna unguiculata submetidos à salinidade. Revista Brasileira de Botânica 26:289-297.
Flexas J, Diaz-espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO₂ concentration around leaves. Plant, Cell and Environment 30:1284-1298.
Foyer CH (1993) Ascorbic acid. In: Alscher RG, Hess JL (eds.) Antioxidants in higher plants, pp. 31-58. Boca Raton: CRC Press.
Freitas VS, Alencar NLM, Lacerda CF, Prisco JT, Gomes-Filho E (2011) Changes in physiological and biochemical indicators associated with salt tolerance in cotton, sorghum and cowpea. African Journal of Biochemistry Research 5:264-271.
Gao Y, Guo YK, Lin SH, Fang YY, Bai JG (2010) Hydrogen peroxide pretreatment alters the activity of antioxidant enzymes and protects chloroplast ultrastructure in heat-stressed cucumber leaves. Scientia Horticulturae 126:20-26.
Gechev T, Gadjev I, Van Breusegem F, Inzé D, Dukiandjiev S, Toneva V, Minkov I (2002) Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cellular and Molecular Life Sciences 59:708-714.
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48:909-930.
Gomes-Filho E, Lima CRFM, Costa JH, Silva ACM, Lima MGS, Lacerda CF, Prisco JT (2008) Cowpea ribonuclease: properties and effect of NaCl-salinity on its activation during seed germination and seedling establishment. Plant Cell Reports 27:147-157.
Gondim FA, Gomes-Filho E, Costa JH, Alencar NLM, Prisco JT (2012) Catalase plays a key role in salt stress acclimation induced by hydrogen peroxide pretreatment in maize. Plant Physiology and Biochemistry 56:62-71.
Gondim FA, Gomes-Filho E, Lacerda CF, Prisco JT, Azevedo Neto AD, Marques EC (2010) Pretreatment with H₂O₂ in maize seeds: effects on germination and seedling acclimation to salt stress. Brazilian Journal of Plant Physiology 22:103-112.
Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochemistry 106:207-211.
Hasegawa PM (2013) Sodium (Na⁺) homeostasis and salt tolerance of plants. Environmental and Experimental Botany 92:19-31.
Hoagland DR, Arnon DI (1950) The water-cultured method for growing plants without soil. California Agricultural Experiment Station, California.
Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. Journal of Experimental Botany 5:3041-3049.
Jain M, Choudhary D, Kale RK, Bhalla-Sarin N (2002) Salt and glyphosate-induced increase in glyoxalase I activity in cell lines of groundnut (Arachis hypogaea). Physiologia Plantarum 114:499-505.
James RA, Munns R, Von Caemmerer S, Trejo C, Miller C, Condon TAG (2006) Photosynthetic capacity is related to the cellular and subcellular partitioning of Na⁺, K⁺ and Cl^- in salt-affected barley and durum wheat. Plant, Cell and Environment 29:2185-2197.
Kampfenkel K, Van Montagu M, Inzé D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Analytical Biochemistry 225:165-167.
Lacerda CF, Oliveira HPM, Oliveira TS, Gomes-Filho E (2003) Crescimento e acúmulo de íons em folhas de sorgo forrageiro submetido a soluções iso-osmóticas de sais (NaCl + KCl). Revista Ciência Agronômica 34:1-6.
Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell and Environment 25:275-94.
Mckersie BD, Leshem YY (1994) Stress and stress coping and cultivated plants, pp. 15-49. Kluwer Academic Publishes, Dordrecht.
Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environmental and Experimental Botany 49:69-76.
Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annual Review of Plant Biology 58:459-481.
Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57:1025-1043.
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59:651-681.
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinash chloroplasts. Plant & Cell Physiology 22:867-880.
Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Current Opinion in Plant Biology 5:388-395.
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology 49:249-279.
Noreen Z, Ashraf M (2009) Assessment of variation in antioxidative defense system in salt treated pea (Pisum sativum L.) cultivars and its putative use as salinity tolerance markers. Journal of Plant Physiology 166:1764-1774.
Ort DR (2001) When there is too much light. Plant Physiology 125:29-32.
Quan L, Zhang B, Shi W, Li H (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. Journal of Integrate Plant Biology 50:2-18.
Renneberg H (1982) Glutathione metabolism and possible biological roles in higher plants. Phytochemistry 21:2771-2781.
Rizhsky L, Liang H, Mittler R (2003) The water-water cycle is essential for chloroplast protection in the absence of stress. The Journal of Biological Chemistry 278:38921-38925.
Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Current Science 86:407-421.
Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comptes Rendus de l'Academie Bulgare des Sciences 51:121-124.
Sgherri C, Navari-Izzo F (1995) Sunflower seedlings subjected to increasing water deficit stress: oxidative stress and defense mechanisms. Physiologia Plantarum 93:25-30.
Shahbaz M, Ashraf M, Akram NA, Hanif A, Hameed S, Joham S, Rehman R (2010) Salt-induced modulation in growth, photosynthetic capacity, proline content and ion accumulation in sunflower (Helianthus annuus L.). Acta Physiologiae Plantarum 33:1113-1122.
Silva EN, Ribeiro RV, Ferreira-Silva SL, Viégas RA, Silveira JAG (2011) Salt stress induced damages on the photosynthesis of physic nut young plants. Scientia Agricola 68:62-68.
Singh AK, Dubey RS (1995) Changes in chlorophyll a and b contents and activities of photosystems I and II in rice seedlings induced by NaCl. Photosynthetica 31:489-499.
Steduto P, Albrizio R, Giorio P, Sorrentino G (2000) Gas-exchange response and stomatal and non-stomatal limitations to carbon assimilation of sunflower under salinity. Environmental and Experimental Botany 44:243-255.
Szechyńska-Hebda M, Skrzypek E, Dąbrowska G, Wędzony M, van Lammeren A (2012) The effect of endogenous hydrogen peroxide induced by cold treatment in the improvement of tissue regeneration efficiency. Acta Physiologiae Plantarum 34:547-560.
Uchida A, Jagendorf AT, Hibino T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science 163:515-523.
Wahid A, Perveen M, Gelani S, Basra SMA (2007) Pretreatment of seed with H₂O₂ improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. Journal of Plant Physiology 164:283-294.
Wang X, Hou C, Liu J, He W, Nan W, Gong H, Bi Y (2013) Hydrogen peroxide is involved in the regulation of rice (Oryza sativa L.) tolerance to salt stress. Acta Physiologiae Plantarum 35:891-900.
Wang Y, Li JL, Wang JZ, Li ZK (2010) Exogenous H₂O₂ improves the chilling tolerance of manila grass and mascarene grass by activating the antioxidative system. Plant Growth Regulation 61:195-204.
Xu FJ, Jin CH, Liu WJ, Zhang YS, Lin XY (2011) Pretreatment with H₂O₂ alleviates aluminum-induced oxidative stress in wheat seedlings. Journal of Integrate Plant Biology 53:44-53.

Publication Dates

Publication in this collection
10 Feb 2014
Date of issue
Dec 2013

History

Received
30 Oct 2013
Accepted
04 Dec 2013

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] Asada K (1994) Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. In: Baker NR, Bower JR (eds.) Photoinhibition of photosynthesis, pp. 131-145. Bios Scientific Publishers, Oxford.

[2] Azevedo Neto AD, Gomes Filho E, Prisco JT (2008) Salinity and oxidative Stress. In: Khan NA, Singh S (eds.) Abiotic stress and plant responses, pp. 58-82.. IK International, New Delhi.

[3] Azevedo Neto AD, Prisco JT, Enéas-Filho J, Medeiros JR, Gomes Filho E (2005) Hydrogen peroxide pre-treatment induces salt-stress acclimation in maize plants. Journal of Plant Physiology 162:1114-1122.

[4] Chakraborty K, Sairam RK, Bhattacharya RC (2012) Differential expression of salt overly sensitive pathway genes determines salinity stress tolerance in Brassica genotypes. Plant Physiology and Biochemistry 51:90-101.

[5] Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. Journal of Experimental Botany 55:2365-2384.

[6] Costa PHA, Silva JF, Bezerra MA, Enéas Filho J, Prisco JT, Gome-Filho E (2003) Crescimento e níveis de solutos orgânicos e inorgânicos de Vigna unguiculata submetidos à salinidade. Revista Brasileira de Botânica 26:289-297.

[7] Flexas J, Diaz-espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO₂ concentration around leaves. Plant, Cell and Environment 30:1284-1298.

[8] Foyer CH (1993) Ascorbic acid. In: Alscher RG, Hess JL (eds.) Antioxidants in higher plants, pp. 31-58. Boca Raton: CRC Press.

[9] Freitas VS, Alencar NLM, Lacerda CF, Prisco JT, Gomes-Filho E (2011) Changes in physiological and biochemical indicators associated with salt tolerance in cotton, sorghum and cowpea. African Journal of Biochemistry Research 5:264-271.

[10] Gao Y, Guo YK, Lin SH, Fang YY, Bai JG (2010) Hydrogen peroxide pretreatment alters the activity of antioxidant enzymes and protects chloroplast ultrastructure in heat-stressed cucumber leaves. Scientia Horticulturae 126:20-26.

[11] Gechev T, Gadjev I, Van Breusegem F, Inzé D, Dukiandjiev S, Toneva V, Minkov I (2002) Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cellular and Molecular Life Sciences 59:708-714.

[12] Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48:909-930.

[13] Gomes-Filho E, Lima CRFM, Costa JH, Silva ACM, Lima MGS, Lacerda CF, Prisco JT (2008) Cowpea ribonuclease: properties and effect of NaCl-salinity on its activation during seed germination and seedling establishment. Plant Cell Reports 27:147-157.

[14] Gondim FA, Gomes-Filho E, Costa JH, Alencar NLM, Prisco JT (2012) Catalase plays a key role in salt stress acclimation induced by hydrogen peroxide pretreatment in maize. Plant Physiology and Biochemistry 56:62-71.

[15] Gondim FA, Gomes-Filho E, Lacerda CF, Prisco JT, Azevedo Neto AD, Marques EC (2010) Pretreatment with H₂O₂ in maize seeds: effects on germination and seedling acclimation to salt stress. Brazilian Journal of Plant Physiology 22:103-112.

[16] Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochemistry 106:207-211.

[17] Hasegawa PM (2013) Sodium (Na⁺) homeostasis and salt tolerance of plants. Environmental and Experimental Botany 92:19-31.

[18] Hoagland DR, Arnon DI (1950) The water-cultured method for growing plants without soil. California Agricultural Experiment Station, California.

[19] Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. Journal of Experimental Botany 5:3041-3049.

[20] Jain M, Choudhary D, Kale RK, Bhalla-Sarin N (2002) Salt and glyphosate-induced increase in glyoxalase I activity in cell lines of groundnut (Arachis hypogaea). Physiologia Plantarum 114:499-505.

[21] James RA, Munns R, Von Caemmerer S, Trejo C, Miller C, Condon TAG (2006) Photosynthetic capacity is related to the cellular and subcellular partitioning of Na⁺, K⁺ and Cl^- in salt-affected barley and durum wheat. Plant, Cell and Environment 29:2185-2197.

[22] Kampfenkel K, Van Montagu M, Inzé D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Analytical Biochemistry 225:165-167.

[23] Lacerda CF, Oliveira HPM, Oliveira TS, Gomes-Filho E (2003) Crescimento e acúmulo de íons em folhas de sorgo forrageiro submetido a soluções iso-osmóticas de sais (NaCl + KCl). Revista Ciência Agronômica 34:1-6.

[24] Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell and Environment 25:275-94.

[25] Mckersie BD, Leshem YY (1994) Stress and stress coping and cultivated plants, pp. 15-49. Kluwer Academic Publishes, Dordrecht.

[26] Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environmental and Experimental Botany 49:69-76.

[27] Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annual Review of Plant Biology 58:459-481.

[28] Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57:1025-1043.

[29] Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59:651-681.

[30] Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinash chloroplasts. Plant & Cell Physiology 22:867-880.

[31] Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Current Opinion in Plant Biology 5:388-395.

[32] Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology 49:249-279.

[33] Noreen Z, Ashraf M (2009) Assessment of variation in antioxidative defense system in salt treated pea (Pisum sativum L.) cultivars and its putative use as salinity tolerance markers. Journal of Plant Physiology 166:1764-1774.

[34] Ort DR (2001) When there is too much light. Plant Physiology 125:29-32.

[35] Quan L, Zhang B, Shi W, Li H (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. Journal of Integrate Plant Biology 50:2-18.

[36] Renneberg H (1982) Glutathione metabolism and possible biological roles in higher plants. Phytochemistry 21:2771-2781.

[37] Rizhsky L, Liang H, Mittler R (2003) The water-water cycle is essential for chloroplast protection in the absence of stress. The Journal of Biological Chemistry 278:38921-38925.

[38] Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Current Science 86:407-421.

[39] Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comptes Rendus de l'Academie Bulgare des Sciences 51:121-124.

[40] Sgherri C, Navari-Izzo F (1995) Sunflower seedlings subjected to increasing water deficit stress: oxidative stress and defense mechanisms. Physiologia Plantarum 93:25-30.

[41] Shahbaz M, Ashraf M, Akram NA, Hanif A, Hameed S, Joham S, Rehman R (2010) Salt-induced modulation in growth, photosynthetic capacity, proline content and ion accumulation in sunflower (Helianthus annuus L.). Acta Physiologiae Plantarum 33:1113-1122.

[42] Silva EN, Ribeiro RV, Ferreira-Silva SL, Viégas RA, Silveira JAG (2011) Salt stress induced damages on the photosynthesis of physic nut young plants. Scientia Agricola 68:62-68.

[43] Singh AK, Dubey RS (1995) Changes in chlorophyll a and b contents and activities of photosystems I and II in rice seedlings induced by NaCl. Photosynthetica 31:489-499.

[44] Steduto P, Albrizio R, Giorio P, Sorrentino G (2000) Gas-exchange response and stomatal and non-stomatal limitations to carbon assimilation of sunflower under salinity. Environmental and Experimental Botany 44:243-255.

[45] Szechyńska-Hebda M, Skrzypek E, Dąbrowska G, Wędzony M, van Lammeren A (2012) The effect of endogenous hydrogen peroxide induced by cold treatment in the improvement of tissue regeneration efficiency. Acta Physiologiae Plantarum 34:547-560.

[46] Uchida A, Jagendorf AT, Hibino T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science 163:515-523.

[47] Wahid A, Perveen M, Gelani S, Basra SMA (2007) Pretreatment of seed with H₂O₂ improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. Journal of Plant Physiology 164:283-294.

[48] Wang X, Hou C, Liu J, He W, Nan W, Gong H, Bi Y (2013) Hydrogen peroxide is involved in the regulation of rice (Oryza sativa L.) tolerance to salt stress. Acta Physiologiae Plantarum 35:891-900.

[49] Wang Y, Li JL, Wang JZ, Li ZK (2010) Exogenous H₂O₂ improves the chilling tolerance of manila grass and mascarene grass by activating the antioxidative system. Plant Growth Regulation 61:195-204.

[50] Xu FJ, Jin CH, Liu WJ, Zhang YS, Lin XY (2011) Pretreatment with H₂O₂ alleviates aluminum-induced oxidative stress in wheat seedlings. Journal of Integrate Plant Biology 53:44-53.

Brasil

Brasil

Enhanced salt tolerance in maize plants induced by H2O2 leaf spraying is associated with improved gas exchange rather than with non-enzymatic antioxidant system

Abstract

Publication Dates

History