SALICYLIC ACID INDUCES PHYSIOLOGICAL AND BIOCHEMICAL CHANGES IN PEONY UNDER WATERLOGGING STRESS

Xiangtao Zhu; Haojie Shi; Xueqin Li; Songheng Jin

doi:10.24326/asphc.2020.1.4

Vol. 19 No. 1 (2020)

Articles

SALICYLIC ACID INDUCES PHYSIOLOGICAL AND BIOCHEMICAL CHANGES IN PEONY UNDER WATERLOGGING STRESS

Xiangtao Zhu⁺⁻
Haojie Shi⁺⁻
Xueqin Li⁺⁻
Songheng Jin⁺⁻

PDF

DOI: https://doi.org/10.24326/asphc.2020.1.4
Submitted: February 5, 2020
Published: 2020-02-21

Abstract

In this study, the effects of salicylic acid to antioxidative activity and photosynthetic characteristics in waterlogging stress of two peony cultivars (‘Fengdanbai’ and ‘Mingxing’) were investigated. 4-year-old peony grown in different levels of waterlogging stress and then different concentration prepared SA (0.0, 0.1, 0.5 and 1.0 mmol L^–1) sprayed on fresh leaves of peony. The antioxidative enzymes activities include superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT), chlorophyll content, relative conductivity and MDA content were measured in leaves about different waterlogging treatment, the photosynthetic characteristics were also measured using photosynthetic measurement system. The results showed that waterlogging stress decreased the chlorophyll content in all peony cultivars leaves, but with SA treatment can inhibit the decrease of chlorophyll content. Relative conductivity increased as the extension of waterlogging time in two cultivars. SA treatment could effectively inhibit the increase of relative conductivity, and 0.5 mmol L^–1 of SA was the most suitable concentration. SOD, POD, CAT activity increased first and then decreased in different waterlogging condition, SA significantly increased the activity of various enzymes. MDA content was increase as the expansion of waterlogging time in two cultivars. SA inhibits the increase of MDA content. Of all concentration of SA, 0.5 mmol L^–1 was the best concentration to inhibit the waterlogging stress. For the photosynthetic characteristics, the net assimilation rate (Pn), stomatal conductance (Gs), transpiration rate (Tr) and intercellular CO₂ (Ci) were decreased under different waterlogging condition. SA treatment can increase Pn, Gs, Tr and Ci of peony.

References

Aeby, H. (1984). Catalase in vitro. Methods Enzymol., 105, 121–126.
Arnon, D.I. (1949). Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol., 124, 1–15.
Asghari, M., Aghdam, M.S. (2010). Impact of salicylic acid on postharvest physiology of horticultural crops. Trend Food Sci. Technol., 21, 502–509.
Beruto, M., Lanteri, L., Portogallo, C. (2004). Micropropagation of tree peony (Paeonia suffruticosa). Plant Cell, Tissue Organ Cult., 79, 249–255.
Colmer, T., Voesenek, L. (2009). Flooding tolerance, suites of plant traits in variable environments. Funct. Plant Biol., 36, 665–681.
Fayez, K.A., Bazaids, A. (2014). Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. J. Saudi Soc. Agric. Sci., 13(1), 45–55．
Han, X.Y., Wang, L.S., Liu, Z.A., Jan, D.R., Shu, Q.Y. (2008). Characterization of sequence-related amplified polymorphism markers analysis of tree peony bud sports. Scientia Horticulturae, 115, 261–267.
Hayat, S., Ahmad, A., Alyemeni, M.N. (2013). Salicylic Acid. Springer, Netherlands.
Irfan, M., Hayat, S., Hayat, Q., Afroz, S., Ahmad, A. (2010). Physiological and biochemical changes in plants under waterlogging. Protoplasma, 241, 3–17.
Jamali, B., Eshghi, S., Tafazoli, E. (2011). Vegetative and reproductive growth of strawberry plants cv. ‘Pajaro’ affected by salicylic acid and nickel. J. Agric. Sci. Technol., 13, 895–904.
Janda, K., Hideg, E., Szalai, G., Kovács, L., Janda, T. (2012). Salicylic acid may indirectly influence the photosynthetic electron transport. J. Plant Physiol., 169, 971–978.
Jayakannan, M., Bose, J., Babourina, O., Rengel, Z., Shabala, S. (2013). Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. J. Exp. Bot., 64(8), 2255–2268.
Kamal, A.H.M., Komatsu, S. (2016). Proteins involved in biophoton emission and flooding-stress responses in soy-bean under light and dark conditions. Mol. Biol. Rep., 43(2), 73–89.
Knorzer, O., Lederer, B., Durner, J., Boger, P. (1999). Antioxidative defense activation insoybean cells. Physiol. Plant, 107, 294–302.
Li, J.J, He, L.X. (2003). Jiangnan Peony History, Species Composition and Flower Selection in Line with Local Conditions. China Flowers Hortic., 12, 9–10.
Li, S.S., Chen, L.G., Xu, Y.J., Wang, L.J., Wang, L.S. (2012). Identification of floral fragrances in tree peony cultivars by gas chromatography–mass spectrometry. Sci. Hortic., 142, 158–165.
Li, T., Hu, Y., Du, X., Tang, H., Shen, C., Wu, J. (2014). Salicylic acid alleviates the adverse effects of salt stress in, Torreya grandis, cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. Plos One, 9(10), 109492.
Li, X., Li, N., Yang, J., Ye, F., Chen, F., Chen, F. (2011). Morphological and photosynthetic responses of riparian plant Distylium chinense seedlings to simulated Autumn and Winter flooding in Three Gorges Reservoir Region of the Yangtze River, China. Acta Ecol. Sin., 31(1), 31–39.
Limami, A.M., Diab, H., Lothier, J. (2014). Nitrogen metabolism in plants under low oxygen stress. Planta, 239, 531–541.
Mehran, S., Ahmad, N., Seyed, A.S., Tayeb, S., Shahram, L. (2013). Effect of salicylic acid on wheat yield and its components under drought stress. Adv. Environ. Biol., 7(4), 629–635.
Mirdehghan, S.H., Rahemi, M., Martínez-Romero, D., Guillén, F., Valverde, J.M., Zapata, P.J., Serrano, M., Valero, D. (2007). Reduction of pomegranate chilling injury during storage after heat treatment, role of polyamines. Postharvest Biol. Technol., 44, 19–25.
Mishra, S.K., Patro, L., Mohapatra, P.K., Biswal, B. (2008). Response of senescing rice leaves to flooding stress. Photosynthetica, 46(2), 315–317.
Movaghatian, A., Khorsandi, F. (2014). Salicylic acid effects on germination of mungbean (Vigna radiata L.) under salinity stress. Adv. Environ. Biol., 8(10), 566–570.
Mutlu, S., Atici, Ö. (2013). Alleviation of high salt toxicity-induced oxidative damage by salicylic acid pretreatment in two wheat cultivars. Toxicol. Ind. Health, 29(1), 89.
Nakai, A., Kisanuki, H. (2007a). Effect of evaluation above the waterline on the growth of current-year Salix gracilistyla seedlings on agravel bar. J. For. Res., 89, 1–6. [in Japanese with English abstract]
Pandey, A., Singh, S.K., Nathawat, M. (2010). Waterlogging and flood hazards vulnerability and risk assessment in Indo-Gangetic Plain. Nat. Hazards, 55, 273–289.
Pandey, P., Srivastava, R.K., Dubey, R.S. (2013). Salicylic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense. Ecotoxicology, 22(4), 656.
Picerno, P., Mencherini, T., Sansone, F., Del Gaudio, P., Granata, I., Porta, A., Aquino, R.P. (2011). Screening of a polar extract of Paeonia rockii, composition and antioxidant and antifungal activities. J. Ethnopharmacol., 138(3), 705–712.
Rood, S.B., Nielsen, J.L., Shenton, L., Gill, K.M., Letts, M.G. (2010). Effects of flooding on leaf development, transpiration, and photosynthesis in narrowleaf cottonwood, a willow-like poplar. Photosynth. Res., 104(1), 31–9.
Sairam, R.K., Kumutha, D., Ezhimathi, K., Deshmukh, P.S., Srivastava, G.C. (2008). Physiology and biochemistry of waterlogging tolerance in plants. Biol. Plant., 52(3), 401–412.
Sayyari, M., Ghanbari, F. (2013). Effect of acetyl salicylic acid on quality and chilling resistance of sweet pepper (Capsicum annuum L.) at different storage temperatures. Acta Hortic., 1012(1012), 559–568.
Shen, C.H., Hu, Y.Y., Du, X.H., Li, T.T., Tang, H., Wu, J.S. (2014). Salicylic acid induces physiological and biochemical changes in Torreya grandis cv. Merrillii seedlings under drought stress. Trees, 28(4), 961–970.
Shi, Q.H., Bao, Z.Y., Zhu, Z.J., Ying, Q.S., Qian, Q.Q. (2008). Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativus L. Plant Growth Regul., 48, 127–135.
Srivastava, S., Dubey, R.S. (2011). Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul., 64, 1–16.
Sun, J., You, X.R., Li, L., Peng, H.X., Su, W.Q., Li, C.B., He, Q.G., Liao, F. (2011). Effects of a phospholipase D inhibitor on postharvest enzymatic browning and oxidative stress of litchi fruit. Postharvest Biol. Technol., 62, 288–294.
Tang, Y., Sun, X., Wen, T., Liu, M., Yang, M., Chen, X. (2016). Implications of terminal oxidase function in regulation of salicylic acid on soybean seedling photosynthetic performance under water stress. Plant Physiol. Biochem., 112, 19.
Tasgin, E., Atici, O., Nalbantoglu, B. Popova, L.P. (2006). Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry, 67, 710–715.
Tuo, X.Q., Li, S., Wu, Q.S., Zou, Y.N. (2015). Alleviation of waterlogged stress in peach seedlings inoculated with Funneliformis mosseae, changes in chlorophyll and proline metabolism. Sci. Hortic., 197, 130–134.
Vasantha, S., Gururaja, R.P.S., Venkataramana, S., Gomathi, R. (2008). Salinity-induced changes in the antioxidant response of sugarcane genotypes. J. Plant Biol., 35(2), 115–119.
Wang, J. (2009). Genetic Diversity of Paeonia ostii and Germplasm Resources of Tree Peony Cultivars from Chinese Jiangnan Area. Doctoral dissertation of Beijing Forestry University.
Wang, L.J., Fan, L., Loescher, W., Duan, W., Liu, G.J., Cheng, J.S., Li, S.H. (2010). Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biol., 10, 34.
Yin, D.M., Chen, S.M., Chen, F.D., Guan, Z.Y., Fang, W.M. (2009). Morphological and physiological responses of two chrysanthemum cultivars differing in their tolerance to waterlogging. Environ. Exp. Bot., 67, 87–93.
Yusuf, M., Hasan, S.A., Ali, B., Hayat, S., Fariduddin, Q. Ahmad, A. (2008). Effect of salicylic acid on salinity induced changes in Brassica juncea. J. Integr. Plant Biol., 50(9), 1096–1102.
Zhang, J.J., Wang, L.S., Shu, Q.Y., Liu, Z.A., Li, C.H., Zhang, J., Wei, X.L., Tian, D.K. (2007). Comparison of anthocyanins in non-blotches and blotches of the petals of Xibei tree peony. Sci. Hortic., 114, 104–111.
Zhang, X.Z. (1992), The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. In: Research Methodology of Crop Physiology, Zhang, X.Z. (ed.). Agriculture Press, Beijing, 208–211.
Zhu, X.T., Jin, S.H., Ai, J.G., Jiang, H.L., Wang, X. (2017). Evaluation of waterlogging tolerance of peony variety. J. Nucl. Agric. Sci., 31(3), 607–613.

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Keywords

peony
salicylic acid
antioxidant enzymes
photosynthetic physiology

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[1] Aeby, H. (1984). Catalase in vitro. Methods Enzymol., 105, 121–126.

[2] Arnon, D.I. (1949). Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol., 124, 1–15.

[3] Asghari, M., Aghdam, M.S. (2010). Impact of salicylic acid on postharvest physiology of horticultural crops. Trend Food Sci. Technol., 21, 502–509.

[4] Beruto, M., Lanteri, L., Portogallo, C. (2004). Micropropagation of tree peony (Paeonia suffruticosa). Plant Cell, Tissue Organ Cult., 79, 249–255.

[5] Colmer, T., Voesenek, L. (2009). Flooding tolerance, suites of plant traits in variable environments. Funct. Plant Biol., 36, 665–681.

[6] Fayez, K.A., Bazaids, A. (2014). Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. J. Saudi Soc. Agric. Sci., 13(1), 45–55．

[7] Han, X.Y., Wang, L.S., Liu, Z.A., Jan, D.R., Shu, Q.Y. (2008). Characterization of sequence-related amplified polymorphism markers analysis of tree peony bud sports. Scientia Horticulturae, 115, 261–267.

[8] Hayat, S., Ahmad, A., Alyemeni, M.N. (2013). Salicylic Acid. Springer, Netherlands.

[9] Irfan, M., Hayat, S., Hayat, Q., Afroz, S., Ahmad, A. (2010). Physiological and biochemical changes in plants under waterlogging. Protoplasma, 241, 3–17.

[10] Jamali, B., Eshghi, S., Tafazoli, E. (2011). Vegetative and reproductive growth of strawberry plants cv. ‘Pajaro’ affected by salicylic acid and nickel. J. Agric. Sci. Technol., 13, 895–904.

[11] Janda, K., Hideg, E., Szalai, G., Kovács, L., Janda, T. (2012). Salicylic acid may indirectly influence the photosynthetic electron transport. J. Plant Physiol., 169, 971–978.

[12] Jayakannan, M., Bose, J., Babourina, O., Rengel, Z., Shabala, S. (2013). Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. J. Exp. Bot., 64(8), 2255–2268.

[13] Kamal, A.H.M., Komatsu, S. (2016). Proteins involved in biophoton emission and flooding-stress responses in soy-bean under light and dark conditions. Mol. Biol. Rep., 43(2), 73–89.

[14] Knorzer, O., Lederer, B., Durner, J., Boger, P. (1999). Antioxidative defense activation insoybean cells. Physiol. Plant, 107, 294–302.

[15] Li, J.J, He, L.X. (2003). Jiangnan Peony History, Species Composition and Flower Selection in Line with Local Conditions. China Flowers Hortic., 12, 9–10.

[16] Li, S.S., Chen, L.G., Xu, Y.J., Wang, L.J., Wang, L.S. (2012). Identification of floral fragrances in tree peony cultivars by gas chromatography–mass spectrometry. Sci. Hortic., 142, 158–165.

[17] Li, T., Hu, Y., Du, X., Tang, H., Shen, C., Wu, J. (2014). Salicylic acid alleviates the adverse effects of salt stress in, Torreya grandis, cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. Plos One, 9(10), 109492.

[18] Li, X., Li, N., Yang, J., Ye, F., Chen, F., Chen, F. (2011). Morphological and photosynthetic responses of riparian plant Distylium chinense seedlings to simulated Autumn and Winter flooding in Three Gorges Reservoir Region of the Yangtze River, China. Acta Ecol. Sin., 31(1), 31–39.

[19] Limami, A.M., Diab, H., Lothier, J. (2014). Nitrogen metabolism in plants under low oxygen stress. Planta, 239, 531–541.

[20] Mehran, S., Ahmad, N., Seyed, A.S., Tayeb, S., Shahram, L. (2013). Effect of salicylic acid on wheat yield and its components under drought stress. Adv. Environ. Biol., 7(4), 629–635.

[21] Mirdehghan, S.H., Rahemi, M., Martínez-Romero, D., Guillén, F., Valverde, J.M., Zapata, P.J., Serrano, M., Valero, D. (2007). Reduction of pomegranate chilling injury during storage after heat treatment, role of polyamines. Postharvest Biol. Technol., 44, 19–25.

[22] Mishra, S.K., Patro, L., Mohapatra, P.K., Biswal, B. (2008). Response of senescing rice leaves to flooding stress. Photosynthetica, 46(2), 315–317.

[23] Movaghatian, A., Khorsandi, F. (2014). Salicylic acid effects on germination of mungbean (Vigna radiata L.) under salinity stress. Adv. Environ. Biol., 8(10), 566–570.

[24] Mutlu, S., Atici, Ö. (2013). Alleviation of high salt toxicity-induced oxidative damage by salicylic acid pretreatment in two wheat cultivars. Toxicol. Ind. Health, 29(1), 89.

[25] Nakai, A., Kisanuki, H. (2007a). Effect of evaluation above the waterline on the growth of current-year Salix gracilistyla seedlings on agravel bar. J. For. Res., 89, 1–6. [in Japanese with English abstract]

[26] Pandey, A., Singh, S.K., Nathawat, M. (2010). Waterlogging and flood hazards vulnerability and risk assessment in Indo-Gangetic Plain. Nat. Hazards, 55, 273–289.

[27] Pandey, P., Srivastava, R.K., Dubey, R.S. (2013). Salicylic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense. Ecotoxicology, 22(4), 656.

[28] Picerno, P., Mencherini, T., Sansone, F., Del Gaudio, P., Granata, I., Porta, A., Aquino, R.P. (2011). Screening of a polar extract of Paeonia rockii, composition and antioxidant and antifungal activities. J. Ethnopharmacol., 138(3), 705–712.

[29] Rood, S.B., Nielsen, J.L., Shenton, L., Gill, K.M., Letts, M.G. (2010). Effects of flooding on leaf development, transpiration, and photosynthesis in narrowleaf cottonwood, a willow-like poplar. Photosynth. Res., 104(1), 31–9.

[30] Sairam, R.K., Kumutha, D., Ezhimathi, K., Deshmukh, P.S., Srivastava, G.C. (2008). Physiology and biochemistry of waterlogging tolerance in plants. Biol. Plant., 52(3), 401–412.

[31] Sayyari, M., Ghanbari, F. (2013). Effect of acetyl salicylic acid on quality and chilling resistance of sweet pepper (Capsicum annuum L.) at different storage temperatures. Acta Hortic., 1012(1012), 559–568.

[32] Shen, C.H., Hu, Y.Y., Du, X.H., Li, T.T., Tang, H., Wu, J.S. (2014). Salicylic acid induces physiological and biochemical changes in Torreya grandis cv. Merrillii seedlings under drought stress. Trees, 28(4), 961–970.

[33] Shi, Q.H., Bao, Z.Y., Zhu, Z.J., Ying, Q.S., Qian, Q.Q. (2008). Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativus L. Plant Growth Regul., 48, 127–135.

[34] Srivastava, S., Dubey, R.S. (2011). Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul., 64, 1–16.

[35] Sun, J., You, X.R., Li, L., Peng, H.X., Su, W.Q., Li, C.B., He, Q.G., Liao, F. (2011). Effects of a phospholipase D inhibitor on postharvest enzymatic browning and oxidative stress of litchi fruit. Postharvest Biol. Technol., 62, 288–294.

[36] Tang, Y., Sun, X., Wen, T., Liu, M., Yang, M., Chen, X. (2016). Implications of terminal oxidase function in regulation of salicylic acid on soybean seedling photosynthetic performance under water stress. Plant Physiol. Biochem., 112, 19.

[37] Tasgin, E., Atici, O., Nalbantoglu, B. Popova, L.P. (2006). Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry, 67, 710–715.

[38] Tuo, X.Q., Li, S., Wu, Q.S., Zou, Y.N. (2015). Alleviation of waterlogged stress in peach seedlings inoculated with Funneliformis mosseae, changes in chlorophyll and proline metabolism. Sci. Hortic., 197, 130–134.

[39] Vasantha, S., Gururaja, R.P.S., Venkataramana, S., Gomathi, R. (2008). Salinity-induced changes in the antioxidant response of sugarcane genotypes. J. Plant Biol., 35(2), 115–119.

[40] Wang, J. (2009). Genetic Diversity of Paeonia ostii and Germplasm Resources of Tree Peony Cultivars from Chinese Jiangnan Area. Doctoral dissertation of Beijing Forestry University.

[41] Wang, L.J., Fan, L., Loescher, W., Duan, W., Liu, G.J., Cheng, J.S., Li, S.H. (2010). Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biol., 10, 34.

[42] Yin, D.M., Chen, S.M., Chen, F.D., Guan, Z.Y., Fang, W.M. (2009). Morphological and physiological responses of two chrysanthemum cultivars differing in their tolerance to waterlogging. Environ. Exp. Bot., 67, 87–93.

[43] Yusuf, M., Hasan, S.A., Ali, B., Hayat, S., Fariduddin, Q. Ahmad, A. (2008). Effect of salicylic acid on salinity induced changes in Brassica juncea. J. Integr. Plant Biol., 50(9), 1096–1102.

[44] Zhang, J.J., Wang, L.S., Shu, Q.Y., Liu, Z.A., Li, C.H., Zhang, J., Wei, X.L., Tian, D.K. (2007). Comparison of anthocyanins in non-blotches and blotches of the petals of Xibei tree peony. Sci. Hortic., 114, 104–111.

[45] Zhang, X.Z. (1992), The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. In: Research Methodology of Crop Physiology, Zhang, X.Z. (ed.). Agriculture Press, Beijing, 208–211.

[46] Zhu, X.T., Jin, S.H., Ai, J.G., Jiang, H.L., Wang, X. (2017). Evaluation of waterlogging tolerance of peony variety. J. Nucl. Agric. Sci., 31(3), 607–613.