Abstract
Foliar applications of osmoprotectants could be a valuable tool to counteract the deleterious effects of salinity and protect plant cells from oxidative damage. Some of the known osmoprotectants used in this field are salicylic acid, proline, and/or glycine betaine but there is no available empirical research exists to figure out which of these chemicals is the most effective in reducing the adverse effects of salt stress. To compare the ameliorating effects of foliar application of these osmoprotectants on growth, some physiological and biochemical parameters, and productivity of cucumber plants under NaCl stress (0, 50, or 100 mM), a factorial experiment was carried out during 2015 and 2016 seasons at the Experimental Farm of Horticulture Department, Faculty of Agriculture, Ain Shams University, Qalubia Governorate, Egypt. Increasing NaCl levels reduced plant growth parameters, leaf relative water content, leaf membrane stability, chlorophyll contents, some macro-nutrients content and yield and the lowest values were recorded with the use of 100 mM of sodium chloride treatment. Foliar application of salicylic acid at 1 mM, proline at 10 mM, or glycine betaine at 10 mM to cucumber plants ameliorated the harmful effects of NaCl stress on the vegetative growth and yield through enhancing both leaf relative water content and leaf membrane stability. In addition, these treatments improved both chlorophyll contents, and nutrient content, altogether resulted in a significant reduction in sodium (Na+) and chloride (Cl−) accumulation toxicity. Moreover, the expression of cucumber peroxidase isozymes was analyzed in cucumber leaves 1, 3 and 7 days after the second application. Native polyacrylamide gel electrophoresis analysis indicated that exogenous applications led to the differential regulation of peroxidase enzyme. In conclusion, salicylic acid was the most effective in attenuating the negative effects of the salt stress and in up-regulating peroxidase enzyme expression followed by proline and by glycine betaine. Peroxidase enzyme appeared to function as one of the main molecular mechanisms underlying the resistance response of cucumber to salinity.
Zusammenfassung
Die Blattanwendung von kompatiblen Soluten (Osmoprotectants) könnte ein wertvolles Hilfsmittel sein, um den Auswirkungen von Salzstress entgegenzuwirken und pflanzliche Zellen vor oxidativen Schäden zu schützen. Einige der bekannten in diesem Bereich verwendeten kompatiblen Soluten sind Salicylsäure, Prolin und/oder Glycin-Betain, es gibt aber keine empirischen Forschungen zu der Frage, welche dieser Chemikalien die Auswirkungen von Salzstress am wirkungsvollsten reduziert. Um die günstigen Auswirkungen von Blattanwendungen dieser kompatiblen Soluten auf das Wachstum, einige physiologische und biochemische Parameter und die Produktivität von Gurkenpflanzen unter NaCl-Stress (0, 50 oder 100 mM) zu vergleichen, wurde während der Anbausaison 2015 und 2016 ein diese Faktoren einbeziehender vollständiger Versuchsplan im Forschungsbetrieb der Gartenbauabteilung der Landwirtschaftsfakultät, Ain-Shams-Universität, Gouvernement Qalubia, Ägypten, durchgeführt. Erhöhte NaCl-Werte reduzierten Pflanzenwachstumsparameter, den relativen Wassergehalt der Blätter, Membranstabilität der Blätter, Chlorophyllgehalt, den Gehalt einiger Makronährstoffe und den Ertrag. Die niedrigsten Werte wurden bei Behandlung mit 100 mM Natriumchlorid verzeichnet. Eine Blattanwendung der Gurkenpflanzen von 1 mM Salicylsäure, 10 mM Prolin oder 10 mM Glycin-Betain verminderte die Auswirkungen des NaCl-Stresses auf das vegetative Wachstum und den Ertrag durch Verbesserung einerseits des Wassergehalts, andererseits der Membranstabilität der Blätter. Zusätzlich verbesserten diese Behandlungen den Gehalt von Chlorophyll und Nährstoffen, was sich insgesamt in einer deutlichen Reduzierung der Toxizität durch die Anreicherung mit Natrium (Na+) und Chlorid (Cl−) auswirkte. Darüber hinaus wurde die Expression von Peroxidase-Isoenzymen in den Blättern der Gurken 1, 3 und 7 Tage nach der zweiten Anwendung analysiert. Die Analyse mittels nativer Polyacrylamid-Gelelektrophorese deutete darauf hin, dass äußerliche Anwendungen die Differenzierung des Peroxidase-Enzyms regulieren. Zusammenfassend lässt sich sagen, dass Salicylsäure am wirksamstem die negativen Auswirkungen von Salzstress abschwächte und zur Upregulation der Expression von Peroxidase-Enzymen führte, gefolgt von Prolin und Glycin-Betain. Das Peroxidase-Enzym zeigte sich als einer der wichtigsten molekularen Mechanismen, die der Abwehrreaktion von Gurken auf Salzstress zugrunde liegen.
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References
Abu-Muriefah SS, Qados AAMS (2015) Effects of genistein on nodulation, nitrogen fixation and physiological characteristics of bean (Phaseolus vulgaris L.) under salt stress conditions. Indian J Sci Res Technol 3(1):51–64
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216. https://doi.org/10.1016/j.envexpbot.2005.12.006
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2):163–190. https://doi.org/10.1007/s11099-013-0021-6
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15(3):413–428. https://doi.org/10.1071/BI9620413
Bayuelo-Jiménez JS, Jasso-Plata N, Ochoa I (2012) Growth and physiological responses of Phaseolus species to salinity stress. Int J Agron. https://doi.org/10.1155/2012/527673
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Bourot S, Sire O, Trautwetter A, Tuoze T, Wu LF, Blanco C, Bernard T (2000) Glycine betaine-assisted protein folding in a lysA mutant of Escherichia coli. J Biol Chem 275:1050–1056. https://doi.org/10.1074/jbc.275.2.1050
Butt M, Ayyub CM, Amjad M, Ahmad R (2016) Proline application enhances growth of chilli by improving physiological and biochemical attributes under salt stress. Pak J Agric Sci 53(1):43–49. https://doi.org/10.21162/PAKJAS/16.4623
Chapman HD, Pratt PF (1961) Methods of analysis for soils, plants and water. Univ. California, Berkeley
Csiszár J, Horváth E, Váry ZS, Gallé Á, Bela K, Brunner S, Tari I (2014) Glutathione transferase supergene family in tomato: salt stress-regulated expression of representative genes from distinct GST classes in plants primed with salicylic acid. Plant Physiol Biochem 78:15–26. https://doi.org/10.1016/j.plaphy.2014.02.010
Dat JF, Lopez-Delago H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357
Deivanai S, Xavier R, Vinod V, Timalata K, Lim OF (2011) Role of exogenous proline in ameliorating salt stress at early stage in two rice cultivars. J Stress Physiol Biochem 7(4):157–174
El-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45(3):215–224. https://doi.org/10.1007/s10725-005-4928-1
Elwan MWM, El-Shatoury RSA (2014) Alleviation of NaCl stress in summer squash ‘eskandrani’ by foliar application of salicylic acid. J Hortic Res 22(2):131–137. https://doi.org/10.2478/johr-2014-0030
FAOSTAT (2014) Food and Agriculture organizations of the United Nations. Statistics Division. http://www.fao.org/faostat/en/#data/QC. Accessed 25 July 2017
Fariduddin O, Varshney P, Yusuf M, Ali A, Ahmad A (2012) Dissecting the role of glycine betaine in plants under abiotic stress. Plant Stress 7(1):8–18
Fielding JL, Hall JL (1978) A biochemical and cytochemical study of peroxidase activity in roots of Pisum sativum. J Exp Bot 29:969–981
Foyer CH, Harbinson J (1994) Oxygen metabolism and the regulation of photosynthetic electron transport. In: Foyer C, Mullineaux P (eds) Causes of photooxidative stresses and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 1–42
Fry SC (1986) Cross-linking of matrix polymers in the growing cells of angiosperms. Annu Rev Plant Physiol 37:165–186. https://doi.org/10.1146/annurev.pp.37.060186.001121
Gadallah MAA (1999) Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 42(2):249–257. https://doi.org/10.1023/A:1002164719609
Gadallah MAA (2000) Effects of indole-3-acetic acid and zinc on the growth, osmotic potential and soluble carbon and nitrogen components of soybean plants growing under water deficit. J Arid Environ 44(4):451–467. https://doi.org/10.1006/jare.1999.0610
Ghorbanli M, Ebrahimzadeh H, Sharifi M (2004) Effects of NaCl and mycorrhizal fungi on antioxidative enzymes in soybean. Biol Plant 48:575–581. https://doi.org/10.1023/B:BIOP.0000047157.49910.69
Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736. https://doi.org/10.1016/j.jplph.2005.12.009
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499. https://doi.org/10.1146/annurev.arplant.51.1.463
Hayat S, Hasan SA, Hayat Q, Irfan M, Ahmad A (2010) Effect of salicylic acid on net photosynthetic rate, chlorophyll fluorescence, and antioxidant enzymes in Vigna radiata plants exposed to temperature and salinity stresses. Plant Stress 4:62–71
He Y, Zhu Z (2008) Exogenous salicylic acid alleviates NaCl toxicity and increases antioxidative enzyme activity in Lycopersicon esculentum. Biol Plant 52:792–795. https://doi.org/10.1007/s10535-008-0155-8
Hoque MA, Okuma E, Banu MN, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline mitigates the detrimental effects of salt stress more than exogenous betaine by increasing antioxidant enzyme activities. J Plant Physiol 164(5):553–561. https://doi.org/10.1016/j.jplph.2006.03.010
Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26(3):290–300. https://doi.org/10.1007/s00344-007-9017-4
Huang Y, Bie Z, Liu Z, Zhen A, Wang W (2009) Protective role of proline against salt stress is partially related to the improvement of water status and peroxidase enzyme activity in cucumber. Soil Sci Plant Nutr 55:698–704. https://doi.org/10.1111/j.1747-0765.2009.00412.x
Huang Y, Bie ZL, Liu ZX, Zhen A, Jiao XR (2011) Improving cucumber photosynthetic capacity under NaCl stress by grafting onto two salt-tolerant pumpkin rootstocks. Biol Plant 55(2):285–290. https://doi.org/10.1007/s10535-011-0040-8
Huh GH, Lee SJ, Bae YS, Liu JR, Kwak SS (1997) Molecular cloning and characterization of cDNAs for anionic and neutral peroxidases from suspension cultured cells of sweet potato and their differential expression in response to stress. Mol Gen Genet 255:382–391
Islam MM, Hoque MA, Okuma E, Banu MN, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166(15):1587–1597. https://doi.org/10.1016/j.jplph.2009.04.002
Janda T, Szalai G, Rios-Gonzalez K, Veisz O, Páldi E (2003) Comparative study of frost tolerance and antioxidant activity in cereals. Plant Sci 164:301–306
Kahlaoui B, Hachicha M, Rejeb S, Rejeb MN, Hanchi B, Misle E (2014) Response of two tomato cultivars to field-applied proline under irrigation with saline water: growth, chlorophyll fluorescence and nutritional aspects. Photosynthetica 52(3):421–429. https://doi.org/10.1007/s11099-014-0053-6
Kere GM, Guo Q, Chen JF (2016) Growth and physiological responses of cucumber (Cucumis sativus L.) to sodium chloride stress under solid hydroponics. J Environ Agric Sci 6:47–57
Khan MIR, Iqbal N, Masood A, Khan NA (2012) Variation in salt tolerance of wheat cultivars: role of glycinebetaine and ethylene. Pedosphere 22(6):746–754. https://doi.org/10.1016/S1002-0160(12)60060-5
Khedr AH, Abbas MA, Wahid AA, Quick WP, Abogadallah GM (2003) Proline induces the expression of salt stress responsive proteins and may improve the adaptation of Pancratium marilimumL. to salt stress. J Exp Bot 54:2553–2562. https://doi.org/10.1093/jxb/erg277
Koller HRC (1972) Leaf area-leaf weight relationships in the soybean canopy. Crop Sci 12(2):180–183. https://doi.org/10.2135/cropsci1972.0011183X001200020007x
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685
Lechno S, Zamski E, Tel-Or E (1997) Salt stress-induced responses in cucumber plants. J Plant Physiol 150:206–211. https://doi.org/10.1016/S0176-1617(97)80204-0
López-Orenes A, Martínez-Moreno JM, Calderón AA, Ferrer MA (2013) Changes in phenolic metabolism in salicylic acid-treated shoots of Cistus heterophyllus. Plant Cell Tissue Organ Cult 113:417–427. https://doi.org/10.1007/s11240-012-0281-z
Maas EV, Hoffman GJ (1977) Crop salt tolerance: current assessment. J Irrigation Drain Div 103(2):115–134
Mady MA (2014) Inducing cold tolerability in squash (Cucurbita pepo L.) plant by using salicylic acid and chelated calcium application. Int J Agric Sci Res 4:9–24
Mäkelä P, Kärkkäinen J, Somersalo S (2000) Effect of glycinebetaine on chloroplast ultrastructure, chlorophyll and protein content, and RuBPCO activities in tomato grown under drought or salinity. Biol Plant 43(3):471–475. https://doi.org/10.1023/A:1026712426180
Malekzadeh P (2015) Influence of exogenous application of glycinebetaine on antioxidative system and growth of salt-stressed soybean seedlings (Glycine max L.). Physiol Mol Biol Plants 21(2):225–232. https://doi.org/10.1007/s12298-015-0292-4
Mansour MMF (1998) Protection of plasma membrane of onion epidermal cells by glycinebetaine and proline against NaCl stress. Plant Physiol Biochem 36:767–772. https://doi.org/10.1016/S0981-9428(98)80028-4
Milone MT, Sgherri C, Clijsters H, Navari-Izzo F (2003) Antioxidative responses of wheat treated with realistic concentration of cadmium. Environ Exp Bot 50:265–276
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 9:405–410. https://doi.org/10.1016/S1360-1385(02)02312-9
Nazar R, Umar S, Khan NA (2015) Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signal Behav 10(3):e1003751. https://doi.org/10.1080/15592324.2014.1003751
Piper CS (1950) Soil and plant analysis, 1st edn. Interscience Publishers Inc, New York, pp 30–59
Qados AAMS (2015) Mechanism of nanosilicon-mediated alleviation of salinity stress in faba bean (Vicia faba L.) plants. Am J Exp Agric 7(2):78–95. https://doi.org/10.9734/AJEA/2015/15110
Rahdari P, Tavakoli S, Hosseini SM (2012) Studying of salinity stress effect on germination, proline, sugar, protein, lipid and chlorophyll content in purslane (Portulaca oleracea L.) leaves. J Stress Physiol Biochem 8(1):182–193
Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44(1):357–384. https://doi.org/10.1146/annurev.pp.44.060193.002041
Romero-Aranda R, Soria T, Cuartero J (2001) Tomato plant-water uptake and plant-water relationships under saline growth conditions. Plant Sci 160(2):265–272. https://doi.org/10.1016/S0168-9452(00)00388-5
Sahu S, Das P, Ray M, Sabat SC (2010) Osmolyte modulated enhanced rice leaf catalase activity under salt-stress. Adv Biosci Biotechnol 1:39–46. https://doi.org/10.4236/abb.2010.11006
Sairam RK, Deshmukh PS, Shukla DS (1997) Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. J Agron Crop Sci 178(3):171–178. https://doi.org/10.1111/j.1439-037X.1997.tb00486.x
Sevengor S, Yasar F, Kusvuran S, Ellialtioglu S (2011) The effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidative enzymes of pumpkin seedling. Afr J Agric Res 6(21):4920–4924. https://doi.org/10.5897/AJAR11.668
Shakirova FM (2007) Role of hormonal system in the manifestation of growth promoting and antistress action of salicylic acid. In: Hayat S, Ahmad A (eds) Salicylic acid. A plant hormone. Springer, Dordrecht, pp 69–89
Shi QH, Bao ZY, Zhu ZJ, Ying QS, Qian QQ (2006) Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regul 48(2):127–135. https://doi.org/10.1007/s10725-005-5482-6
Stevens J, Senaratna T, Sivasithamparam K (2006) Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. Roma): associated changes in gas exchange, water relations and membrane stabilisation. Plant Growth Regul 49(1):77–83. https://doi.org/10.1007/s10725-006-0019-1
Straus MR, Rietz S, van ver Loren Themaat E, Bartsch M, Parker JE (2010) Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J 62:628–640. https://doi.org/10.1111/j.1365-313X.2010.04178.x
Szabados L, Savouré A (2009) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97. https://doi.org/10.1016/j.tplants.2009.11.009
Szepesi A, Csiszár J, Bajkán S, Gémes K, Horváth F, Erdei L, Deér AK, Simon ML, Tari I (2005) Role of salicylic acid pre-treatment on the acclimation of tomato plants to salt- and osmotic stress. Acta Biol Szeged 49:123–125
Trajkova F, Papadantonakis N, Savvas D (2006) Comparative effects of NaCl and CaCl2 salinity on cucumber grown in a closed hydroponic system. HortScience 41(2):437–441
Turk H, Erdal S, Genisel M, Atici O, Demir Y, Yanmis D (2014) The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul 74:139–152. https://doi.org/10.1007/s10725-014-9905-0
Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:1–10
Wan S, Kanga Y, Wang D, Liu S (2010) Effect of saline water on cucumber (Cucumis sativus L.) yield and water use under drip irrigation in North China. Agric Water Manag 98(1):105–113. https://doi.org/10.1016/j.agwat.2010.08.003
Watanabe FS, Olsen SR (1965) Test of an ascorbic acid method for determining phosphorus in water and sodium bicarbonate extracts from soil. Soil Sci Soc Am Proc 29:677–678
Willekens H, Inzé D, Van Montagu M (1995) Catalases in plants. Mol Breed 1(3):207–228
Woodbury W, Spencer AK, Stahmann MA (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301–305
Yadav S, Irfan M, Ahmad A, Hayat S (2011) Causes of salinity and plant manifestations to salt stress: a review. J Environ Biol 32(5):667–685
Yildirim E, Turan M, Guvenc I (2008) Effect of foliar salicylic acid applications on growth, chlorophyll, and mineral content of cucumber grown under salt stress. J Plant Nutr 31(3):593–612. https://doi.org/10.1080/01904160801895118
Yousry MM, El-Mesirry DS, Shama MA (2015) Effect of proline on resistance of potato crop (Solanum tuberosum L.) for the negative effects of water irrigation salinity. Curr Sci Int 4(1):172–177
Zamaninejad M, Khorasani SK, Moeini MJ, Heidarian AR (2013) Effect of salicylic acid on morphological characteristics, yield and yield components of corn (Zea mays L.) under drought condition. European. J Exp Biol 3(2):153–161
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S.M. Youssef, S.A. Abd Elhady, R.M. Aref and G.S. Riad declare that they have no competing interests.
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Youssef, S.M., Abd Elhady, S.A., Aref, R.M. et al. Salicylic Acid Attenuates the Adverse Effects of Salinity on Growth and Yield and Enhances Peroxidase Isozymes Expression more Competently than Proline and Glycine Betaine in Cucumber Plants. Gesunde Pflanzen 70, 75–90 (2018). https://doi.org/10.1007/s10343-017-0413-9
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DOI: https://doi.org/10.1007/s10343-017-0413-9
Keywords
- Abiotic Stress
- Cucumis sativus
- Photosynthesis
- Relative water content
- Leaf membrane stability index
- Growth
- Yield
- Native-PAGE