The Effects of NPR1 Dependent Salicylic Acid Change in Increasing Salt Tolerance of Soybean Leaves by Acclimation

Ufkun SARISOY, Burcu SECKIN DINLER, Eda TASCI

Abstract


Non-expressor of Pathogen Related 1 (NPR1) is a regulatory gene of the salicylic acid (SA) signaling pathway, the detailed mechanism of which is still not well understood. This study investigated the effects of NPR1-dependent SA level change on increasing salt tolerance of soybean leaves with acclimation. Salt-sensitive (‘SA88’) and salt-tolerant (‘Erensoy’) soybean (Glycine max L.) plants were treated with increasing NaCl concentrations (25, 50, 75, and 100 mM; acclimation) and with 100 mM NaCl directly (non-acclimation) in two groups. The results showed that acclimation treatment alleviated salt-induced damage in the sensitive cultivar with increasing superoxide anion radical scavenging activity, and decreasing hydrogen peroxide (H2O2) and malondialdehyde (MDA) content. However, the APX, CAT, and GST enzyme activities were increased by acclimation treatment, with the highest increase observed in GST enzymes. Interestingly, the Gmnpr1 gene expression was upregulated in all treatments but was more pronounced in non-acclimation. Furthermore, the highest increase in endogenous SA level was under acclimation treatment in ‘SA88’. In conclusion, the results firstly showed that an acclimation process is useful for increasing salt tolerance in sensitive soybean plants with only ROS-inducted NPR1-independent SA accumulation but not through the NPR1-dependent SA signaling pathway.


Keywords


acclimation; NPR1; salt stress; salicylic acid; soybean

Full Text:

PDF

References


Aksoy M, Dinler BS (2014). Different responses in acclimated and non-acclimated processes of soybean leaves to salinity. Fresenius Environmental Bulletin 238:1915-1919.

Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS, Iqbal M, Lukatkin AS, Pereira E, Duarte AC, Ahmad I (2015). Lipids and proteins - major targets of oxidative modifications in abiotic stressed plants. Environmental Science and Pollution Research 22:4099-4121.

Ardebili NO, Saadatmand S, Niknam V, Khavari-Nejad RA (2014). The alleviating effects of selenium and salicylic acid in salinity exposed soybean. Acta Physiologiae Plantarum 36: 3199-3205.

Asgher M, Khan MIR, Anjum NA, Khan NA (2015). Minimizing toxicity of cadmium in plants - role of plant growth regulators. Protoplasma 252:399-413.

Ashraf M, Akram NA, Arteca RN, Foolad MR (2010). The physiological biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. Critical Reviews in Plant Sciences 29:162-190.

Beauchamp CO, Fridovich I (1973). Isozymes of superoxide dismutase from wheat germ. Biochimica et Biophysica Acta (BBA) - Protein Structure 317:50-64.

Belin C, Bashandy T, Cela J, Delorme?Hinoux V, Riondet C, Reichheld JP (2015). A comprehensive study of thiol reduction gene expression under stress conditions in Arabidopsis thaliana. Plant Cell and Environment 38:299-314.

Bergmeyer N (1970). Methoden der Enzymatischen Analyse. Akademie Verlag, Berlin pp 599-607.

Blanco F, Salinas P, Cecchini NM, Jordana X, Van Hummelen P, Alvarez ME, Holuigue L (2009). Early genomic responses to salicylic acid in Arabidopsis. Plant Molecular Biology 70:79-102.

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

Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009). Biosynthesis of salicylic acid in plants. Plant Signaling and Behavior 4:493-496.

Claussen W (2005). Proline as a measure of stress in tomato plants. Plant Science 168:241-248.

De Azevedo Neto AD, Prisco JT, Enéas-Filho J, de Abreu CEB, Gomes-Filho E (2006). Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environmental and Experimental Botany 56:87-94.

De Rosa G, Duncan DS, Keen CL, Hurley LS (1979). Evaluation of negative staining technique for determination of CN-insensitive superoxide dismutase activity. Biochimica et Biophysica Acta (BBA) – Enzymology 566:32-39.

Dempsey DMA, Shah J, Klessig DF (1999). Salicylic acid and disease resistance in plants. Critical Reviews in Plant Science 18:547-575.

Djanaguiraman M, Sheeba JA, Shanker AK, Devi DD, Bangarusamy U (2006). Rice can acclimate to lethal level of salinity by pretreatment with sublethal level of salinity through osmotic adjustment. Plant and Soil 284: 363-373.

Durrant WE, Dong X (2004). Systemic acquired resistance. Annual Review of Phytopathology 42:185-209.

Etehadnia M, Schoenau J, Waterer D, Karen T (2010). The effect of CaCl2 and NaCl salt acclimation in stress tolerance and its potential role in ABA and scion/rootstock-mediated salt stress responses. Plant Stress 4:72-81.

Fayez KA, Bazaid SA (2014). Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. Journal of the Saudi Society of Agricultural Science 13:45-55.

Flores MIA, Romero-González R, Frenich AG, Vidal JLM (2011). QuEChERS?based extraction procedure for multifamily analysis of phytohormones in vegetables by UHPLC?MS/MS. Journal of Separating Science 34:1517-1524.

Habig WH, Pabst MJ, Jakoby WB (1974). Glutathione S-transferases the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249:7130-7139.

Hayat Q, Hayat S, Irfan M, Ahmad A (2010). Effect of exogenous salicylic acid under changing environment: a review. Environmental and Experimental Botany 68:14-25.

Herrera-Vásquez A, Carvallo L, Blanco F, Tobar M, Villarroel-Candia E, Vicente-Carbajosa J, Holuigue L (2015). Transcriptional control of glutaredoxin GRXC9 expression by a salicylic acid-dependent and NPR1-independent pathway in Arabidopsis. Plant Molecular Biology Reporter 33:624-637.

Herzog V, Fahimi H (1973). Determination of the activity of peroxidase. Anaytical Biochemistry 5:554-562.

Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2015). Salicylic acid in plant salinity stress signalling and tolerance. Plant Growth Regulation 76:25-40.

Jayakannan M, Bose J, Babourina O, Shabala S, Massart A, Poschenrieder C, Rengel Z (2015). The NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. Journal of Experimental Botany 66:1865-1875.

Khan MIR, Asgher M, Khan NA (2014). Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L). Plant Physiology and Biochemistry 80:67-74.

Khan NA, Nazar R, Iqbal N, Anjum NA (Eds) (2012). Phytohormones and abiotic stress tolerance in plants. Springer Science Business Media.

Kinkema M, Fan W, Dong X (2000). Nuclear localization of NPR1 is required for activation of PR gene expression. The Plant Cell 12:2339-2350.

Kneeshaw S, Gelineau S, Tada Y, Loake GJ, Spoel SH (2014). Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Molecular Cell 56:153-162.

Kuai X, Després C (2016). Defining Arabidopsis NPR1 orthologues in crops for translational plant immunity. Canadian Journal of Plant Pathology 38:25-30.

Laemmli UK (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.

Laloi C, Mestres-Ortega D, Marco Y, Meyer Y, Reichheld JP (2004). The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor. Plant Physiology 134:1006-1016.

Li G, Peng X, Wei L, Kang G (2013). Salicylic acid increases the contents of glutathione and ascorbate and temporally regulates the related gene expression in salt-stressed wheat seedlings. Gene 529:321-325.

Lin J, Wang Y, Wang G (2006). Salt stress-induced programmed cell death in tobacco protoplasts is mediated by reactive oxygen species and mitochondrial permeability transition pore status. Journal of Plant Physiology 163:731-739.

Lindermayr C, Sell S, Müller B, Leister D, Durner J (2010). Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. The Plant Cell 22:2894-2907.

Mai LQ, Hang HT (2016). Evaluation of the proline content in tissues of soybean Glycine max [L] Merr dt26 cultivar during salt acclimation. VNU Journal of Science: Natural Sciences and Technology 32:307-312.

Miller GAD, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell and Environment 33:453-467.

Mittler R, Zilinskas BA (1993). Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium. Analytical Biochemistry 212:540-546.

Miura K, Tada Y (2014). Regulation of water salinity and cold stress responses by salicylic acid. Frontiers Plant Science 5:4.

Mou Z, Fan W, Dong X (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935-944.

Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell and Physiology 22:867-880.

Navari?Izzo F, Quartacci MF, Pinzino C, Vecchia FD, Sgherri CL (1998). Thylakoid?bound and stromal antioxidative enzymes in wheat treated with excess copper. Physiologia Plantarum 104:630-638.

Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS (2013). Tell me more: roles of NPRs in plant immunity. Trends in Plant Science 18:402-411.

Pandolfi C, Azzarello E, Mancuso S, Shabala S (2016). Acclimation improves salt stress tolerance in Zea mays plants. Journal of Plant Physiology 201:1-8.

Pandolfi C, Mancuso S, Shabala S (2012). Physiology of acclimation to salinity stress in pea (Pisum sativum). Environmental and Experimental Botany 84:44-51.

Parida AK, Das AB (2005). Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60:324-349.

Parida AK, Das AB, Mohanty P (2004). Defense potentials to NaCl in a mangrove Bruguiera parviflora: differential changes of isoforms of some antioxidative enzymes. Journal of Plant Physiology 161:531-542.

Pfaffl MW, Horgan GW, Dempfle L (2002). Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Researh 30:e36-e36.

Rao KM, Sresty TVS (2000). Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L) Millspaugh) in response to Zn and Ni stresses. Plant Science 157:113-128.

Ricci G, Bello ML, Caccuri AM, Galiazzo F, Federici G (1984). Detection of glutathione transferase activity on polyacrylamide gels. Analytical Biochemistry 143:226-230.

Saha P, Chatterjee P, Biswas AK (2010). NaCl pretreatment alleviates salt stress by enhancement of antioxidant defense system and osmolyte accumulation in mungbean (Vigna radiata L Wilczek). Indian Journal of Experimental Biology 48:593-600.

Seckin B, Turkan I, Sekmen AH, Ozfidan C (2010). The role of antioxidant defense systems at differential salt tolerance of Hordeum marinum Huds. (sea barleygrass) and Hordeum vulgare L. (cultivated barley). Environmental and Experimental Botany 69:76-85.

Seevers PM, Daly JM, Catedral FF (1971). The role of peroxidase isozymes in resistance to wheat stem rust disease. Plant Physiology 48:353-360.

Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001). Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiologia Plantarum 112:487-494.

Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Dong X (2008). Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:952-956.

Umezawa T, Shimizu K, Kato M, Ueda T (2000). Enhancement of salt tolerance in soybean with NaCl pretreatment. Physiologia Plantarum 110:59-63.

Velikova V, Yordanov I, Edreva A (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science 151:59-66.

Woodbury W, Spencer AK, Stahmann MA (1971). An improved procedure using ferricyanide for detecting catalase isozymes. Analytical Biochemistry 44:301-305.

Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, Després C (2012). The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Reports 1:639-647.




DOI: http://dx.doi.org/10.15835/nbha46211016

June 1, 2018: Notulae Botanicae Horti Agrobotanici Cluj-Napoca in Scopus – Elsevier CiteScore 2017=0.78, Horticulture; Agronomy and Crop Science; Plant Science


 
http://not-bot-horti-agrobo.blogspot.com/
https://www.facebook.com/NotBotHA
https://twitter.com/NotBotHA