Abstract
Soil salinity is a major abiotic stress that adversely affects crop growth, development and productivity worldwide. In this study, the individual and synergistic roles of putrescine (Put) and spermidine (Spd) in salinity stress tolerance of foxtail millet (Setaria italica L.) was assessed. In the present study, plants treated with combined biogenic amines Put + Spd possess very efficient antioxidant enzyme systems which help to control the uninhibited oxidation and protect the plants from oxidative damage by ROS scavenging. Additionally, lower concentration of Put + Spd under NaCl stress showed reduced hydrogen peroxide, electrolyte leakage and caspase-like activity than control. FTIR analysis underlying the ability of PAs induced tolerance and the chemical bonds of Put + Spd treated plants were reminiscent of control plants. Moreover, histochemical analysis with 2′,7′–dichlorofluorescein diacetate (DCF-DA), 3,3′–Diaminobenzidine (DAB) and nitrotetrazolium blue chloride (NBT) revealed that ROS accumulation was inhibited by combined PAs under salt stress condition. These results showed that Put + Spd significantly improve the endogenous PAs, which enhance high-salinity stress tolerance by detoxifying ROS. For the first time, the synergistic ROS scavenging ability of Put along with Spd was investigated upon salinity tolerance in C4 model foxtail millet crop. Overall, our findings illustrated the implication for improving salinity tolerance of agronomically important crop species.
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Abbreviations
- APX:
-
Ascorbate peroxidae
- CAT:
-
Catalase
- CLSM:
-
Confocal laser scanning microscope
- DAB:
-
3,3-diaminobenzidine
- DAO:
-
Diamine oxidase
- EL:
-
Electrolyte leakage
- FTIR:
-
Fourier transform-infrared spectroscopy
- GPX:
-
Guaiacol peroxidise
- GR:
-
Glutathione reductase
- GSH:
-
Glutathione
- GSSG:
-
Glutathione disulfide
- H2O2 :
-
Hydrogen peroxide
- MDA:
-
Malondialdehyde
- NaCl:
-
Sodium chloride
- NADH+ :
-
Nicotinamide adenine dinucleotide
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate
- NBT:
-
Nitrotetrazolium blue chloride
- PAO:
-
Polyamine oxidase
- PAs:
-
Polyamines
- POD:
-
Peroxidase
- Put:
-
Putrescine
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
- SOD:
-
Superoxide dismutase
- Spd:
-
Spermidine
References
Abdel-Latef AA (2005) Salt tolerance of some wheat cultivars. Ph.D. Thesis. South Valley Univ in Qena, Egypt, pp 1–159
Aebi H (1984) Catalase in vitro. Oxy Radic Biologic Sys 10:121–126
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396
Barth A (2000) The infrared absorption of amino acid side chains. Progress Biophys Mol Boil 74:141–173
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Carlberg I, Mannervik EB (1975) Glutathione level in rat brain. J Biol Chem 250:5475–5480
Chawla S, Jain S, Jain V (2013) Salinity induced oxidative stress and antioxidant system in salt-tolerant and salt-sensitive cultivars of rice (Oryza sativa L.). J Plant Biochem Biotechnol 22:27–34
Chen J, Fang J, Guo Z, Lu S (2018) Polyamines and antioxidant defense system are associated with cold tolerance in centipede grass. Front Agr Sci Eng 5:129–138
Dąbrowski P, Kalaji MH, Baczewska AH, Pawluśkiewicz B, Mastalerczuk G, Borawska-Jarmułowicz B, Paunov M, Goltsev V (2017) Delayed chlorophyll a fluorescence, MR 820: and gas exchange changes in perennial ryegrass under salt stress. J Luminescence 183:322–333
Del Pozo O, Lam E (1998) Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol 8:1129–1132
Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635
Fariduddin Q, Khan TA, Yusuf M, Aafaqee ST, Khalil RR (2018) Ameliorative role of salicylic acid and spermidine in the presence of excess salt in Lycopersicon esculentum. Photosynthetica 56:750–762
Fu Y, Zhang Z, Liu J, Chen M, Pan R, Hu W, Guan Y, Hu J (2019) Seed priming with spermidine and trehalose enhances chilling tolerance of rice via different mechanisms. J Plant Growth Regul 10:1–11
Gong X, Liu Y, Huang D, Zeng G, Liu S, Tang H, Zhou L, Hu X, Zhou Y, Tan X (2016) Effects of exogenous calcium and spermidine on cadmium stress moderation and metal accumulation in Boehmeria nivea (L.) Gaudich. Environ Sci Pollut Res 23:8699–8708
Griffiths PR (1978) Fourier transform infrared spectroscopy: recent developments. Appl Opt 17:1315–1317. https://doi.org/10.1364/ao.17.001315
Hameed M, Ashraf M (2008) Physiological and biochemical adaptations of Cynodon dactylon (L.) Pers. from the salt range (Pakistan) to salinity stress. Flora 203:683–694
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stechiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hu X, Zhang Y, Shi Y, Zhang Z, Zou Z, Zhang H, Zhao J (2012) Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity–alkalinity mixed stress. Plant Physiol Biochem 57:200–209
Huang CC, Chen KL, Cheung CH, Chang JY (2013) Autophagy induced by cathepsin S inhibition induces early ROS production, oxidative DNA damage, and cell death via xanthine oxidase. Free Radical Biol Medicine 65:1473–1486
Hussain T, Koyro HW, Huchzermeyer B, Khan MA (2015) Eco-physiological adaptations of Panicum antidotale to hyperosmotic salinity: water and ion relations and anti-oxidant feedback. Flora 212:30–37
Kannappan A, Sivaranjani M, Srinivasan R, Rathna J, Pandian SK, Ravi AV (2017) Inhibitory efficacy of geraniol on biofilm formation and development of adaptive resistance in Staphylococcus epidermidis RP62A. J Med Microbiol 66:1506–1515
Khan MI, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18
Kissoudis C, van de Wiel C, Visser RG, van der Linden G (2014) Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk. Front Plant Sci 5:207
Kong-Ngern K, Daduang S, Wongkham C, Bunnag S, Kosittrakun M, Theerakulpisut P (2005) Protein profiles in response to salt stress in leaf sheaths of rice seedlings. Sci Asia 31:403–408
Lahlali R, Jiang Y, Kumar S, Karunakaran C, Liu X, Borondics F, Hallin E, Bueckert R (2014) ATR–FTIR spectroscopy reveals involvement of lipids and proteins of intact pea pollen grains to heat stress tolerance. Front Plant Sci 5:747
Li S, Jin H, Zhang Q (2016) The effect of exogenous spermidine concentration on polyamine metabolism and salt tolerance in zoysia grass (Zoysia japonica Steud) subjected to short-term salinity stress. Front Plant Sci 7:1221
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Proto Food Anal Chem 1:3–4
Lin CC, Kao CH (1999) NaCl induced changes in ionically bounds peroxidase activity in roots of rice seedlings. Plant Soil 216:147–153
Liu JH, Wang W, Wu H, Gong X, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6:10
Mandal C, Ghosh N, Maiti S, Das K, Gupta S, Dey N, Adak MK (2013) Antioxidative responses of Salvinia (Salvinia natans Linn.) to aluminium stress and it’s modulation by polyamine. Physiol Mol Biol Plants 19:91–103
Miller GA, Suzuki N, Ciftci-Yilmaz SU, Mittler RO (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Questions and future challenges. Trends Plant Sci 9:490–498
Mostofa MG, Rahman A, Ansary MM, Watanabe A, Fujita M, Tran LS (2015) Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep 5:14078
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum 15:473–497
Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nayyar H, Chander S (2004) Protective effects of polyamines against oxidative stress induced by water and cold stress in chick pea. J Agro Crop Sci 190:355–365
Nemeth M, Janda T, Horvath E, Paldi E, Szalai G (2002) Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Sci 162:569–574
Panuccio MR, Chaabani S, Roula R, Muscolo A (2018) Bio-priming mitigates detrimental effects of salinity on maize improving antioxidant defense and preserving photosynthetic efficiency. Plant Physiol Biochem 132:465–474
Paoletti F, Mocali A (1990) Determination of superoxide dismutase activity by purely chemical system based on NAD (P) H. Oxidation. Methods Enzymol 186:209–220
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants. Ecotoxicol Env Saf 60:324–349
Parvin S, Lee OR, Sathiyaraj G, Khorolragchaa A, Kim YJ, Yang DC (2014) Spermidine alleviates the growth of saline-stressed ginseng seedlings through antioxidative defense system. Gene 537:70–78
Paul S, Banerjee A, Roychoudhury A (2018) Role of polyamines in mediating antioxidant defense and epigenetic regulation in plants exposed to heavy metal toxicity. Plants under metal and metalloid stress: responses, tolerance and remediation. Nature 5:229–247
Poborilova Z, Opatrilova R, Babula P (2013) Toxicity of aluminium oxide nanoparticles demonstrated using a BY-2 plant cell suspension culture model. Environ Exp Bot 91:1–11
Rady MM, Hemida KA (2015) Modulation of cadmium toxicity and enhancing cadmium-tolerance in wheat seedlings by exogenous application of polyamines. Ecotoxicol Env Saf 119:178–185
Rasool S, Hameed A, Azooz MM, Siddiqi TO, Ahmad P (2013) Salt stress: causes, types and responses of plants. Ecophysiol Responses Plants Under Salt Stress 3:1–24
Rathinapriya P, Satish L, Rameshkumar R, Pandian S, Rency AS, Ramesh M (2018) Role of activated charcoal and amino acids in developing an efficient regeneration system for Foxtail Millet (Setaria italica (L.) Beauv.) using leaf base segments. Physiol Mol Biol Plants 25:533–548
Rossi FR, Krapp AR, Bisaro F, Maiale SJ, Pieckenstain FL, Carrillo N (2017) Reactive oxygen species generated in chloroplasts contribute to tobacco leaf infection by the necrotrophic fungus Botrytis cinerea. Plant J 92:761–773
Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168:317–328
Sang T, Shan X, Li B, Shu S, Sun J, Guo SR (2016) Comparative proteomic analysis reveals the positive effect of exogenous spermidine on photosynthesis and salinity tolerance in cucumber seedlings. Plant Cell Rep 35:1769–1782
Sapeta H, Costa JM, Lourenco T, Maroco J, Van der Linde P, Oliveira MM (2013) Drought stress response in Jatropha curcas: growth and physiology. Environ Experim Botany 85:76–84
Satish L, Rathinapriya P, Rency AS, Ceasar SA, Prathibha M, Pandian S, Rameshkumar R, Ramesh M (2016) Effect of salinity stress on finger millet (Eleusine coracana (L.) Gaertn): histochemical and morphological analysis of coleoptile and coleorhizae. Flora 222:111–120
Satish L, Rency AS, Ramesh M (2018) Spermidine sprays alleviate the water deficit-induced oxidative stress in finger millet (Eleusine coracana L. Gaertn.) plants. Biotech 8:63
Savvides A, Ali S, Tester M, Fotopoulos V (2016) Chemical priming of plants against multiple abiotic stresses: mission possible? Trend Plant Sci 21:329–340
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205
Singh M, Singh VP, Prasad SM (2019) Nitrogen alleviates salinity toxicity in Solanum lycopersicum seedlings by regulating ROS homeostasis. Plant Physiol Biochem 141:466–476
Sreenivasulu N, Ramanjulu S, Ramachandra-Kini K, Prakash HS, Shekar-Shetty H, Savithri HS, Sudhakar C (1999) Total peroxidase activity and peroxidase isoforms as modified by salt stress in two cultivars of fox-tail millet with differential salt tolerance. Plant Sci 141:1–9
Sreenivasulu N, Grimm B, Wobus U, Weschke W (2000) Differential response of antioxidant compounds to salinity stress in salt-tolerant and salt-sensitive seedlings of foxtail millet (Setaria italica). Physiol Planta 109:435–442
Su G, An Z, Zhang W, Liu Y (2005) Light promotes the synthesis of lignin through the production of H2O2 mediated by diamine oxidases in soybean hypocotyls. J Plant Physiol 162:1297–1303
Sudhakar C, Veeranagamallaiah G, Nareshkumar A, Sudhakarbabu O, Sivakumar M, Pandurangaiah M, Kiranmai K, Lokesh U (2015) Polyamine metabolism influences antioxidant defense mechanism in foxtail millet (Setaria italica L.) cultivars with different salinity tolerance. Plant Cell Rep 34:141–156
Sun M, Wang T, Fan L, Wang H, Pan H, Cui X, Lou Y, Zhuge Y (2020) Foliar applications of spermidine improve foxtail millet seedling characteristics under salt stress. Biol Plantarum 64:353–362
Tabot PT, Adams JB (2013) Early responses of Bassia diffusa (Thunb.) Kuntze to submergence for different salinity treatments. South Afr J Bot 84:19–29
Tajti J, Janda T, Majláth I, Szalai G, Pal M (2018) Comparative study on the effects of putrescine and spermidine pre-treatment on cadmium stress in wheat. Ecotoxicol Env Saf 148:546–554
Tang S, Zhang H, Li L, Liu X, Chen L, Chen W, Ding Y (2018) Exogenous spermidine enhances the photosynthetic and antioxidant capacity of rice under heat stress during early grain-filling period. Funct Plant Biol 45:911–921
Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240:1–18
Van Ha C, Leyva-González MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Van Dong N, Yamaguchi-Shinozaki K (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci 111:851–856
Wang F, Manku S, Hall DG (2000) Solid phase syntheses of polyamine toxins ho-416b and phtx-433. Use of an efficient polyamide reduction strategy that facilitates access to branched analogues. Organic Let 2:1581–1583
Wang H, Liang W, Huang J (2013) Putrescine mediates aluminum tolerance in red kidney bean by modulating aluminum-induced oxidative stress. Crop Sci 53:2120–2128
Wasti S, Mimouni H, Smiti S, Zid E, Ben Ahmed H (2012) Enhanced salt tolerance of tomatoes by exogenous salicylic acid applied through rooting medium. J Integr Bio 16:200–207
Wu J, Shu S, Li C, Sun J, Guo S (2018) Spermidine-mediated hydrogenperoxide signaling enhances the antioxidant capacity of salt-stressed cucumber roots. Plant Physiol Biochem 128:152–162
Yang J, Yen HE (2002) Early salt stress effects on the changes in chemical composition in leaves of ice plant and Arabidopsis. A Fourier transform infrared spectroscopy study. Plant Physiol 130:1032–1042
Yoon JY, Hamayun M, Lee SK, Lee IJ (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol 12:63–68
Zhang JP, Wang MY, Bai YF, Jia JP, Wang GY (2005) Rapid evaluation on drought tolerance of foxtail millet at seedling stage. J Plant Genet Resour 6:59–62
Zhang Y, Zhang L, Hu XH (2014) Exogenous spermidine-induced changes at physiological and biochemical parameters levels in tomato seedling grown in saline-alkaline condition. Bot studies 55:1–8
Zhao Q, Bai J, Lu Q, Zhang G (2017) Effects of salinity on dynamics of soil carbon in degraded coastal wetlands: implications on wetland restoration. Phys Chem Earth Parts A/B/C 97:12–18
Zhou L, Zhou H, Peng Y, Zhang X, Ma X, Huang L, Yan Y (2015) Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. J Plant Growth Regul 76:71–82
Acknowledgement
The author P. Rathinapriya (UGC order no: F.25-1/2013-14 (BSR)/7-326/2011 dt 30.05.2014) thank the University Grants Commission, New Delhi, India for financial support in the form of fellowship. The authors sincerely acknowledge the computational and Bioinformatics facility provided by the Alagappa University Bioinformatics Infrastructure Facility (funded by DBT, GOI; File No. BT/BI/25/012/2012, BIF). The authors also thankfully acknowledge RUSA 2.0 [F. 24-51/2014-U, Policy (TN Multi-Gen), Dept of Edn, GOI], DST-FIST (Grant No. SR/FST/LSI-639/2015(C)), UGC-SAP (Grant No. F.5-1/2018/DRS-II (SAP-II)) and DST-PURSE (Grant No. SR/PURSE Phase 2/38 (G)) for providing instrumentation facilities.
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Conceived and designed the experiments: PR & MR. Performed the experiments: PR MB KR RA RR. Analyzed the data: PR LS SP. Contributed reagents/materials/analysis tools: MR. Wrote the paper: PR. All the authors have read the manuscript and approved for publication.
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Rathinapriya, P., Pandian, S., Rakkammal, K. et al. The protective effects of polyamines on salinity stress tolerance in foxtail millet (Setaria italica L.), an important C4 model crop. Physiol Mol Biol Plants 26, 1815–1829 (2020). https://doi.org/10.1007/s12298-020-00869-0
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DOI: https://doi.org/10.1007/s12298-020-00869-0