Abstract
Aims
Selenium (Se) has been reported to mitigate the harmful effects of salt stress on plants; however, the internal mechanisms remain unknown. Here, the effects of Se supplementation on tomato plants under salt stress were investigated.
Methods
The biomass, relative electrical conductivity (REC), relative water content (RWC),
photosynthetic parameter, inorganic ion contents, malondialdehyde (MDA), soluble sugar and proline contents, as well as the regulation of plant hormones of Se application in tomato plants were investigated after exposure to Se and salt stress treatments.
Results
Exogenous Se application improved photosynthesis and the water use efficiency (WUE) of tomato plants under salt stress, thereby promoting the growth of tomato plants under salt stress. Se supplementation also maintained the K+ and Na+ homeostasis, reduced the REC, decreased MDA, H2O2 and O2•− contents, and mitigated the oxidative damage caused by salt stress. In addition, exogenous Se increased the salicylic acid (SA) content in tomato leaves and roots via up-regulating the PAL or ICS pathways involved in SA biosynthesis. After pre-treatment with the SA inhibitor 1-aminobenzotriazole, the photosynthetic efficiency of tomato plants decreased, plant growth was weakened, and the REC was increased, indicating that the alleviating role of Se on salt stress was abolished.
Conclusions
Our results clarified the roles of Se and its regulation mechanisms in plant salt stress tolerance and the critical involvement of SA in this process. The study of Se in plant abiotic stress tolerance will give a more theoretical foundation for using exogenous Se in agricultural production to enhance crop growth and yield under adversity stresses.
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Data availability
The data generated during the current study are available from the corresponding author on reasonable request.
Abbreviations
- ABT:
-
1-Aminobenzotriazole
- DAB:
-
Diaminobenzidine
- H2O2 :
-
Hydrogen peroxide
- ICS:
-
Isochorismate synthase
- MDA:
-
Malondialdehyde
- NBT:
-
Nitroblue tetrazolium
- O2 • − :
-
Superoxide anion
- PAL1:
-
Phenylalanine ammonia-lyase 1
- qRT-PCR:
-
Quantitative real-time PCR
- ROS:
-
Reactive oxygen species
- SA:
-
Salicylic acid
- SABP2:
-
Salicylic acid-binding protein 2
- SAMT:
-
Carboxymethyltransferase
- Se:
-
Selenium
- WUE:
-
Water use efficiency
References
Ahmed W, Imran M, Yaseen M, Haq TU, Jamshaid MU, Rukh S, Ikram RM, Ali M, Ali A, Maqbool M, Arif M, Khan MA (2020) Role of salicylic acid in regulating ethylene and physiological characteristics for alleviating salinity stress on germination, growth and yield of sweet pepper. Peer J 8:e8475. https://doi.org/10.7717/peerj.8475
Ardebili NO, Saadatmand S, Niknam V, Khavari-Nejad RA (2014) The alleviating effects of selenium and salicylic acid in salinity exposed soybean. Acta Physiol Plant 36:3199–3205. https://doi.org/10.1007/s11738-014-1686-6
Arnon DI (1949) Copper enzymes in isolated chloroplasts Polyphenoloxidase in Beta vulgris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Ashraf MA, Akbar A, Parveen A, Rasheed R, Hussain I, Iqbal M (2018) Phenological application of selenium differentially improves growth, oxidative defense and ion homeostasis in maize under salinity stress. Plant Physiol Biochem 123:268–280. https://doi.org/10.1016/j.plaphy.2017.12.023
Benlloch-Gonzalez M, Romera J, Cristescu S, Harren F, Fournier JM, Benlloch M (2010) K starvation inhibits water - stress - induced stomatal closure via ethylene synthesis in sunflower plants. J Exp Bot 61:1139–1145. https://doi.org/10.1093/jxb/erp379
Borbély P, Molnár Á, Valyon E, Ördög A, Horváth-Boros K, Csupor D, Fehér A, Kolbert Z (2021) The effect of foliar selenium (Se) treatment on growth, photosynthesis, and oxidative-nitrosative signalling of Stevia rebaudiana leaves. Antioxidants 10:72. https://doi.org/10.3390/antiox10010072
Boriboonkaset T, Theerawitaya C, Yamada N, Pichakum A, Supaibulwatana K, Cha-Um S, Takabe T, Kirdmanee C (2013) Regulation of some carbohydrate metabolism-related genes, starch and soluble sugar contents, photosynthetic activities and yield attributes of two contrasting rice genotypes subjected to salt stress. Protoplasma 250:1157–1167. https://doi.org/10.1007/s00709-013-0496-9
Diao M, Ma L, Wang J, Cui J, Fu A, Liu H (2014) Selenium promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast. J Plant Growth Regul 33:671–682. https://doi.org/10.1007/s00344-014-9416-2
Dien DC, Mochizuki T, Yamakawa T (2019) Effect of various drought stresses and subsequent recovery on proline, total soluble sugar and starch metabolisms in Rice (Oryza sativa L.) varieties. Plant Prod Sci 22:530–545. https://doi.org/10.1080/1343943X.2019.1647787
Ding P, Ding Y (2020) Stories of salicylic acid: a plant defense hormone. Trends Plant Sci 25:549–565. https://doi.org/10.1016/j.tplants.2020.01.004
El Moukhtari A, Cabassa-Hourton C, Farissi M, Savouré A (2020) How does proline treatment promote salt stress tolerance during crop plant development? Front Plant Sci 11:1127. https://doi.org/10.3389/fpls.2020.01127
El-Katony TM, Ward FM, Deyab MA, El-Adl MF (2021) Algal amendment improved yield and grain quality of rice with alleviation of the impacts of salt stress and water stress. Heliyon 7:e07911. https://doi.org/10.1016/j.heliyon.2021.e07911
Elkelish AA, Soliman MH, Alhaithloul HA, El-Esawi MA (2019) Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism. Plant Physiol Biochem 137:144–153. https://doi.org/10.1016/j.plaphy.2019.02.004
Fan S, Han N, Wu H, Jia J, Guo J (2021) Plasma membrane intrinsic protein SlPIP1;7 promotes root growth and enhances drought stress tolerance in transgenic tomato (Solanum lycopersicum) plants. Plant Breeding 140:1102–1114. https://doi.org/10.1111/pbr.12978
Fan S, Wu H, Gong H, Guo J (2022) The salicylic acid mediates selenium-induced tolerance to drought stress in tomato plants. Sci Hortic 300:111092. https://doi.org/10.1016/j.scienta.2022.111092
Freeman JL, Tamaoki M, Stushnoff C, Quinn CF, Cappa JJ, Devonshire J, Fakra SC, Marcus MA, McGrath SP, Van Hoewyk D, Pilon-Smits EA (2010) Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiol 153:1630–1652. https://doi.org/10.1104/pp.110.156570
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Gou T, Yang L, Hu W, Chen X, Zhu Y, Guo J, Gong H (2020a) Silicon improves the growth of cucumber under excess nitrate stress by enhancing nitrogen assimilation and chlorophyll synthesis. Plant Physiol Bioch 152:53–61. https://doi.org/10.1016/j.plaphy.2020.04.031
Gou T, Chen X, Han R, Liu J, Zhu Y, Gong H (2020b) Silicon can improve seed germination and ameliorate oxidative damage of bud seedlings in cucumber under salt stress. Acta Physiol Plant 42:12. https://doi.org/10.1007/s11738-019-3007-6
Gupta M, Gupta S (2017) An overview of selenium uptake, metabolism, and toxicity in plants. Front Plant Sci 7:2074. https://doi.org/10.3389/fpls.2016.02074
Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:701596. https://doi.org/10.1155/2014/701596
Hajiboland R, Rahmat S, Zeinalzadeh N, Farsad-Akhtar N, Hosseinpour-Feizi MA (2019) Senescence is delayed by selenium in oilseed rape plants. J Trace Elem Med Biol 55:96–106. https://doi.org/10.1016/j.jtemb.2019.06.005
Han N, Fan S, Zhang T, Sun H, Zhu Y, Gong H, Guo J (2020) SlHY5 is a necessary regulator of the cold acclimation response in tomato. Plant Growth Regul 91:1–12. https://doi.org/10.1007/s10725-020-00583-7
Jia H, Song Z, Wu F, Ma M, Li Y, Han D, Yang Y, Zhang S, Cui H (2018) Low selenium increases the auxin concentration and enhances tolerance to low phosphorous stress in tobacco. Environ Exp Bot 153:127–134. https://doi.org/10.1016/j.envexpbot.2018.05.017
Jiang C, Zu C, Lu D, Zheng Q, Shen J, Wang H, Li D (2017) Effect of exogenous selenium supply on photosynthesis, Na+ accumulation and antioxidative capacity of maize (Zea mays L.) under salinity stress. Sci Rep 7:42039. https://doi.org/10.1038/srep42039
Jiang L, Liu C, Cao H, Chen Z, Yang J, Cao S, Wei Z (2019) The role of cytokinin in selenium stress response in Arabidopsis. Plant Sci 281:122–132. https://doi.org/10.1016/j.plantsci.2019.01.028
Kanai M, Higuchi K, Hagihara T, Konishi T, Ishii T, Fujita N, Nakamura Y, Maeda Y, Yoshiba M, Tadano T (2007) Common reed produces starch granules at the shoot base in response to salt stress. New Phytol 176:572–580. https://doi.org/10.1111/j.1469-8137.2007.02188.x
Kaur S, Nayyar H (2015) Selenium fertilization to salt-stressed mungbean (Vigna radiata L. Wilczek) plants reduces sodium uptake, improves reproductive function, pod set and seed yield. Sci Hortic 197:304–317. https://doi.org/10.1016/j.scienta.2015.09.048
Khalvandi M, Siosemardeh A, Roohi E, Keramati S (2021) Salicylic acid alleviated the effect of drought stress on photosynthetic characteristics and leaf protein pattern in winter wheat. Heliyon 7:e05908. https://doi.org/10.1016/j.heliyon.2021.e05908
Khan MI, 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 Physiol Biochem 80:67–74. https://doi.org/10.1016/j.plaphy.2014.03.026
Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462. https://doi.org/10.3389/fpls.2015.00462
Khare T, Kumar V, Kishor PB (2015) Na+ and Cl- ions show additive effects under NaCl stress on induction of oxidative stress and the responsive antioxidative defense in rice. Protoplasma 252:1149–1165. https://doi.org/10.1007/s00709-014-0749-2
Koo YM, Heo AY, Choi HW (2020) Salicylic acid as a safe plant protector and growth regulator. Plant Pathol J 36:1–10. https://doi.org/10.5423/PPJ.RW.12.2019.0295
Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CM (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147:1358–1368. https://doi.org/10.1104/pp.108.121392
La VH, Lee BR, Zhang Q, Park SH, Islam MT, Kim TH (2019) Salicylic acid improves drought-stress tolerance by regulating the redox status and proline metabolism in Brassica rapa. Hortic Environ Biotechnol 60:31–40. https://doi.org/10.1007/s13580-018-0099-7
Leon J, Shulaev V, Yalpani N, Lawton MA, Raskin I (1995) Benzoicacid 2-hydroxylase, a soluble oxygenase from tobacco, catalyzes salicylic-acid biosynthesis. Proc Natl Acad Sci USA 92:10413–10417. https://doi.org/10.1073/pnas.92.22.10413
Leon-Reyes A, Van der Does D, De Lange ES, Delker C, Wasternack C, Van Wees SC, Ritsema T, Pieterse CM (2010) Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232:1423–1432. https://doi.org/10.1007/s00425-010-1265-z
Lotfi R, Ghassemi-Golezani K, Pessarakli M (2020) Salicylic acid regulates photosynthetic electron transfer and stomatal conductance of mung bean (Vigna radiata L.) under salinity stress. Biocatal Agric Biotechnol 26:101635. https://doi.org/10.1016/j.bcab.2020.101635
Ma X, Zheng J, Zhang X, Hu Q, Qian R (2017) Salicylic acid alleviates the adverse effects of salt stress on dianthus superbus (caryophyllaceae) by activating photosynthesis, protecting morphological structure, and enhancing the antioxidant system. Front Plant Sci 8:600. https://doi.org/10.3389/fpls.2017.00600
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998. https://doi.org/10.1093/jxb/ert208
Naliwajski M, Skłodowska M (2021) The relationship between the antioxidant system and proline metabolism in the leaves of cucumber plants acclimated to salt stress. Cells 10:609. https://doi.org/10.3390/cells10030609
Nemat Alla MM, Badran EG, Mohammed FA, Hassan NM, Abdelhamid MA (2020) Overexpression of Na+-manipulating genes in wheat by selenium is associated with antioxidant enforcement for enhancement of salinity tolerance. Rend Fis Acc Lincei 31:177–187. https://doi.org/10.1007/s12210-019-00868-8
Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116. https://doi.org/10.1126/science.1147113
Puccinelli M, Malorgio F, Pezzarossa B (2017) Selenium enrichment of horticultural crops. Molecules 22:933. https://doi.org/10.3390/molecules22060933
Rady MM, Belal HEE, Gadallah FM, Semida WM (2020) Selenium application in two methods promotes drought tolerance in Solanum lycopersicum plant by inducing the antioxidant defense system. Sci Hortic 266:109290. https://doi.org/10.1016/j.scienta.2020.109290
Rayman MP (2012) Selenium and human health. Lancet 379:1256–1268. https://doi.org/10.1016/S0140-6736(11)61452-9
Riffat A, Ahmad MSA (2018) Changes in organic and inorganic osmolytes of maize (Zea mays L.) by sulfur application under salt stress conditions. J Agric Sci 10:543–561. https://doi.org/10.5539/jas.v10n12p543
Shamsul H, Qaiser H, Alyemeni MN, Wani AS, Pichtel J, Aqil A (2012) Role of proline under changing environments: A review. Plant Signal Behav 7:1456–1466. https://doi.org/10.4161/psb.21949
Shan F, Zhang R, Zhang J, Wang C, Lyu X, Xin T, Yan C, Dong S, Ma C, Gong Z (2021) Study on the regulatory effects of GA3 on soybean internode elongation. Plants 10:1737. https://doi.org/10.3390/plants10081737
Shi Y, Zhang Yi, Yao H, Jiawen Wu, Sun H, Gong H (2014) Silicon improves seed germination and alleviates oxidative stress of bud seedlings in tomato under water deficit stress. Plant Physiol Biochem 78:27–36. https://doi.org/10.1016/j.plaphy.2014.02.009
Shi Y, Zhang Y, Han W, Feng R, Hu Y, Guo J, Gong H (2016) Silicon enhances water stress tolerance by improving root hydraulic conductance in Solanum lycopersicum L. Front Plant Sci 7:196. https://doi.org/10.3389/fpls.2016.00196
Shrivastava P, Kumar R (2015) Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131. https://doi.org/10.1016/j.sjbs.2014.12.001
Soltabayeva A, Ongaltay A, Omondi JO, Srivastava S (2021) Morphological, physiological and molecular markers for salt-stressed plants. Plants (Basel) 10:243. https://doi.org/10.3390/plants10020243
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 49:77–83. https://doi.org/10.1007/s10725-006-0019-1
Tamaoki M, Freeman J, Marqusè L, Pilon-Smits E (2008) New insights into the roles of ethylene and jasmonic acid in the acquisition of selenium resistance in plants. Plant Signal Behav 3:865–867. https://doi.org/10.4161/psb.3.10.6050
Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T, Van Wees SC, Pieterse CM (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25:744–761. https://doi.org/10.1105/tpc.112.108548
Wang J, Cappa JJ, Harris JP, Edger PP, Zhou W, Pires JC, Adair M, Unruh SA, Simmons MP, Schiavon M, Pilon-Smits EAH (2018) Transcriptome-wide comparison of selenium hyperaccumulator and nonaccumulator Stanleya species provides new insight into key processes mediating the hyperaccumulation syndrome. Plant Biotechnol J 16:1582–1594. https://doi.org/10.1111/pbi.12897
Wang L, Liu S, Gao M, Wang L, Wang L, Wang Y, Dai L, Zhao J, Liu M, Liu Z (2022) The crosstalk of the salicylic acid and jasmonic acid signaling pathways contributed to different resistance to phytoplasma infection between the two genotypes in Chinese Jujube. Front Microbiol 13:800762. https://doi.org/10.3389/fmicb.2022.800762
Wassie M, Zhang W, Zhang Q, Ji K, Cao L, Chen L (2020) Exogenous salicylic acid ameliorates heat stress-induced damages and improves growth and photosynthetic efficiency in alfalfa (Medicago sativa L.). Ecotoxicol Environ Saf 191:110206. https://doi.org/10.1016/j.ecoenv.2020.110206
Watanabe S, Kojima K, Ide Y, Sasaki S (2000) Effects of saline and osmotic stress on proline and sugar accumulation in Populus euphratica in vitro. Plant Cell Tissue Organ Cult 63:199. https://doi.org/10.1023/A:1010619503680
Wichern F, Islam MR, Hemkemeyer M, Watson C, Joergensen RG (2020) Organic amendments alleviate salinity effects on soil microorganisms and mineralisation processes in aerobic and anaerobic paddy rice soils. Front Sustain Food Syst 4:30. https://doi.org/10.3389/fsufs.2020.00030
Xu W, Cui K, Xu A, Nie L, Huang J, Peng S (2015) Drought stress condition increases root to shoot ratio via alteration of carbohydrate partitioning and enzymatic activity in rice seedlings. Acta Physiol Plant 37:1–11. https://doi.org/10.1007/s11738-014-1760-0
Yang T, Zhu LS, Meng Y, Lv R, Zhou Z, Zhu L, Lin HH, Xi DH (2018) Alpha-momorcharin enhances tobacco mosaic virus resistance in tobacco NN by manipulating jasmonic acid-salicylic acid crosstalk. J Plant Physiol 223:116–126. https://doi.org/10.1016/j.jplph.2017.04.011
Yang Z, Li JL, Liu LN, Xie Q, Sui N (2020) Photosynthetic Regulation under salt stress and salt-tolerance mechanism of sweet sorghum. Front Plant Sci 10:1722. https://doi.org/10.3389/fpls.2019.01722
Yu Z, Duan X, Luo L, Dai S, Ding Z, Xia G (2020) How plant hormones mediate salt stress responses. Trends Plant Sci 25:1117–1130. https://doi.org/10.1016/j.tplants.2020.06.008
Zahedi SM, Abdelrahman M, Hosseini MS, Hoveizeh NF, Tran LP (2019) Alleviation of the effect of salinity on growth and yield of strawberry by foliar spray of selenium-nanoparticles. Environ Pollut 253:246–258. https://doi.org/10.1016/j.envpol.2019.04.078
Zhang XK, Zhou QH, Cao JH, Yu BJ (2011) Differential Cl−/Salt tolerance and NaCl-induced alternations of tissue and cellular ion fluxes in Glycine max, Glycine soja and their hybrid seedlings. J Agron Crop Sci 197:329–339. https://doi.org/10.1111/j.1439-037X.2011.00467.x
Zhang M, Smith JA, Harberd NP, Jiang C (2016) The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol Biol 91:651–659. https://doi.org/10.1007/s11103-016-0488-1
Zhang L, Li D, Yao Y, Zhang S (2020) H2O2, Ca2+, and K+ in subsidiary cells of maize leaves are involved in regulatory signaling of stomatal movement. Plant Physiol Biochem 152:243–251. https://doi.org/10.1016/j.plaphy.2020.04.045
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445. https://doi.org/10.1016/s1369-5266(03)00085-2
Zhu Z, Zhang Y, Liu J, Chen Y, Zhang X (2018) Exploring the effects of selenium treatment on the nutritional quality of tomato fruit. Food Chem 252:9–15. https://doi.org/10.1016/j.foodchem.2018.01.064
Zhu Y, Jiang X, Zhang J, He Y, Zhu X, Zhou X, Gong H, Yin J, Liu Y (2020) Silicon confers cucumber resistance to salinity stress through regulation of proline and cytokinins. Plant Physiol Biochem 156:209–220. https://doi.org/10.1016/j.plaphy.2020.09.014
Zsiros O, Nagy V, Párducz Á, Nagy G, Ünnep R, El-Ramady H, Prokisch J, Lisztes-Szabó Z, Fári M, Csajbók J, Tóth SZ, Garab G, Domokos-Szabolcsy É (2019) Effects of selenate and red Se-nanoparticles on the photosynthetic apparatus of Nicotiana tabacum. Photosynth Res 139:449–460. https://doi.org/10.1007/s11120-018-0599-4
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Hong Wu and Shuya Fan. HG analyzed the original data. The first draft of the manuscript was written by Jia Guo.
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Wu, H., Fan, S., Gong, H. et al. Roles of salicylic acid in selenium-enhanced salt tolerance in tomato plants. Plant Soil 484, 569–588 (2023). https://doi.org/10.1007/s11104-022-05819-1
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DOI: https://doi.org/10.1007/s11104-022-05819-1