The Effects of Exogenous Salicylic Acid on Endogenous Phytohormone Status in Hordeum vulgare L. under Salt Stress
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.1.01/0.0/0.0/16_019/0000827
the Ministry of Education, Youth and Sports of the Czech Republic from European Regional De-velopment Fund
19-00973S
Internal Grant Agency of Palacký University (IGA_PrF_2021_016)
PubMed
35270088
PubMed Central
PMC8912680
DOI
10.3390/plants11050618
PII: plants11050618
Knihovny.cz E-zdroje
- Klíčová slova
- Hordeum vulgare, barley, phytohormones, salicylic acid, salt stress,
- Publikační typ
- časopisecké články MeSH
Acclimation to salt stress in plants is regulated by complex signaling pathways involving endogenous phytohormones. The signaling role of salicylic acid (SA) in regulating crosstalk between endogenous plant growth regulators' levels was investigated in barley (Hordeum vulgare L. 'Ince'; 2n = 14) leaves and roots under salt stress. Salinity (150 and 300 mM NaCl) markedly reduced leaf relative water content (RWC), growth parameters, and leaf water potential (LWP), but increased proline levels in both vegetative organs. Exogenous SA treatment did not significantly affect salt-induced negative effects on RWC, LWP, and growth parameters but increased the leaf proline content of plants under 150 mM salt stress by 23.1%, suggesting that SA enhances the accumulation of proline, which acts as a compatible solute that helps preserve the leaf's water status under salt stress. Changes in endogenous phytohormone levels were also investigated to identify agents that may be involved in responses to increased salinity and exogenous SA. Salt stress strongly affected endogenous cytokinin (CK) levels in both vegetative organs, increasing the concentrations of CK free bases, ribosides, and nucleotides. Indole-3-acetic acid (IAA, auxin) levels were largely unaffected by salinity alone, especially in barley leaves, but SA strongly increased IAA levels in leaves at high salt concentration and suppressed salinity-induced reductions in IAA levels in roots. Salt stress also significantly increased abscisic acid (ABA) and ethylene levels; the magnitude of this increase was reduced by treatment with exogenous SA. Both salinity and SA treatment reduced jasmonic acid (JA) levels at 300 mM NaCl but had little effect at 150 mM NaCl, especially in leaves. These results indicate that under high salinity, SA has antagonistic effects on levels of ABA, JA, ethylene, and most CKs, as well as basic morphological and physiological parameters, but has a synergistic effect on IAA, which was well exhibited by principal component analysis (PCA).
Faculty of Agriculture Düzce University 81620 Düzce Turkey
Faculty of Science Karadeniz Technical University 61080 Trabzon Turkey
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The Food and Agriculture Organization of the United Nations (FAO), the International Fund for Agricultural Development (IFAD) the World Food Programme (WFP) The State of Food Insecurity in the World 2014. Food and Agriculture Organization of the United Nations; Rome, Italy: 2014.
Aerts N., Pereira Mendes M., Van Wees S.C.M. Multiple levels of crosstalk in hormone networks regulating plant defense. Plant J. 2021;105:489–504. doi: 10.1111/tpj.15124. PubMed DOI PMC
Peleg Z., Blumwald E. Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 2011;14:290–295. doi: 10.1016/j.pbi.2011.02.001. PubMed DOI
Pinheiro C., António C., Ortuño M.F., Dobrev P.I., Hartung W., Thomas-Oates J., Ricardo C.P., Vanková R., Chaves M.M., Wilson J.C. Initial water deficit effects on Lupinus albus photosynthetic performance, carbon metabolism, and hormonal balance: Metabolic reorganization prior to early stress responses. J. Exp. Bot. 2011;62:4965–4974. doi: 10.1093/jxb/err194. PubMed DOI
Pavlović I., Petřík I., Tarkowská D., Lepeduš H., Vujčić Bok V., Radić Brkanac S., Novák O., Salopek-Sondi B. Correlations between Phytohormones and drought tolerance in selected brassica crops: Chinese cabbage, white cabbage and kale. Int. J. Mol. Sci. 2018;19:2866. doi: 10.3390/ijms19102866. PubMed DOI PMC
Albacete A., Ghanem M.E., Martínez-Andújar C., Acosta M., Sánchez-Bravo J., Martínez V., Lutts S., Dodd I.C., Pérez-Alfocea F. Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J. Exp. Bot. 2008;59:4119–4131. doi: 10.1093/jxb/ern251. PubMed DOI PMC
Dobra J., Motyka V., Dobrev P., Malbeck J., Prasil I.T., Haisel D., Gaudinova A., Havlova M., Gubis J., Vankova R. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J. Plant Physiol. 2010;167:1360–1370. doi: 10.1016/j.jplph.2010.05.013. PubMed DOI
Majláth I., Szalai G., Soós V., Sebestyén E., Balázs E., Vanková R., Dobrev P.I., Tari I., Tandori J., Janda T. Effect of light on the gene expression and hormonal status of winter and spring wheat plants during cold hardening. Physiol. Plant. 2012;145:296–314. doi: 10.1111/j.1399-3054.2012.01579.x. PubMed DOI
Kosová K., Prasil I.T., Vitamvas P., Dobrev P., Motyka V., Flokova K., Novák O., Turečková V., Rolčik J., Pešek B., et al. Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J. Plant Physiol. 2012;169:567–576. doi: 10.1016/j.jplph.2011.12.013. PubMed DOI
Vanková R., Kosová K., Dobrev P., Vitamvas P., Trávničková A., Cvikrova M., Pešek B., Gaudinova A., Prerostova S., Musilova J., et al. Dynamics of cold acclimation and complex phytohormone responses in Triticum monococcum lines G3116 and DV92 differing in vernalization and frost tolerance level. Environ. Exp. Bot. 2014;101:12–25. doi: 10.1016/j.envexpbot.2014.01.002. DOI
Shakirova F.M., Sakhabutdinova A.R., Bezrukova M.V., Fatkhutdinova R.A., Fatkhutdinova D.R. Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci. 2003;164:317–322. doi: 10.1016/S0168-9452(02)00415-6. DOI
Raskin I. Role of salicylic acid in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 1992;43:439–463. doi: 10.1146/annurev.pp.43.060192.002255. DOI
Singh V., Roy S., Giri M.K., Chaturvedi R., Chowdhury Z., Shah J., Nandi A.K. Arabidopsis thaliana FLOWERING LOCUS D is required for systemic acquired resistance. Mol. Plant Microbe Interact. 2013;26:1079–1088. doi: 10.1094/MPMI-04-13-0096-R. PubMed DOI
Arfan M., Athar H.R., Ashraf M. Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress? J. Plant Physiol. 2007;164:685–694. doi: 10.1016/j.jplph.2006.05.010. PubMed DOI
Borsani O., Valpuesta V., Botella M.A. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol. 2001;126:1024–1030. doi: 10.1104/pp.126.3.1024. PubMed DOI PMC
Jayakannan M., Bose J., Babourina O., Rengel Z., Shabala S. Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. J. Exp. Bot. 2013;64:2255–2268. doi: 10.1093/jxb/ert085. PubMed DOI PMC
EI-Tayeb M.A. Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul. 2005;4:215–224. doi: 10.1007/s10725-005-4928-1. DOI
Tahjib-Ul-Arif M., Siddiqui M.N., Sohag A.A.M., Sakil M.A., Rahman M.M., Polash M.A.S., Mostofa M.G., Tran L.S.P. Salicylic acid-mediated enhancement of photosynthesis attributes and antioxidant capacity contributes to yield improvement of maize plants under salt stress. J. Plant Growth Regul. 2018;37:1318–1330. doi: 10.1007/s00344-018-9867-y. DOI
Yusuf M., Hasan S.A., Ali B., Hayat S., Fariduddin Q., Ahmad A. Effect of salicylic acid on salinity induced changes in Brassica juncea. J. Integr. Plant Biol. 2008;50:1–4. doi: 10.1111/j.1744-7909.2008.00697.x. PubMed DOI
Lotfi R., Ghassemi-Golezani K., Pessarakli M. Salicylic acid regulates photosynthetic electron transfer and stomatal conductance of mung bean (Vigna radiata L.) under salinity stress. Biocatal. Agric. Biotechnol. 2020;26:101635. doi: 10.1016/j.bcab.2020.101635. DOI
Li T., Hu Y.Y., Du X.H., Tang H., Shen C.H., Wu J.S. Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. PLoS ONE. 2014;9:e109492. doi: 10.1371/journal.pone.0109492. PubMed DOI PMC
Baik B.K., Ullrich S.E. Barley for food: Characteristics, improvement, and renewed interest. J. Cereal Sci. 2008;48:233–242. doi: 10.1016/j.jcs.2008.02.002. DOI
Seckin B., Türkan I., Sekmen A.H., Ozfidan C. The role of antioxidant defense system at differential salt tolerance of Hordeum marinum Huds. (sea barleygrass) and Hordeum vulgare L. (cultivated barley) Environ. Exp. Bot. 2010;69:76–85. doi: 10.1016/j.envexpbot.2010.02.013. DOI
Torun H., Novák O., Mikulík J., Pěnčík A., Strnad M., Ayaz F.A. Timing-dependent effects of salicylic acid treatment on phytohormonal changes, ROS regulation, and antioxidant defense in salinized barley (Hordeum vulgare L.) Sci. Rep. 2020;10:13886. doi: 10.1038/s41598-020-70807-3. PubMed DOI PMC
FAO . Agribusiness Handbook: Barley, Malt and Beer. Food and Agriculture Organization of the United Nations; Rome, Italy: 2009.
Sah S.K., Reddy K.R., Li J. Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 2016;7:571. doi: 10.3389/fpls.2016.00571. PubMed DOI PMC
Mardia L.V., Keni J.T., Bibby J.M. Multivariate Analysis. Academic Press; London, UK: 1979. p. 521.
Maggio A., Barbieri G., Raimondi G., De Pascale S. Contrasting effects of GA3 treatments on tomato plants exposed to increasing salinity. J. Plant Growth Regul. 2010;29:63–72. doi: 10.1007/s00344-009-9114-7. DOI
Jackson M. Hormones from roots as signal for the shoots of stressed plants. Trends Plant Sci. 1997;2:22–28. doi: 10.1016/S1360-1385(96)10050-9. DOI
Ma X., Zheng J., Zhang X., Hu Q., Qian R. 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. 2017;8:600. doi: 10.3389/fpls.2017.00600. PubMed DOI PMC
Islam S., Malik A.I., Islam A.K., Colmer T.D. Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents. J. Exp. Bot. 2007;58:1219–1229. doi: 10.1093/jxb/erl293. PubMed DOI
Jia T.J., An J., Liu Z., Yu B.J., Chen J.J. Salt stress induced soybean GmIFS1 expression and isoflavone accumulation and salt tolerance in transgenic soybean cotyledon hairy roots and tobacco. Plant Cell Tiss. Organ Cult. 2017;128:469–477. doi: 10.1007/s11240-016-1124-0. DOI
Meloni D.A., Oliva M.A., Ruiz H.A., Martinez C.A. Contribution of proline and inorganic solutes to osmotic adjustment in cotton under salt stress. J. Plant Nutr. 2001;24:599–612. doi: 10.1081/PLN-100104983. DOI
Ghoulam C.F., Ahmed F., Khalid F. Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ. Exp. Bot. 2001;47:39–50. doi: 10.1016/S0098-8472(01)00109-5. DOI
Misra N., Saxena P. Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci. 2009;177:181–189. doi: 10.1016/j.plantsci.2009.05.007. DOI
Hsu S.Y., Hsu Y.T., Kao C.H. The effect of polyethylene glycol on proline accumulation in rice leaves. Biol. Plant. 2003;46:73–78. doi: 10.1023/A:1022362117395. DOI
Hayat S., Hayat Q., Alyemeni M.S., Wani A.S., Pichtel J., Ahmad A. Role of proline under changing environments. Plant Signal. Behav. 2012;7:1456–1466. doi: 10.4161/psb.21949. PubMed DOI PMC
Ryu H., Cho Y. Plant hormones in salt stress tolerance. J. Plant Sci. 2015;58:147–155. doi: 10.1007/s12374-015-0103-z. DOI
Dunlap J.R., Binzel M.L. NaCl reduces indole-3-acetic acid levels in the roots of tomato plants independent of stress-induced abscisic acid. Plant Physiol. 1996;112:379–384. doi: 10.1104/pp.112.1.379. PubMed DOI PMC
Wang Y., Mopper S., Hasentein K.H. Effects of salinity on endogenous ABA, IAA, JA, and SA in Iris hexagona. J. Chem. Ecol. 2001;27:327–342. doi: 10.1023/A:1005632506230. PubMed DOI
Székács A., Hegedüs G., Tóbiás I., Pogány M., Barna B. Immunoassays for plant cytokinins as tools for the assessment of environmental stress and disease resistance. Anal. Chim. Acta. 2000;42:135–146. doi: 10.1016/S0003-2670(00)01046-1. DOI
Javid M.G., Sorooshzadeh A., Moradi F., Sanavy S.A.M.M., Allahdadi I. The role of phytohormones in alleviating salt stress in crop plants. Aust. J. Crop Sci. 2011;5:726–734.
Kuiper D., Schuit J., Kuiper P.J.C. Actual cytokinin concentrations in plant tissue as an indicator for salt resistance in cereals. Plant Soil. 1990;123:243–250. doi: 10.1007/BF00011276. DOI
Nishiyama R., Watanabe Y., Fujita Y., Le D.T., Kojima M., Werner T., Vankova R., Yamaguchi-Shinozaki K., Shinozaki K., Kakimoto T., et al. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell. 2011;23:2169–2183. doi: 10.1105/tpc.111.087395. PubMed DOI PMC
Tardieu F., Davies W.J. Stomatal response to abscisic acid is a function of current plant water status. Plant Physiol. 1992;98:540–545. doi: 10.1104/pp.98.2.540. PubMed DOI PMC
Alves A.A.C., Setter T.L. Abscisic acid accumulation and osmotic adjustment in cassava under water deficit. Environ. Exp. Bot. 2004;5:259–271. doi: 10.1016/j.envexpbot.2003.11.005. DOI
Pedranzani H., Racagni G., Alemano S., Miersch O., Ramirez I., Pena-Cortes H., Taleisnik E., Machado-Domenech E., Abdala G. Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul. 2003;41:149–158. doi: 10.1023/A:1027311319940. DOI
Kurotani K., Hayashi K., Hatanaka S., Toda Y., Ogawa D., Ichikawa H., Ishimaru Y., Tashita R., Suzuki T., Ueda M., et al. Elevated levels of CYP94 family gene expression alleviate the jasmonate response and enhance salt tolerance in rice. Plant Cell Physiol. 2015;56:779–789. doi: 10.1093/pcp/pcv006. PubMed DOI
Halim V.A., Vess A., Scheel D., Rosah S. The role of salicylic acid and jasmonic acid in pathogen defence. Plant Biol. 2006;8:307–313. doi: 10.1055/s-2006-924025. PubMed DOI
Tamaoki D., Seo S., Yamada S., Kano A., Miyamoto A., Shishido H., Miyoshi S., Taniguchi S., Akimitsu K., Gomi K. Jasmonic acid and salicylic acid activate a common defense system in rice. Plant Signal. Behav. 2013;8:e24260. doi: 10.4161/psb.24260. PubMed DOI PMC
Proietti S., Bertini L., Timperio A.M., Zolla L., Caporale C., Caruso C. Crosstalk between salicylic acid and jasmonate in Arabidopsis investigated by an integrated proteomic and transcriptomic approach. Mol Biosyst. 2013;9:1169–1187. doi: 10.1039/c3mb25569g. PubMed DOI
Riemann M., Dhakarey R., Hazman M., Miro B., Kohli A., Nick P. Exploring jasmonates in the hormonal network of drought and salinity responses. Front. Plant Sci. 2015;6:1077. doi: 10.3389/fpls.2015.01077. PubMed DOI PMC
Brodersen P., Petersen M., Bjørn Nielsen H., Zhu S., Newman M.A., Shokat K.M., Rietz S., Parker J., Mundy J. Arabidopsis MAPkinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J. 2006;47:532–546. doi: 10.1111/j.1365-313X.2006.02806.x. PubMed DOI
Harms K., Ramirez I., Penacortes H. Inhibition of wound-induced accumulation of allene oxide synthase transcripts in flax leaves by aspirin and salicylic acid. Plant Physiol. 1998;118:1057–1065. doi: 10.1104/pp.118.3.1057. PubMed DOI PMC
Anderson J.P., Badruzsaufari E., Schenk P.M., Manners J.M., Desmond O.J., Ehlert C., Maclean D.J., Ebert P.R., Kazan K. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell. 2004;16:3460–3479. doi: 10.1105/tpc.104.025833. PubMed DOI PMC
Tirani M.M., Nasibi F., Kalantari K.M. Interaction of salicylic acid and ethylene and their effects on some physiological and biochemical parameter in canola plants (Brassica napus L.) Photosynthetica. 2013;51:411–418. doi: 10.1007/s11099-013-0041-2. DOI
Clarke J.D., Volko S.M., Ledford H., Ausubel F.M., Dong X.N. Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell. 2000;12:2175–2190. doi: 10.1105/tpc.12.11.2175. PubMed DOI PMC
He X., Jiang J.S., Wang C.Q., Dehesh K. ORA59 and EIN3 interaction couples jasmonate-ethylene synergistic action to antagonistic salicylic acid regulation of PDF expression. J. Integr. Plant Biol. 2017;59:275–287. doi: 10.1111/jipb.12524. PubMed DOI PMC
Hoagland D.R., Arnon D.I. The water culture method for growing plants without soil. Calif. Agric. Exp. Stn. Circ. 1950;347:1–32.
Bates L.S., Waldren R.P., Teare I.D. Rapid determination of free proline for water stres studies. Plant Soil. 1973;39:205–207. doi: 10.1007/BF00018060. DOI
Pěnčík A., Rolcik J., Novák O., Magnus V., Bartak P., Buchtik R., Salopek-Sondi B., Strnad M. Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. Talanta. 2009;80:651–655. doi: 10.1016/j.talanta.2009.07.043. PubMed DOI
Novák O., Tarkowski P., Tarkowska D., Dolezal K., Lenobel R., Strnad M. Quantitative analysis of cytokinins in plants by liquid chromatography/single-quadrupole mass spectrometry. Anal. Chim. Acta. 2003;480:207–218. doi: 10.1016/S0003-2670(03)00025-4. DOI
Novák O., Hauserová E., Amakorova P., Dolezal K., Strnad M. Cytokinin profiling in plant tissues using ultra-performance liquid chromatography–electrospray tandem mass spectrometry. Phytochemistry. 2008;69:2214–2224. doi: 10.1016/j.phytochem.2008.04.022. PubMed DOI
Turečková V., Novák O., Strnad M. Profiling ABA metabolites in Nicotiana tabacum L. leaves by ultra-performance liquid chromatography–electrospray tandem mass spectrometry. Talanta. 2009;80:390–399. doi: 10.1016/j.talanta.2009.06.027. PubMed DOI
Floková K., Tarkowská D., Miersch O., Strnad M., Wasternack C., Novák O. UHPLC–MS/MS based target profiling of stress-induced phytohormones. Phytochemistry. 2014;105:147–157. doi: 10.1016/j.phytochem.2014.05.015. PubMed DOI
Malá J., Máchová P., Cvrčková H., Karady M., Novák O., Mikulík J., Hauserová E., Greplová J., Strnad M., Doležal K. Micropropagation of wild service tree (Sorbus torminalis [L.] Crantz): The regulative role of different aromatic cytokinins during organogenesis. J. Plant Growth Regul. 2009;28:341–348. doi: 10.1007/s00344-009-9099-2. DOI
The Phenolics and Antioxidant Properties of Black and Purple versus White Eggplant Cultivars