The Effects of Exogenous Salicylic Acid on Endogenous Phytohormone Status in Hordeum vulgare L. under Salt Stress

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).

[1]  Brian C. Baldwin,et al.  The International Fund for Agricultural Development , 2021, Food for All.

[2]  S. V. Van Wees,et al.  Multiple levels of crosstalk in hormone networks regulating plant defense , 2020, The Plant journal : for cell and molecular biology.

[3]  M. Strnad,et al.  Timing-dependent effects of salicylic acid treatment on phytohormonal changes, ROS regulation, and antioxidant defense in salinized barley (Hordeum vulgare L.) , 2020, Scientific Reports.

[4]  R. Lotfi,et al.  Salicylic acid regulates photosynthetic electron transfer and stomatal conductance of mung bean (Vigna radiata L.) under salinity stress , 2020 .

[5]  L. Tran,et al.  Salicylic Acid-Mediated Enhancement of Photosynthesis Attributes and Antioxidant Capacity Contributes to Yield Improvement of Maize Plants Under Salt Stress , 2018, Journal of Plant Growth Regulation.

[6]  O. Novák,et al.  Correlations between Phytohormones and Drought Tolerance in Selected Brassica Crops: Chinese Cabbage, White Cabbage and Kale , 2018, International journal of molecular sciences.

[7]  D. R. Hoagland,et al.  The Water-Culture Method for Growing Plants Without Soil , 2018 .

[8]  Xiaohua Ma,et al.  Salicylic Acid Alleviates the Adverse Effects of Salt Stress on Dianthus superbus (Caryophyllaceae) by Activating Photosynthesis, Protecting Morphological Structure, and Enhancing the Antioxidant System , 2017, Front. Plant Sci..

[9]  K. Dehesh,et al.  ORA59 and EIN3 interaction couples jasmonate-ethylene synergistic action to antagonistic salicylic acid regulation of PDF expression. , 2017, Journal of integrative plant biology.

[10]  Jianjun Chen,et al.  Salt stress induced soybean GmIFS1 expression and isoflavone accumulation and salt tolerance in transgenic soybean cotyledon hairy roots and tobacco , 2017, Plant Cell, Tissue and Organ Culture (PCTOC).

[11]  K. R. Reddy,et al.  Abscisic Acid and Abiotic Stress Tolerance in Crop Plants , 2016, Front. Plant Sci..

[12]  A. Kohli,et al.  Exploring Jasmonates in the Hormonal Network of Drought and Salinity Responses , 2015, Front. Plant Sci..

[13]  H. Ryu,et al.  Plant hormones in salt stress tolerance , 2015, Journal of Plant Biology.

[14]  H. Ichikawa,et al.  Elevated levels of CYP94 family gene expression alleviate the jasmonate response and enhance salt tolerance in rice. , 2015, Plant & cell physiology.

[15]  Yuanyuan Hu,et al.  Salicylic Acid Alleviates the Adverse Effects of Salt Stress in Torreya grandis cv. Merrillii Seedlings by Activating Photosynthesis and Enhancing Antioxidant Systems , 2014, PloS one.

[16]  C. Wasternack,et al.  UHPLC-MS/MS based target profiling of stress-induced phytohormones. , 2014, Phytochemistry.

[17]  K. Kosová,et al.  Dynamics of cold acclimation and complex phytohormone responses in Triticum monococcum lines G3116 and DV92 differing in vernalization and frost tolerance level , 2014 .

[18]  J. Shah,et al.  Arabidopsis thaliana FLOWERING LOCUS D is required for systemic acquired resistance. , 2013, Molecular plant-microbe interactions : MPMI.

[19]  F. Nasibi,et al.  Interaction of salicylic acid and ethylene and their effects on some physiological and biochemical parameters in canola plants (Brassica napus L.) , 2013, Photosynthetica.

[20]  L. Zolla,et al.  Crosstalk between salicylic acid and jasmonate in Arabidopsis investigated by an integrated proteomic and transcriptomic approach. , 2013, Molecular bioSystems.

[21]  Z. Rengel,et al.  Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel , 2013, Journal of experimental botany.

[22]  K. Akimitsu,et al.  Jasmonic acid and salicylic acid activate a common defense system in rice , 2013, Plant signaling & behavior.

[23]  J. Pichtel,et al.  Role of proline under changing environments , 2012, Plant signaling & behavior.

[24]  E. Balázs,et al.  Effect of light on the gene expression and hormonal status of winter and spring wheat plants during cold hardening. , 2012, Physiologia plantarum.

[25]  K. Kosová,et al.  Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. , 2012, Journal of plant physiology.

[26]  J. Thomas-Oates,et al.  Initial water deficit effects on Lupinus albus photosynthetic performance, carbon metabolism, and hormonal balance: metabolic reorganization prior to early stress responses. , 2011, Journal of experimental botany.

[27]  K. Shinozaki,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[C][W] , 2011, Plant Cell.

[28]  E. Blumwald,et al.  Hormone balance and abiotic stress tolerance in crop plants. , 2011, Current opinion in plant biology.

[29]  M. Javid,et al.  The Role of Phytohormones in Alleviating Salt Stress in Crop Plants , 2011 .

[30]  I. Prášil,et al.  Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. , 2010, Journal of plant physiology.

[31]  I. Turkan,et al.  The role of antioxidant defense systems at differential salt tolerance of Hordeum marinum Huds. (sea barleygrass) and Hordeum vulgare L. (cultivated barley) , 2010 .

[32]  S. Pascale,et al.  Contrasting Effects of GA3 Treatments on Tomato Plants Exposed to Increasing Salinity , 2010, Journal of Plant Growth Regulation.

[33]  M. Strnad,et al.  Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. , 2009, Talanta.

[34]  M. Strnad,et al.  Profiling ABA metabolites in Nicotiana tabacum L. leaves by ultra-performance liquid chromatography-electrospray tandem mass spectrometry. , 2009, Talanta.

[35]  P. Saxena,et al.  Effect of salicylic acid on proline metabolism in lentil grown under salinity stress , 2009 .

[36]  M. Strnad,et al.  Micropropagation of Wild Service Tree (Sorbus torminalis [L.] Crantz): The Regulative Role of Different Aromatic Cytokinins During Organogenesis , 2009, Journal of Plant Growth Regulation.

[37]  V. Martínez,et al.  Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants , 2008, Journal of experimental botany.

[38]  S. Ullrich,et al.  Barley for food: Characteristics, improvement, and renewed interest , 2008 .

[39]  M. Yusuf,et al.  Effect of salicylic acid on salinity-induced changes in Brassica juncea. , 2008, Journal of integrative plant biology.

[40]  M. Strnad,et al.  Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. , 2008, Phytochemistry.

[41]  M. Ashraf,et al.  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? , 2007, Journal of plant physiology.

[42]  T. Colmer,et al.  Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents. , 2007, Journal of experimental botany.

[43]  K. Shokat,et al.  Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. , 2006, The Plant journal : for cell and molecular biology.

[44]  S. Rosahl,et al.  The Role of Salicylic Acid and Jasmonic Acid in Pathogen Defence , 2006, Plant biology.

[45]  M. El-Tayeb Response of barley grains to the interactive e.ect of salinity and salicylic acid , 2005, Plant Growth Regulation.

[46]  Paul R. Ebert,et al.  Antagonistic Interaction between Abscisic Acid and Jasmonate-Ethylene Signaling Pathways Modulates Defense Gene Expression and Disease Resistance in Arabidopsis , 2004, The Plant Cell Online.

[47]  T. Setter,et al.  Abscisic acid accumulation and osmotic adjustment in cassava under water deficit , 2004 .

[48]  H. Peña-Cortés,et al.  Salt tolerant tomato plants show increased levels of jasmonic acid , 2003, Plant Growth Regulation.

[49]  C. Kao,et al.  The Effect of Polyethylene Glycol on Proline Accumulation in Rice Leaves , 2003, Biologia Plantarum.

[50]  M. Strnad,et al.  Quantitative analysis of cytokinins in plants by liquid chromatography–single-quadrupole mass spectrometry , 2003 .

[51]  A. R. Sakhabutdinova,et al.  Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity , 2003 .

[52]  O. Borsani,et al.  Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. , 2001, Plant physiology.

[53]  H. Ruiz,et al.  CONTRIBUTION OF PROLINE AND INORGANIC SOLUTES TO OSMOTIC ADJUSTMENT IN COTTON UNDER SALT STRESS , 2001 .

[54]  K. Hasenstein,et al.  Effects of Salinity on Endogenous Aba, Iaa, Ja, and Sa in Iris hexagona , 2001, Journal of Chemical Ecology.

[55]  F. Ausubel,et al.  Roles of Salicylic Acid, Jasmonic Acid, and Ethylene in cpr-Induced Resistance in Arabidopsis , 2000, Plant Cell.

[56]  A. Székács,et al.  Immunoassays for plant cytokinins as tools for the assessment of environmental stress and disease resistance , 2000 .

[57]  H. Peña-Cortés,et al.  Inhibition of wound-induced accumulation of allene oxide synthase transcripts in flax leaves by aspirin and salicylic acid , 1998, Plant physiology.

[58]  M. V. Boland,et al.  Multivariate Analysis , 1998, Current protocols in cytometry.

[59]  J. R. Dunlap,et al.  NaCI Reduces Indole-3-Acetic Acid Levels in the Roots of Tomato Plants Independent of Stress-Induced Abscisic Acid , 1996, Plant physiology.

[60]  W. Davies,et al.  Stomatal response to abscisic Acid is a function of current plant water status. , 1992, Plant physiology.

[61]  D. Kuiper,et al.  Actual cytokinin concentrations in plant tissue as an indicator for salt resistance in cereals , 1990, Plant and Soil.

[62]  I. D. Teare,et al.  Rapid determination of free proline for water-stress studies , 1973, Plant and Soil.

[63]  C. Ghoulam,et al.  Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars , 2002 .

[64]  M. Jackson Hormones from roots as signals for the shoots of stressed plants , 1997 .

[65]  I. Raskin Role of Salicylic Acid in Plants , 1992 .