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Exogenous Salicylic Acid Improves Photosynthetic and Antioxidant Capacities and Alleviates Adverse Effects of Cherry Rootstocks Under Salt Stress

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Abstract

Salt stress affects the physiological processes and morphological structure of plants, thereby inhibiting plant growth and development and reducing the fruit yield and quality. Most cherry rootstocks are sensitive to excessive salt and alkaline conditions. Salicylic acid (SA) plays a role in the response to various abiotic stresses. To determine the effects of SA on the resistance of cherry rootstocks to salt stress, a salt environment was simulated by watering with a 100-mM NaCl solution and then spraying leaves with 1.0-mM SA. Salt treatment significantly decreased the photosynthetic rate (Pn) and ratio of variable fluorescence to maximum fluorescence (Fv/Fm) of cherry rootstocks, whereas SA application increased the Pn and Fv/Fm in the salt stress with SA-treat group. Meanwhile, SA reduces the accumulation of Na+ and H2O2 in leaves. Additionally, the activities of antioxidant enzyme (peroxidase, catalase, and superoxide dismutase) were increased under salt stress, and this increase was more obvious under salt stress with SA application treatment, indicating SA contribution in improving the salt tolerance. RNA-seq analysis of cherry rootstocks treated with 1.0-mM SA, 100-mM NaCl, and both 1.0-mM SA with 100-mM NaCl, revealed 537, 298, and 521 significantly differentially expressed genes (DEGs), respectively. The main DEGs were phytohormone-related genes, stress-related transcription factors, Ca2+ signaling-related genes, and other functional protein-related genes. Overall, our study contributes to the understanding of the molecular mechanisms of SA-induced salt tolerance in cherry rootstocks.

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References

  • Aerts N, Pereira Mendes M, Van Wees SCM (2021) Multiple levels of crosstalk in hormone networks regulating plant defense. Plant J 105:489–504

    Article  CAS  PubMed  Google Scholar 

  • Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal RM (2017) Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiol Mol Biol Pla 23:731–744

    Article  Google Scholar 

  • Alam M, Sharmin S, Nabi Z, Mondal SI, Islam S, Nayeem SB, Shoyaib M, Khan H (2010) A putative leucine-rich repeat receptor-like kinase of jute involved in stress response. Plant Mol Biol Rep 28:394–402

    Article  CAS  Google Scholar 

  • Amin B, Atif MJ, Wang X, Meng H, Ghani MI, Ali M, Ding Y, Li X, Cheng Z (2021) Effect of low temperature and high humidity stress on physiology of cucumber at different leaf stages. Plant Biol 23(5):785–796

    Article  CAS  PubMed  Google Scholar 

  • Amin B, Atif MJ, Meng H, Ghani MI, Ali M, Wang X, Ding Y, Li X, Cheng Z (2023) Biochemical and physiological responses of Cucumis sativus cultivars to different combinations of low-temperature and high humidity. J Plant Growth Regul 42(1):390–406

    Article  CAS  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arfan M, Athar HR, Ashraf M (2007) 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? Plant Physiol 6:685–694

    Article  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141(2):391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986

    Article  CAS  PubMed  Google Scholar 

  • Bailey-Serres J, Parker JE, Ainsworth EA, Oldroyd GED, Schroeder JI (2019) Genetic strategies for improving crop yields. Nature 575:109–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baillo EH, Kimotho RN, Zhang Z, Xu P (2019) Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes 10:771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolhar-Nordenkampf HR, Long SP, Baker NR, Oquist G, Leichner EG (1989) Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current instrumentation. Funct Ecol 3:497–514

    Article  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    Article  CAS  PubMed  Google Scholar 

  • Chandrasekaran M, Chanratana M, Kim K, Seshadri S, Sa T (2019) Impact of arbuscular mycorrhizal fungi on photosynthesis, water status, and gas exchange of plants under salt stress–a meta-analysis. Front Plant Sci 10:457

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Ren Y, Zhang G, An J, Yang J, Yong W, Wei W (2018) Overexpression of the wheat expansin gene TaEXPA2 improves oxidative stress tolerance in transgenic Arabidopsis plants. Plant Physiol Bioch 124:190–198

    Article  CAS  Google Scholar 

  • Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signaling in plant responses to abiotic stress. J Exp Biol 217:67–75

    Article  CAS  PubMed  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Env Sci-Switz 2:53

    Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:6

    Article  Google Scholar 

  • Dubey RS (2018) Photosynthesis in plants under stressful conditions. In: Pessarakli M (ed) Handbook of photosynthesis. CRC Press, Boca Raton, pp 629–649

    Chapter  Google Scholar 

  • Durner J, Shah J, Klessig DF (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2(7):266–274

    Article  Google Scholar 

  • El-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45:215–224

    Article  CAS  Google Scholar 

  • Farouk S, Elhindi KM, Alotaibi MA (2020) Silicon supplementation mitigates salinity stress on Ocimum basilicum L. via improving water balance, ion homeostasis, and antioxidant defense system. Ecotox Environ Safe. 206:111396

    Article  CAS  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. P Natl Acad Sci 106(20):8380–8385

    Article  CAS  Google Scholar 

  • Gao M, Gan H, Li Q, Li B, Chu J (2018) The effect of exogenous salicylic acid on the physiological characteristics of Ulmus pumila plantlet under NaCl stress. For Res 31(6):138–143

    Google Scholar 

  • Ghasemi N, Omidi H, Bostani A (2021) Morphological properties of Catharanthus roseus L. seedlings affected by priming techniques under natural salinity stress. J Plant Growth Regul 40(2):550–557

    Article  CAS  Google Scholar 

  • Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164(6):728–736

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Xu CB, Sun XJ, Zheng HU, Fan SJ, Jiang QY, Zhang H (2018) TaSAUR78 enhances multiple abiotic stress tolerance by regulating the interacting gene TaVDAC1. J Integr Agr 18(12):2682–2690

    Article  Google Scholar 

  • Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1787

    Article  PubMed  PubMed Central  Google Scholar 

  • Hara M, Furukawa J, Sato A, Mizoguchi T, Miura K (2012) Abiotic stress and role of salicylic acid in plants. In: Prasad MNV (ed) Parvaiz Ahmad. Abiotic stress responses in plants. Springer, New York, pp 235–251

    Google Scholar 

  • Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25

    Article  CAS  Google Scholar 

  • Horvath E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26(3):290–300

    Article  CAS  Google Scholar 

  • Hu W, Yan Y, Shi H, Liu J, Miao H, Tie W, Ding Z, Ding Xu, Wu C, Liu Y, Wang J, Xu B, Jin Z (2017) The core regulatory network of the abscisic acid pathway in banana: genome-wide identification and expression analyses during development, ripening, and abiotic stress. BMC Plant Bio 17(1):1–16

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jia H, Jiu S, Zhang C, Wang C, Tariq P, Liu Z, Wang B, Cui L, Fang J (2016) Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress ripening transcription factor. Plant Biotechnol J 14:2045–2065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jini D, Joseph B (2017) Physiological mechanism of salicylic acid for alleviation of salt stress in rice. Rice Sci 24(2):97–108

    Article  Google Scholar 

  • Jiu S, Xu Y, Wang J, Wang L, Wang S, Ma C, Guan L, Abdullah M, Zhao M, Xu W, Ma W, Zhang C (2019) Genome-wide identification, characterization, and transcript analysis of the TCP transcription factors in Vitis vinifera. Front Genet 10:1276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiu S, Xu Y, Wang J, Wang L, Liu X, Sun W, Sabir IA, Ma C, Xu W, Wang S, Abdullah M, Zhang C (2020) The cytochrome P450 monooxygenase inventory of grapevine (Vitis Vinifera L.): Genome-wide identification, evolutionary characterization and expression analysis. Front Genet 11:44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plantarum 74(3):566–574

    Article  CAS  Google Scholar 

  • Ku YS, Sintaha M, Cheung MY, Lam HM (2018) Plant hormone signaling crosstalks between biotic and abiotic stress responses. Int J Mol Sci 19(10):3206

    Article  PubMed  PubMed Central  Google Scholar 

  • Kudla J, Batistič O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22(3):541–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lan J, Lin Q, Zhou C, Ren Y, Liu X, Miao R, Jing R, Mou C, Nguyen T, Zhu X, Wang Q, Zhang X, Guo X, Liu S, Jiang L, Wan J (2020) Small grain and semi-dwarf 3, a WRKY transcription factor, negatively regulates plant height and grain size by stabilizing SLR1 expression in rice. Plant Mol Biol 104(4):429–450

    Article  CAS  PubMed  Google Scholar 

  • Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35(1):53–60

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Kim SG, Park CM (2010) Salicylic acid promotes seed germination under high salinity by modulating antioxidant activity in Arabidopsis. New Phytol 188(2):626–637

    Article  CAS  PubMed  Google Scholar 

  • Li T, Hu Y, Du X, Tang H, Shen C, Wu J (2014) Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. PLoS ONE 9(10):e109492

    Article  PubMed  PubMed Central  Google Scholar 

  • Li M, Zhang K, Sun Y, Cui H, Cao S, Yan L, Xu M (2018) Growth, physiology, and transcriptional analysis of two contrasting Carex rigescens genotypes under salt stress reveals salt-tolerance mechanisms. J Plant Physiol 229:77–88

    Article  CAS  PubMed  Google Scholar 

  • Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochem Bioph Res Co 495:286–291

    Article  CAS  Google Scholar 

  • Liu L, Wang B (2021) Protection of halophytes and their uses for cultivation of saline-alkali soil in China. Biology 10(5):353

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu W, Zhang Y, Yuan X, Xuan Y, Gao Y, Yan Y (2016) Exogenous salicylic acid improves salinity tolerance of Nitraria tangutorum. Russ J Plant Physiol 63(1):132–142

    Article  CAS  Google Scholar 

  • Liu F, Huang N, Wang L, Ling H, Sun T, Ahmad W, Muhammad K, Guo J, Xu L, Gao S, Que Y, Su Y (2018) A novel L-ascorbate peroxidase 6 gene, ScAPX6, plays an important role in the regulation of response to biotic and abiotic stresses in sugarcane. Front Plant Sci 8:2262

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Pi B, Du Z, Yang T, Gu M, Sun S, Yu B (2022a) The transcription factor GmbHLH3 confers Cl−/salt tolerance to soybean by upregulating GmCLC1 expression for maintenance of anion homeostasis. Environ Exp Bot 194:104755

    Article  CAS  Google Scholar 

  • Liu Z, Ma C, Hou L, Wu X, Wang D, Zhang L, Liu P (2022b) Exogenous SA affects rice seed germination under salt stress by regulating Na+/K+ balance and endogenous GAs and ABA homeostasis. Int J Mol Sci 23(6):3293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu C, Vonshak A (1999) Characterization of PSII photochemistry in salt-adapted cells of cyanobacterium Spirulina platensis. New Phytol 141(2):231–239

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma S, Zhou X, Jahan MS, Guo S, Tian M, Zhou R, Liu H, Feng B, Shu S (2022) Putrescine regulates stomatal opening of cucumber leaves under salt stress via the H2O2-mediated signaling pathway. Plant Physiol Bioch 170:87–97

    Article  CAS  Google Scholar 

  • Magnani R, Dirk L, Trievel RC, Houtz RL (2010) Calmodulin methyltransferase is an evolutionarily conserved enzyme that trimethylates Lys-115 in calmodulin. Nat Commun 1:43

    Article  PubMed  Google Scholar 

  • Mansouri M, Naghavi MR, Alizadeh H, Mohammadi-Nejad G, Mousavi SA, Salekdeh GH, Tada Y (2019) Transcriptomic analysis of Aegilops tauschii during long-term salinity stress. Funct Integr Genomic 19(1):13–28

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyake C (2010) Alternative electron flows (water–water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51(12):1951–1963

    Article  CAS  PubMed  Google Scholar 

  • Molina A, Bueno P, Marín MC, Rodríguez-Rosales MP, Belver A, Venema K, Donaire JP (2002) Involvement of endogenous salicylic acid content, lipoxygenase and antioxidant enzyme activities in the response of tomato cell suspension cultures to NaCl. New Phytol 156(3):409–415

    Article  CAS  PubMed  Google Scholar 

  • Munns R (2007) Prophylactively parking sodium in the plant. New Phytol 176:501–504

    Article  CAS  PubMed  Google Scholar 

  • Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168(8):807–815

    Article  CAS  PubMed  Google Scholar 

  • Neto A, Prisco JT, Enéas-Filho J, Enéas-Filho J, Abreu C, 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. Environ Exp Bot 56(1):87–94

    Article  Google Scholar 

  • Okumura T, Nomoto Y, Kobayashi K, Suzuki T, Takatsuka H, Ito M (2021) MYB3R-mediated active repression of cell cycle and growth under salt stress in Arabidopsis thaliana. J Plant Res 134(2):261–277

    Article  CAS  PubMed  Google Scholar 

  • Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2014) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 202(1):35–49

    Article  PubMed  Google Scholar 

  • Pandey N, Ranjan A, Pant P, Tripathi RK, Ateek F, Pandey HP, Patre UV, Sawant SV (2013) CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14(1):1–23

    Article  Google Scholar 

  • Papadakis IE, Veneti G, Chatzissavvidis C, Sotiropoulos TE, Dimassi KN, Therios IN (2007) Growth, mineral composition, leaf chlorophyll and water relationships of two cherry varieties under NaCl-induced salinity stress. Soil Sci Plant Nutr 53(3):252–258

    Article  CAS  Google Scholar 

  • Quan J, Meng S, Guo E, Zhang S, Zhao Z, Yang X (2017) De novo sequencing and comparative transcriptome analysis of adventitious root development induced by exogenous indole-3-butyric acid in cuttings of tetraploid black locust. BMC Genomics 18:1–14

    Article  Google Scholar 

  • Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu J, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63(3):417–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Santos AP, Belfiore C, Úrbez C, Ferrando A, Blázquez MA, Farías ME (2023) Extremophiles as plant probiotics to promote germination and alleviate salt stress in soybean. J Plant Growth Regul 42(2):946–959

    Article  CAS  Google Scholar 

  • Sawada H, Shim IS, Usui K (2006) Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis-modulation by salt stress in rice seedling. Plant Sci 171:263–270

    Article  CAS  Google Scholar 

  • Shaki F, Maboud HE, Niknam V (2019) Effects of salicylic acid on hormonal cross talk, fatty acids profile, and ions homeostasis from salt-stressed safflower. J Plant Interact 14:340–346

    Article  CAS  Google Scholar 

  • Shakirova FM, Sakhabutdinova AR, Bezrukova MV, Fatkhutdinova RA, Fatkhutdinova DR (2003) Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci 164(3):317–322

    Article  CAS  Google Scholar 

  • Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902

    Article  PubMed  PubMed Central  Google Scholar 

  • Shavrukov Y (2013) Salt stress or salt shock: which genes are we studying? J Exp Bot 64(1):119–127

    Article  CAS  PubMed  Google Scholar 

  • Shen C, Hu Y, Du X, Li T, Tang H, Wu J (2014) Salicylic acid induces physiological and biochemical changes in Torreya grandis cv Merrillii seedlings under drought stress. Trees 28(4):961–970

    Article  CAS  Google Scholar 

  • Shen X, Guo X, Guo X, Zhao D, Zhao W, Chen J, Li T (2017) PacMYBA, a sweet cherry R2R3-MYB transcription factor, is a positive regulator of salt stress tolerance and pathogen resistance. Plant Physiol Bioch 112:302–311

    Article  CAS  Google Scholar 

  • Sicilia A, Testa G, Santoro DF, Cosentino SL, Lo-Piero AR (2019) RNASeq analysis of giant cane reveals the leaf transcriptome dynamics under long-term salt stress. BMC Plant Biol 19(1):1–24

    Article  CAS  Google Scholar 

  • Talaat NB, Shawky BT (2022) Synergistic effects of salicylic acid and melatonin on modulating ion homeostasis in salt-stressed wheat (Triticum aestivum L.) plants by enhancing root H+-pump activity. Plants 11(3):416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torun H, Novák O, Mikulík J, Strnad M, Ayaz FA (2022) The Effects of exogenous salicylic acid on endogenous phytohormone status in Hordeum vulgare L. under salt stress. Plants 11(5):618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsukagoshi H, Suzuki T, Nishikawa K, Agarie S, Ishiguro S, Higashiyama T (2015) RNA-Seq analysis of the response of the halophyte, Mesembryanthemum crystallinum (IcePlant) to high salinity. PLoS ONE 10(2):e0118339

    Article  PubMed  PubMed Central  Google Scholar 

  • Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2(3):135–138

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166:1637–1645

    Article  CAS  PubMed  Google Scholar 

  • Wani AB, Chadar H, Wani AH, Singh S, Upadhyay N (2017) Salicylic acid to decrease plant stress. Environ Chem Lett 15(1):101–123

    Article  CAS  Google Scholar 

  • Wu T, Tian Z, Liu J, Xie C (2009) A novel leucine-rich repeat receptor-like kinase gene in potato, StLRPK1, is involved in response to diverse stresses. Mol Biol Rep 36(8):2365–2374

    Article  CAS  PubMed  Google Scholar 

  • Xia J, Ren J, Zhang S, Wang Y, Fang Y (2019) Forest and grass composite patterns improve the soil quality in the coastal saline-alkali land of the Yellow River Delta. China Geoderma 349:25–35

    Article  CAS  Google Scholar 

  • Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217(2):523–539

    Article  CAS  PubMed  Google Scholar 

  • Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63(7):2541–2556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Z, Duan X, Luo L, Dai S, Ding Z, Xia G (2020) How plant hormones mediate salt stress responses. Trends Plant Sci 25(11):1117–1130

    Article  CAS  PubMed  Google Scholar 

  • Zahra S, Amin B, Ali VSM, Ali Y, Mehdi Y (2010) The salicylic acid effect on the tomato (Lycopersicum esculentum Mill.) sugar, protein and proline contents under salinity stress (NaCl). J Biophys Struct Biol 2(3):35–41

    Google Scholar 

  • Zhai Y, Zhang L, Xia C, Fu S, Zhao G, Jia J, Kong X (2016) The wheat transcription factor, TabHLH39, improves tolerance to multiple abiotic stressors in transgenic plants. Biochem Bioph Res Co 473(4):1321–1327

    Article  CAS  Google Scholar 

  • Zhang Z, Lu S, Yu W, Ehsan S, Zhang Y, Jia H, Fang J (2022) Jasmonate increases terpene synthase expression, leading to strawberry resistance to Botrytis cinerea infection. Plant Cell Rep 41(5):1243–1260

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Qu D, Wang L, Gao Y, An N, Wang A, Li Y, Yang J, Wu F, Su H (2022) Genome-wide identification of cysteine-rich receptor-like kinases in sweet cherry reveals that PaCRK1 enhances sweet cherry resistance to salt stress. Plant Cell Rep 41(10):2037–2088

    Article  CAS  PubMed  Google Scholar 

  • Zheng J, Ma X, Zhang X, Hu Q, Qian R (2018) Salicylic acid promotes plant growth and salt-related gene expression in Dianthus superbus L. (Caryophyllaceae) grown under different salt stress conditions. Physiol Mol Biol Pla 24(2):231–238

    Article  CAS  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6(5):441–445

    Article  CAS  PubMed  Google Scholar 

  • Zhu D, Hou L, Xiao P, Guo Y, Deyholos MK, Liu X (2019) VvWRKY30, a grape WRKY transcription factor, plays a positive regulatory role under salinity stress. Plant Sci 280:132–142

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank assistant professor Muhammad Salman Haider from Ghazi University for proofreading the manuscript. We also thank Professor Jiang Lu and associate professor Lu Liu from Shanghai Jiaotong University for the equipment assistance.

Funding

This study was funded by China Agriculture Research System (Grant No. CARS-30-2-08), Shanghai Agriculture Applied Technology Development Program, China (Grant No. 2022-02-08–00-12-F01111), Natural Science Foundation of Shanghai (23ZR1430600), Shanghai Sailing Program (Grant No. 21YF1422100), Startup Fund for Young Faculty at SJTU (Grant No. 21X010500643), and Science and Technology Plan Project in Haining City, Zhejiang Province (2021001).

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  1. Department of Plant Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Minhang District Jianchuan Road No. 601, Shanghai, 200240, People’s Republic of China

    Jieming Xu, Yan Xu, Yuxuan Wang, Zhengxin Lv, Xunju Liu, Wanxia Sun, Muhammad Aamir Manzoor, Ruie Liu, Shiping Wang, Songtao Jiu & Caixi Zhang

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  1. Jieming Xu
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  2. Yan Xu
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Contributions

JX conducted the experiments, prepared figures, and wrote the manuscript. YX, YW, and ZL participated in the experiments and data analysis. WS and XL contributed to the experimental methods. MAM, RL, and SW contributed with consultation. CZ and SJ managed the research and revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Songtao Jiu or Caixi Zhang.

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Supplementary Information

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344_2023_11195_MOESM1_ESM.tif

Supplementary file1 (TIF 9954 KB) Pearson’s correlation analysis revealed a strong association among the three biological replicates of each group (CK, T1, T2, and T3). The correlation coefficient between 0.8 and 1.0 is extremely strong, indicating that the expression patterns between samples are similar

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Supplementary file2 (TIF 1621 KB) Principal component analysis on each group (CK, T1, T2, and T3) according to the expression level clusters similar samples together and the distance indicates the similarity between samples

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Supplementary file3 (TIF 8022 KB) Circular visualization of the DEGs in cherry rootstocks (Cerasus spp.) under control and salt stress with or without SA application. The red and green histograms represent the log2Fold-change values of upregulated and downregulated genes, respectively, and the gray scatter plot shows the log2Fold-change values for the non-differentially expressed genes

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Supplementary file4 (TIF 1577 KB) Difference and significance analysis for the DEGs in CK vs. T1, CK vs. T2, CK vs. T3, T1 vs. T3 and T2 vs. T3 comparisons using volcano plots. CK, control; T1, 1.0-mM SA treatment; T2, salt stress; T3, salt stress with 1.0-mM SA treatment

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Supplementary file5 (TIF 10991 KB) Gene ontology classification and enrichment analysis of the differentially expressed genes in CK vs. T1, CK vs. T2, CK vs. T3, T1 vs. T3 and T2 vs. T3 comparisons

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Supplementary file6 (TIF 10488 KB) KEGG pathway classification and enrichment analysis of the differentially expressed genes in CK vs. T1, CK vs. T2, CK vs. T3, T1 vs. T3, and T2 vs. T3 comparisons

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Supplementary file7 (TIF 1336 KB) Expression profiles of the DEGs related to CTK biosynthesis and signaling pathway are shown by a heatmap. The scale of color intensity is shown in the lower left quarter of the heatmap, representing the log2fold-change values. Fold-change refers to the ratio of gene expression levels in cherry rootstock leaves between the CK and treatments (T1/T2/T3)

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Supplementary file8 (TIF 1133 KB) Expression profiles of the DEGs related to GA biosynthesis and signaling pathway are shown by a heatmap. The scale of color intensity is shown in the lower left quarter of the heatmap, representing the log2fold-change values. Fold-change refers to the ratio of gene expression levels in cherry rootstock leaves between the CK and treatments (T1/T2/T3)

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Supplementary file9 (TIF 1865 KB) Expression profiles of the DEGs related to ETH biosynthesis and signaling pathway are shown by a heatmap. The scale of color intensity is shown in the lower left quarter of the heatmap, representing the log2fold-change values. Fold-change refers to the ratio of gene expression levels in cherry rootstock leaves between the CK and treatments (T1/T2/T3)

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Supplementary file10 (TIF 2622 KB) A heatmap shows the expression profiles of the DEGs related to stress-associated proteins. The scale of color intensity is shown in the lower left quarter of the heatmap, representing the log2fold-change values. Fold-change refers to the ratio of gene expression levels in cherry rootstock leaves between the CK and treatments (T1/T2/T3)

Supplementary file11 (DOCX 115 KB)

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Xu, J., Xu, Y., Wang, Y. et al. Exogenous Salicylic Acid Improves Photosynthetic and Antioxidant Capacities and Alleviates Adverse Effects of Cherry Rootstocks Under Salt Stress. J Plant Growth Regul 43, 1428–1446 (2024). https://doi.org/10.1007/s00344-023-11195-6

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