Abstract
Salinity is the major environmental factor that limits plant growth and productivity. High concentrations of Na+ and Cl− ions in soil solution negatively affect K+ uptake and may cause physiological and metabolic disorders, which adversely affect the plant growth and crop yield. In plants, NHX antiporters play an important role in salt tolerance by catalyzing Na+ accumulation in vacuoles. In this work, we studied the effect of exogenous plants hormones auxin (IAA) and gibberellic acid (GA3), on salinity tolerance, fruit production and quality in transgenic tomato plants overexpressing LeNHX4 antiporter grown under 125 mM NaCl. Here, we have found that IAA and GA3 positively affected leaf proline, glucose, soluble proteins and ortho-diphenol. In addition, both hormones increased tomato production and fruit quality parameters. These results suggest that GA3 and IAA improved salinity tolerance and increased fruit yield and quality, probably by increasing the expression or the activity of LeNHX4 antiporter.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- ABRE:
-
ABA-Responsive Element
- ARF2:
-
Auxin response factor
- AuxRE-core:
-
Core of the auxin response region
- CHX:
-
Cation/H+ exchanger
- CPA:
-
Cation-proton antiporter
- DELLA:
-
Aspartic acid-glutamic acid-leucine-leucine-alanine
- GA:
-
Gibberellins/gibberellic acid
- GARE:
-
Gibberellin-responsive element
- HAK5:
-
High-affinity K+ transporter 5
- IAA:
-
Indole-3-aceticacid
- NHX:
-
Na+/H+ exchanger
- KEA:
-
K+-efflux antiporter
- TGA element:
-
TGA sequence
References
Achard P, Baghour M, Chapple A, Hedden P, Van Der Straeten D, Genschik P, Mortiz T, Harberd NP (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc Natl Acad Sci USA 104:484–6489. https://doi.org/10.1073/pnas.0610717104
Baghour M, Gálvez FJ, Sánchez ME, Aranda MN, Venema K, Rodríguez-Rosales MP (2019) Overexpression of LeNHX2 and SlSOS2 increases salt tolerance and fruit production in double transgenic tomato plants. Plant Physiol Bioch 135:77–86. https://doi.org/10.1016/j.plaphy.2018.11.028
Blanco-Touriñán N, Serrano-Mislata A, Alabadi D (2020) Regulation of DELLA proteins by post-translational modifications. Am J Physiol 61:1891–1901. https://doi.org/10.1093/pcp/pcaa113
Bhattacharyya D, Yu SM, Lee YH (2015) Volatile compounds from Alcaligenes faecalis JBCS1294 confer salt tolerance in Arabidopsis thaliana through the auxin and gibberellin pathways and differential modulation of gene expression in root and shoot tissues. Plant Growth Regul 75:297–306. https://doi.org/10.1007/s10725-014-9953-5
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Cagnac O, Baghour M, Jaime-Pérez N, Aranda MN, Sánchez ME, Rodríguez-Rosales MP, Venema K (2020) Deletion of the N‑terminal domain of the yeast vacuolar (Na+, K+)/H+ antiporter Vnx1p improves salt tolerance in yeast and transgenic Arabidopsis. Yeast 37:173–185. https://doi.org/10.1002/yea.3450
Caliskan O, Radusiene J, Temizel KE, Staunis Z, Cirak C, Kurt D, Odabas MS (2017) The effects of salt and drought stress on phenolic accumulation in greenhouse-grown Hypericum pruinatum. Ital J Agron 12:3. https://doi.org/10.4081/ija.2017.918
Conti L, Nelis S, Zhang C, Woodcock A, Swarup R, Galbiati M, Chiara RN, Peter H, Malcolm B, Sadanandom A (2014) Small ubiquitin-like modifier protein SUMO enables plants to control growth independently of the phytohormone gibberellin. Dev Cell 28:102–110. https://doi.org/10.1016/j.devcel.2013.12.004
Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4:397. https://doi.org/10.3389/fpls.2013.00397
Frías I, Caldeira MT, Pérez-Castiñeira JR, Navarro-Aviñó JP, Culiañez-Maciá FA, Kuppinger O, Stransky H, Pagés M, Hager A, Serrano R (1996) A major isoform of the maize plasma membrane H (+)-ATPase: characterization and induction by auxin in coleoptiles. Plant Cell 8:1533–1544. https://doi.org/10.1105/tpc.8.9.1533
Fu X, Lu Z, Wei H, Zhang J, Yang X, Wu A, Ma L, Kang M, Wang H, Yu S (2020) Genome-Wide identification and expression analysis of the NHX (Sodium/Hydrogen Antiporter) gene family in cotton. Front Genet 11:964. https://doi.org/10.3389/fgene.2020.00964
Fukuda A, Tanaka Y (2006) Effects of ABA, auxin, and gibberellin on the expression of genes for vacuolar H+-inorganic pyrophosphatase, H+-ATPase subunit A, and Na+/H+ antiporter in barley. Plant Physiol Biochem 44:351–358. https://doi.org/10.1016/j.plaphy.2006.06.012
Gálvez FJ, Baghour M, Hao G, Cagnac O, Rodríguez-Rosales MP, Venema K (2012) Expression of LeNHX isoforms in response to salt stress in salt sensitive and salt tolerant tomato species. Plant Physiol Biochem 51:109–115. https://doi.org/10.1016/j.plaphy.2011.10.012
Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214
Geng X, Chen S, Yilan E, Zhang W, Mao H, Qiqige A, Wang Y, Qi Z, Lin X (2020) Overexpression of a tonoplast Na+/H+ antiporter from root development in transgenic poplar. Tree Genet Genom 16:81. https://doi.org/10.1007/s11295-020-01475-7
Gupta R, Chakrabarty SK (2013) Gibberellic acid in plant: still a mystery unresolved. Plant Signal Behav 8:9–e2550. https://doi.org/10.4161/psb.25504
Hager A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116:483–505. https://doi.org/10.1007/s10265-003-0110-x
Hanana M, Cagnac O, Zarrouk M, Blumwald E (2009) Rôles biologiques des antiports vacuolaires NHX : acquis et perspectives d’amélioration génétique des plantes. Botanique 87:1023–1035. https://doi.org/10.1139/B09-073
Iqbal N, Nazar R, Khan MIR, Masood A, Khan NA (2011) Role of gibberellins in regulation of source-sink relations under optimal and limiting environmental conditions. Curr Sci 100:998–1007
Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42. https://doi.org/10.1016/j.envexpbot.2013.12.006
Irigoyen JJ, Emerich DW, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60. https://doi.org/10.1111/j.1399-3054.1992.tb08764.x
Jia Q, Zheng C, Sun S, Amjad H, Liang K, Lin W (2018) The role of plant cation/proton antiporter gene family in salt tolerance. Biol Plantarum 62:617–629. https://doi.org/10.1007/s10535-018-0801-8
Kong M, Luo M, Li J, Feng Z, Zhang Y, Song W, Zhang R, Wang R, Wang Y, Zhao J, Tao Y, Zhao Y (2021) Genome-wide identification, characterization, and expression analysis of the monovalent cation-proton antiporter superfamily in maize, and functional analysis of its role in salt tolerance. Genomics 113:1940–1951. https://doi.org/10.1016/j.ygeno.2021.04.032
Konishi H, Maeshima M, Komatsu S (2005) Characterization of vacuolar membrane proteins changed in rice root treated with gibberellin. J Proteome Res 4:1775–1780. https://doi.org/10.1021/pr050079c
Lalonde S, Tegeder M, Throne-Holst M (2003) Phloem loading and unloading of sugars and amino acids. Plant Cell Environ 26:37–56. https://doi.org/10.1046/j.1365-3040.2003.00847.x
Lantzouni O, Alkofer A, Falter-Braun P, Schwechheimer C (2020) GROWTH-REGULATING FACTORS interact with DELLAs and regulate growth in cold stress. Plant Cell 32:1018–1034. https://doi.org/10.1105/tpc.19.00784
Liu W, Li RJ, Han TT, Cai W, Fu ZW, Lu YT (2015) Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol 16:343–356. https://doi.org/10.1104/pp.15.00030
Lu C, Chen MX, Liu R, Zhang L, Hou X, Liu S, Ding X, Jiang Y, Xu J, Zhang J, Zhao X, Liu Y‑G (2019) Abscisic acid regulates auxin distribution to mediate maize lateral root development under salt stress. Front Plant Sci 10:716. https://doi.org/10.3389/fpls.2019.00716
Luo Y, Pang D, Jin M, Chen J, Kong X, Li W, Chang Y, Li Y, Wang Z (2019) Identification of plant hormones and candidate hub genes regulating flag leaf senescence in wheat response to water deficit stress at the grain-filling stage. Plant Direct 3:e152. https://doi.org/10.1002/pld3.152
Maach M, Baghour M, Akodad M, Gálvez FJ, Sánchez ME, Aranda MN, Venem K, Rodríguez-Rosales MP (2020) Overexpression of LeNHX4 improved yield, fruit quality and salt tolerance in tomato plants (Solanum lycopersicum L.). Mol Biol Rep 47:4145–4153. https://doi.org/10.1007/s11033-020-05499-z
Maach M, Rodríguez-Rosales MP, Venema K, Akodad M, Moumen A, Skalli A, Baghour M (2021) Improved yield, fruit quality, and salt resistance in tomato co-overexpressing LeNHX2 and SlSOS2 genes. Physiol Mol Biol Plants 27:703–712. https://doi.org/10.1007/s12298-021-00974-8
Malakar P, Chattopadhyay D (2021) Adaptation of plants to salt stress: the role of the ion transporters. J Plant Biochem Biotechnol 30:668–683. https://doi.org/10.1007/s13562-021-00741-6
Nuccio ML, Wu J, Mowers R, Zhou HP, Meghji M, Primavesi LF, Paul MJ, Chen X, Gao Y, Haque E, Basu SS, Lagrimini LM (2015) Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nat Biotechnol 33:862–869. https://doi.org/10.1038/nbt.3277
Paquin R, Lechasseur P (1979) Observations sur une méthode de dosage de la proline libre dans les extraits de plantes. Can J Bot 57:1851–1854. https://doi.org/10.1139/b79-233
Riemann M, Dhakarey R, Hazman M, Miro B, Kohli A, Nick P (2015) Exploring jasmonates in the hormonal network of droughtand salinity responses. Front Plant Sci 6:1077. https://doi.org/10.3389/fpls.2015.01077
Rodríguez-Rosales MP, Galvez FJ, Huertas R, Aranda MN, Baghour M, Cagnac O, Venema K (2009) Plant NHX cation/proton antiporters. Plant Signal Behav 4:265–276. https://doi.org/10.4161/psb.4.4.7919
Ruiz JM, Bretones G, Baghour M, Ragala L, Belakbir A, Romero L (1998) Relationship between boron and phenolic metabolism in tobacco leaves. Phytochemistry 48:269–272. https://doi.org/10.1016/S0031-9422(97)01132-1
Saeidi-Sar S, Abbaspour H, Afshari H, Yaghoobi SR (2013) Effects of ascorbic acid and gibberellin A3 on alleviation of salt stress in common bean (Phaseolus vulgaris L.) seedlings. Acta Physiol Plant 35:667–677. https://doi.org/10.1007/s11738-012-1107-7
Salem MA, Yoshida T, de Souza PL, Alseekh S, Bajdzienko K, Fernie AR, Giavalisco P (2020) An improved extraction method enables the comprehensive analysis of lipids, proteins, metabolites and phytohormones from a single sample of leaf tissue under water-deficit stress. Plant J 103:1614–1632. https://doi.org/10.1111/tpj.14800
Schobert C, Zhong WJ, Komor E (1998) Inorganic ions modulate the path of phloem loading of sucrose in Ricinus communis L. seedlings. Plant Cell Environ 21:1047–1054. https://doi.org/10.1046/j.1365-3040.1998.00354.x
Shahzad K, Hussain S, Arfan M, Hussain S, Wariach EA, Zamir S, Saddique M, Rauf A, Kamal KY, Hano C, El-Essawi MA (2021) Exogenously applied gibberellic acid enhances growth and salinity stress tolerance of maize through modulating the morpho-physiological, biochemical and molecular attributes. Biomolecules. https://doi.org/10.3390/biom11071005
Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223. https://doi.org/10.1016/S1369-5266(00)80068-0
Singleton VL, Rossi JA Jr. (1965) Colorimetric of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599. https://doi.org/10.1146/annurev.arplant.50.1.571
Wang P, Shen L, Guo J, Jing W, Qu Y, Li W, Bi R, Xuan W, Zhang Q, Zhang W (2019) Phosphatidic acid directly regulates PINOID-dependent phosphorylation and activation of the PIN-FORMED2 auxin efflux transporter in response to salt stress. Plant Cell 31:250–271. https://doi.org/10.1105/tpc.18.00528
Wu L, Wu M, Liu H, Gao Y, Chen Y, Xiang Y (2021) Identification and characterisation of monovalent catión/proton antiporters (CPAs) in Phyllostachys edulis and the functional analysis of PheNHX2 in Arabidopsis thaliana. Plant Physiol Biochem 164:205–221. https://doi.org/10.1016/j.plaphy.2021.05.002
Acknowledgements
The authors wish to thank Professor Dr. Boujamaa El Kouy from the English Studies Department at Multidisciplinary Faculty of Nador for this careful reading of the paper and improving the quality of English language of our manuscript
Funding
This work was supported by grants from National Centre for Scientific and Technical Research and Minister for Higher Education, Scientific Research and Executive Training (Morocco) Ref: PPR/2015/21. CSIC Progamme for scientific cooperation for development (I-COOP-B + 2013; Ref: COOPB20053)
Author information
Authors and Affiliations
Contributions
Concepts: KV, MA, MB, MPRR. Study design: AM, AS, KV, MB, MPRR. Literature research: AD, KV, MB, MPRR. Experimental studies: AD, HE, MM. Data analysis/interpretation: AD, MB, KV, MPRR. Statistical analysis: MB. Manuscript preparation: MA, MB, MM, MPRR.
Corresponding author
Ethics declarations
Conflict of interest
M. Baghour, M. Akodad, A. Dariouche, M. Maach, H. El Haddaji, A. Moumen, A. Skalli, K. Venema and M.P. Rodríguez-Rosales declare that they have no competing interests.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Baghour, M., Akodad, M., Dariouche, A. et al. Gibberellic Acid and Indole Acetic Acid Improves Salt Tolerance in Transgenic Tomato Plants Overexpressing LeNHX4 Antiporter. Gesunde Pflanzen 75, 687–693 (2023). https://doi.org/10.1007/s10343-022-00734-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10343-022-00734-y