Abstract
Salicylic acid (SA) is involved in the salt-resistance of the halophyte plant species Solanum chilense. The SA analog 2,6-dichloroisonicotinc acid (INA) is commonly used to elicit SA signal transduction in response to biotic stress and is frequently used to confirm the SA involvement in plant response to pathogens. Data are lacking concerning its impact on plant response to salinity, especially in the halophyte species. Solanum chilense was cultivated in the absence or presence of 125 mM NaCl in nutrient solution and exposed to 0.01 mM exogenous SA or sprayed with 0.5 mM INA. Exogenous SA increased the shoot dry weight while INA did not. Exogenous INA, in contrast to SA, increased the shoot Na+ concentration in NaCl-treated plants and decreased the root K+ concentration. In the absence of salt, both SA and INA induced an increase in H2O2 which was not due to ascorbate peroxidase (EC 1.11.1.11) inhibition. In salt-treated plants, SA stimulated the ascorbate peroxidase activity while INA did not. Exogenous SA increased the root putrescine and spermidine concentrations while INA significantly decreased the concentration of these protecting compounds. It is concluded that exogenous SA and INA do not have similar impacts on the plant behavior and that the difference between these compounds may be influenced by NaCl. The use of INA as a reliable SA analog should therefore be considered with caution in halophyte plant species.
Abbreviations
- A :
-
Net photosynthesis
- APX:
-
Ascorbate peroxidase
- AsA:
-
Ascorbic acid
- DW:
-
Dry weight
- EDTA:
-
Ethylenediaminetetraacetic acid
- FW:
-
Fresh weight
- g s :
-
Stomatal conductance
- INA:
-
2,6-dichloroisonicotinic acid
- PAs:
-
Polyamines
- Put:
-
Putrescine
- SA:
-
Salicylic acid
- SAR:
-
Systemic acquired resistance
- Spd:
-
Spermidine
- Spm:
-
Spermine
- Ψs:
-
Osmotic potential
- WC:
-
Water content
References
Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462
Boatwright JL, Pajerowska-Mukhtar K (2013) Salicylic acid: an old hormone up to new tricks. Mol Plant Pathol 14:623–634
Bokshi AI, Morris SC, Mcconchie RM, Deverall BJ (2006) Pre-harvest application of 2,6-dichloroisonicotinic acid—aminobutryric acid or benzothiadiazole to control pos-harvest storage diseases of melons by inducing systemic acquired resistance. J Hort Sci Biotechnol 81:700–706
Chandrashekar S, Umesha S (2014) 2,6-dichloroisonicotinic acid enhances the expression of defense genes in tomato seedling against Xanthomonas perforans. Physiol Mol Plant Pathol 86:49–56
Cillo F, Pasciuto MM, De Giovanni C, Finetti-Sialer MM, Ricciardi L, Gallitelli D (2007) Response of tomato and its wild relatives in the genus Solanum to cucumber mosaic virus and satellite RNA combinations. J Gen Virol 88:3166–3176
Colson-Hanks ES, Deverall BJ (2000) Effect of 2,6-dichloroisonicotinic acid, its formulation materials and benzothiadiazole on systemic resistance to alternaria leaf spot in cotton. Plant Pathol 49:171–178
Cristescu SM, De Martinis D, Te Linthel Hekkert S, Parker DH, Harren FJM (2002) Ethylene production by Botrytis cinerea in vitro and in tomatoes. Appl Environ Microbiol 68:5342–5350
Dann EK, Deverall BJ (1996) 2,6-dichloro-isonicotinic acid (INA) induces resistance in green beans to the rust pathogen, Uromyces appendiculatus, under field conditions. Aust Plant Pathol 25:199–204
Dann E, Diers B, Byrum J, Hammerschmidt R (1998) Effect of treating soybean with 2,6-dichloroisonicotinic acid (INA) and benzothiadiazole (BTH) on seed yield and the level of disease caused by Sclerotinbia sclerotiorum in field and greenhouse studies. Eur J Plant Pathol 104:271–278
Durbak A, Yao H, McSteen P (2012) Hormone signaling in plant development. Curr Opin Plant Biol 15:92–96
Durner J, Klessig DF (1995) Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid two inducers of plant defense responses. Proc Natl Acad sci USA 92:11312–11316
Fobert PR, Després C (2005) Redox control of systemic acquired resistance. Curr Opin Plant Biol 8:378–382
Gharbi E, Martínez JP, Benahmed H, Fauconnier ML, Lutts S, Quinet M (2016) Salicylic acid differently impacts ethylene and polyamine synthesis in the glycophyte Solanum lycopersicum and the wild-related halophyte Solanum chilense exposed to mild salt stress. Physiol Plant 158:152–167
Gharbi E, Martínez JP, Benahmed H, Lepoint G, Vanpee B, Quinet M, Lutts S (2017a) Inhibition of ethylene synthesis reduces salt-tolerance in tomato wild relative species Solanum chilense. J Plant Physiol 210:24–37
Gharbi E, Martínez JP, Benahmed H, Hichri I, Dobrev PI, Motyka V, Quinet M, Lutts S (2017b) Phytohormone profiling in relation to osmotic adjustment in NaCl-treated plants of the halophyte tomato wild relative species Solanum chilense comparatively to the cultivated glycophyte Solanum lycopersicum. Plant Sci 258:77–89
Gupta K, Sengupta A, Chakraborty M, Gupta B (2016) Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses. Front Plant Sci 7:1343
Harris MO, Friesen TL, Xu SS, Chen MS, Giron D, Stuart JJ (2015) Pivoting from Arabidopsis to wheat to understand how agricultural plants integrate responses to biotic stress. J Exp Bot 66:513–531
Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300
Iqbal N, Nazar R, Syeed S, Masood A, Ferrante A, Khan NA (2013) Current understanding on ethylene signaling in plants: the influence of nutrient availability. Plant Physiol Biochem 73:128–138
Kawano T, Bouteau F (2013) Crosstalk between intracellular and extracellular salicylic acid signaling events leading to long-distance spread of signals. Plant Cell Rep 32:1125–1138
Khan MIR, 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
Kumari A, Das P, Parida AK, Agarwal PK (2015) Proteomics, metabolomics and ionomics perspective of salinity tolerance in halophytes. Front Plant Sci 6:357
Liu X, Rockett KS, Kørner CJ, Pajerowska-Mukhtar KM (2015) Salicylic acid signaling: new insights and prospects at a quarter-century milestone. Essay Biochem 58:101–113
Lutts S, Bouharmont J, Kinet JM (1999) Physiological characterization of salt-resistant rice somaclones. Aust J Bot 47:835–849
Mimouni H, Wasti S, Manaa A, Gharbi E, Chalh A, Vandoorne B, Lutts S, Ben Ahmed H (2016) Does salicylic acid (SA) improve tolerance to salt stress in plants ? A study of SA effects on tomato plant growth, water dynamics, photosynthesis and biochemical parameters. OMICS J Int Biol 20:180–190
Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:4
Molinari S, Loffredo E (2006) The role of salicylic acid in defense response of tomato to root-knot nematodes. Physiol Mol Plant Pathol 68:69–78
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nazar R, Umar S, Khan NA (2015) Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signal Behav 10(3):e1003751. doi:10.1080/15592324.2014.1003751
Nosenko T, Böndel KB, Kumpfmüller G, Stephan S (2016) Adaptation to low temperatures in the wild tomato species Solanum chilense. Mol Ecol 25:2853–2869
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295
Pillonel C (2001) Identification of a 2,6-dichloroisonicotinic-acid-sensitive protein kinase from tobacco by affinity chromatography on benzothiadiazole-sepharose and NIM-metal chelate adsorbent. Pest Manag Sci 57:676–682
Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Front Plant Sci 5:154
Pye MF, Hakuno F, Mac Donald JD, Bostock RM (2013) Induced resistance in tomato by SAR activators during predisposing salinity stress. Front Plant Sci 4:116
Quinet M, Bataille G, Dobrev PI, Capel C, Gómez P, Capel J, Lutts S, Motyka V, Angostso T, Lozano R (2014) Transcriptional and hormonal regulation of petal and stamen development by STAMENLESS, the tomato (Solanum lycopersicum L.) orthologue to the B-class APETALA3 gene. J Exp Bot 65:2243–2256
Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defense: its role in plant growth and development. J Exp Bot 62:3321–3338
Ross JJ, Weston DE, Davidson SE, Reid JB (2011) Plant hormone interactions: how complex are they? Physiol Plant 141:299–309
Schweizer P, Buchala A, Métraux JP (1997) Gene-expression patterns and levels of jasmonic acid in rice treated with the resistance inducer 2,6-Dichloroisonicotinic acid. Plant Physiol 115:61–70
Seyfferth C, Tsuda K (2014) Salicylic acuid signal transduction: the initiation of biosynthesis, perception and transcriptional reprogramming. Front Plant Sci 65:697
Shan X, Yan J, Xie D (2012) Comparison of phytohormone signaling mechanisms. Curr Opin Plant Biol 15:84–91
Singh PK, Gautam S (2013) Role of salicylic acid on physiological and biochemical mechanism of salinity stress tolerance in plants. Acta Physiol Plant 35:2345–2353
Tapia G, Méndez J, Inostroza L (2016) Different combinations of morpho-physiological traits are responsible for tolerance to drought in wild tomatoes Solanum chilense and Solanum peruvianum. Plant Biol 18:406–416
van Kan JAL, Cozijnsen T, Danash N, De Wit PJGM (1995) Induction of tomato stress protein mRNAs by etephon, 2,6-dichloroisonicotinic acid and salicylate. Plant Mol Biol 27:1205–1213
Verlaan MG, Szinay D, Hutton SF, de Jong H, Kormelink R, Visser RGF, Scott JW, Bai Y (2011) Chromosomal rearrangements between tomato and Solanum chilense hamper mapping and breeding of the TYLC resistance gene Ty-1. Plant J 68:1093–1103
Vernooij B, Friedrich L, Goy PA, Styaub T, Kessmann H, Ryals J (1995) 2,3-Dichloroisonicotinic acid-induced resistance to pathogens without accumulation of salicylic acid. Am Phytpopathol Soc 8:228–234
Wei D, Zhang W, Wang C, Meng Q, Li G, Chen THH, Yang X (2017) Genetic engineering of the biosynthesis of glycinebetaine leads to alleviate salt-induced potassium efflux and enhances salt tolerance in tomato plants. Plant Sci 257:74–83
Yan S, Dong X (2014) Perception of the plant immune signal salicylic acid. Curr Opin Plant Biol 20:64–68
Yang Y, Qi M, Mei C (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919
Zhai Y, Yang Q, Hou M (2015) The effects of saline water drip irrigation on tomato yield, quality, and blossom-end rot incidence—A 3a case study in the South of China. PLoS ONE 10:11
Zhao F, Song CP, He J, Zhu H (2007) Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145:1061–1072
Zhou B, Wang J, Guo Z, Tan H, Zhu X (2006) A simple colorimetric method for determination of hydrogen peroxide in plant tissues. Plant Growth Regul 49:113–118
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324
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This work was supported by Wallonie Bruxelles Intenational (WBI; 15/63179).
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Gharbi, E., Martínez, J.P., Benahmed, H. et al. The salicylic acid analog 2,6-dichloroisonicotinic acid has specific impact on the response of the halophyte plant species Solanum chilense to salinity. Plant Growth Regul 82, 517–525 (2017). https://doi.org/10.1007/s10725-017-0278-z
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DOI: https://doi.org/10.1007/s10725-017-0278-z