The newly synthesized plant growth regulator S-methylmethionine salicylate may provide protection against high salinity in wheat
Abstract
High salinity is one of the major environmental factors limiting the productivity of crop species worldwide. Improving the stress tolerance of cultivated plants and thus increasing crop yields in an environmentally friendly way is a crucial task in agriculture. In the present work the ability of a new derivative, S-methylmethionine-salicylate (MMS), to improve the salt tolerance of wheat plants was tested parallel with its related compounds salicylic acid and S-methylmethionine. The results show that while these compounds are harmful at relatively high concentration (0.5 mM), they may provide protection against high salinity at lower (0.1 mM) concentration. This was confirmed by gas exchange, chlorophyll content and chlorophyll-a fluorescence induction measurements. While osmotic adjustment probably plays a critical role in the improved salt tolerance, neither Na or K transport from the roots to the shoots nor proline synthesis are the main factors in the tolerance induced by the compounds tested. MMS, S-methylmethionine and Na-salicylate had different effects on flavonol biosynthesis. It was also shown that salt treatment had a substantial influence on the SA metabolism in wheat roots and leaves. Present results suggest that the investigated compounds can be used to improve salt tolerance in plants.
Keywords
Gene expression Osmotic adjustment Salicylic acid Salt stress S-methylmethionine Triticum aestivum LNotes
Acknowledgements
This work was funded by the National Research, Development and Innovation Office (K 108838).
Supplementary material
References
- Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Sci 196:67–76CrossRefPubMedGoogle Scholar
- Anton A, Rékási M, Uzinger N, Széplábi G, Makó A (2012) Modelling the potential effects of the Hungarian red mud disaster on soil properties. Water Air Soil Pollut 223:5175–5188CrossRefGoogle Scholar
- Bajji M, Lutts S, Kinet J (2001) Water deficit effects on solute contribution to osmotic adjustment as a function of leaf ageing in three durum wheat (Triticum durum Desf.) cultivars performing differently in arid conditions. Plant Sci 160:669–681CrossRefPubMedGoogle Scholar
- Bassil E, Blumwald E (2014) The ins and outs of intracellular ion homeostasis: NHX-type cation/H+ transporters. Curr Opin Plant Biol 22:1–6CrossRefPubMedGoogle Scholar
- Bates BL, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
- Cao Y, Zhang ZW, Xue LW, Du JB, Shang J, Xu F et al (2009) Lack of salicylic acid in Arabidopsis protects plants against moderate salt stress. Z Naturforsch C 64:231–238CrossRefPubMedGoogle Scholar
- Darko E, Janda T, Majláth I, Szopko D, Dulai S, Molnár I, Türkösi E, Molnár-Láng M (2015) Salt stress response of wheat–barley addition lines carrying chromosomes from the winter barley “Manas”. Euphytica 203:491–504CrossRefGoogle Scholar
- Darko E, Gierczik K, Hudák O, Forgó P, Pál M, Türkösi E, Kovács V, Dulai S, Majláth I, Molnár I, Janda T, Molnár-Láng M (2017) Differing metabolic responses to salt stress in wheat-barley addition lines containing different 7H chromosomal fragments. PLoS ONE 12(3):e0174170CrossRefPubMedPubMedCentralGoogle Scholar
- Davenport RJ, Munoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30:497–507CrossRefPubMedGoogle Scholar
- Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379CrossRefPubMedPubMedCentralGoogle Scholar
- Gémes K, Poór P, Horváth E, Kolbert Z, Szopkó D, Szepesi Á, Tari I (2011) Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiol Plant 142:179–192CrossRefPubMedGoogle Scholar
- Gharbi E, Martínez JP. Benahmed H, Dailly H, Quinet M, Lutts S (2017) 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 82:517–525CrossRefGoogle Scholar
- Gondor OK, Pal M, Darko E, Janda T, Szalai G (2016a) Salicylic acid and sodium salicylate alleviate cadmium toxicity to different extents in maize (Zea mays L.). PLoS ONE 11(8): Paper e0160157CrossRefGoogle Scholar
- Gondor OK, Janda T, Soós V, Pál M, Majláth I, Adak MK, Balázs E, Szalai G (2016b) Salicylic acid induction of flavonoid biosynthesis pathways in wheat varies by treatment. Front Plant Sci 7:1447CrossRefPubMedPubMedCentralGoogle Scholar
- Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499CrossRefPubMedGoogle Scholar
- Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300CrossRefGoogle Scholar
- Horváth E, Brunner S, Bela K, Papdi C, Szabados L, Tari I, Csiszár J (2015) Exogenous salicylic acid-triggered changes in the glutathione transferases and peroxidases are key factors in the successful salt stress acclimation of Arabidopsis thaliana. Func Plant Biol 42:1129–1140Google Scholar
- Janda T, Gondor OK, Yordanova R, Szalai G, Pál M (2014) Salicylic acid and photosynthesis: signalling and effects. Acta Physiol Plant 36:2537–2546CrossRefGoogle Scholar
- Janda T, Darko É, Shehata S, Kovács V, Pál M, Szalai G (2016) Salt acclimation processes in wheat. Plant Physiol Biochem 101:68–75CrossRefPubMedGoogle Scholar
- Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2013) Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. J Exp Bot 64:2255–2268CrossRefPubMedPubMedCentralGoogle Scholar
- Khan NA, Syeed S, Masood A, Nazar R, Iqbal N (2010) Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress. Int J Plant Biol 1:e1CrossRefGoogle Scholar
- Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462PubMedPubMedCentralGoogle Scholar
- Klughammer C, Schreiber U (2008) Saturation Pulse method for assessment of energy conversion in PS I. PAM Appl Notes 1:11–14Google Scholar
- Lu H, Greenberg JT, Holuigue L (2016) Editorial: salicylic acid signaling networks. Front Plant Sci 7:238PubMedPubMedCentralGoogle Scholar
- Ludmerszki E, Chounramany S, Oláh C, Kátay G, Rácz I, Almási A, Solti Á, Bélai I, Rudnóy S (2017) Protective role of S-methylmethionine-salicylate in maize plants infected with Maize dwarf mosaic virus. Eur J Plant Pathol 149:145–156CrossRefGoogle Scholar
- Martinez V, Mestre TC, Rubio F, Girones-Vilaplana A, Moreno DA, Mittler R, Rivero RM (2016) Accumulation of flavonols over hydroxy cinnamic acids favors oxidative damage protection under abiotic stress. Front Plant Sci 7:838CrossRefPubMedPubMedCentralGoogle Scholar
- Meuwly P, Métraux JP (1993) Ortho-anisic acid as internal standard for the simultaneous quantitation of salicylic acid and its putative biosynthetic precursors in cucumber leaves. Anal Biochem 214:500–505CrossRefPubMedGoogle Scholar
- Mittova V, Tal M, Volokita M, Guy M (2002) Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol Plant 115:393–400CrossRefPubMedGoogle Scholar
- Neto MCL, Lobo AKM, Martins MO, Fontenele AV, Silveira JAG (2014) Dissipation of excess photosynthetic energy contributes to salinity tolerance: a comparative study of salt-tolerant Ricinus communis and salt-sensitive Jatropha curcas. J Plant Physiol 171:23–30CrossRefGoogle Scholar
- Pál M, Horváth E, Janda T, Páldi E, Szalai G (2005) Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays L.) plants. Physiol Plant 125:356–364CrossRefGoogle Scholar
- Páldi K, Rácz I, Szigeti Z, Rudnóy S (2014) S-methylmethionine alleviates the cold stress damage in maize through protection of the photosynthetic apparatus and stimulation of the phenylpropanoid pathway. Biol Plant 58:189–194CrossRefGoogle Scholar
- Paolacci AR, Tanzarella OA, Porceddu E, Ciaffi M (2009) Identification and validation of reference genes for quantitative RT-PCR normalization in wheat. BMC Mol Biol 10:11CrossRefPubMedPubMedCentralGoogle Scholar
- Poór P, Gémes K, Horváth F, Szepesi Á, Simon ML, Tari I (2011) Salicylic acid treatment via the rooting medium interferes with stomatal response, CO2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. Plant Biol 13:105–114CrossRefPubMedGoogle Scholar
- Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224–231CrossRefPubMedGoogle Scholar
- Rácz I, Páldi E, Szalai G, Janda T, Lásztity D (2008) S-methylmethionine reduces cell membrane damage in higher plants exposed to low temperature stress. J Plant Physiol 165:1483–1490CrossRefPubMedGoogle Scholar
- Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571CrossRefPubMedPubMedCentralGoogle Scholar
- Sun Z, Hou S, Yang W, Han Y (2012) Exogenous application of salicylic acid enhanced the rutin accumulation and influenced the expression patterns of rutin biosynthesis related genes in Fagopyrum tartaricum Gaertn. leaves. Plant Growth Regul 68:9–15CrossRefGoogle Scholar
- Szalai G, Janda T (2009) Effect of salt stress on the salicylic acid synthesis in young maize (Zea mays L.) plants. J Agron Crop Sci 195:165–171CrossRefGoogle Scholar
- Szalai G, Pál M, Árendás T, Janda T (2016) Priming seed with salicylic acid increases grain yield and modifies polyamine levels in maize. Cereal Res Commun 44:537–548CrossRefGoogle Scholar
- Wan S, Wang W, Zhou T, Zhang Y, Chen J, Xiao B, Yang Y, Yu Y (2018) Transcriptomic analysis reveals the molecular mechanisms of Camellia sinensis in response to salt stress. Plant Growth Regul 84:481–492CrossRefGoogle Scholar
- Xiong JL, Dai LL, Ma N, Zhang CL (2018) Transcriptome and physiological analyses reveal that AM1 as an ABA-mimicking ligand improves drought resistance in Brassica napus. Plant Growth Regul 85:73–90CrossRefGoogle Scholar
- Zhao G, Yu H, Liu M, Lu Y, Ouyang B (2017) Identification of salt-stress responsive microRNAs from Solanum lycopersicum and Solanum pimpinellifolium. Plant Growth Regul 83:129–140CrossRefGoogle Scholar