Skip to main content
Springer Nature Link
Log in

SNP Mitigates Malignant Salt Effects on Apple Plants

SNP mindert die gefährlichen Auswirkungen von Salzbelastungen bei Apfelbäumen

  • Original Article
  • Published:
Erwerbs-Obstbau Aims and scope Submit manuscript

Abstract

Sodium nitroprusside (SNP) a nitric oxide donor is utilized as an antioxidant under stress conditions in order to mitigate stress damages. To probe into the potential relieving salinity malignant effects, we investigated the protective roles of SNP. An apple plant (Malus domestica Borkh.) cv. Fuji grafted on MM106 and M9 clonal rootstocks was chosen for the experiment and imposed to salinity stress for 4 months with 35 mM NaCl. SNP with different three doses (1, 2 and 4 mM) was applied to the roots of the salt-stressed apple plants except control. SNP applications inhibited apple plants growth depression through increasing stomatal conductivity, chlorophyll and protein content and decreasing electrolyte leakage and lipid peroxidation. Beside that, SNP triggered chlorophyll biosynthesis and maintained better cell membrane stability compared to control. In cv. Fuji/MM106, 1 mM SNP application had the highest SPAD value (48.6) even more than control plants (44.8). 4 mM SNP showed the highest stomatal conductivity (313 mmol m−2 s−1) and the lowest value was obtained from salt plant (141 mmol m−2 s−1). In cv. Fuji/M9, 4 mM SNP elevated the protein content by 73% compared to control. Information from current experiment SNP can be utilized to improve soil management practises under salt stress condition. Moreover, SNP affected apple plants through antioxidant mechanism, but did not have impact on osmotical adjustment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

  • Arbona V, Iglesias DJ, Jacas J, Primo-Millo E, Talon M, Gomez-Cadenas A (2005) Hydrogel substrate amendment alleviates drought effects on young citrus plants. Plant Soil 270:73–82

    Article  CAS  Google Scholar 

  • Awika JM, Rooney LW, Wu X, Prior RL, Zevallos LC (2003) Screening methods to measure antioxidant activity of sorghum (Sorghum bicolor) and sorghum products. J Agric Food Chem 51:6657–6662

    Article  CAS  PubMed  Google Scholar 

  • Banuls J, Primo-Millo E (1992) Effects of chloride and sodium on gas exchange parameters and water relations of citrus plants. Physiol Plant 86:115–123

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beligni MV, Lamattina L (1999) Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta 208:337–344

    Article  CAS  Google Scholar 

  • Beligni MV, Lamattina L (2001) Nitric oxide: a non-traditional regulator of plant growth. Trends Plant Sci 6:508–509

    Article  CAS  PubMed  Google Scholar 

  • Bellin D, Asai S, Delledonne M, Yoshioka H (2013) Nitric oxide as a mediator for defense responses. Mol Plant Microbe Interact 26:271–277

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Caro A, Puntarulo S (1998) Nitric oxide decreases superoxide anion generation by microsomes from soybean embryonic axes. Physiol Plant 104:357–364

    Article  CAS  Google Scholar 

  • Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Desouky SA, Atawia AAR (1998) Growth performance of some citrus rootstocks under saline conditions. Alex J Agri Res 43:231–254

    Google Scholar 

  • Fan H, Guo S, Jiao Y, Zhang R, Li J (2007) Effects of exogenous nitric oxide on growth, active oxygen species metabolism, and photosynthetic characteristics in cucumber seedlings under NaCl stress. Front Agri China 1:308–314

    Article  Google Scholar 

  • Filippou P, Antoniou C, Yelamanchili S, Fotopoulos V (2012) NO loading:efficiency assessment of five commonly used application methods of sodium nitroprusside in Medicago truncatula plants. Plant Physiol Biochem 60:115–118

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279

    Article  CAS  PubMed  Google Scholar 

  • Foissner I, Wendehenne D, Langebartels C, Durner J (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J 23:817–824

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146:359–388

    Article  CAS  Google Scholar 

  • García-Mata C, Lamattina L (2007) Abscisic acid (ABA) inhibits light-induced stomatal opening through calcium- and nitric oxide-mediated signaling pathways. Nitric Oxide 17:143–151

    Article  PubMed  CAS  Google Scholar 

  • Gould KS, Lamotte O, Klinguer A, Pugin A, Wendehenne D (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ 26:1851–1862

    Article  CAS  Google Scholar 

  • Hai-Hua R, Wen-Biao S, Luang-Lai XU (2004) Nitric oxide involved in the abscisic acid induced proline accumulation in wheat seedling leaves under salt stress. Acta Bot Sinica 46(11):1307–1315

    Google Scholar 

  • Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmad P et al (ed) In Ecophysiology and responses of plants under salt stress. Springer, New York, pp 25–87

    Chapter  Google Scholar 

  • He YK, Tang RH, Yi H, Stevens RD, Cook CW, Ahn SM, Jing L, Yang Z, Chen L, Guo F, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971

    Article  CAS  PubMed  Google Scholar 

  • Hernández JA, Almansa MS (2002) Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol Plant 115:251–257

    Article  PubMed  Google Scholar 

  • Jian W, Zhang DW, Zhu F, Wang SX, Pu XJ, Deng XG, Luo SS, Lin HH (2016) Alternative oxidase pathway is involved in the exogenous SNP-elevated tolerance of Medicago truncatula to salt stress. J Plant Physiol 193:79–87

    Article  CAS  PubMed  Google Scholar 

  • Karabal E, Yucel M, Oktem HA (2003) Antioxidant responses of tolerant and sensitive barley cultivars to boron toxicity. Plant Sci 164:925–930

    Article  CAS  Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide 27:210–218

    Article  CAS  PubMed  Google Scholar 

  • Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci 97:8849–8855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kopyra M, Gwóźdź EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017

    Article  CAS  Google Scholar 

  • Leshem YY, Haramaty E (1996) The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum foliage. J Plant Physiol 148:258–263

    Article  CAS  Google Scholar 

  • Li Y (2009) Physiological responses of tomato seedlings (Lycopersicon esculentum) to salt stress. Mod Appl Sci 3:171–176

    CAS  Google Scholar 

  • Li QY, Niu HB, Yin J, Wang MB, Shao HB, Deng DZ, Chen XX, Ren JP, Li YC (2008) Protective role of exogenous nitric oxide against oxidative-stress induced by salt stress in barley (Hordeum vulgare). Colloids Surf B: Biointerfaces 65:220–225

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Dong Y, Xu L, Kong J (2014) Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings. Plant Growth Regul 73:67–78

    Article  CAS  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398

    Article  CAS  Google Scholar 

  • Madhava RKV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stress. Plant Sci 157:113–128

    Article  Google Scholar 

  • Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exper Bot 49:69–76

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Murkute AA, Sharma S, Singh SK (2006) Studies on salt stress tolerance of citrus rootstock genotypes with arbuscular mycorrhizal fungi. Hort Sci 33:70–76

    Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Syeed S, Khan NA (2011) Understanding the significance of sulfur in improving salinity tolerance in plants. Environ Exp Bot 70:80–87

    Article  CAS  Google Scholar 

  • Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109:735–742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parida AK, Das AB, Sanada Y, Mohanty P (2004) Effects of salinity on biochemical components of the mangrove, Aegiceras corniculatum. Aquat Bot 80:77–87

    Article  CAS  Google Scholar 

  • Pedroso MC, Durzan DJ (2000) Effect of different gravity environments on DNA fragmentation and cell death in Kalanchoe leaves. Ann Bot 86:983–994

    Article  CAS  PubMed  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Radi R, Beckman JS, Bash KM, Freeman RA (1991) Peroxynitrite induced membrane lipid peroxidation: cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 228:481–487

    Article  Google Scholar 

  • Remorini D, Melgar JC, Guidi L, Degl’Innocenti E, Castelli S, Traversi ML, Massai R, Tattini M (2009) Interaction effects of root-zone salinity and solar irradiance on the physiology and biochemistry of Olea europaea. Environ Exp Bot 65:210–219

    Article  CAS  Google Scholar 

  • Rice-Evans C, Miller N, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–159

    Article  Google Scholar 

  • Ruiz-Carrasco K, Antognoni F, Coulibaly AK, Lizardi S, Covarrubias A, Martinez EA, Molina-Montenegro MA, Biondi S, Zurita-Silva A (2011) Variation in salinity tolerance of four lowland genotypes of quinoa (Chenopodium quinoa Willd.) as assessed by growth, physiological traits, and sodium transporter gene expression. Plant Physiol Biochem 49:1333–1341

    Article  CAS  PubMed  Google Scholar 

  • Sairam RK, Deshmukh PS, Shukla DS (1997) Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. J Agro Crop Sci 178:171–178

    Article  CAS  Google Scholar 

  • Sheokand S, Kumari A, Sawhney V (2008) Effect of nitric oxide and putrescine on antioxidative responses under NaCl stress in chickpea plants. Physiol Mol Biol Plants 14:355–362

    Article  CAS  PubMed  Google Scholar 

  • Shetty KG, Hetrick BAD, Schwab AP (1995) Effects of mycorrhizae and fertilizer amendments on zinc tolerance of plants. Environ Pollut 88:307–314

    Article  CAS  PubMed  Google Scholar 

  • Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45(8):542–550

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide intolerance of plants to abiotic stress. Protoplasma 248:447–455

    Article  CAS  PubMed  Google Scholar 

  • Singleton VL, Rossi JR (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid. Amer J Enol Vitic 16:144–158

    CAS  Google Scholar 

  • Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi S, Yamasaki H (2002) Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. FEBS Lett 512:145–148

    Article  CAS  PubMed  Google Scholar 

  • Tanou G, Molassiotis A, Diamantidis G (2009a) Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environ Exp Bot 65:270–281

    Article  CAS  Google Scholar 

  • Tanou G, Molassiotis A, Diamantidis G (2009b) Hydrogen peroxide-and nitric oxide-induced systemic antioxidant prime-like activity under NaCl-stress and stress-free conditions in citrus plants. J Plant Physiol 166:1904–1913

    Article  CAS  PubMed  Google Scholar 

  • Tavallali V, Rahemi M, Panahi B (2008) Calcium induces salinity tolerance in pistachio rootstocks. Fruits 63:285–296

    Article  CAS  Google Scholar 

  • Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defence system. J Plant Physiol 162:669–677

    Article  CAS  PubMed  Google Scholar 

  • Wendehenne D, Pugin A, Klessig DF, Durner J (2001) Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci 6:177–183

    Article  CAS  PubMed  Google Scholar 

  • Wink DA, Hanbauer I, Krishna MC, DeGraff W, Gamson J, Mitchell JB (1993) Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci USA 90:9813–9817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin R, Bai T, Ma F, Wang X, Li Y, Yue Z (2010) Physiological responses and relative tolerance by Chinese apple rootstocks to NaCl stress. Sci Hort 126:247–252

    Article  CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Agriculture, Department of Horticulture, Bozok University, 66200, Yozgat, Turkey

    Servet Aras & Hakan Keles

  2. Faculty of Agriculture, Department of Horticulture, Selcuk University, 42030, Konya, Turkey

    Ahmet Eşitken

Authors
  1. Servet Aras
    View author publications

    Search author on:PubMed Google Scholar

  2. Hakan Keles
    View author publications

    Search author on:PubMed Google Scholar

  3. Ahmet Eşitken
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Servet Aras.

Ethics declarations

Conflict of interest

S. Aras, H. Keles and A. Eşitken declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aras, S., Keles, H. & Eşitken, A. SNP Mitigates Malignant Salt Effects on Apple Plants. Erwerbs-Obstbau 62, 107–115 (2020). https://doi.org/10.1007/s10341-019-00445-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10341-019-00445-1

Keywords

Schlüsselwörter