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Plant function and evolutionary biology
RESEARCH ARTICLE

Salt tolerance of the halophyte Limonium delicatulum is more associated with antioxidant enzyme activities than phenolic compounds

Aymen Souid A , Morena Gabriele B , Vincenzo Longo B , Laura Pucci B , Lorenza Bellani B C , Abderrazak Smaoui A , Chedly Abdelly A and Karim Ben Hamed A D
+ Author Affiliations
- Author Affiliations

A Laboratoire des Plantes Extrêmophiles, Centre de Biotechnologie de Borj Cedria, BP 901, Hammam Lif 2050, Tunisia.

B National Research Council, Institute of Biology and Agricultural Biotechnology (IBBA), Pisa Unit, Research Area of Pisa, Via Moruzzi 1, 56124 Pisa, Italy.

C Department of Life Sciences, University of Siena, Via A. Moro 2, 53100 Siena, Italy.

D Corresponding author. Email: kbenhamed@yahoo.fr

Functional Plant Biology 43(7) 607-619 https://doi.org/10.1071/FP15284
Submitted: 12 September 2015  Accepted: 6 March 2016   Published: 13 May 2016

Abstract

In this work we studied the effect of salinity (ranging from 50 to 500 mM NaCl) on the physiological and the antioxidant responses of the local halophyte Limonium delicatulum Kuntze. We based our analysis on 12 biochemical assays that are commonly used to measure the antioxidant responses under stress such as oxidative stress markers, enzymes activities and polyphenolic compounds. Our aim was to study parameters that are strongly correlated with the growth response to salinity. Results showed two different growth responses depending on the concentration of NaCl in the medium. Under 50 to 200 mM, the growth was stimulated before it decreased significantly at 300–500 mM. L. delicatulum revealed a good aptitude to maintain photosynthetic machinery by increasing the concentrations of photosynthetic pigments, which is essential for the stabilisation of photosystems and the photosynthesis process under optimal NaCl concentration. Their breakdown at higher salinity decreased the photosynthetic performance of plants resulting in growth inhibition. Moreover, to reduce the damaging effect of oxidative stress and to tolerate the accumulation of salt ions, L. delicatulum induced the activities of their antioxidant enzymes more than their contents in polyphenolic compounds.

Additional keywords: antioxidant enzymes, halophyte, Limonium delicatulum, polyphenols, salinity.


References

Abideen Z, Qassim M, Rasheed A, Adnan MY, Gul B, Khan MA (2015) Antioxidant activity and polyphenol content of Phragmites karka under saline conditions. Pakistan Journal of Botany 47, 813–818.

Aebi H (1984) Catalase in vitro Methods in Enzymology 105, 121–126.
Catalase in vitro Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXltVKis7s%3D&md5=a787c8d94f03cc2abe3e410eac513bf6CAS | 6727660PubMed |

Agastian P, Kingsley SJ, Vivekanandan M (2000) Effect of salinity on photosynthesis and biochemical characteristics in mulberry genotypes. Photosynthetica 38, 287–290.
Effect of salinity on photosynthesis and biochemical characteristics in mulberry genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptVeht70%3D&md5=eef225253dfe6f685734a8984d3b93bbCAS |

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=99fa8bbb1f5b69ffca6fc56116a2dc3fCAS | 15377225PubMed |

Arbona V, Flors V, Garcia-Agustin P, Gomez-Cadenas A (2003) Enzymatic and non-enzymatic antioxidant responses of Carrizo citrange, salt-sensitive citrus rootstock, to different levels of salinity. Plant & Cell Physiology 44, 388–394.
Enzymatic and non-enzymatic antioxidant responses of Carrizo citrange, salt-sensitive citrus rootstock, to different levels of salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt1Wms7k%3D&md5=56516d1802baea564d8b1e533c5f1616CAS |

Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141, 391–396.
Production and scavenging of reactive oxygen species in chloroplasts and their functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aksbY%3D&md5=02aa399fad32027ca0622e210b7c849bCAS | 16760493PubMed |

Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Science 166, 3–16.
Potential biochemical indicators of salinity tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVOqsA%3D%3D&md5=3b0f0cc62abc821e694d743555aeafecCAS |

Azevedo Neto AD, Prisco JT, Enéas-Filho J, Abreu CEB, 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. Environmental and Experimental Botany 56, 87–94.
Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes.Crossref | GoogleScholarGoogle Scholar |

Azevedo Neto AD, Gomes-Filho E, Prisco JT (2008) Salinity and oxidative stress. In ‘Abiotic stress and plant responses’. (Eds NA Khan, S Sarvajeet) pp. 58–82. (IK International: New Delhi)

Bacchiocca M, Biagiotti E, Ninfali P (2006) Nutritional and technological reasons for evaluating the antioxidant capacity of vegetable products. Italian Journal of Food Science 18, 1–9.

Bangerth F (1979) Calcium related physiological disorders of plants. Annual Review of Phytopathology 17, 97–122.
Calcium related physiological disorders of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXlslWmuro%3D&md5=779f324230dbe9aa19b147109951dd11CAS |

Barhoumi Z, Djebali W, Smaoui A, Chaïbi W, Abdelly C (2007) Contribution of NaCl excretion to salt resistance of Aeluropus littoralis (Wild). Journal of Plant Physiology 164, 842–850.
Contribution of NaCl excretion to salt resistance of Aeluropus littoralis (Wild).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXoslSisbc%3D&md5=acc919c1df416626a44845df2a23ca66CAS | 16876911PubMed |

Ben Amor N, Ben Hamed K, Debez A, Grignon C, Abdelly C (2005) Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity. Plant Science 168, 889–899.
Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslWnsbo%3D&md5=fed262de331473d580b8ce4c0430c1deCAS |

Ben Amor N, Jimenez A, Megdiche W, Lundqvist M, Sevilla F, Abdelly C (2006) Response of antioxidant systems to NaCl stress in the halophyte Cakile maritima. Plant Physiology 126, 446–457.
Response of antioxidant systems to NaCl stress in the halophyte Cakile maritima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVehur8%3D&md5=8ba2223a72f73592955d14a2002bf134CAS |

Ben Hamed K, Castagna A, Salem E, Ranieri AM, Abdelly C (2007) Sea fennel (Crithmum maritimum L.) under salinity conditions: a comparison of leaf and root antioxidant responses. Plant Growth Regulation 53, 185–194.
Sea fennel (Crithmum maritimum L.) under salinity conditions: a comparison of leaf and root antioxidant responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ahs7jN&md5=109efbfa782943c6fd920ddc2da7ad68CAS |

Ben Hamed K, Chibani F, Abdelly C, Magne C (2014) Growth, sodium uptake and antioxidant responses of coastal plants differing in their ecological status under increasing salinity. Biologia 69, 193–201.
Growth, sodium uptake and antioxidant responses of coastal plants differing in their ecological status under increasing salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVSqtL%2FO&md5=93644624b00977338f44425a226f6f14CAS |

Benzarti M, Rejeb KB, Debez A, Abdelly C (2014) Effect of high salinity on Atriplex portulacoides: growth, leaf water relations and solute accumulation in relation with osmotic adjustment. South African Journal of Botany 95, 70–77.
Effect of high salinity on Atriplex portulacoides: growth, leaf water relations and solute accumulation in relation with osmotic adjustment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFShs7jN&md5=48e5f2e9358a6cc84aed3ba5a55a775eCAS |

Boestfleisch C, Wagenseil NB, Buhmann AK, Seal CE, Wade EM, Muscolo A, Papenbrock J (2014) Manipulating the antioxidant capacity of halophytes to increase their cultural and economic value through saline cultivation. AoB Plants 6, plu046
Manipulating the antioxidant capacity of halophytes to increase their cultural and economic value through saline cultivation.Crossref | GoogleScholarGoogle Scholar | 25125698PubMed |

Bor M, Özdemir F, Türkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Science 164, 77–84.
The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFertrw%3D&md5=252702310b14fc4440e20595e4109d96CAS |

Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany 65, 1241–1257.
ROS homeostasis in halophytes in the context of salinity stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks12htbY%3D&md5=75f259e49c111146271aa61a36df1a47CAS | 24368505PubMed |

Bouchenak F, Henri P, Benrebiha FZ, Rey P (2012) Differential responses to salinity of two Atriplex halimus populations in relation to organic solutes and antioxidant systems involving thiol reductases. Journal of Plant Physiology 169, 1445–1453.
Differential responses to salinity of two Atriplex halimus populations in relation to organic solutes and antioxidant systems involving thiol reductases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtV2nurrK&md5=f0385732502af1c14832a0a5fe2bd882CAS | 22840322PubMed |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=436242ae9b449e7335b086f00b7e6e5fCAS | 942051PubMed |

Cayuela E, Esta MT, Parra M, Caro M, Bolarin MC (2001) NaCl pre-treatment at the seedling stage enhances fruit yield of tomato irrigated with salt water. Plant and Soil 230, 231–238.
NaCl pre-treatment at the seedling stage enhances fruit yield of tomato irrigated with salt water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt12qs70%3D&md5=1d8cd6e3efd767b8104b0bcb911f3e18CAS |

Chance B, Maehly A (1955) Assay of catalases and peroxidases. Methods in Enzymology 2, 764–775.
Assay of catalases and peroxidases.Crossref | GoogleScholarGoogle Scholar |

Debez A, Ben Hamed K, Grignon C, Abdelly C (2004) Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima. Plant and Soil 262, 179–189.
Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlGnsrg%3D&md5=713a16196bcaec67c9d98c7e97eba427CAS |

Dewanto V, Wu X, Adom KK, Liu RH (2002) Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. Journal of Agricultural and Food Chemistry 50, 3010–3014.
Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivVGns7c%3D&md5=149026fada4f42fff061f54fead5b9f2CAS | 11982434PubMed |

Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Science 135, 1–9.
Antioxidant responses of rice seedlings to salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkslGjtr0%3D&md5=4328701d354ef2168477e78532717995CAS |

Ellouzi H, Ben Hamed K, Cela J, Munné‐Bosch S, Abdelly C (2011) Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte). Physiologia Plantarum 142, 128–143.
Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFeru7c%3D&md5=90bae94f86372fae6529dc518f1490a3CAS | 21288246PubMed |

Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=ead9e0f52d5a777986f79fa03e42e1abCAS | 18565144PubMed |

Flowers TJ, Muscolo A (2015) Halophytes in a changing world. Annals of Botany 7,
Halophytes in a changing world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXoslWntrk%3D&md5=a61a759b7e9ade518faf20208592cf05CAS |

Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology 37, 604–612.
Evolution of halophytes: multiple origins of salt tolerance in land plants.Crossref | GoogleScholarGoogle Scholar |

Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Annals of Botany 115, 419–431.
Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 25466549PubMed |

Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in physiological context. Plant, Cell & Environment 28, 1056–1071.
Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in physiological context.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslSgs70%3D&md5=efa45151c717ef09e07d8cb08c254f8cCAS |

Gadetskaya AV, Tarawneh AH, Zhusupova GE, Gemejiyeva NG, Cantrell CL, Cutler SJ, Ross SA (2015) Sulfated phenolic compounds from Limonium caspium: isolation, structural elucidation, and biological evaluation. Fitoterapia 104, 80–85.
Sulfated phenolic compounds from Limonium caspium: isolation, structural elucidation, and biological evaluation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpsVyqtbc%3D&md5=a7b6d883e6a2d2b21ff2ef5f3ca0b350CAS | 26025854PubMed |

Galmés J, Flexas J, Savé R, Medrano H (2007) Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant and Soil 290, 139–155.
Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery.Crossref | GoogleScholarGoogle Scholar |

Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiology 59, 309–314.
Superoxide dismutases I. Occurrence in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhtlKgtrs%3D&md5=abeeff152b0c6330980b8b3b517b17b5CAS | 16659839PubMed |

Glenn E, Pfister R, Brown JJ, Thompson TL, O’leary J (1996) Na and K accumulation and salt tolerance of Atriplex Canescens (Chenopodiaceae) Genotypes. American Journal of Botany 83, 997–1005.
Na and K accumulation and salt tolerance of Atriplex Canescens (Chenopodiaceae) Genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlslyltL4%3D&md5=704b927f831068040fdbe7cf844adf8dCAS |

Gómez JM, Hernández JA, Jiménez A, del Río LA, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plants. Free Radical Research 31, 11–18.
Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plants.Crossref | GoogleScholarGoogle Scholar |

Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Annual Review of Plant Physiology 31, 149–190.
Mechanisms of salt tolerance in non-halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWntb4%3D&md5=61cb9bcc484c17fdb79bcc6025e26374CAS |

Grieve CM, Poss JA, Grattan SR, Shouse PJ, Leith JH, Zeng L (2005) Productivity and mineral nutrition of Limonium species irrigated with saline waste waters. Horticultural Science 40, 654–665.

Gul B, Khan MA (1998) Population characteristics of a coastal halophyte Arthrocnemum macrostachyum. Pakistan Journal of Botany 30, 189–197.

Gulzar S, Khan MA (2006) Comparative salt tolerance of perennial grasses. In ‘Ecophysiology of high salinity tolerant plants’. (Eds MA Khan, DJ Weber) pp. 239 253. (Springer, Dordrecht, The Netherlands)

Hameed A, Hussain T, Gulzar S, Aziz I, Gul B, Khan MA (2015) Effects of salinity and ascorbic acid on growth, water status and antioxidant system in a perennial halophyte. Annals of Botany 7, plv004
Effects of salinity and ascorbic acid on growth, water status and antioxidant system in a perennial halophyte.Crossref | GoogleScholarGoogle Scholar |

Harris MJ, Outlaw WH (1991) Rapid adjustment of guard-cell abscisic acid levels to current leaf-water status. Plant Physiology 95, 171–173.
Rapid adjustment of guard-cell abscisic acid levels to current leaf-water status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXnvVyrsw%3D%3D&md5=b90740a6e92371d0f7ce11ecac2b4358CAS | 16667946PubMed |

Hatano T, Kagawa H, Yasuhara T, Okuda T (1988) Two new flavonoids and other constituents in licorice root their relative astringency and radical scavenging effect. Chemical & Pharmaceutical Bulletin 36, 2090–2097.
Two new flavonoids and other constituents in licorice root their relative astringency and radical scavenging effect.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlsVajsLc%3D&md5=c0ef3dd7e2f05c76a7ea32d2feb0efe9CAS |

Hernandez JA, Almansa MS (2002) Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Plant Physiology 115, 251–257.
Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltVGms7w%3D&md5=ce05131c80dae93532d7f567562042cfCAS |

Hernandez JA, Corpas FJ, Gomez M, del Rio LA, Sevilla F (1993) Salt induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Plant Physiology 89, 103–110.
Salt induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsFyrtLg%3D&md5=2d8ea2423fa82f0a5e73146f7b399631CAS |

Hernandez JA, Campillo A, Jimenez A, Alacon JJ, Sevilla F (1999) Response of antioxidant systems and leaf water relations to NaCl stress in pea plants. New Phytologist 141, 241–251.
Response of antioxidant systems and leaf water relations to NaCl stress in pea plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFeku7c%3D&md5=404e395093153bfd8a02b3e81f9e33a8CAS |

Hewitt EJ (1966) ‘Sand and water culture methods used in the study of plant nutrition.’ (Commonwealth Agricultural Bureaux: Farnham Royal, England)

Ismail H, Shabala L, Tian Y, Jacobsen SE, Shabala S (2016) Rutin, a flavonoid with antioxidant activity, improves plant salinity tolerance by regulating K+ retention and Na+ exclusion from leaf mesophyll in quinoa and broad beans. Functional Plant Biology 43, 75–86.

Ivan MA, Zamfirache MM, Grigore MN, Oprica L (2012) Determination of antioxidant enzymatic activity in several halophytes from Dobrogea area. Analele Stiintifice ale Universitatii’ Alexandru Ioan Cuza’ din Iasi Sec. II a. Genetica si Biologie Moleculara 13, 47–53.

Khan MA, Ungar IA, Showalter AM (2000a) The effect of salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa (L.) Forssk. Journal of Arid Environments 45, 73–84.
The effect of salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa (L.) Forssk.Crossref | GoogleScholarGoogle Scholar |

Khan MA, Ungar IA, Showalter AM (2000b) Effects of salinity on growth, water relations and ion accumulation in the subtropical perennial halophyte, Atriplex griffithii var. stocksii. Annals of Botany 85, 225–232.
Effects of salinity on growth, water relations and ion accumulation in the subtropical perennial halophyte, Atriplex griffithii var. stocksii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsFCisw%3D%3D&md5=bd843067f62d257e50021292f2b6d3c0CAS |

Ksouri R, Megdiche W, Debez A, Falleh H, Grignon C, Abdelly C (2007) Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiology and Biochemistry 45, 244–249.
Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkslCiu70%3D&md5=de44ca3559a1da9b8c1c424d3d9a4b62CAS | 17408958PubMed |

Li Y (2008) Kinetics of the antioxidant response to salinity in the halophyte Limonium bicolor. Plant, Soil and Environment 54, 493–497.

Lichtenthaler HK, Welburn A (1983) Determination of total carotenoids and chlorophylls a and b of leaf extract in different solvents. Biochemical Society Transactions 11, 591–592.
Determination of total carotenoids and chlorophylls a and b of leaf extract in different solvents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhslSquro%3D&md5=dd864ca85d5608b7563b856afdfeb43dCAS |

Lokhande VH, Srivastava AK, Srivastava S, Nikam TD, Suprasanna P (2011) Regulated alterations in redox and energetic status are the key mediators of salinity tolerance in the halophyte Sesuvium portulacastrum (L.) L. Plant Growth Regulation 65, 287–298.
Regulated alterations in redox and energetic status are the key mediators of salinity tolerance in the halophyte Sesuvium portulacastrum (L.) L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtleru7fO&md5=03faf3b045c3d793c8bd4f714cd79a16CAS |

Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology 127, 1781–1787.
Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVWltA%3D%3D&md5=4c784a29eeb7a08a682f40cef723e808CAS | 11743121PubMed |

Maxwell K, Johnson N (2000) Chlorophyll fluorescence: a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence: a practical guide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2js74%3D&md5=b2079d1ff209536207d91054c5b02220CAS | 10938857PubMed |

Medini F, Ksouri R, Falleh H, Megdiche W, Trabelsi N, Abdelly C (2011) Effects of physiological stage and solvent on polyphenol composition, antioxidant and antimicrobial activities of Limonium densiflorum. Journal Medicinal Plant Research 5, 6719–6730.

Medini F, Legault J, Pichette A, Abdelly C, Ksouri R (2014) Antiviral efficacy of Limonium densiflorum against HSV-1 and influenza viruses. South African Journal of Botany 92, 65–72.
Antiviral efficacy of Limonium densiflorum against HSV-1 and influenza viruses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsVCjtb4%3D&md5=6c31451021dfc1ac31597ab6e528eeceCAS |

Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environmental and Experimental Botany 49, 69–76.
Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsFars7Y%3D&md5=4c45dc0b1d3d729dc4b1ef66400d1052CAS |

Miller G, Suzuki N, Ciftci-yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33, 453–467.
Reactive oxygen species homeostasis and signalling during drought and salinity stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltV2hur8%3D&md5=42f2cbcf2143d1c8e9db6fbe95dfa198CAS |

Møller MI, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annual Review of Plant Biology 58, 459–481.
Oxidative modifications to cellular components in plants.Crossref | GoogleScholarGoogle Scholar |

Munns R, Passioura JB (1984) Hydraulic resistance of plants. III. Effects of NaCl in barley and lupin. Australian Journal of Plant Physiology 11, 351–359.
Hydraulic resistance of plants. III. Effects of NaCl in barley and lupin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvFGgtQ%3D%3D&md5=49938db7b1b51cf253c4bc8d598edebdCAS |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=dd68a82a6d2c6414e1266213f98edac3CAS | 18444910PubMed |

Naidoo G, Rughunanan R (1990) Salt tolerance in the succulent, coastal halophyte, Sarcocornia natalensis. Journal of Experimental Botany 41, 497–502.
Salt tolerance in the succulent, coastal halophyte, Sarcocornia natalensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslGit7s%3D&md5=120d18d6b632332896f95073c052002cCAS |

Nakamura T, Nomura M, Mori H, Jagendorf AT, Ueda A, Takabe T (2001) An isozyme of betaine aldehyde dehydrogenase in barley. Plant & Cell Physiology 42, 1088–1092.
An isozyme of betaine aldehyde dehydrogenase in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvV2ktr0%3D&md5=599c3a197665b6e6fabea5974ef144b9CAS |

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

Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Biology 49, 249–279.
Ascorbate and glutathione: keeping active oxygen under control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVShtrc%3D&md5=87d91a87e031b21640ffe872c6ca679dCAS |

Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? Journal of Experimental Botany 46, 1351–1362.
Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFans78%3D&md5=7e590f456aa6fa44083c6eba472ace16CAS |

Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Functional Plant Biology 40, 832–847.

Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60, 324–349.
Salt tolerance and salinity effects on plants: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKlt7nN&md5=9d55e0ad2b8888272c2ab5e3fe9be232CAS | 15590011PubMed |

Pereira GJG, Molina SMG, Lea PJ, Azevedo RA (2002) Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea Plant and Soil 239, 123–132.
Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktVGhur4%3D&md5=f889b1fce2bd852a2bdb5360348b4e89CAS |

Redondo-Gómez S, Wharmby C, Castillo JM, Mateos-Naranjo E, Luque CJ, de Cires A, Luque T, Davy AJ, Figueroa ME (2006) Growth and photosynthetic responses to salinity in an extreme halophyte, Sarcocornia fruticosa. Physiologia Plantarum 128, 116–124.
Growth and photosynthetic responses to salinity in an extreme halophyte, Sarcocornia fruticosa.Crossref | GoogleScholarGoogle Scholar |

Reginato MA, Castagna A, Furlan A, Castro S, Ranieri A, Luna V (2014) Physiological responses of a halophytic shrub to salt stress by Na2SO4 and NaCl: oxidative damage and the role of polyphenols in antioxidant protection. AoB PLANTS 6, plu042
Physiological responses of a halophytic shrub to salt stress by Na2SO4 and NaCl: oxidative damage and the role of polyphenols in antioxidant protection.Crossref | GoogleScholarGoogle Scholar | 25063834PubMed |

Rengasamy P (2006) World salinization with emphasis on Australia. Journal of Experimental Botany 57, 1017–1023.
World salinization with emphasis on Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Gls74%3D&md5=38b33da6770809aae839b398e820dea4CAS | 16510516PubMed |

Rengel Z (1992) The role of calcium in salt toxicity. Plant, Cell & Environment 15, 625–632.
The role of calcium in salt toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtlSjtL4%3D&md5=1de5988b624acc62a077200a06261d0aCAS |

Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Science 163, 1037–1046.
Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosFeqtrk%3D&md5=6b05bb6ea03512bafea2103503efdf4eCAS |

Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Annals of Botany 112, 1209–1221.
Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops.Crossref | GoogleScholarGoogle Scholar | 24085482PubMed |

Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiologia Plantarum 151, 257–279.
Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXps1OjtL0%3D&md5=a0acade96ec4a194c130a751673c8ed0CAS | 24506225PubMed |

Strizhov N, Abraham E, Okresz L, Blickling S, Zilberstein A, Schell J (1997) Differential expression of two P5CS genes controlling proline accumulation during salt stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. The Plant Journal 12, 557–569.
Differential expression of two P5CS genes controlling proline accumulation during salt stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntVCktb4%3D&md5=7cacb6c2bdbe724ed9d2b721dd766d63CAS | 9351242PubMed |

Telesiñski A, Nowak J, Smolik B, Dubowska A, Skrzypiec N (2008) Effect of soil salinity on activity of antioxidant enzymes and content of ascorbic acid and phenols in bean (Phaseolus vulgaris L.) plants. Journal of Elementology 13, 401–409.

Ungar IA (1996) Effect of salinity on seed germination, growth, and ion accumulation of Atriplex patula (Chenopodiaceae). American Journal of Botany 83, 604–607.
Effect of salinity on seed germination, growth, and ion accumulation of Atriplex patula (Chenopodiaceae).Crossref | GoogleScholarGoogle Scholar |

Uzilday B, Ozgur R, Sekmen AH, Yildiztugay E, Turkan I (2015) Changes in the alternative electron sinks and antioxidant defence in chloroplasts of the extreme halophyte Eutrema parvulum (Thellungiella parvula) under salinity. Annals of Botany 115, 449–463.
Changes in the alternative electron sinks and antioxidant defence in chloroplasts of the extreme halophyte Eutrema parvulum (Thellungiella parvula) under salinity.Crossref | GoogleScholarGoogle Scholar | 25231894PubMed |

Yang C, Shi D, Wang D (2008) Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge.). Plant Growth Regulation 56, 179–190.
Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKjur%2FP&md5=90182f4b9260c255729c2b8b3e19ec03CAS |

Yeo AR (1998) Molecular biology of salt tolerance in the context of whole-plant physiology. Journal of Experimental Botany 49, 915–928.