Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Early effects of salt stress on the physiological and oxidative status of the halophyte Lobularia maritima

Anis Ben Hsouna A B , Thaura Ghneim-Herrera C , Walid Ben Romdhane A D , Amira Dabbous E , Rania Ben Saad A , Faical Brini A , Chedly Abdelly E and Karim Ben Hamed https://orcid.org/0000-0002-5781-3809 E F
+ Author Affiliations
- Author Affiliations

A Biotechnology and Plant Improvement Laboratory, Centre of Biotechnology of Sfax, University of Sfax, PO Box 1177, 3018 Sfax, Tunisia.

B Departments of Life Sciences, Faculty of Sciences of Gafsa, 2112 Gafsa, Tunisia.

C Departamento de Ciencias Biológicas, Universidad Icesi, Calle 18 No. 122-135, Cali, Colombia.

D Plant Production Department, College of Food and Agricultural Sciences, King Saud University, PO Box 2460, 11451 Riyadh, Saudi Arabia.

E Laboratory of Extremophile Plants, Center of Biotechnology of Borj Cedria, PO Box 901, 2050 Hammam Lif, Tunisia.

F Corresponding author. Email: kbenhamed@yahoo.fr

Functional Plant Biology 47(10) 912-924 https://doi.org/10.1071/FP19303
Submitted: 21 October 2019  Accepted: 18 April 2020   Published: 2 July 2020

Abstract

Soil salinity is an abiotic stress that reduces agricultural productivity. For decades, halophytes have been studied to elucidate the physiological and biochemical processes involved in alleviating cellular ionic imbalance and conferring salt tolerance. Recently, several interesting genes with proven influence on salt tolerance were isolated from the Mediterranean halophyte Lobularia maritima (L.) Desv. A better understanding of salt response in this species is needed to exploit its potential as a source of stress-related genes. We report the characterisation of L. maritima’s response to increasing NaCl concentrations (100–400 mM) at the physiological, biochemical and molecular levels. L. maritima growth was unaffected by salinity up to 100 mM NaCl and it was able to survive at 400 mM NaCl without exhibiting visual symptoms of damage. Lobularia maritima showed a Na+ and K+ accumulation pattern typical of a salt-includer halophyte, with higher contents of Na+ in the leaves and K+ in the roots of salt-treated plants. The expression profiles of NHX1, SOS1, HKT1, KT1 and VHA-E1 in salt-treated plants matched this Na+ and K+ accumulation pattern, suggesting an important role for these transporters in the regulation of ion homeostasis in leaves and roots of L. maritima. A concomitant stimulation in phenolic biosynthesis and antioxidant enzyme activity was observed under moderate salinity, suggesting a potential link between the production of polyphenolic antioxidants and protection against salt stress in L. maritima. Our findings indicate that the halophyte L. maritima can rapidly develop physiological and antioxidant mechanisms to adapt to salt and manage oxidative stress.

Additional keywords: antioxidant enzymes, gene expression, ion homeostasis, polyphenols, short-term responses, sweet alyssum.


References

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 6727660PubMed |

Agati G, Tattini M (2010) Multiple functional roles of flavonoids in photoprotection. New Phytologist 186, 786–793.
Multiple functional roles of flavonoids in photoprotection.Crossref | GoogleScholarGoogle Scholar | 20569414PubMed |

Al-Shehbaz IA, Beilstein MA, Kellogg EA (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Systematics and Evolution 259, 89–120.
Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview.Crossref | GoogleScholarGoogle Scholar |

Arvouet-Grand A, Vennat B, Pourrat A, Legret P (1994) Standardization of propolis extract and identification of principal constituents. Journal de Pharmacie de Belgique 49, 462–468.

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 |

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar |

Ben Saad R, Ben Hsouna A, Saibi W, Ben Hamed K, Brini F, Ghneim-Herrera T (2018a) A stress-associated protein, LmSAP, from the halophyte Lobularia maritima provides tolerance to heavy metals in tobacco through increased ROS scavenging and metal detoxification processes. Journal of Plant Physiology 231, 234–243.
A stress-associated protein, LmSAP, from the halophyte Lobularia maritima provides tolerance to heavy metals in tobacco through increased ROS scavenging and metal detoxification processes.Crossref | GoogleScholarGoogle Scholar |

Ben Saad R, Farhat-Khemekhem A, Ben Halima N, Ben Hamed K, Brini F, Saibi W (2018b) The LmSAP gene isolated from the halotolerant Lobularia maritima improves salt and ionic tolerance in transgenic tobacco lines. Functional Plant Biology 45, 378–391.
The LmSAP gene isolated from the halotolerant Lobularia maritima improves salt and ionic tolerance in transgenic tobacco lines.Crossref | GoogleScholarGoogle Scholar | 32290960PubMed |

Benzarti M, Ben Rejeb K, Messedi D, Ben Mna A, Hessini K, Ksontini M, Abdelly C, Debez A (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 |

Blum A, Munns R, Passioura JB, Turner NC, Sharp RE, Boyer JS, Nguyen HT, Hsiao TC, Verma DPS, Hong Z (1996) Genetically engineered plants resistant to soil drying and salt stress: how to interpret osmotic relations? Plant Physiology 110, 1051–1053.
Genetically engineered plants resistant to soil drying and salt stress: how to interpret osmotic relations?Crossref | GoogleScholarGoogle Scholar | 12226240PubMed |

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 | 24368505PubMed |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |

Chaparzadeh N, D’Amico ML, Khavari-Nejad RA, Izzo R, Navari-Izzo F (2004) Antioxidative responses of Calendula officinalis under salinity conditions. Plant Physiology and Biochemistry 42, 695–701.
Antioxidative responses of Calendula officinalis under salinity conditions.Crossref | GoogleScholarGoogle Scholar | 15474374PubMed |

Dabbous A, Ben Saad R, Brini F, Farhat-Khemekhem A, Zorrig W, Abdely C, Ben Hamed K (2017) Over-expression of a subunit E1 of a vacuolar H+-ATPase gene (LmVHA-E1) cloned from the halophyte Lobularia maritima improves the tolerance of Arabidopsis thaliana to salt and osmotic stresses. Environmental and Experimental Botany 137, 128–141.
Over-expression of a subunit E1 of a vacuolar H+-ATPase gene (LmVHA-E1) cloned from the halophyte Lobularia maritima improves the tolerance of Arabidopsis thaliana to salt and osmotic stresses.Crossref | GoogleScholarGoogle Scholar |

Debez A, Saadaoui D, Ramani B, Ouerghi Z, Koyro HW, Huchzermeyer B, Abdelly C (2006) Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity. Environmental and Experimental Botany 57, 285–295.
Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity.Crossref | GoogleScholarGoogle Scholar |

Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimental Botany 65, 1259–1270.
Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment.Crossref | GoogleScholarGoogle Scholar | 24520019PubMed |

Diaz-Pérez JC, Shackel KA, Sutter EG (1995) Relative water content and water potential of tissue 1. Journal of Experimental Botany 46, 111–118.
Relative water content and water potential of tissue 1.Crossref | GoogleScholarGoogle Scholar |

Draper HH, Squires EJ, Mahmoodi H, Wu J, Agarwal S, Hadley M (1993) A comparative evaluation of thiobarbituric acid methods for the determination of malondialdehyde in biological materials. Free Radical Biology & Medicine 15, 353–363.
A comparative evaluation of thiobarbituric acid methods for the determination of malondialdehyde in biological materials.Crossref | GoogleScholarGoogle Scholar |

Ellouzi H, Ben Hamed K, Cela J, Munne-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 | 21288246PubMed |

Ellouzi H, Ben Hamed K, Hernandez I, Cela J, Muller M, Magne C, Abdelly C, Munne-Bosch S (2014) A comparative study of the early osmotic, ionic, redox and hormonal signaling response in leaves and roots of two halophytes and a glycophyte to salinity. Planta 240, 1299–1317.
A comparative study of the early osmotic, ionic, redox and hormonal signaling response in leaves and roots of two halophytes and a glycophyte to salinity.Crossref | GoogleScholarGoogle Scholar | 25156490PubMed |

Epstein E (1972) ‘Mineral nutrition of plants: principles and perspectives.’ (John Wiley and Sons: New York)

Faller ALK, Fialho E (2010) Polyphenol content and antioxidant capacity in organic and conventional plant foods. Journal of Food Composition and Analysis 23, 561–568.
Polyphenol content and antioxidant capacity in organic and conventional plant foods.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 |

Hajiboland R, Bahrami-Rad S, Zeinalzade N, Atazadeh E, Akhani H, Poschenrieder C (2020) Differential functional traits underlying the contrasting salt tolerance in Lepidium species. Plant and Soil 448, 315–334.
Differential functional traits underlying the contrasting salt tolerance in Lepidium species.Crossref | GoogleScholarGoogle Scholar |

Han RM, Lefevre I, Albacete A, Perez-Alfocea F, Barba-Espin G, Diaz-Vivancos P, Quinet M, Ruan CJ, Hernandez JA, Cantero-Navarro E, Lutts S (2013) Antioxidant enzyme activities and hormonal status in response to Cd stress in the wetland halophyte Kosteletzkya virginica under saline conditions. Physiologia Plantarum 147, 352–368.
Antioxidant enzyme activities and hormonal status in response to Cd stress in the wetland halophyte Kosteletzkya virginica under saline conditions.Crossref | GoogleScholarGoogle Scholar | 22697433PubMed |

Hasegawa PM (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environmental and Experimental Botany 92, 19–31.
Sodium (Na+) homeostasis and salt tolerance of plants.Crossref | GoogleScholarGoogle Scholar |

Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
Plant cellular and molecular responses to high salinity.Crossref | GoogleScholarGoogle Scholar | 15012199PubMed |

Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant, Cell & Environment 33, 552–565.
A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress.Crossref | GoogleScholarGoogle Scholar |

Kirby AJ, Schmidt RJ (1997) The antioxidant activity of Chinese herbs for eczema and of placebo herbs. Journal of Ethnopharmacology 56, 103–108.
The antioxidant activity of Chinese herbs for eczema and of placebo herbs.Crossref | GoogleScholarGoogle Scholar | 9174970PubMed |

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 | 17408958PubMed |

Kumari A, Das P, Parida AK, Agarwal PK (2015) Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Frontiers in Plant Science 6, 537
Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 26284080PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods (San Diego, Calif.) 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar |

Maathuis FJM (2006) The role of monovalent cation transporters in plant responses to salinity. Journal of Experimental Botany 57, 1137–1147.
The role of monovalent cation transporters in plant responses to salinity.Crossref | GoogleScholarGoogle Scholar |

Maathuis FJM (2014) Sodium in plants: perception, signalling, and regulation of sodium fluxes. Journal of Experimental Botany 65, 849–858.
Sodium in plants: perception, signalling, and regulation of sodium fluxes.Crossref | GoogleScholarGoogle Scholar |

Maehly AC, Chance B (1954) The assay of catalases and peroxidases. Methods of Biochemical Analysis 1, 357–424.

Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology 52, 561–591.
Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 11337409PubMed |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 18444910PubMed |

Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
A revised medium for rapid growth and bio assays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar |

Muthukumarasamy M, Gupta SD, Panneerselvam R (2000) Enhancement of peroxidase, polyphenol oxidase and superoxide dismutase activities by triadimefon in NaCl stressed Raphanus sativus L. Biologia Plantarum 43, 317–320.
Enhancement of peroxidase, polyphenol oxidase and superoxide dismutase activities by triadimefon in NaCl stressed Raphanus sativus L.Crossref | GoogleScholarGoogle Scholar |

Navarro-González I, González-Barrio R, García-Valverde V, Bautista-Ortín AB, Periago MJ (2015) Nutritional composition and antioxidant capacity in edible flowers: characterisation of phenolic compounds by HPLC-DAD-ESI/MSn. International Journal of Molecular Sciences 16, 805–822.
Nutritional composition and antioxidant capacity in edible flowers: characterisation of phenolic compounds by HPLC-DAD-ESI/MSn.Crossref | GoogleScholarGoogle Scholar |

Nikalje GC, Variyar PS, Joshi MV, Nikam TD, Suprasanna P (2018) Temporal and spatial changes in ion homeostasis, antioxidant defense and accumulation of flavonoids and glycolipid in a halophyte Sesuvium portulacastrum (L.) L. PLoS One 13, e0193394
Temporal and spatial changes in ion homeostasis, antioxidant defense and accumulation of flavonoids and glycolipid in a halophyte Sesuvium portulacastrum (L.) L.Crossref | GoogleScholarGoogle Scholar | 29641593PubMed |

Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
Ascorbate and glutathione: keeping active oxygen under control.Crossref | GoogleScholarGoogle Scholar | 15012235PubMed |

Oueslati S, Ksouri R, Falleh H, Pichette A, Abdelly C, Legault J (2012) Phenolic content, antioxidant, anti-inflammatory and anticancer activities of the edible halophyte Suaeda fruticosa Forssk. Food Chemistry 132, 943–947.
Phenolic content, antioxidant, anti-inflammatory and anticancer activities of the edible halophyte Suaeda fruticosa Forssk.Crossref | GoogleScholarGoogle Scholar |

Panta S, Flowers T, Lane P, Doyle R, Haros G, Shabala S (2014) Halophyte agriculture: success stories. Environmental and Experimental Botany 107, 71–83.
Halophyte agriculture: success stories.Crossref | GoogleScholarGoogle Scholar |

Parida AK, Das AB, Mohanty P (2004) Investigations on the antioxidative defense responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes. Plant Growth Regulation 42, 213–226.
Investigations on the antioxidative defense responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes.Crossref | GoogleScholarGoogle Scholar |

Pico FX, Retana J (2001) The flowering pattern of the perennial herb Lobularia maritima: an unusual case in the Mediterranean basin. Acta Oecologica 22, 209–217.
The flowering pattern of the perennial herb Lobularia maritima: an unusual case in the Mediterranean basin.Crossref | GoogleScholarGoogle Scholar |

Pirie A, Parsons D, Renggli J, Narkowicz C, Jacobson GA, Shabala S (2013) Modulation of flavonoid and tannin production of Carpobrotus rossii by environmental conditions. Environmental and Experimental Botany 87, 19–31.
Modulation of flavonoid and tannin production of Carpobrotus rossii by environmental conditions.Crossref | GoogleScholarGoogle Scholar |

Pokorny J, Yanishlieva N, Gordon M (2001) ‘Antioxidants in food: practical applications.’ (CRC Press: Boca Raton, FL)

Pollastri S, Tattini M (2011) Flavonols: old compounds for old roles. Annals of Botany 108, 1225–1233.
Flavonols: old compounds for old roles.Crossref | GoogleScholarGoogle Scholar | 21880658PubMed |

Popova OV, Golldack D (2007) In the halotolerant Lobularia maritima (Brassicaceae) salt adaptation correlates with activation of the vacuolar H+-ATPase and the vacuolar Na+/H+ antiporter. Journal of Plant Physiology 164, 1278–1288.
In the halotolerant Lobularia maritima (Brassicaceae) salt adaptation correlates with activation of the vacuolar H+-ATPase and the vacuolar Na+/H+ antiporter.Crossref | GoogleScholarGoogle Scholar | 17166622PubMed |

Popova OV, Yang O, Dietz KJ, Golldack D (2008) Differential transcript regulation in Arabidopsis thaliana and the halotolerant Lobularia maritima indicates genes with potential function in plant salt adaptation. Gene 423, 142–148.
Differential transcript regulation in Arabidopsis thaliana and the halotolerant Lobularia maritima indicates genes with potential function in plant salt adaptation.Crossref | GoogleScholarGoogle Scholar | 18703123PubMed |

Qiu N, Chen M, Guo J, Bao H, Ma X, Wang B (2007) Coordinate up-regulation of V-H+-ATPase and vacuolar Na+/H+ antiporter as a response to NaCl treatment in a C3 halophyte Suaeda salsa. Plant Science 172, 1218–1225.
Coordinate up-regulation of V-H+-ATPase and vacuolar Na+/H+ antiporter as a response to NaCl treatment in a C3 halophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar |

Rezaei-Moshaei M, Nematzadeh GA, Askari H, Nejad ASM, Pakdin A (2014) Quantitative gene expression analysis of some sodium ion transporters under salinity stress in Aeluropus littoralis. Saudi Journal of Biological Sciences 21, 394–399.
Quantitative gene expression analysis of some sodium ion transporters under salinity stress in Aeluropus littoralis.Crossref | GoogleScholarGoogle Scholar | 25313273PubMed |

Rodrigues MJ, Soszynski A, Martins A, Rauter AP, Neng NR, Nogueira JMF, Varela J, Barreira L, Custódio L (2015) Unravelling the antioxidant potential and the phenolic composition of different anatomical organs of the marine halophyte Limonium algarvense. Industrial Crops and Products 77, 315–322.
Unravelling the antioxidant potential and the phenolic composition of different anatomical organs of the marine halophyte Limonium algarvense.Crossref | GoogleScholarGoogle Scholar |

Rodríguez AA, Taleisnik EL (2012) Determination of reactive oxygen species in salt-stressed plant tissues. Methods in Molecular Biology (Clifton, N.J.) 913, 225–236.
Determination of reactive oxygen species in salt-stressed plant tissues.Crossref | GoogleScholarGoogle Scholar |

Sanadhya P, Agarwal P, Agarwal PK (2015) Ion homeostasis in a salt-secreting halophytic grass. AoB Plants 7, plv055
Ion homeostasis in a salt-secreting halophytic grass.Crossref | GoogleScholarGoogle Scholar | 25990364PubMed |

Scebba F, Sebastiani L, Vitagliano C (1999) Protective enzymes against activated oxygen species in wheat (Triticum aestivum L.) seedlings: responses to cold acclimation. Journal of Plant Physiology 155, 762–768.
Protective enzymes against activated oxygen species in wheat (Triticum aestivum L.) seedlings: responses to cold acclimation.Crossref | GoogleScholarGoogle Scholar |

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, Mackay A (2011) Ion transport in halophytes. Advances in Botanical Research 57, 151–199.
Ion transport in halophytes.Crossref | GoogleScholarGoogle Scholar |

Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. The Plant Cell 14, 465–477.
The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants.Crossref | GoogleScholarGoogle Scholar | 11884687PubMed |

Silva P, Geros H (2009) Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange. Plant Signaling & Behavior 4, 718–726.
Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange.Crossref | GoogleScholarGoogle Scholar |

Slama I, Ghnaya T, Savoure A, Abdelly C (2008) Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum. Comptes Rendus Biologies 331, 442–451.
Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum.Crossref | GoogleScholarGoogle Scholar | 18510997PubMed |

Sokal RR Rohlf FJ (1969) ‘The principles and practice of statistics in biological research.’ (WH Freeman and Co.: San Francisco, CA)

Souid A, Gabriele M, Longo V, Pucci L, Bellani L, Smaoui A, Abdelly C, Ben Hamed K (2016) Salt tolerance of the halophyte Limonium delicatulum is more associated with antioxidant enzyme activities than phenolic compounds. Functional Plant Biology 43, 607–619.
Salt tolerance of the halophyte Limonium delicatulum is more associated with antioxidant enzyme activities than phenolic compounds.Crossref | GoogleScholarGoogle Scholar |

Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP-test. In ‘Photosynthesis: from light to biosphere’. (Ed. P Mathis) pp. 977–980. (Kluwer Academic Publisher: Dordrecht)

Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends in Plant Science 15, 89–97.
Proline: a multifunctional amino acid.Crossref | GoogleScholarGoogle Scholar | 20036181PubMed |

Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiology 135, 1697–1709.
Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray.Crossref | GoogleScholarGoogle Scholar | 15247402PubMed |

Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
Na+ tolerance and Na+ transport in higher plants.Crossref | GoogleScholarGoogle Scholar | 12646496PubMed |

Turkan I, Uzilday B, Dietz KJ, Brautigam A, Ozgur R (2018) Reactive oxygen species and redox regulation in mesophyll and bundle sheath cells of C4 plants. Journal of Experimental Botany 69, 3321–3331.
Reactive oxygen species and redox regulation in mesophyll and bundle sheath cells of C4 plants.Crossref | GoogleScholarGoogle Scholar | 29529246PubMed |

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3 – new capabilities and interfaces. Nucleic Acids Research 40, e115
Primer3 – new capabilities and interfaces.Crossref | GoogleScholarGoogle Scholar | 22730293PubMed |

Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants – protective role of exogenous polyamines. Plant Science 151, 59–66.
Oxidative stress and some antioxidant systems in acid rain-treated bean plants – protective role of exogenous polyamines.Crossref | GoogleScholarGoogle Scholar |

Wang MC, Peng ZY, Li CL, Li F, Liu C, Xia GM (2008) Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics 8, 1470–1489.
Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum.Crossref | GoogleScholarGoogle Scholar | 18383010PubMed |

Waterman PG, Mole S (1994) ‘Analysis of phenolic plant metabolites.’ Methods in Ecology. (Blackwell Scientific Publications: Oxford)

Zhang H (2002) A study on the characters of content of inorganic ions in salt-stressed Suaeda salsa. Xibei Zhiwu Xuebao 25, 129–135.

Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
Plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 11173290PubMed |

Zouari N, Ben Saad R, Legavre T, Azaza J, Sabau X, Jaoua M, Masmoudi K, Hassairi A (2007) Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis. Gene 404, 61–69.
Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis.Crossref | GoogleScholarGoogle Scholar | 17916418PubMed |