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

Hordeum vulgare and Hordeum maritimum respond to extended salinity stress displaying different temporal accumulation pattern of metabolites

Selma Ferchichi A , Kamel Hessini A B , Emilia Dell’Aversana C , Luisa D’Amelia C , Pasqualina Woodrow C , Loredana F. Ciarmiello C , Amodio Fuggi C and Petronia Carillo C D
+ Author Affiliations
- Author Affiliations

A Laboratory of Extremophile Plants, Center of Biotechnology of Borj Cedria, University of Elmanar, B.P. 901, Hammam-Lif 2050, Tunisia.

B Biology Department, Faculty of Science, Taif University, 21974 Taif, P.O. Box 888, Saudi Arabia.

C Department of Environmental, Biological and Pharmaceutical Sciences and Technologies, University of Campania ‘Luigi Vanvitelli’, Via Vivaldi 43, 81100 Caserta, Italy.

D Corresponding author. Email: petronia.carillo@unicampania.it

Functional Plant Biology 45(11) 1096-1109 https://doi.org/10.1071/FP18046
Submitted: 27 February 2018  Accepted: 21 April 2018   Published: 18 May 2018

Abstract

Hordeum maritimum With. (= H. marinum Huds. subsp. marinum, 2n = 14) is a wild cereal present in the saline depressions of the Soliman and Kelbia Sebkhas, which contributes significantly to annual biomass production in Tunisia. This species is able to tolerate high NaCl concentrations at the seedling stage without showing symptoms of toxicity; however, the tolerance strategy mechanisms of this plant have not yet been unravelled. Our metabolite analysis, performed on leaves of H. maritimum during extended stress in comparison with Hordeum vulgare L. cv. Lamsi, has revealed an adaptive response of the wild species based on a different temporal accumulation pattern of ions and compatible metabolites. Further, wild and cultivated genotypes with contrasting salt-tolerant behaviour display different pattern of metabolites when salt stress is prolonged over 2 weeks. In particular, when exposed to up to 3 weeks of 200 mM NaCl salt stress, H. maritimum is able to maintain lower leaf concentrations of sodium and chloride, and higher concentrations of potassium compared with H. vulgare. This likely restricts sodium entry into plants at the root level, and uses the toxic ions, glycine betaine and low levels of proline for osmotic adjustment. Under prolonged stress, the accumulation of proline increases, reaching the highest levels in concomitance with the decrease of potassium to sodium ratio, the increase of hydrogen peroxide and decrease of chlorophylls. The modulation of proline accumulation over time can be interpreted as an adaptive response to long-term salinity. Moreover, once synthetised glycine betaine is transported but not metabolised, it can contribute together with proline to osmotically balance H. maritimum leaves and protect them from oxidative stress. The 2–3 week delay of H. maritimum in showing the symptoms of stress and damages compared with H. vulgare could be important in the survival of plants when soil salinity is not a permanent condition, but just a transient state of stress.

Additional keywords: osmolality, osmotic adjustment, potassium-to-sodium ratio, proline, wild barley.


References

Abdelly C (2017) Exploring genotypic diversity to optimize barley grain and straw quality under marginal/stressful growth conditions. BarlEy Stress Tolerance (BEST) ARIMNet 2 Midterm Project Evaluation Meeting, 12 October 2017, Montpellier, France. Available at http://www.arimnet2.net/files/presentations_mid-term_montpellier2017/BEST_ARIMNet2_MidTerm_12-10-2017.pdf [Verified 30 April 2018]

Abdelly C, Lachaal M, Grignon C, Soltani A, Hajji M (1995) Association épisodique d’halophytes strictes et de glycophytes dans un écosystème hydromorphe salé en zone semi-aride. Agronomie 15, 557–568.
Association épisodique d’halophytes strictes et de glycophytes dans un écosystème hydromorphe salé en zone semi-aride.Crossref | GoogleScholarGoogle Scholar |

Abdi N, Wasti S, Slama A, Ben Salem M (2016) Comparative study of salinity effect on some Tunisian barley cultivars at germination and early seedling growth stages. Journal of Plant Physiology & Pathology 4, 3
Comparative study of salinity effect on some Tunisian barley cultivars at germination and early seedling growth stages.Crossref | GoogleScholarGoogle Scholar |

Ahmed IM, Nadira UA, Bibi N, Cao F, He X, Zhang G, Wu F (2015) Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley. Environmental and Experimental Botany 111, 1–12.
Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley.Crossref | GoogleScholarGoogle Scholar |

Alamri SA, Barrett-Lennard EG, Teakle NL, Colmer TD (2013) Improvement of salt and waterlogging tolerance in wheat: comparative physiology of Hordeum marinumTriticum aestivum amphiploids with their H. marinum and wheat parents. Functional Plant Biology 40, 1168–1178.
Improvement of salt and waterlogging tolerance in wheat: comparative physiology of Hordeum marinumTriticum aestivum amphiploids with their H. marinum and wheat parents.Crossref | GoogleScholarGoogle Scholar |

Annunziata MG, Attico A, Woodrow P, Oliva MA, Fuggi A, Carillo P (2012) An improved fluorimetric HPLC method for quantifying tocopherols in Brassica rapa L. subsp. sylvestris after harvest. Journal of Food Composition and Analysis 27, 145–150.
An improved fluorimetric HPLC method for quantifying tocopherols in Brassica rapa L. subsp. sylvestris after harvest.Crossref | GoogleScholarGoogle Scholar |

Annunziata MG, Carillo P, Fuggi A, Troccoli A, Woodrow P (2013) Metabolic profiling of cauliflower under traditional and reduced tillage systems. Australian Journal of Crop Science 7, 1317–1323.

Annunziata MG, Ciarmiello LF, Woodrow P, Maximova E, Fuggi A, Carillo P (2017) Durum wheat roots adapt to salinity remodeling the cellular content of nitrogen metabolites and sucrose. Frontiers in Plant Science 7, 2035
Durum wheat roots adapt to salinity remodeling the cellular content of nitrogen metabolites and sucrose.Crossref | GoogleScholarGoogle Scholar |

Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59, 206–216.
Roles of glycine betaine and proline in improving plant abiotic stress resistance.Crossref | GoogleScholarGoogle Scholar |

Avrova A, Knogge W (2012) Rhynchosporium commune: a persistent threat to barley cultivation. Molecular Plant Pathology 13, 986–997.
Rhynchosporium commune: a persistent threat to barley cultivation.Crossref | GoogleScholarGoogle Scholar |

Baptista P, Martins A, Pais M, Tavares R, Lino-Neto T (2007) Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius. Mycorrhiza 17, 185–193.
Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius.Crossref | GoogleScholarGoogle Scholar |

Blattner FR (2009) Progress in phylogenetic analysis and a new infrageneric classification of the barley genus Hordeum (Poaceae: Triticeae). Breeding Science 59, 471–480.
Progress in phylogenetic analysis and a new infrageneric classification of the barley genus Hordeum (Poaceae: Triticeae).Crossref | GoogleScholarGoogle Scholar |

Bothmer RJF, Jacobsen N, Jørgensen RB (1989) Variation and differentiation in Hordeum marinum (Poaceae). Nordic Journal of Botany 9, 1–10.
Variation and differentiation in Hordeum marinum (Poaceae).Crossref | GoogleScholarGoogle Scholar |

Carillo P (2018) GABA shunt in durum wheat. Frontiers in Plant Science 9, 100
GABA shunt in durum wheat.Crossref | GoogleScholarGoogle Scholar |

Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A (2008) Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Functional Plant Biology 35, 412–426.
Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine.Crossref | GoogleScholarGoogle Scholar |

Carillo P, Annunziata M, Pontecorvo G, Fuggi A, Woodrow P (2011a) Salinity stress and salt tolerance. In ‘Abiotic stress in plants – mechanisms and adaptations’. (Ed. A Shanker) pp. 21–38. (IntechOpen Limited: London) Available at https://www.intechopen.com/books/abiotic-stress-in-plants-mechanisms-and-adaptations/salinity-stress-and-salt-tolerance [Verified 30 April 2018]

Carillo P, Parisi D, Woodrow P, Pontecorvo G, Massaro G, Annunziata M, Fuggi A, Sulpice R (2011b) Salt-induced accumulation of glycine betaine is inhibited by high light in durum wheat. Functional Plant Biology 38, 139–150.
Salt-induced accumulation of glycine betaine is inhibited by high light in durum wheat.Crossref | GoogleScholarGoogle Scholar |

Carillo P, Cacace D, De Pascale S, Rapacciuolo M, Fuggi A (2012) Organic vs. traditional potato powder. Food Chemistry 133, 1264–1273.
Organic vs. traditional potato powder.Crossref | GoogleScholarGoogle Scholar |

Chalbi N, Hessini K, Gandour M, Mohamed SN, Smaoui A, Abdelly C, Youssef NB (2013) Are changes in membrane lipids and fatty acid composition related to salt-stress resistance in wild and cultivated barley? Journal of Plant Nutrition and Soil Science 176, 138–147.
Are changes in membrane lipids and fatty acid composition related to salt-stress resistance in wild and cultivated barley?Crossref | GoogleScholarGoogle Scholar |

Chikha MB, Hessini K, Ourteni RN, Ghorbel A, Zoghlami N (2016) Identification of barley landrace genotypes with contrasting salinity tolerance at vegetative growth stage. Plant Biotechnology (Sheffield, England) 33, 287–295.
Identification of barley landrace genotypes with contrasting salinity tolerance at vegetative growth stage.Crossref | GoogleScholarGoogle Scholar |

Ciarmiello LF, Woodrow P, Piccirillo P, De Luca A, Carillo P (2014) Transcription factors and environmental stresses in plants. In ‘Emerging technologies and management of crop stress tolerance’. (Eds A Paraviz, R Saiema) pp. 57–78. (Academic Press: San Diego, CA, USA)

Ciarmiello LF, Piccirillo P, Carillo P, De Luca A, Woodrow P (2015) Determination of the genetic relatedness of fig (Ficus carica L.) accessions using RAPD fingerprint and their agro-morphological characterization. South African Journal of Botany 97, 40–47.
Determination of the genetic relatedness of fig (Ficus carica L.) accessions using RAPD fingerprint and their agro-morphological characterization.Crossref | GoogleScholarGoogle Scholar |

Colla G, Rouphael Y, Leonardi C, Bie Z (2010) Role of grafting in vegetable crops grown under saline conditions. Scientia Horticulturae 127, 147–155.
Role of grafting in vegetable crops grown under saline conditions.Crossref | GoogleScholarGoogle Scholar |

Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. Journal of Experimental Botany 57, 1059–1078.
Use of wild relatives to improve salt tolerance in wheat.Crossref | GoogleScholarGoogle Scholar |

Cuadrado Á, Carmona A, Jouve N (2013) Chromosomal characterization of the three subgenomes in the polyploids of Hordeum murinum L.: new insight into the evolution of this complex. PLoS One 8, e81385
Chromosomal characterization of the three subgenomes in the polyploids of Hordeum murinum L.: new insight into the evolution of this complex.Crossref | GoogleScholarGoogle Scholar |

Cuin TA, Tian Y, Betts SA, Chalmandrier R, Shabala S (2009) Ionic relations and osmotic adjustment in durum and bread wheat under saline conditions. Functional Plant Biology 36, 1110–1119.
Ionic relations and osmotic adjustment in durum and bread wheat under saline conditions.Crossref | GoogleScholarGoogle Scholar |

de Lacerda CF, Cambraia J, Oliva MA, Ruiz HA, Prisco JT (2003) Solute accumulation and distribution during shoot and leaf development in two sorghum genotypes under salt stress. Environmental and Experimental Botany 49, 107–120.
Solute accumulation and distribution during shoot and leaf development in two sorghum genotypes under salt stress.Crossref | GoogleScholarGoogle Scholar |

de Lacerda CF, Cambraia J, Oliva MA, Ruiz HA (2005) Changes in growth and in solute concentrations in sorghum leaves and roots during salt stress recovery. Environmental and Experimental Botany 54, 69–76.
Changes in growth and in solute concentrations in sorghum leaves and roots during salt stress recovery.Crossref | GoogleScholarGoogle Scholar |

FAO (2015) ‘FAO Land and Plant Nutrition Management Service.’ (Food and Agriculture Organization of the United Nations: Rome) Available at https://www.eldis.org/organisation/A3599 [Verified 30 April 2018]

Flowers TJ (2004) Improving crop salt tolerance. Journal of Experimental Botany 55, 307–319.
Improving crop salt tolerance.Crossref | GoogleScholarGoogle Scholar |

Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annual Review of Plant Physiology 28, 89–121.
The mechanism of salt tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar |

Gao R, Curtis TY, Powers SJ, Xu H, Huang J, Halford NG (2016) Food safety: structure and expression of the asparagine synthetase gene family of wheat. Journal of Cereal Science 68, 122–131.
Food safety: structure and expression of the asparagine synthetase gene family of wheat.Crossref | GoogleScholarGoogle Scholar |

Garthwaite AJ, von Bothmer R, Colmer TD (2005) Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl− into the shoots. Journal of Experimental Botany 56, 2365–2378.
Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl into the shoots.Crossref | GoogleScholarGoogle Scholar |

Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Critical Reviews in Plant Sciences 18, 227–255.
Salt tolerance and crop potential of halophytes.Crossref | GoogleScholarGoogle Scholar |

Gorham J, Jones RGW, Bristol A (1990) Partial characterization of the trait for enhanced K+-Na+ discrimination in the D genome of wheat. Planta 180, 590–597.
Partial characterization of the trait for enhanced K+-Na+ discrimination in the D genome of wheat.Crossref | GoogleScholarGoogle Scholar |

Gorham J, Läuchli A, Leidi EO (2010) Plant responses to salinity. In ‘Physiology of cotton’. (Eds JM Stewart, DM Oosterhuis, JJ Heitholt, JR Mauney) pp. 129–141. (Springer: Dordrecht, The Netherlands)

Greene R, Timms W, Rengasamy P, Arshad M, Cresswell R (2016) Soil and aquifer salinization: toward an integrated approach for salinity management of groundwater. In ‘Integrated groundwater management’. (Eds AJ Jakeman, O Barreteau, RJ Hunt, J-D Rinaudo, A Ross) pp. 377–412. (SpringerOpen: Basel, Switzerland)

Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annual Review of Plant Physiology 31, 149–190.
Mechanisms of salt tolerance in nonhalophytes.Crossref | GoogleScholarGoogle Scholar |

Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. Journal of Biosciences 30, 761–776.
Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants.Crossref | GoogleScholarGoogle Scholar |

Hafsi C, Lakhdhar A, Rabhi M, Debez A, Abdelly C, Ouerghi Z (2007) Interactive effects of salinity and potassium availability on growth, water status, and ionic composition of Hordeum maritimum. Journal of Plant Nutrition and Soil Science 170, 469–473.
Interactive effects of salinity and potassium availability on growth, water status, and ionic composition of Hordeum maritimum.Crossref | GoogleScholarGoogle Scholar |

Hammami H, Baptista P, Martins F, Gomes T, Abdelly C, Mahmoud OM-B (2016) Impact of a natural soil salinity gradient on fungal endophytes in wild barley (Hordeum maritimum With.). World Journal of Microbiology & Biotechnology 32, 184
Impact of a natural soil salinity gradient on fungal endophytes in wild barley (Hordeum maritimum With.).Crossref | GoogleScholarGoogle Scholar |

Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000a) 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 |

Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000b) 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 |

Havaux M, Eymery F, Porfirova S, Rey P, Dörmann P (2005) Vitamin E protects against photoinhibition and photo-oxidative stress in Arabidopsis thaliana. The Plant Cell 17, 3451–3469.
Vitamin E protects against photoinhibition and photo-oxidative stress in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Hessini K, Ferchichi S, Ben Youssef S, Werner KH, Cruz C, Gandour M (2015) How does salinity duration affect growth and productivity of cultivated barley? Agronomy Journal 107, 174–180.
How does salinity duration affect growth and productivity of cultivated barley?Crossref | GoogleScholarGoogle Scholar |

Hewitt EJ (1966) ‘Sand and Water Culture Methods Used in Study of Plant Nutrition. 2nd Edition.’ (Commonwealth Agricultural Bureaux, Farnham Royal: Bucks, England)

Jacobsen N Bothmer R 1995 Taxonomy in the Hordeum murinum complex (Poaceae). Nordic Journal of Botany 15 449 458

Komatsuda T, Tanno K-i, Salomon B, Bryngelsson T, von Bothmer R (1999) Phylogeny in the genus Hordeum based on nucleotide sequences closely linked to the vrs1 locus (row number of spikelets). Genome 42, 973–981.
Phylogeny in the genus Hordeum based on nucleotide sequences closely linked to the vrs1 locus (row number of spikelets).Crossref | GoogleScholarGoogle Scholar |

Läuchli A, Grattan SR (2007) Plant growth and development under salinity stress. In ‘Advances in molecular breeding toward drought and salt tolerant crops’. (Eds MA Jenks, PM Hasegawa, SM Jain) pp. 1–32. (Springer: Dordrecht, The Netherlands)

Lombardi T, Lupi B (2006) Salt tolerance in wild Hordeum (Poaceae) species: differences between H. maritimum With. and H. hystrix Roth. Atti della Società toscana di scienze naturali residente in Pisa. Memorie. Serie B 113, 31–35.

Lombardi T, Fochetti T, Onnis A (2000) Comparative salt tolerance of two wild Hordeum species (H. maritimum With. and H. murinum L.) from the coast of Tuscany (Italy). Plant Biosystems 134, 333–339.
Comparative salt tolerance of two wild Hordeum species (H. maritimum With. and H. murinum L.) from the coast of Tuscany (Italy).Crossref | GoogleScholarGoogle Scholar |

Maggio A, De Pascale S, Fagnano M, Barbieri G (2011) Saline agriculture in Mediterranean environments. Italian Journal of Agronomy
Saline agriculture in Mediterranean environments.Crossref | GoogleScholarGoogle Scholar |

Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biologia Plantarum 43, 491–500.
Nitrogen containing compounds and adaptation of plants to salinity stress.Crossref | GoogleScholarGoogle Scholar |

Mejri M, Siddique KHM, Saif T, Abdelly C, Hessini K (2016) Comparative effect of drought duration on growth, photosynthesis, water relations, and solute accumulation in wild and cultivated barley species. Journal of Plant Nutrition and Soil Science 179, 327–335.
Comparative effect of drought duration on growth, photosynthesis, water relations, and solute accumulation in wild and cultivated barley species.Crossref | GoogleScholarGoogle Scholar |

Morgan JM (1984) Osmoregulation and water stress in higher plants. Annual Review of Plant Physiology 35, 299–319.
Osmoregulation and water stress in higher plants.Crossref | GoogleScholarGoogle Scholar |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar |

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

Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57, 1025–1043.
Approaches to increasing the salt tolerance of wheat and other cereals.Crossref | GoogleScholarGoogle Scholar |

Naseer S, Nisar A, Ashraf M (2001) Effect of salt stress on germination and seedling growth of barley (Hordeum vulgare L.). Pakistan Journal of Biological Sciences 4, 359–360.
Effect of salt stress on germination and seedling growth of barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar |

Obata T, Witt S, Lisec J, Palacios-Rojas N, Florez-Sarasa I, Araus JL, Cairns JE, Yousfi S, Fernie AR (2015) Metabolite profiles of maize leaves in drought, heat and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiology 169, 2665–2283.

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 |

Pitman MG, Läuchli A (2002) Global impact of salinity and agricultural ecosystems. In ‘Salinity: environment – plants – molecules’. (Eds A Läuchli, U Lüttge) pp. 3–20. (Springer: Dordrecht, The Netherlands)

Puniran-Hartley N, Hartley J, Shabala L, Shabala S (2014) Salinity-induced accumulation of organic osmolytes in barley and wheat leaves correlates with increased oxidative stress tolerance: In planta evidence for cross-tolerance. Plant Physiology and Biochemistry 83, 32–39.
Salinity-induced accumulation of organic osmolytes in barley and wheat leaves correlates with increased oxidative stress tolerance: In planta evidence for cross-tolerance.Crossref | GoogleScholarGoogle Scholar |

Rabhi M, Hafsi C, Lakhdar A, Hajji S, Zouhaier B, Hédi Hamrouni M, Abdelly C, Smaoui A (2009) Evaluation of the capacity of three halophytes to desalinize their rhizosphere as grown on saline soils under nonleaching conditions. African Journal of Ecology 47, 463–468.
Evaluation of the capacity of three halophytes to desalinize their rhizosphere as grown on saline soils under nonleaching conditions.Crossref | GoogleScholarGoogle Scholar |

Rana G, Katerji N (2000) Measurement and estimation of actual evapotranspiration in the field under Mediterranean climate: a review. European Journal of Agronomy 13, 125–153.
Measurement and estimation of actual evapotranspiration in the field under Mediterranean climate: a review.Crossref | GoogleScholarGoogle Scholar |

Raven JA (1985) Tansley Review No. 2. Regulation of pH and generation of osmolarity in vascular plants: a cost–benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytologist 101, 25–77.
Tansley Review No. 2. Regulation of pH and generation of osmolarity in vascular plants: a cost–benefit analysis in relation to efficiency of use of energy, nitrogen and water.Crossref | GoogleScholarGoogle Scholar |

Rouphael Y, Raimondi G, Lucini L, Carillo P, Kyriacou MC, Colla G, Cirillo V, Pannico A, El-Nakhel C, De Pascale S (2018) Physiological and metabolic responses triggered by omeprazole improve tomato plant tolerance to NaCl stress. Frontiers in Plant Science 9, 249
Physiological and metabolic responses triggered by omeprazole improve tomato plant tolerance to NaCl stress.Crossref | GoogleScholarGoogle Scholar |

Sairam R, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Current Science 86, 407–421.

Saoudi W, Badri M, Gandour M, Smaoui A, Abdelly C, Taamalli W (2017) Assessment of genetic variability among Tunisian populations of Hordeum marinum using morpho-agronomic traits. Crop Science 57, 302–309.
Assessment of genetic variability among Tunisian populations of Hordeum marinum using morpho-agronomic traits.Crossref | GoogleScholarGoogle Scholar |

Scholander PF, Bradstreet ED, Hemmingsen EA, Hammel HT (1965) Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148, 339–346.
Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants.Crossref | GoogleScholarGoogle Scholar |

Seckin B, Turkan I, Sekmen A, Ozfidan-Konakci C (2010) The role of antioxidant defense systems at differential salt tolerance of Hordeum marinum Huds. (sea barley grass) and Hordeum vulgare L. (cultivated barley). Environmental and Experimental Botany 69, 76–85.
The role of antioxidant defense systems at differential salt tolerance of Hordeum marinum Huds. (sea barley grass) and Hordeum vulgare L. (cultivated barley).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 |

Shabala S, Munns R (2012) ‘Salinity stress: physiological constraints and adaptive mechanisms.’ (CABI: Wallingford, UK)

Shavrukov Y, Gupta NK, Miyazaki J, Baho MN, Chalmers KJ, Tester M, Langridge P, Collins NC (2010) HvNax3 – a locus controlling shoot sodium exclusion derived from wild barley (Hordeum vulgare ssp. spontaneum). Functional & Integrative Genomics 10, 277–291.
HvNax3 – a locus controlling shoot sodium exclusion derived from wild barley (Hordeum vulgare ssp. spontaneum).Crossref | GoogleScholarGoogle Scholar |

Shavrukov Y, Bovill J, Afzal I, Hayes JE, Roy SJ, Tester M, Collins NC (2013) HVP10 encoding V-PPase is a prime candidate for the barley HvNax3 sodium exclusion gene: evidence from fine mapping and expression analysis. Planta 237, 1111–1122.
HVP10 encoding V-PPase is a prime candidate for the barley HvNax3 sodium exclusion gene: evidence from fine mapping and expression analysis.Crossref | GoogleScholarGoogle Scholar |

Shelden MC, Dias DA, Jayasinghe NS, Bacic A, Roessner U (2016) Root spatial metabolite profiling of two genotypes of barley (Hordeum vulgare L.) reveals differences in response to short-term salt stress. Journal of Experimental Botany 67, 3731–3745.
Root spatial metabolite profiling of two genotypes of barley (Hordeum vulgare L.) reveals differences in response to short-term salt stress.Crossref | GoogleScholarGoogle Scholar |

Schonfeld MA, Johnson RC, Carwer BF, Mornhinweg DW (1988) Water relations in winter wheat as drought resistance indicators. Crop Science 28, 526–531.

Slama A, Ben Salem M, Ben Naceur Mb, Zid E (2005) Les céréales en Tunisie: Production, effet de la sécheresse et mécanismes de résistance. Sécheresse 16, 225–229.

Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany 115, 433–447.
Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress.Crossref | GoogleScholarGoogle Scholar |

Suprasanna P, Nikalje GC, Rai AN (2016) Osmolyte accumulation and implications in plant abiotic stress tolerance. In ‘Osmolytes and plants acclimation to changing environment: emerging omics technologies’. (Eds N Iqbal, R Nazar, NA Khan) pp. 1–12. (Springer India: New Delhi)

Van Oosten MJ, Silletti S, Guida G, Cirillo V, Di Stasio E, Carillo P, Woodrow P, Maggio A, Raimondi G (2017) A benzimidazole proton pump inhibitor increases growth and tolerance to salt stress in tomato. Frontiers in Plant Science 8, 1220
A benzimidazole proton pump inhibitor increases growth and tolerance to salt stress in tomato.Crossref | GoogleScholarGoogle Scholar |

Volkmar K, Hu Y, Steppuhn H (1998) Physiological responses of plants to salinity: a review. Canadian Journal of Plant Science 78, 19–27.
Physiological responses of plants to salinity: a review.Crossref | GoogleScholarGoogle Scholar |

Vysotskaya L, Hedley PE, Sharipova G, Veselov D, Kudoyarova G, Morris J, Jones HG (2010) Effect of salinity on water relations of wild barley plants differing in salt tolerance. AoB Plants 2010, plq006
Effect of salinity on water relations of wild barley plants differing in salt tolerance.Crossref | GoogleScholarGoogle Scholar |

Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiology 132, 556–567.
Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism.Crossref | GoogleScholarGoogle Scholar |

Winter H, Robinson DG, Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191, 180–190.
Subcellular volumes and metabolite concentrations in barley leaves.Crossref | GoogleScholarGoogle Scholar |

Woodrow P, Pontecorvo G, Ciarmiello L, Fuggi A, Carillo P (2011) Ttd1a promoter is involved in DNA-protein binding by salt and light stresses. Molecular Biology Reports 38, 3787–3794.
Ttd1a promoter is involved in DNA-protein binding by salt and light stresses.Crossref | GoogleScholarGoogle Scholar |

Woodrow P, Fuggi A, Pontecorvo G, Kafantaris I, Annunziata MG, Massaro G, Carillo P (2012) cDNA cloning and differential expression patterns of ascorbate peroxidase during post-harvest in Brassica rapa L. Molecular Biology Reports 39, 7843–7853.
cDNA cloning and differential expression patterns of ascorbate peroxidase during post-harvest in Brassica rapa L.Crossref | GoogleScholarGoogle Scholar |

Woodrow P, Ciarmiello LF, Annunziata MG, Pacifico S, Iannuzzi F, Mirto A, D’Amelia L, Dell’Aversana E, Piccolella S, Fuggi A, Carillo P (2017) Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiologia Plantarum 159, 290–312.
Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism.Crossref | GoogleScholarGoogle Scholar |

Wu D, Cai S, Chen M, Ye L, Chen Z, Zhang H, Dai F, Wu F, Zhang G (2013) Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS One 8, e55431
Tissue metabolic responses to salt stress in wild and cultivated barley.Crossref | GoogleScholarGoogle Scholar |

Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. Journal of Experimental Biology 208, 2819–2830.
Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses.Crossref | GoogleScholarGoogle Scholar |

Yousfi S, Rabhi M, Hessini K, Abdelly C, Gharsalli M (2010) Differences in efficient metabolite management and nutrient metabolic regulation between wild and cultivated barley grown at high salinity. Plant Biology 12, 650–658.

Zaffarano PL, McDonald BA, Linde CC (2008) Rapid speciation following recent host shifts in the plant pathogenic fungus Rhynchosporium. Evolution 62, 1418–1436.

Zhu J-K (2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
Plant salt tolerance.Crossref | GoogleScholarGoogle Scholar |