Abstract
In some areas of the world, high levels of sodium sulfate (Na2SO4) are found in the soil together with sodium chloride (NaCl). However, most studies on salinity are performed utilizing only NaCl as a salinizing agent. Generally, plant species have different tolerance/susceptibility responses when grown in the presence of these salts. Some studies showed that Na2SO4 seems to be more inhibitory than NaCl for the growth of species such as barley, wheat, sugar cane, beet, tomato, wild potato, and others. However, studies focusing on how Na2SO4 can affect the biochemical and physiological processes of plants are very scarce. This review provides an overview on the effects of Na2SO4 on different crops and plants species with a special emphasis on the tolerance/non-tolerance mechanisms of the halophyte Prosopis strombulifera under elevated NaCl and Na2SO4. A better understanding of the tolerance mechanisms in this particular species will help to identify cultivars of crop species that are more tolerant to Na2SO4. This knowledge could be used to extent cultivation of certain crop plants on Na2SO4 containing soils.
Similar content being viewed by others
References
Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Sci 196:67–76
Aghajanzadeh TA, Reich M, Kopriva S, De Kok LJ (2018) Impact of chloride (NaCl, KCl) and sulphate (Na2SO4, K2SO4) salinity on glucosinolate metabolism in Brassica rapa. J Agro Crop Sci 204:137–146. https://doi.org/10.1111/jac.12243
Aghajanzadeh TA, Reich M, Hawkesford MJ, Burow M (2019) Sulfur metabolism in Allium cepa is hardly affected by chloride and sulfate salinity. Arch Agron Soil Sci 65:945–956. https://doi.org/10.1080/03650340.2018.1540037
Al-Hamzawi M (2007) Effect of sodium chloride and sodium sulfate on growth, and ions content in faba-bean (Vicia faba). J Kerbala Univ 5:152–216
Anesini C, Perez C (1993) Screening of plants used in Argentine folk medicine for antimicrobial activity. J Ethnopharmacol 39:119–128
Arbona V, Argamasilla R, Gomez-Cadenas A (2010) Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress. J Plant Physiol 167:1342–1350
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Assareh MH, Rasouli B, Amiri B (2010) Effects of NaCl and Na2SO4 on germination and initial growth phase of Halostachys caspica. Desert 15:119–125
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
Bañuelos GS, Mead R, Hoffman GJ (1993) Accumulation of selenium in wild mustard irrigated with agricultural effluent. Agric Ecosyst Environ 43:119–126
Barhoumi Z (2018) Physiological response of the facultative halophyte, Aeluropus littoralis, to different salt types and levels. Plant Biosyst 153:298–305
Bilski J, Nelson D, Conlon R (1988) Response of six wild potato species to chloride and sulfate salinity. Am Potato J 65:605–612
Boestfleisch C, Papenbrock J (2017) Changes in secondary metabolites in the halophytic putative crop species Crithmum maritimum L., Triglochin maritima L. and Halimione portulacoides (L.) Aellen as reaction to mild salinity. PLoS One 12:1–18
Boestfleisch C, Wagenseil NB, Buhmann AK, Seal CE, Wade EM, Muscolo A (2014) Manipulating the antioxidant capacity of halophytes to increase their cultural and economic value through saline cultivation. AoB Plants 6:plu046
Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot 115:481–494. https://doi.org/10.1093/aob/mcu219
Boursier P, Läuchli A (1990) Growth responses and mineral nutrient relations of salt-stressed sorghum. Crop Sci 30:1226–1233
Burkart A (1976) A monograph of the genus Prosopis (Leguminosae subfam Mimosoideae). Catalogue of the recognized species of Prosopis. J Arnold Arbor 57:450–525
Cabrera AL (1976) Regiones fitogeográficas Argentinas: In: Kugler WF (ed) Enciclopedia Argentina de Agricultura y Jardinería, Tomo 2, Fasc. 1. ACME, Buenos Aires, pp 1–85
Cambrollé J, Mateos-Naranjo E, Redondo-Gómez LT, Figueroa ME (2011) Growth, reproductive and photosynthetic responses to copper in the yellow-horned poppy, Glaucium flavum Crantz. Environ Exp Bot 71:57–64
Can-Chulim A, Cruz-Crespo E, Ortega-Escobar HM, Sánchez-Bernal EI, Madueño Molina A, Bojórquez-Serrano JI, Mancilla-Villa OR (2017) Phaseolus vulgaris response to salinity generated by NaCl, Na2SO4 and NaHCO3. Rev Mex Cienc Agríc 8:1287–1300
Cao MJ, Wang Z, Wirtz M, Hell R, Oliver DJ, Xiang C (2013) Bin SULTR3;1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana. Plant J 73:607–616
Cerović ZG, Kalezić R, Plesničar M (1982) The role of photophosphorylation in SO2 and SO32– inhibition of photosynthesis in isolated chloroplasts. Planta 156:249–254
Chang C, Sommerfeldt TG, Carefoot JM, Schaalje GB (1983) Relationships of electrical conductivity with total dissolved salts and cation concentration of sulfate-dominant soil extracts. Can J Soil Sci 63:79–86. https://doi.org/10.4141/cjss83-008
Chavan PD, Karadge BA (1980) Influence of sodium chloride and sodium sulfate salinities on photosynthetic carbon assimilation in peanut. Plant Soil 56:201–207
Coley D, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899
Colla G, Rouphael Y, Rea E, Cardarelli M (2012) Grafting cucumber plants enhance tolerance to sodium chloride and sulfate salinization. Sci Horticul 135:177–185
Curtin DH, Steppuhn H, Selles F (1993) Plant responses to sulfate and chloride salinity: growth and ionic relations. SSSA 57:1304–1310
Dadshani S, Sharma RC, Baum M, Ogbonnaya FC, León J, Ballvora A (2019) Multidimensional evaluation of response to salt stress in wheat. PLoS One 14(9):e0222659. https://doi.org/10.1371/journal.pone.0222659
Datta KS, Kumar A, Varma SK, Angrish R (1995) Differentiation of chloride and sulphate salinity on the basis of ionic distribution in genetically diverse cultivars of wheat. J Plant Nutr 18:2199–2212
Degano C (1999) Respuestas morfológicas y anatómicas de Tessaria absinthioides (Hook. et Arn.) DC. a la salinidad. Rev Bras Bot 22:357–363
Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626
El-Samad H, Shaddad MAK (1996) Comparative effect of sodium carbonate, sodium sulphate, and sodium chloride on the growth and related metabolic activities of pea plants. J Plant Nutr 19:717–728. https://doi.org/10.1080/01904169609365155
FAO (1988) FAO/Unesco Soil Map of the World. Revised Legend, with corrections and updates. World Soils Resources Report 60, FAO, Rome
Felker P, Ewens M, Velarde M, Medina D (2008) Initial evaluation of Prosopis alba Griseb clones selected for growth at seawater salinities. Arid Land Res Manag 22:334–345
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963
Flowers TJ, Muscolo A ( 2015) Introduction to the Special Issue: Halophytes in a changing world. AoB Plants 7:plv020. https://doi.org/10.1093/aobpla/plv020
Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Quart Rev Biol 61:313–337
Fortmeier R, Schubert S (1995) Salt tolerance of maize (Zea mays L.): the role of sodium exclusion. Plant Cell Environ 18:1041–1047
Freedman B, Hutchinson TC (1980) Pollutant inputs from the atmosphere and accumulations in soils and vegetation near a nickel-copper smelter at Sudbury, Ontario, Canada. Can J Bot 58:108–132
Gagneul D, Aınouche A, Duhazé C, Lugan R, Larher FR, Bouchereau A (2007) A reassessment of the function of the so called compatible solutes in the halophytic Plumbaginaceae Limonium latifolium. Plant Physiol 144:1598–1611
Ghars MA, Parre E, Debez A (2008) Comparative salt tolerance analysis between Arabidopsis thaliana and Thellungiella halophila, with special emphasis on K+/Na+ selectivity and proline accumulation. J Plant Physiol 165:588–599
Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255
Graßes T, Pesaresi P, Schiavon F, Varotto C, Salamini F, Jahns P, Leister D (2002) The role of ΔpH-dependent dissipation of excitation energy in protecting photosystem II against light-induced damage in Arabidopsis thaliana. Plant Physiol Biochem 40:41–49
Grigore MN, Toma C (2017) Anatomical adaptations of halophytes. A review of classic literature and recent findings. Springer, New York (ISBN 978-3-319-66479-8)
Grigore MN (2008) Introducere ın Halofitologie. Elemente de anatomie integrativa˘. Edit. Pim, Iasi.
Gupta VK, Gupta SP (1984) Effect of zinc sources and levels on the growth and Zn nutrition of soybean (Glycine max L.) in the presence of chloride and sulphate salinity. Plant Soil 81:299–304
Hapon MB, Hapon MV, Persia FA, Pochettino A, Lucero GS (2014) Aqueous extract of Prosopis strombulifera (Lam) Benth induces cytotoxic effects against tumor cell lines without systemic alterations in BALB/c mice. J Clin Toxicol 4:222. https://doi.org/10.4172/2161-0495.1000222
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51:463–499
Hasson-Porath E, Kahana I, Poijakoff-Mayber A (1972) The effect of chloride and sulfate types of salinity on growth and on osmotic adaptation of pea seedlings. Plant Soil 36:449–459
Hawkesford MJ, De Kok LJ (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29:382–395
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Quart Rev Biol 67:283–335. https://doi.org/10.1086/417659
Huang J, Redmann R (1995) Salt tolerance of Hordeum and Brassica species during germination and early seedling growth. Can J Plant Sci 75:815–819
Inal A (2002) Growth proline accumulation and ionic relations of tomato (Licopersicum esculentum L.) as influence by NaCl and Na2SO4 salinity. Turk J Bot 26:285–290
Inal A, Gunes A, Pilbeam DJ, Kadioglu YK, Eraslan F (2009) Concentrations of essential and nonessential elements in shoots and storage roots of carrot grown in NaCl and Na2SO4 salinity. X-Ray Spectromet 38:45–51
Iqbal RM (2003) Leaf area and ion content of wheat grown under NaCl and Na2SO4 salinity. Pakistan J Biol Sci 6:1512–1514
Irakoze W, Vanpee B, Rufyikiri G, Dailly H, Nijimbere S, Lutts S (2019) Comparative effects of chloride and sulfate salinities on two contrasting rice cultivars (Oryza sativa L.) at the seedling stage. J Plant Nutr 42:1–15. https://doi.org/10.1080/01904167.2019.1584222
Irakoze W, Prodjinoto H, Nijimbere S, Rufyikiri G, Lutts S (2020) NaCl and Na2SO4 salinities have different impact on photosynthesis and yield-related parameters in rice (Oryza sativa L.). Agronomy 10:864. https://doi.org/10.3390/agronomy10060864
Joshi G, Naik R (1980) Response of sugarcane to different types of salt stress. Plant Soil 56:255–263
Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704
Kaymakanova M (2009) Effect of salinity on germination and seed physiology in bean (Phaseolus vulgaris L.). Biotechnol Biotechnol Equip 23(sup1):326–329
Khan R, Rehman F, Gulafshan KA (2020) Effect of salinity (Na2SO4) on stomata, and yield parameters of Indian mustard (Brassica juncea L.) var. Goldi. Int J Nanomater Nanotechnol Nanomed 6:021–023. https://doi.org/10.17352/2455-3492.000036
Koralewska A, Posthumus FS, Stuiver CEE, Buchner P, Hawkesford MJ, De Kok LJ (2007) The characteristic high sulfate content in Brassica oleracea is controlled by the expression and activity of sulfate transporters. Plant Biol 9:654–661
Koralewska A, Stuiver CEE, Posthumus FS, Kopriva S, Hawkesford MJ, De Kok LJ (2008) Regulation of sulfate uptake, expression of the sulfate transporters Sultr1;1 and Sultr1;2, and APS reductase in Chinese cabbage (Brassica pekinensis) as affected by atmospheric H2S nutrition and sulfate deprivation. Funct Plant Biol 35:318–327
Koralewska A, Buchner P, Stuiver CEE, Posthumus FS, Kopriva S, Hawkesford MJ, De Kok LJ (2009) Expression and activity of sulfate transporters and APS reductase in curly kale in response to sulfate deprivation and re-supply. J Plant Physiol 166:168–179
Koyro HW (2006) Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte Plantago coronopus (L.). Environ Exp Bot 56:136–146
Kurunc A, Aslan G, Karaca C, Tezcan A, Turgut K, Karhan M, Kaplan B (2020) Effects of salt source and irrigation water salinity on growth, yield and quality parameters of Stevia rebaudiana Bertoni. Sci Horticul 270:109458
Leonova T, Ovchinnykova V, Souer E, de Boer A, Kharchenko P, Babakov A (2009) Isolated Thellungiella shoots do not require roots to survive NaCl and Na2SO4 salt stresses. Plant Signal Behav 4:1059–1062. https://doi.org/10.4161/psb.4.11.9799
Llanes A, Reinoso H, Luna V (2005) Germination and early growth of Prosopis strombulifera seedlings in different saline solutions. World J Agric Sci 1:120–128
Llanes A, Bertazza G, Palacio G, Luna V (2013) Different sodium salts cause different solute accumulation in the halophyte Prosopis strombulifera. Plant Biol 15:118–125
Llanes A, Arbona V, Gómez-Cadenas A, Luna V (2016) Metabolomic profiling of the halophyte Prosopis strombulifera shows sodium salt-specific response. Plant Physiol Biochem108:145–157
Lugan R, Niogret MF, Leport L (2010) Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. Plant J 64:215–229
Manivannan P, Jaleel C, Kishorekumar A, Sankar B, Somasundaram R, Panneerselvam R (2008) Protection of Vigna unguiculata (L.) Walp. plants from salt stress by paclobutrazol. Colloids Surf B Biointerfaces 61:315–318
Maruyama-Nakashita A (2017) Metabolic changes sustain the plant life in low-sulfur environments. Curr Opinion Plant Biol 39:144–151
Mastrogiannidou E, Chatzissavvidis C, Antonopoulou C, Tsabardoukas V, Giannakoula A, Therios I (2016) Response of pomegranate cv. wonderful plants tο salinity. J Soil Sci Plant Nutr 16:621–636
Mills AJ, Fey MV, Johnson CE (2004) Effects of sodium sulphate, sodium chloride and manganese sulphate on kikuyu (Pennisetum clandestinum) growth and ion uptake. South Afr J Plant Soil 21:209–213
Miyamoto S, Nesbitt M (2011) Effectiveness of soil salinity management practices in basic irrigated pecan orchards. Hort Technol 21:569–576
Mor RP, Manchanda HR (1992) Influence of phosphorus on the tolerance of table pea to chloride and sulphate salinity in a sandy soil. Arid Soil Res Rehab 6:41–52
Moreno-Izaguirre E, Ojeda-Barrios D, Avila-Quezada G, Guerrero-Prieto V, Parra-Quezada R, Ruiz-Anchondo T (2015) Sodium sulfate exposure slows growth of native pecan seedlings. ΦYTON 84:80–85
Morrone JJ (2014) Biogeographical regionalisation of the Neotropical region. Zootaxa 3782:1e110
Moss M (1978) Sources of sulfur in the environment: the global sulfur cycle. In: Nriagu JO (ed) Sulfur in the environment, part 1: the atmospheric cycle. Wiley, New York, pp 23–50
Naik VV, Karadge BA (2017) Effect of NaCl and Na2SO4 salinities and light conditions on seed germination of purslane (Portulaca oleracea Linn.). J Plant Stress Physiol 3:1–4
Navarro JM, Garrido C, Carvajal M, Martinez V (2002) Yield and fruit quality of pepper plants under sulphate and chloride salinity. J Hortic Sci Biotech 77:52–57
Navarro JM, Garrido C, Martínez V (2003) Water relations and xylem transport of nutrients in pepper plants grown under two different salts stress regimes. Plant Growth Regul 41:237–245
Nawaz K, Hussain K, Siddiqi E, Majeed A (2018) Effect of Na2SO4 salinity on Brinjal (Solanum melongena). LGU J Life Sci 2:176–189
Nedjimi B, Daoud Y (2006) Effect of Na2SO4 on the growth, water relations, proline, total soluble sugars and ion content of Atriplex halimus subsp schweinfurthii through in vitro culture. Anales Biologia 28:35–43
Niu G, Rodriguez D, Dever J, Zhang J (2013) Growth and physiological responses of five cotton genotypes to sodium chloride and sodium sulfate saline water irrigation. J Cotton Sci 17:233–244
Nriagu JO (1978) Production and uses of sulfur. In: Nriagu JO (ed) Sulfur in the environment, part 1: the atmospheric cycle. Wiley, New York, pp 1–21
Ou B, Huang D, Woodill-Hampsch M, Flanagan JA, Deemer EK, Prior RL, Huang D (2002) Novel fluorometric assay for hydroxyl radical prevention capacity using fluorescein as theprobe. J Agric Food Chem 50:2772
Oyetunji OJ, Imade FN (2015) Effect of different levels of NaCl and Na2SO4 salinity on dry matter and ionic contents of cowpea (Vigna unguiculata L. Walp.). Afr J Agric Res 10:1239–1243
Paek KY, Chandler S, Thorpe T (1988) Physiological effects of Na2SO4 and NaCl on callus cultures of Brassica campestris (Chinese cabbage). Physiol Planta 72:160–166
Pagter M, Bragato C, Malagoli M, Brix H (2009) Osmotic and ionic effects of NaCl and Na2SO4 salinity on Phragmites australis. Aquatic Bot 90:43–51
Patil JM, Karadge BA (2017) Effect of Na2SO4 salinity on growth, chlorophyll content, polyphenols and proline contents of Trianthema portulacastrum L. Int J Adv Res 5:1670–1675
Peleg Z, Apse MP, Blumwald E (2011) Engineering salinity and water stress tolerance in crop plants: getting closer to the field. Adv Bot Res 57:406–432
Pérez C, Anesini C (1994a) Antibacterial activity of alimentary plants against Staphylococcus aureus growth. Am J Chin Med 22:169–174
Pérez C, Anesini C (1994b) In vitro antibacterial activity of Argentine folk medicinal plants against Salmonella typhi. J Ethnopharmacol 44:41–46
Persia FA, Troncoso M, Rinaldini E, Simirgiotis MJ, Tapia A (2020) UHPLC–Q/Orbitrap/MS/MS fingerprinting and antitumoral effects of Prosopis strombulifera (LAM.) BENTH. aqueous extract on allograft colorectal and melanoma cancer models. Heliyon 6:1–11
Peterson A, Murphy K (2015) Tolerance of lowland quinoa cultivars to sodium chloride and sodium sulfate salinity. Crop Sci 55:331–338
Poljakoff-Mayber A (1975) Morphological and anatomical changes in plants as a response to salinity. In: Poljakoff-Mayber A, Gale J (eds) Plants in saline environments. Springer, Berlin, pp 97–117
Raven JA (1985) 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 Phytol 101:25–77
Reginato M, Reinoso H, Llanes A, Luna V (2013) Stomatal abundance and distribution in Prosopis strombulifera plants growing under different iso-osmotic salt treatments. Am J Plant Sci 4:80–90
Reginato M, Castagna A, Furlán A, Castro S, Ranieri A, Luna V (2014a) Analysis of the oxidative damage in the halophyte Prosopis strombulifera salinized with NaCl and Na2SO4. Role of polyphenols as antioxidant protection. AoB Plants 6:plu042. https://doi.org/10.1093/aobpla/plu042
Reginato M, Sosa L, Llanes A, Hampp E, Vettorazzi N, Reinoso H, Luna V (2014b) Na2SO4 and NaCl determine different growth responses and ion accumulation in the halophytic legume Prosopis strombulifera. Plant Biol 16:97–106
Reginato M, Travaglia C, Reinoso H, Garello F, Luna V (2016) Anatomical modifications in the halophyte Prosopis strombulifera caused by salt mixture. Flora 218:75–85
Reginato M, Turcios A, Luna V, Papenbrock J (2019) Differential effects of NaCl and Na2SO4 on the halophyte Prosopis strombulifera are explained by different responses of photosynthesis and metabolism. Plant Physiol Biochem 141:306–314
Reich M, Aghajanzadeh T, Stuiver CEE, Koralewska A, De Kok LJ (2015) Impact of sulfate salinity on the uptake and metabolism of sulfur in Chinese cabbage. In: De Kok LJ, Hawkesford MJ, Rennenberg H, Saito K, Schnug E (eds) Molecular physiology and ecophysiology of sulfur. Springer International Publishing, New York, pp 227–238
Reich M, Aghajanzadeh T, Helm J, Parmar S, Hawkesford MJ, De Kok LJ (2017) Chloride and sulfate salinity differently affect biomass, mineral nutrient composition and expression of sulfate transport and assimilation genes in Brassica rapa. Plant Soil 411:319–332
Reich M, Aghajanzadeh T, Parmar S, Hawkesford MJ, De Kok LJ (2018) Calcium ameliorates the toxicity of sulfate salinity in Brassica rapa. J Plant Physiol 231:1–8
Reinoso H, Sosa L, Ramirez L, Luna V (2004) Salt-induced changes in the vegetative anatomy of Prosopis strombulifera (Leguminosae). Can J Bot 82:618–628
Reinoso H, Sosa L, Reginato M, Luna V (2005) Histological alterations induced by sodium sulfate in the vegetative anatomy of Prosopis strombulifera (Lam.) Benth. World J Agric Sci 1:109–119
Renault S, Croser C, Franklin J, Zwiazek J (2001) Effects of NaCl and Na2SO4 on red-osier dogwood (Cornus stolonifera Michx) seedlings. Plant Soil 233:261
Rengasamy P (2010) Soil processes affecting crop production in salt-affected soils. Funct Plant Biol 37:613–620
Rennenberg H (1984) The fate of excess sulfur in higher plants. Annu Rev Plant Physiol 35:121–153
Rennenberg H (1989) Synthesis and emission of hydrogen sulfide by higher plants. In: Saltzman ES, Cooper WJ (eds) Biogenic sulfur in the environment. American Chemical Society, Washington, DC, pp 44–57
Rhodes D, Nadolska-Orczyk A, Rich PJ (2002) Salinity, osmolytes and compatible solutes. In: Läuchli A, Lüttge U (eds) Salinity: environment-plants-molecules. Kluwer Academic Publishers, Netherlands, pp 181–204
Rogers ME, Grieve CM, Shannon MC (1998) Variation in the growth of lucerne (Medicago sativa L.) in response to sulphate salinity. Plant Soil 202:271–280
Ruiz JM, Lopez-Cantarero I, Rivero R, Romero L (2003) Sulphur phytoaccumulation in plant species characteristic of gypsiferous soils. Int J Phytoremediation 5:203–210
Ryrie IJ, Jagendorf AT (1971) Inhibition of photophosphorylation in spinach chloroplasts by inorganic sulfate. J Biol Chem 246:582–688
Saragusti A, Bustos P, Pierosan L, Chiabrando G (2012) Involvement of the l-arginine-nitric oxide pathway in the antinociception caused by fruits of Prosopis strombulifera (Lam.) Benth. J Ethnopharmacol 140:117–122
Schmidt A (2005) Metabolic background of H2S release from plants. Landbauforschung Völkenrode Special Issue 283:121–129
Selmar D, Kleinwächter M (2013) Influencing the product quality by deliberately applying drought stress during the cultivation of medicinal plants. Ind Crops Products 42:558–566
Sosa L, Llanes A, Reinoso H, Reginato M, Luna V (2005) Osmotic and specific ion effects on the germination of Prosopis strombulifera. Ann Bot 96:261–267
Storey R, Thomson WW (1994) An X-ray microanalysis study of the salt glands and intracellular calcium crystals of Tamarix. Ann Bot 73:307–313
Strogonov BP (1964) Physiological basis of salt tolerance of plants (as affected by various types of salinity). In: Poljakoff-Mayber A, Mayer AM (eds) Israel program for scientific translations, Jerusalem
Szabados L, Savouré A (2009) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–93
Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184
Tarchoune I, Sgherri C, Izzo R, Lachaâl M, Navari-Izzo F, Ouerghi Z (2012a) Changes in the antioxidative system of Ocimum basilicum L. (cv Fine) under different sodium salts. Act Physiol Plant 34:1873–1881. https://doi.org/10.1007/s11738-012-0985
Tarchoune I, Sgherri C, Baâtour O, Izzo R, Lachaâl M, Navari Izzo F, Ouerghi Z (2012b) Phenolic acids and total antioxidant activity in Ocimum basilicum L. grown under Na2SO4 medium. J Med Plant Res 6:5868–5875
Tattini M, Guidi L, Morassi-Bonzi L, Pinelli P, Remorini D, Degl’Innocenti E, Giordano C, Massai R, Agati G (2005) On the role of flavonoids in the integrated mechanisms of response of Ligustrum vulgare and Phillyrea latifolia to high solar radiation. New Phytol 167:457–470
Tipirdamaz R, Gagneul D, Duhazé C, Aïnouche A, Monnier C, Özkum D, Larher F (2006) Clustering of halophytes from an inland salt marsh in Turkey according to their ability to accumulate sodium and nitrogenous osmolytes. Environ Exp Bot 57:139–153
Toderich KN, Mamadrahimov AA, Khaitov BB, Karimov AA, Soliev AA, Nanduri KR, Shuyskaya EV (2020) Differential impact of salinity stress on seeds minerals, storage proteins, fatty acids, and squalene composition of new Quinoa genotype, grown in hyper-arid desert environments. Front Plant Sci 11:607102. https://doi.org/10.3389/fpls.2020.607102
Trelka T, Bres W, Politycka B, Starzyk J (2016) Influence of sodium chloride and sodium sulfate on zonal Pelargonium and microorganisms colonizing root environment. Bulgarian J Agric Sci 22:401–407
Vigo C, Therios IN, Nastou A, Patakas A (2004) Changes in photosynthetic parameters and nutrient distribution in olive plants (Olea europaea L.) of cultivar Chondrolia Chalkidikis under NaCl—Na2SO4 and KCl salinities. Agris 46:33–46
Waisel Y (1972) Biology of halophytes. Academic Press, New York
Warne P, Guy RD, Rollins L, Reid DM (1990) The effects of sodium sulphate and sodium chloride on growth, morphology, photosynthesis, and water use efficiency of Chenopodium rubrum. Can J Bot 68:999–1006
Weinberg RW, Lerner HR, Poljakoff-Mayber A (1984) Changes in growth and water-soluble solute concentrations in Sorghum bicolor stressed with sodium and potassium salts. Physiol Plant 62:472–480
Wright G, Patten K, Drew M (1992) Salinity and supplemental calcium influence Growth of rabbiteye and southern highbush blueberry. J Am Soc Hort Sci 117:749–756
Wu G (2015) Nutritional properties of quinoa. In: Murphy K, Matanguihan J (eds) Quinoa: improvement and sustainable production. Wiley, Hoboken, pp 193–210. https://doi.org/10.1002/9781118628041.ch11
Yeo AR (1983) Salinity resistance: physiologies and prices. Physiol Plantarum 58:214–222
Zaman B, Ali A, Salim M, Hussain K (2002) Growth of wheat as affected by sodium chloride and sodium sulphate salinity. Pakistan J Biol Sci 5:1313–1315
Zangerl AR, Arntz A, Berenbaum M (1997) Physiological price of an induced chemical defense: photosynthesis, respiration, biosynthesis, and growth. Oecologia 109:433–441
Zhang HH, Zhang XL, Li X, Ding JN, Zhu WX, Qi F, Zhang T, Tian Y, Sun GY (2012) Effects of NaCl and Na2CO3 stresses on the growth and photosynthesis characteristics of Morus alba seedlings. Ying Yong Sheng Tai Xue Bao 23:625–631 (Chinese)
Acknowledgements
The collaboration and joints visits were funded by the PPP program for the project-related personal exchange of CONICET No. 2019-22669909 and the DAAD 57468556. We would like to thank Dr. Sascha Offermann, Hannover, for correcting the English language.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Reginato, M., Luna, V. & Papenbrock, J. Current knowledge about Na2SO4 effects on plants: what is different in comparison to NaCl?. J Plant Res 134, 1159–1179 (2021). https://doi.org/10.1007/s10265-021-01335-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-021-01335-y