Salt Tolerance in the Halophyte Suaeda maritima L. Dum. Growth, Ion and Water Relations and Gas Exchange in Response to Altered Salinity

Clipson, N. J. W. 1987. Salt tolerance in the halophyte Suaedamaritima L. Dum. Growth, ion and water relations and gas exchangein response to altered salinity.—J. exp. Bot. 38: 1996–2004. Shoot and root fresh and dry weights and shoot sodium, chlorideand potassium contents were measured and shoot relative growthrates calculated in seedlings of Suaeda maritima over a periodof 11 d following a raising of culture solution salinity from0 to 200 mol m₃– NaCl. Growth, growth rates and sodiumand chloride contents, as compared to plants growing in theabsence of salt were increased whilst potassium contents declined.Shoot sodium accumulation rate and the rate of transport ofsodium from root to shoot, osmotic potential, and rates of photosynthesisand transpiration were also measured for up to 72 h after transferof plants originally growing at 0 and 200 mol₃– NaCl to200 and 400 mol m₃– NaCl respectively. Ion uptake andtransport rates were maximal 6-12 h after transfer and thendeclined to new steady-state levels within 48 h; osmotic potentialswere lowered over a 72 h period on average by approximately1·0 MPa; and after 9 h photosynthetic and transpirationrates were reduced by about 20percnt; and 30% respectively.Results are discussed in terms of the ability of halophytesto adjust to fluctuating salinity and to salt tolerance mechanismsin general. Key words: Suaeda maritima, salinity, gas exchange, growth, ion and water relations     

Salt Tolerance in the Halophyte Suaeda maritima (L.) Dum.: Interaction between Aluminium and Salinity

Growth of Suaeda maritima was stimulated by low aluminium concentrationsin saline solution culture with an increase in the number andextent of lateral roots. Under non-saline conditions the sameAl concentrations inhibited growth and led to an abnormal lateralroot initiation. Increasing the level of Al led to growth inhibitionunder both culture conditions. Salinity reduced the uptake of A1 into plant tissue, and therewas no evidence that A1 was tolerated internally. Although short-term³²P influx was increased by A1 there were no long-term effectsof significance on levels of Na, K, Ca nor P in the shoots. The results are discussed in relation to proposed mechanismsof A1 toxicity and the interaction between A1 and salt toxicities.An explanation is proposed for both stimulatory and inhibitoryeffects of A1 as a quantitative expression of a single primaryeffect upon the root system.     

Salt Tolerance in the Halophyte Suaeda maritima L. Dum.: Intracellular Compartmentation of Ions

The time-course of exchange of sodium and potassium ions fromroot and leaf material of the halophyte Suaeda maritima hasbeen followed and the data analysed according to the phenomenologyof efflux, or compartmental, analysis. Sodium ions were exchangedmuch more slowly (c. 4 times) from the vacuoles of leaf cellsof plants grown in sodium chloride than were potassium ionsfrom the vacuoles of leaf cells of plants grown either in similarconcentrations of potassium chloride or in low concentrationsof potassium. In plants grown in sodium chloride, sodium ionswere exchanged 9 times more slowly from the vacuoles of leafcells than from the vacuoles of root cells. The concentration of sodium ions in the cytoplasm of leaf cellsof plants growing in 340 mol m^–3 sodium chloride was estimatedto be 165 mol m^–3 when the average concentration in theleaf tissue was about 600 mol m^–3. As measured by movement from mature to developing leaves inintact plants; there was less in vivo retranslocation of ²²Naand ³⁶CI in plants growing in sodium chloride than there wasof ⁸⁶Rb in plants growing either in potassium chloride or innon-saline conditions. The results are discussed in terms of the concept and energeticsof compartmentation of ions in the cells of halophytes.     

Salt Tolerance in the Halophyte, Suaeda maritima (L.) Dum.: Properties of Malic Enzyme and PEP carboxylase

Malic enzyme and phosphenol pyruvate carboxylase activitieshave been isolated and characterized from the shoots of Suaedamaritima plants grown in culture solution (with and withoutNaCl) or in tap water. The enzymes isolated from the lattershowed increases in both specific activity and K_m values incomparison with plants grown in culture solution: however, theaddition of NaCl to the culture solution had no significanteffect on either enzyme. Malate levels were high in plants grownin tap water, reduced by an ordeT of magnitude by the additionof culture solution and then halved by the addition of NaCl. Both enzymes were inhibited in vitro by NaCl, although the additionof high concentrations of betaine and proline to the assay mediumdid not further inhibit enzyme activity. The significance ofthese results is discussed in relation to the proposed roleof betaine and proline as cytoplasmic osmoregulators. Suaeda maritima, halophyte, salt tolerance, malic enzyme, PEP carboxylase     

Salt tolerance in the halophyte Suaeda maritima L. Dum.

Osmotic potentials and individual epidermal cell turgor pressures were measured in the leaves of seedlings of Suaeda maritima growing over a range of salinities. Leaf osmotic potentials were lower (more negative) the higher the salt concentration of the solution and were lowest in the youngest leaves and stem apices, producing a gradient of osmotic potential towards the apex of the plant. Epidermal cell turgor pressures were of the order of 0.25 to 0.3 MPa in the youngest leaves measured, decreasing to under 0.05 MPa for the oldest leaves. This pattern of turgor pressure was largely unaffected by external salinity. Calculation of leaf water potential indicated that the gradient between young leaves and the external medium was not altered by salinity, but with older leaves, however, this gradient diminished from being the same as that for young leaves in the absence of NaCl, to under 30% of this value at 400 mM NaCl. These results are discussed in relation to the growth response of S. maritima.     

Salt Tolerance in the Halophyte, Suaeda maritima (L.) Dum.: The Influence of the Salinity of the Culture Solution on the Content of Various Organic Compounds

Plants of the halophyte Suaeda maritima were grown in tap wateror in a culture solution in the presence or absence of sodiumchloride and the levels of sugars, amino acids, organic acidsand quaternary ammonium compounds determined in relation tothe balance between cytoplasmic and vacuolar water potentials.The sugar content (some 7 µmol. g f. wt^–1) was unaffectedby the salinity of the growth medium as was the overall contentof amino acids (about 4 µmol. g f. wt^–1). The organicacid content was maximal in plants kept in tap water alone wherethe dominant acid was malic. Plants grown in culture solutioncontained the same acids, although addition of sodium chlorideto the medium brought about the apparent loss of glycolic acidand the appearance of oxalic acid. Only a single quaternaryammonium compound, glycinebetaine, was apparently present inthe tissues: the content of betaine doubled (to 37·5µrmol. g f. wt^–) when sodium chloride was addedto the culture solution. The content of these various compoundsis discussed in relation to the relative values of the cytoplasmicand vacuolar components of the overall tissue water potential Suaeda maritima, halophyte, salt tolerance, betaine, organic compounds, water potential     

Stereological Analysis of Leaf Cells of the Halophyte Suaeda maritima (L.) Dum

A stereological analysis of cells from the mesophyll, vascularbundles and central parenchyma in leaves of the halophyte Suaedamaritima (L.) Dum is described. The volume fraction of vacuolewas greater in plants grown under saline conditions when comparedwith those under non-saline conditions, and there was a concurrentincrease in the surface density of the tonoplast. The volumefraction of chloroplasts and cell wall fell under saline conditions,while that of the intercellular spaces increased. Salinizationof the growth medium was accompanied by a large increase inthe fraction of the cell volume occupied by the mitochondria:the increase in surface density of mitochondrial membranes wassome 72% when averaged over all the cell types analysed. Key words: Salt tolerance, Halophyte, Suaeda maritima, Stereology     

Sodium Chloride Compartmentation in Leaf Vacuoles of the Halophyte Suaeda maritima (L.) Dum. and its Relation to Tonoplast Permeability

Single channel properties, whole vacuole currents and protonpumping capacity were investigated in the intact vacuoles andmembrane patches of leaf tonoplast from the halophyte Suaedamaritima. ATP-dependent proton pumping capacity was similarto non-halophytes whether the plants were or were not grownwith added sodium chloride (200 mM). The most abundant ion channelwas inward rectifying and had a single channel conductance of58 pS in symmetrical KCl solutions (100 mM) to 170 pS usingphysiological conditions (50/150 mM KCl/NaCl cytoplasmic side,50/450 mM KCl/NaCl vacuolar side). The channel showed all thecharacteristics of the SV type channel described in many otherspecies. In the open state these channels caused tonoplast conductancesin excess of 0.5 nS m²– but conductances were much lowerusing physiological ion concentrations and membrane potentials.In spite of the poor selectivity and the potentially large tonoplastconductance it is calculated that compartmentation of NaCl inleaf vacuoles can be sustained by about 30% of ATP-dependentproton pumping capacity. The results do not indicate any specialadaptation of the tonoplast ion channels in the halophyte. Key words: Ion-channels, patch-clamp, salt-tolerance, vacuole     

Chloroplast Implication in the Tolerance to Salinity of the Halophyte Cakile maritima

Russian Journal of Plant Physiology - In this study, the response of the chloroplastic antioxidant system of the halophyte Cakile maritima Scop. and its tolerance to NaCl stress have been studied...     

Kinetics of the Anti-oxidant Response to Salinity in the Halophyte Cakile maritima

The effects of NaCl stress on the activity of anti-oxidant enzymes (superoxide dismutase, catalase (CAT),peroxidase (POD),ascorbate peroxidase (APX), monodehydroascorbate reductase, dehydroascorbate reductase (DHAR), and glutathionereductase (GR)), anti-oxidant molecules (ascorbate and glutathione), and parameters of oxidative stress (malondialdehyde(MDA), electrolyte leakage, and H_2O_2 concentrations) were investigated in Cakile maritima, a halophyte frequent along theTunisian seashore. Seedlings were grown in the presence of salt (100, 200, and 400 mmol/L NaCI). Plants were harvestedperiodically over 20 days. Growth was maximal in the presence of 0-100 mmol/L NaCl. At 400 mmol/L NaCl, growthdecreased significantly. The salt tolerance of C. maritima, at moderate salinities, was associated with the lowest values ofthe parameters indicative of oxidative stress, namely the highest activities of POD, CAT, APX, DHAR, and GR and high tissuecontent of ascorbate and glutathione. However, prolonged exposure to high salinity resulted in a decrease in anti-oxidantactivities and high MDA content, electrolyte leakage, and H_2O_2 concentrations. These results suggest that anti-oxidantsystems participate in the tolerance of C. maritima to moderate salinities.     

Kinetics of the Anti-oxidant Response to Salinity in the Halophyte Cakile maritima

The effects of NaCl stress on the activity of anti-oxidant enzymes （superoxide dismutase, catalase （CAT）, peroxidase （POD）, ascorbate peroxidase （APX）, monodehydroascorbate reductase, dehydroascorbate reductase （DHAR）, and glutathione reductase （GR））, anti-oxidant molecules （ascorbate and glutathione）, and parameters of oxidative stress （malondialdehyde （MDA）, electrolyte leakage, and H2O2 concentrations） were investigated in Cakile maritima, a halophyte frequent along the Tunisian seashore. Seedlings were grown in the presence of salt （100, 200, and 400 mmol/L NaCl）. Plants were harvested periodically over 20 days. Growth was maximal in the presence of 0-100 mmol/L NaCl. At 400 mmol/L NaCl, growth decreased significantly. The salt tolerance of C. maritima, at moderate salinities, was associated with the lowest values of the parameters indicative of oxidative stress, namely the highest activities of POD, CAT, APX, DHAR, and GR and high tissue content of ascorbate and glutathione. However, prolonged exposure to high salinity resulted in a decrease in anti-oxidant activities and high MDA content, electrolyte leakage, and H2O2 concentrations. These results suggest that anti-oxidant systems participate in the tolerance of C. maritima to moderate salinities.     

Salt tolerance in Suaeda maritima (L.) Dum: A COMPARISON OF MITOCHONDRIA ISOLATED FROM GREEN TISSUES OF SUAEDA AND PISUM

Mitochondria were isolated from green leaves and stems of theglycophyte Pisum sativum and the halophyte Suaeda maritima.The preparations oxidized malate, succinate, and 2-oxoglutarateas well as externally added NADH. Acceptor control ratios wereabout 2.8 for mitochondria from Pisum and 1.8 for mitochondriafrom Suaeda oxidizing malate+pyruvate in 125 mM sodium chloride.The mitochondrial fraction was contaminated with chloroplastfragments which resulted in relatively low rates of oxygen uptakewhen these were expressed on a protein basis. The addition of sodium chloride at concentrations greater than200 mM considerably reduced the rates of oxygen uptake by bothspecies in the presence and absence of phosphate acceptor (ADP).Acceptor control ratios were reduced and there was a markeddecline in the ADP/O ratio. Sucrose at equivalent molar concentrationshad a much less drastic effect on the mitochondria. There was no significant difference in the effects of thesetwo solutes on mitochondria from the two species and the similarityof response is discussed in relation to the cytoplasmic ioncontent of the halophyte.     

Salt Tolerance in Suaeda maritima (L.) Dum: THE EFFECT OF SODIUM CHLORIDE ON GROWTH, RESPIRATION, AND SOLUBLE ENZYMES IN A COMPARATIVE STUDY WITH PISUM SATIVUM L

The effect of sodium, chloride on the growth of a halophyte,Suaeda maritima (L.) Dum., was compared with its effect on Pisumsativum L. cv. Alaska under controlled environmental conditions.The salt stimulated the growth of Suaeda maximally at concentrationsof 170 to 340 mM while the growth of Pisum was inhibited evenby 100 mM. Both species accumulated ions in the tops and themaximum concentrations of Na⁺ and Cl^– rose in Suaeda to860 mM (based on the water content) and 730 mM and in Pisumto 170 mM and 300 mM respectively. Respiration in both specieswas inhibited as the NaCl level in the culture solution wasraised. Four supernatant enzymes (malic dehydrogenase, glucose-6-phosphatedehydrogenase, peroxidase, and acid phosphatase) prepared fromPisum and from Suaeda (grown either in the absence of addedNaCl or in the presence of 340 mM NaCl) were assayed in variouslevels of sodium chloride. The dehydrogenases were markedlyinhibited by increasing salt concentrations while there wasa smaller effect on the peroxidase and acid phosphatase. Therewas no difference in the effect of salt on the enzymes preparedfrom the two species although one is halophilic and the otherhalophobic.     

Salt tolerance in the halophyte Suaeda maritima (L.) Dum. The influence of the salinity of the culture solution on leaf starch and phosphate content

Abstract. The starch concentration in mature leaves of the halophyte Suaeda maritima increased from 4.7 to 7.3 mg mg⁻¹ chlorophyll when sodium chloride (680 mol M⁻³) was added to the solution in which the plants were grown. This effect of salinity on the starch: chlorophyll ratio was greater in young than in old leaves. Electron micrographs showed the starch to be in the chloroplasts and this was confirmed by measurements on isolated chloroplasts. Total phosphorus concentration (mg mg⁻¹ chlorophyll) in leaves of all ages from plants of S. maritima decreased on salinization of the growth medium suggesting an inverse relationship between phosphorus and starch concentrations. However, although leaf starch concentration varied with leaf age, phosphorus concentration did not. The cause of starch accumulation in chloroplasts at salinities which are optimal for growth (340 mol m⁻³) remains unclear.     

X-ray microanalysis of ion distribution within root cortical cells of the halophyte Suaeda maritima (L.) Dum.

The ion content of compartments within cortical cells of mature roots of the halophyte Suaeda maritima grown at 200 mol·m^-3 NaCl has been studied by X-ray microanalysis of freeze-substituted thin sections. Sodium and Cl were found in the vacuoles at about four-times the concentration in the cytoplasm or cell walls, whereas K was more concentrated in the cell walls and cytoplasm than in vacuoles. The vacuolar Na concentration was 12- to 13-times higher than that of K. The Na concentration of cell walls of cortical cells was about 95 mol·m^-3 of analysed volume. The cytoplasmic K concentration within the mature cortical cells was estimated to be 55 mol·m^-3 of analysed volume.     

Osmotic Stress and Ion-Specific Effects on Xylem Abscisic Acid and the Relevance to Salinity Tolerance in Poplar

We designed two experiments to investigate the osmotic stress and ion-specific effects on xylem abscisic acid (ABA) and the relevance to salinity tolerance in one-year-old seedlings of Populus euphratica Oliv. (a salt-resistant genotype) and one-year-old rooted cuttings of P. 'popularis 35-44' (P. popularis) (a salt-sensitive genotype). Net photosynthetic rates (Pn) and unit transpiration rates (TRN) of the two genotypes were significantly decreased upon osmotic shock caused by PEG 6000 (osmotic potential = -0.24 MPa) or iso-NaCl (50 mM). Shoot xylem ABA concentrations in both genotypes increased rapidly after the onset of PEG stress, resulting from a decreased water flow. NaCl-treated trees of P. euphratica maintained considerably greater concentrations of ABA than PEG-treated plants in a longer term, whereas salinized P. popularis exhibited a transient accumulation of ABA in the shoot. TRN was greatly enhanced in both genotypes when pressure (0.24 MPa) was applied to counteract the osmotic suction of 50 mM NaCl. Pressurizing of root systems diluted solutes in the root xylem, but the dilution effect was more pronounced in P. popularis. Root xylem ABA concentrations in P. euphratica steadily increased with salt stress although pressurization lowered its levels. In contrast, there were no observed changes in ABA response to salinity in pressured P. popularis. Therefore, we concluded that the salt-tolerant P. euphratica had a greater capacity to synthesize ABA under saline conditions, which may partially result from specific salt effects. In addition, P. euphratica exhibited a higher capacity for salt (Na+ and Cl-) transport control under salt stress, compared with P. popularis. The possible association between ABA and salt transport limitation, and the relevance to salinity tolerance were discussed.     

Osmotic Stress and Ion-Specific Effects on Xylem Abscisic Acid and the Relevance to Salinity Tolerance in Poplar

We designed two experiments to investigate the osmotic stress and ion-specific effects on xylem abscisic acid (ABA) and the relevance to salinity tolerance in one-year-old seedlings of Populus euphratica Oliv. (a salt-resistant genotype) and one-year-old rooted cuttings of P. 'popularis 35-44' (P. popularis) (a salt-sensitive genotype). Net photosynthetic rates (Pn) and unit transpiration rates (TRN) of the two genotypes were significantly decreased upon osmotic shock caused by PEG 6000 (osmotic potential = -0.24 MPa) or iso-NaCl (50 mM). Shoot xylem ABA concentrations in both genotypes increased rapidly after the onset of PEG stress, resulting from a decreased water flow. NaCl-treated trees of P. euphratica maintained considerably greater concentrations of ABA than PEG-treated plants in a longer term, whereas salinized P. popularis exhibited a transient accumulation of ABA in the shoot. TRN was greatly enhanced in both genotypes when pressure (0.24 MPa) was applied to counteract the osmotic suction of 50 mM NaCl. Pressurizing of root systems diluted solutes in the root xylem, but the dilution effect was more pronounced in P. popularis. Root xylem ABA concentrations in P. euphratica steadily increased with salt stress although pressurization lowered its levels. In contrast, there were no observed changes in ABA response to salinity in pressured P. popularis. Therefore, we concluded that the salt-tolerant P. euphratica had a greater capacity to synthesize ABA under saline conditions, which may partially result from specific salt effects. In addition, P. euphratica exhibited a higher capacity for salt (Na+ and Cl-) transport control under salt stress, compared with P. popularis. The possible association between ABA and salt transport limitation, and the relevance to salinity tolerance were discussed.     

Abscisic Acid Reduces Leaf Abscission and Increases Salt Tolerance in Citrus Plants

This paper describes the physiological effects of abscisic acid (ABA) and 100 mM NaCl on citrus plants. Water potential, leaf abscission, ethylene production, photosynthetic rate, stomatal conductance, and chloride accumulation in roots and leaves were measured in plants of Salustiana scion [Citrus sinensis (L) Osbeck] grafted onto Carrizo citrange (Citrus sinensis [L.] Osbeck × Poncirus trifoliata [L.] Raf) rootstock. Plants under salt stress accumulated high amounts of chloride, increased ethylene production, and induced leaf abscission. Stomatal conductance and photosynthetic rates rapidly dropped after salinization. The addition of 10 mM ABA to the nutrient solution 10 days before the exposure to salt stress reduced ethylene release and leaf abscission. These effects were probably due to a decrease in the accumulation of toxic Cl- ions in leaves. In non-salinized plants, ABA reduced stomatal conductance and CO2 assimilation, whereas in salinized plants the treatment slightly increased these two parameters. The results suggest a protective role for ABA in citrus under salinity.