Progetto cofinanziato dal programma LIFE+ Stefania De Pascale. Department ofagriculturalengineering and Agronomy University of Naples Federico II
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1 Progetto cofinanziato dal programma LIFE+ Salinity Stress Stefania De Pascale D t t fa i lt le i i d A Department ofagriculturalengineering and Agronomy University of Naples Federico II
2 Salt affected soil According to the FAO Land and Plant Nutrition Management Service, over 6% of the world's land is affected by either salinity or sodicity. The term salt-affected refers to soils that are saline or sodic, and these cover over 400 million hectares, which is over 6% of the world land area. Much of the world s land is not cultivated, but a significant proportion of cultivated land is salt-affected. Of the current 230 million ha of irrigated land, 45 million ha are salt-affected affected (19.5%) and of the 1,500 million ha under dryland agriculture, 32 million are salt-affected to varying degrees (2.1%).
3 Regional distribution of salt-affected soils, in million hectares Regions Total area Saline soils Sodic soils Mha Mha % Mha % Africa Asia, the Pacific and Australia Europe Latin America Near East North America Total % % Source: FAO Land and Plant Nutrition Management Service
4 Salinization in Italy (source ENEA)
5 Natural or primary salinity (1) Primary salinity results from the accumulation of salts over long periods of time, through natural processes, in the soil or groundwater. It is caused by two natural processes. The first is the weathering of parent materials containing soluble salts. Weathering processes break down rocks and release soluble salts of various types, mainly chlorides of sodium, calcium and magnesium, and to a lesser extent, sulphates and carbonates. Sodium chloride is the most soluble salt.
6 Natural or primary salinity (2) The second is the deposition of oceanic salt carried in wind and rain. 'Cyclic salts' are ocean salts carried inland by wind and deposited by rainfall, and are mainly sodium chloride. Rainwater contains from 6 to 50 mg/kg of salt, the concentration ti of salts decreasing with distance from the coast. If the concentration is 10 mg/kg, this would add 10 kg/ha of salt for each100 mm ofrainfall a per year. The amount of salt stored in the soil varies with the soil type, being low for sandy soils and high for soils contain a high percentage of clay minerals. It also varies inversely with average annual rainfall.
7 Concentration of salts in rain and seawater (source: Encyclopaedia Britannica) i Ion rainwater (local) l) seawater (global) l) mg/kg (ppm) (µmol/l) µm g/kg ( ) (mmol/l) mm Sodium (Na + ) Chloride (Cl - ) Sulfate (SO 2-4 ) Magnesium (Mg 2+ ) Calcium (Ca 2+ ) Potassium (K + ) Total The composition of rainwater varies greatly depending on prevailing winds and distance from the coast. The composition of seawater is uniform around the globe. The electrical l conductivity it of rainwater is about ds/m, and of seawater is 55 ds/m.
8 Secondary or human-induced salinity (1) Secondary salinisation results from human activities that change the hydrologic balance of the soil between water applied (irrigation or rainfall) and water used by crops (transpiration). The most common causes are: land clearing and the replacement of perennial vegetation with annual crops irrigation schemes using salt-rich irrigation water or having insufficient drainage. Prior to human activities, in arid or semi-arid climates, the water used by natural vegetation was in balance with the rainfall, with the deep roots of native vegetation ensuring that the water tables were well below the surface. Clearing and irrigation changed this balance, so that rainfall on the one hand, and irrigation water on the other, provided more water than the crops could use.
9 Secondary or human-induced d salinity it (2) The excess water raises water tbl table and mobilises salts previously stored in the subsoil and brings them up to the root zone. Plants use the water and leave the salt behind until the soil water becomes too salty for further water uptake tk by roots. The water table continues to rise, and when it comes close to the surface, water evaporates leaving salts behind on the surface and thus forming a salt scald. The mobilised salt can also move laterally to water courses and increase their salinity.
10 Soil sodicity Sodic soils have a low concentration of soluble salts, but a high percent of exchangeable Na+; that is, Na+ forms a high percent of all cations bound to the negative charges on the clay particles that make up the soil complex. Sodicity it is defined d in terms of the threshold h ESP (exchangable sodium percentage) that causes degradation of soil structure. The negatively charged clay particles are held together by divalent cations. When monovalent cations such as Na+ displace the divalent cations on the soil complex, and the concentration of free soluble salts is low, the complex swells and the clay particles separate ('disperse'). The USDA Salinity Laboratory defines a sodic soil as having an ESP greater than 15. If the concentration of soluble salts is sufficiently low, hydrolysis of the sodic clay will occur, creating a highly alkaline soil. Alkaline soils are a type of sodic soil with a high ph due to carbonate salts, and are defined as having an ESP of 15 or more with a ph of
11 Measuring soil salinity Soil salinity is measured by its electrical conductivity. The SI unit of electrical conductivity (EC) is ds/m (10 mm NaCl has an EC close to 1 ds/m). Originally the conductivity was measured in a saturated paste extract t (ECe), btth but the method is tdi tedious as first the saturated t paste has to be made, second the water needs to be extracted by a powerful vacuum pump, and third a very sandy soil does not make a saturated paste. A more convenient and universal method is a '1:5 extract'. The soil is dried or compressed, shaken with 5 g deionised water per 1 g soil, the probe of a hand-held held conductivity meter is placed in the suspension, and the EC measured. The EC of the soil that was sampled can be calculated if its water content is known at the time of sampling. Alternatively, the measurement can be related to the field capacity of the soil using conversion factors. As a rough guide, a sandy soil will have a field capacity of 0.2 g water per g soil, and a clay soil about 0.4 g/g.
12 Units for measuring salinity, and conversion factors Measurement and units Conductivity (ds/m) Conductivity (µs/cm) Application 1 ds/m is equal to: Equivalent units soils 1 1 ds/m = 1 ms/cm = 1 mmho/cm water 1000 µs/cm 1 µs/cm = 1 µmho/cm Total dissolved salts water 640 mg/l (approx.) 1 mg/l = 1mg/kg= 1 (mg/l) ppm Molarity of NaCl (mm) laboratory 10 mm 1 mm = 1 mmol/l Conversion factors relating total dissolved salts or pure NaCl to an electrical conductivity (EC) of 1 ds/m (1 decisiemen/metre) are given, along with equivalent units of various types, old and new. The conversion of EC of 1 ds/m to total dissolved salts (640 mg/l) assumes a composition of salts that is common in groundwater across the world. The exact factor varies from 530 (if the salt is predominantly NaCl) to 900 (if the salts are formed predominantly from divalent ions).
13 Classifying Species Halophytes are plants adapted to living in saline soils (salt-tolerant). Glycophytes are salt-intolerant plants from non-saline environments.
14 Suaeda maritima Sugar beet Bean Cotton
15 Salt Tolerance Strategies Salt exclusion from roots Absorption from the transpiration stream secretory salt glands. compatible solutes throughout the cell expensive. Accumulate salt in vacuoles, compatible solutes in cytosol less expensive. Ion dilution succulents. Altered protein synthesis.
16 The Effect of Salinity on Plants Salts in the soil water may inhibit plant growth for two reasons. the presence of salt in the soil solution reduces the ability of the plant to take up water, and this leads to reductions in the growth rate. This is referred to as the osmotic or water-deficit effect of salinity. if excessive amounts of salt enter the plant in the transpiration stream there will be injury to cells in the transpiring leaves and this may cause further reductions in growth. This is called the salt-specific specific or ion-excess effect of salinity. The definition of salt tolerance is usually the percent biomass production in saline soil relative to plants in non-saline soil, after growth for an extended period of time. For slow-growing, long-lived, or uncultivated species it is often difficult to assess the reduction in biomass production, so percent survival li isoften used.
17 Biomass production of four diverse and important plant species in a range of salinities. Wheat is one of the more salt-tolerant crops, and rice is one of the more salt-sensitive crops.two halophytes: a saltbush species Atriplex amnicola and a grass Diplachne (syn. Leptochloa) fusca or Kallar grass. Both halophytes show outstanding salt tolerance withhigh growth rates.
18 The Maas and Hoffman model Another criterion of salt tolerance of crops is their yield in saline versus non- saline conditions. A survey of salt tolerance of crops, vegetables and fruit trees was made by the USDA Salinity Laboratory. This shows for each species a threshold salinity below which there is no reduction in yield, and then a regression for thereduction ti inyield ild with increasing i salinity. it Limits: The data in some cases are for a single cultivar of the species, or a limited number of cultivars at a single site, so they are not necessarily representative of the species. The data are related to an ECe value, which is not an appropriate reference point for a sandy soil, or for many current soil salinity estimates that based merely on a 1:5 extract. Yield always shows a threshold in response to a range of salinities, but with young plants a threshold is rarely seen. However, the data are useful in that they show the wide range of tolerance across species, and also show that yield has a different pattern of response than does vegetative biomass.
19 ECe ECe is the electrical conductivity of the saturated paste extract, that is, of the solution extracted from a soil sample after being mixed with sufficient water to produce a saturated paste. The moisture content of a drained soil at field capacity may be much lower than the water content of its saturated paste. Further, under dryland agriculture, the soil water content might drop to half of field capacity during the life of the crop. The actual salinity of a rain-fed field whose soil had an ECe of 4 ds/m could be 8-12 ds/m.
20 Defining Salinity Tolerance threshold Yield EC e
21 Categories for classifying crop tolerance to salinity according to the Maas and Hoffman model. Note that the ECe is more applicable to an irrigated than a rainfed field, in the latter the soil moisture content might be 2-4 time less than in a saturated paste.
22 Causes of the Growth Reduction under Saline Conditions The effects of a saline soil are two-fold: there are effects of the salt outside the roots, and there are effects of the salt taken up by plants. The salt in the soil solution lti (the osmotic stress ) reduces leaf growth and to a lesser extent root growth, and decreases stomatal conductance and thereby photosynthesis. The cellular and metabolic processes involved are in common to drought-affected plants.
23 Salinity and Roots Roots must exclude most of the Na+ and Cl- dissolved in the soil solution or the salt will gradually build up with time in the shoot and become so high that it kills it. Roots themselves do not accumulate excessively high concentrations of salt. The Na+ and Cl- concentration in roots is rarely higherthanintheexternalsolution, and often is lower.
24 ABA content in xylem, sap, leaves and roots of Atriplex canescens as affected by external NaCl concentration (Kefu et al., 1991, Aust.J.Plant Physiol., 18: 17-24)
25 Salinity and plant growth The salt within the plant enhances the senescence of old leaves. The rate at which new leaves are produced depends largely on the water potential of the soil solution, in the same way as for a drought-stressed plant. Salts themselves do not build up in the growing tissues at concentrations that inhibit growth: meristematic tissues are fed largely by the phloem from which salt is effectively excluded, and rapidly elongating cells can accommodate the salt that t arrives in the xylem within their expanding vacuoles. So, the salt taken up by the plant does not directly inhibit the growth of new leaves.
26 Salinity and plant growth Continued transport of salt into transpiring leaves over a long period of time eventually results in very high Na+ and Cl- concentrations, and they die. The rate of leaf death is crucial for the survival of the plant. If new leaves are continually produced at a rate greater than that at which old leaves die, then there might be enough photosynthesising leaves for the plant to produce some flowers and seeds. However, if the rate of leaf death exceeds the rate at which new leaves are produced, then the plant may not survive to produce seed. For an annual plant there is a race against time to initiate flowers and form seeds, while the leaf area is still adequate to supply the necessary photosynthate. For perennial species, there is an opportunity to enter a state of dormancy, and thus survive the stress. The two responses occur sequentially, giving rise to a two-phase growth response to salinity
27 The two-phase growth response to salinity model The first phase of growth reduction is quickly apparent, and is due to the salt outside the roots. It is essentially a water stress or osmotic phase, for which there is surprisingly little genotypic difference. Then there is a second phase of growth reduction, which takes time to develop, and results from internal injury.
28 The two-phase growth response Two accessions of the diploid wheat progenitor Ae. tauschii grown in supported hydroponics in control solution (closed symbols) and in 150 mm NaCl (open symbols). Circles denote the tolerant accession, triangles the sensitive one. The arrow marks the time at which symptoms of salt injury could be seen on the sensitive accession; at that time the proportion of dead d leaves was 10% for the sensitive and 1% for the tolerant accession (Munns et al., 1995).
29 The Relationship between Transpiration and Salt Uptake The fundamental processes governing the relationship between water and ion flow through roots are complex and not well understood. NaCl does not move passively with the transpiration stream, neither is its movement entirely independent of it, at least in some species, or over certain ranges of transpiration. Measurements of ion concentrations in leaves of most plants grown at different humidities are consistent with the hypothesis that salt transport to leaves is substantially affected only from very low to moderate water flow. An effect might be seen more with species that are very poor excluders which carry much more salt in an apoplastic or transpirational "bypass" pathway than other species.
30 The relation between ion flux to the shoot and transpiration (water flow) (Munns, 1985).
31 Salt stress effects Pr rimary Ion-Excess Osmotic (Na + Cl - ) stress Nutrient t Water deficit imbalance Growth Reduction ts y effect Sec condar Reduced cell expansion and division Reduced membrane function Production of reactive oxygen specie Reduced photosynthesis Toxicity Reduced nutrient uptake Cell Death
32 Salinity stress: at cellular level Salinity stress can have different effects: 1) toxicity of specific ions» high levels of Cl -,Na + can be toxic - also aluminum, other heavy metals» Na+ tends to displace Ca 2+, which is necessary for proper cell function» plants have mechanisms to exclude Na +, out of cell, into vacuole, into glands 2) osmotic stress» plants can synthesize compatible solutes-amino acids, carbohydrates» these increase osmotic pressure, make cell water potential more negative
33 Primary effects Water deficit same stress effects as occurs under drought Ion disequilibrium Na + rapidly enters the cell because the membrane potential is inside negative (~- 120 to -200 mv), Na + can accumulate lt to 10 2 to 10 3 fold greater concentration than in the apoplast, driven by the membrane potential (sea water 457 mm Na + ) Na + is cytotoxic and K + is an essential nutrient Ca 2+ disequilibrium affects K + /Na + selective uptake
34 Secondary effects Reduced cell expansion and assimilate production as is the case for water deficit, adaptation includes a reduction in cell expansion rate that affects photosynthate production Photosynthate production is reduced carbon metabolism or photophosphorylation is salt sensitive Decreased cytosolic metabolism metabolic poisoning, enzymes of halophytes and glycophytes are equally sensitive to NaCl Production of reactive oxygen species (ROS) products of photorespiration and mitochondrial respiration when electron flow is too great for the normal electron acceptors of metabolism, e.g. NADPH, resulting in the production reactive oxygen species ROSs are potent oxidants that can lead to cell death because of lipid peroxidation (membrane destruction), protein oxidation, enzyme inactivation and RNA/DNA damage
35 NaCl Uptake into Roots and Movement in the Plant Radial transport from the soil solution into roots is apoplastic/symplastic (epidermis and cortex), symplastic across the endodermis and then loaded into the xylem
36 NaCl Uptake into Roots and Movement in the Plant Radial transport may be regulated, i.e., Na + and Cl - transport to the xylem may be limited in epidermal and cortical cells, i.e., prior to the endodermis, but xylem loading is passive, plants seem to have capacity to regulate K + /Na + concentration in the xylem sap Salt movement through the xylem is determined by the transpirational flux moves through the xylem to the shoot Plants minimize exposure of meristematic cells to Na + and Cl - the lack of vasculature to the meristem reduces transport to cells in this tissue, fully expanded leaves are ion sinks and may abscise Some halophytes deposit salt on the surface of leaves (sink) via glands or bladders
37 Relationship between stomatal conductance and water salinity in Aster (Kerstiens et al., 2002, New Phytologist, 153: )
38 Decreased cytosolic metabolism A. spongiosa and S. australis are halophytes py
39 Osmotic Adjustment and Ion Comparmentalization Osmotic Adjustment and Ion Comparmentalization cellular level response is osmotic adjustment (water status adaptation) that is mediated by compartmentalization of Na + and Cl - into the vacuole, compatible osmolytes are accumulated in the cytosol Cell volume increases 10- to 100-fold during growth and development due almost entirely to an increase in the vacuole size, i.e., water uptake into the vacuole drives cell expansion Na + and Cl - compartmentalization in the vacuole is a necessary component of osmotic adjustment in saline environments, net uptake of these ions across the plasma membrane is restricted and organic osmolytes mediate osmotic adjustment in the cytosol or organelles
40 Osmotic Adjustment and Ion Comparmentalization K + (Na + ) + H K + (Na + ) Na + /H +K+ mt cp OH-*-scavenging perox Plasma -120 to -200 mv Membrane ATP ATP H + H + PPi H + ATP Ca 2+ Ca 2+ Ca 2+ ATP Ca 2+ H + Ca 2+ K + polyols Na + Tonoplast Na + Cl - proline ph 7.5 betaine trehalose ectoine ph 5.5 DMSP +20to+50mV +50 H + Na + Ca 2+ H + H H + 2 O Na+ Ca 2+ Cl - Cl - Cl - H +Cl- ph 5.5 NaCl Na +Inositol H 2 O
41 Ion Homeostasis Ion Homeostasis Transport Determinants coordinate net Na+ and Cl- uptake across the plasma membrane with cellular l capacity to compartmentalize the ions into the vacuole, i.e., cytosolic Na+ and Cl- concentrations in the cytosol are maintained below toxic levels Plasma membrane: Influx Efflux Tonoplast: Influx Salt stress signaling that regulates Na + homeostasis H + driven antiporter SOS
42 The Arabidospsis SOS signalling g pathway for Na + homeostasis can be reconstituted in yeast Salt Na+ SOS1 Sensor? [Ca 2+ ] SOS3 SOS2 H+
43 SALT STRESS ABA synthesis Proteins for the signal-transduction pathway (DNA e RNA binding proteins, protein kinases) Enzymes directly involved in the synthesis of compounds involved in plant response to salt stress (compatible solutes, antioxidants, aquaporins, membrane protectors,...) SALT TOLERANCE
44 Mechanisms of Control of Salt Transport The rate at which h old leaves die depends d on the rate at which h salts accumulate to toxic levels. Thus, control of the rate at which salt arrives in leaves is essential, as are mechanisms that reduce the toxicity of the salt. For species lacking the ability to compartmentalise salts in the vacuoles to high concentrations, continued transport of salt to the leaves will eventually result in either excessive build-up of salts in the cell walls or in the cytoplasm. The former will cause death through dehydration, and the latter will cause death through poisoning of metabolic systems such as photosynthesis or respiration.
45 Control at the whole plant level Control of salt transport into and through the plant takes place at five sites in the plant. Control occurs in the root cortex, at the loading of the xylem, at the retrieval from the xylem in upper parts of the roots. These three processes serve to reduce the transport to the leaves. Control in the shoot occurs by the exclusion of salt from the phloem sap flowing to meristematic regions of the shoot. An additional mechanism occurs in most halophytes: specialised cells to excrete salt from leaves.
46 Control points at which salt transport is regulated. These are: 1. selectivity of uptake from the soil solution 2. loading of the xylem 3. removal of salt from the xylem in the upper part of the plant 4. loading of the phloem 5. excretion through salt glands or bladders For a salt tolerant plant growing for some time in a soil solution of 100 mm NaCl, the root concentrations of Na+ and Cl- are typically about 50 mm, the xylem concentration about 5 mm, and the concentration in the oldest leaf as high as 500 mm (Munns et al., 2002).
47 Control at the whole plant level Exclusion is particularly important for perennial species whose leaves may live for a year or more. For these species there is greater need to regulate the incoming salt load than for annual species whose leaves may live for only one month. There are contributory features that function to maintain low rates of salt accumulation in leaves. High shoot/root ratios High intrinsic growth rates Absence of an apoplastic pathway in roots All will serve to reduce the rate at which salt enters the transpiration stream and accumulates in the shoot.
48 Control at the cellular level: ion compartmentation There is no evidence of adaptations in enzymes to the presence of salt, so mechanisms for salt tolerance at the cellular level involve keeping the salt out of the cytoplasm, and sequestering it in the vacuole. That this occurs in most species is indicated by the high concentrations found in leaves that are still functioning normally, concentrations well over 200 mm, which are known to completely repress enzyme activity in vitro Generally, Na+ starts to inhibit most enzymes at a concentration above 100 mm. The concentration at which Cl- becomes toxic is is probably in the same range If Na+ and Cl- are sequestered in the vacuole of the cell, K+ and organic solutes should accumulate in the cytoplasm and organelles to balance the osmotic pressure of the ions in the vacuole. The organic solutes that accumulate most commonly under salinity are proline and glycinebetaine, although other molecules can accumulate to lesser degrees. Salt tolerant species have transport systems on the tonoplast that can sequester Na+ and Cl- at high concentrations within the vacuoles, while maintaining much lower concentrations in the cytoplasmic compartments.
49 H 2 O H 2 O Na + Na + Na + Cl - Cl - Cl - Na + Cl - Cl NaCl - Na + Na + Cl - Na + Na + Na + Na + Na + H 2 O Na + [Compatible solutes] H 2 O
50 Osmotic Adjustment Many plants cell by osmotic adjustment in which levels of osmotically active solutes. is lowered without any loss of cell volume or turgor. An active mechanism, modest, of the order of > -0.8 MPa. Due to increases in simple sugars, organic acids or ions such as K+.
51 Compatible Solutes Many cytosolic enzymes are inhibited by high ion concentration. Ion accumulation in osmotic adjustment occurs mainly in the vacuole. To balance between the vacuole and the cytosol, compatible solutes in the cytosol. Compatible solutes do not interfere with the metabolic functions of the cell or its organelles. E.g. proline, sorbitol, glycine betaine. Response develops over several days.
52 F MK i BD dl h YY (1994) St d St C i i C lti t d From: McKersie, B.D. and Leshem, Y.Y. (1994) Stress andstress Coping in Cultivated Plants. Kluwer Academic Publishers, London.
53 solut tes Co ompa atible Relationship between compatible solutes and growth growth Promotor
54 morphological and physiological traits - root architecture; - hydraulic conductivity properties (aquaporins). escaping and avoidance - shifting the time of flowering, stomatal response; - leaf shape and area; - leaf reflection of radiation i (hairiness, i leaf angle, waxiness).
55 Saline stress adaptation in plant S1 S2 S3 Osmotic ad Agg djustm giustament to t osmot tico (MPa) Days after transplant
56 NaCl NaCl NaCl Saline water
57 Summary: Salinity 33% of irrigated land on earth is salt-affected. Salts alter soil structure, lower soil, havespecific ion effects (toxicity). Na + most important, but Cl -, Ca 2+, Mg 2+, SO 2-4 also significant. High Na + /K + ratio: Inactivates enzymes Disrupts Ca 2+ /K + balance in plasma membranes Inhibits Photosynthesis
58 Summary: Salinity The initial growth reduction is due to the osmotic effect of the salt outside the roots, and that what distinguishes a salt- sensitive plant from a more tolerant one is the inability to prevent salt from reaching toxic levels in the transpiring leaves, which takes time. To grow in saline conditions, plants must maintain a high water status in the face of soil water deficits and potential ion toxicity. A plant can only grow or survive in a saline soil if it can both continue to take up water and exclude a large proportion of the salt in the soil solution.
59 Summary: Salinity Roots do most of the work in protecting the plant from excessive uptake of salts, and filter out most of the salt in the soil while taking up water. Even so, there are mechanisms for coping with the continuous delivery of relatively small amounts of salt that arrive in the leaves, the most important being the cellular compartmentalisation of salts in the vacuoles of the mesophyll cells. This strategy t allows plants to minimize ii i or dl delay the toxic effects of high concentrations of ions on important and sensitive cytoplasmic processes. The rate at which h leaves die is the rate at which h salts accumulate to toxic levels, so genotypes that have poor control of the rate at which salt arrives in leaves, or a poor ability to sequester that salt in cell vacuoles, have a greater rate of leaf death.
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