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Effect of salinization of soil on growth and macro- and micro-nutrient accumulation in seedlings of Salvadora persica (Salvadoraceae)
Forest Ecology and Management 202 (2004) 181–193 www.elsevier.com/locate/foreco
Effect of salinization of soil on growth and macro- and micro-nutrient accumulation in seedlings of Salvadora persica (Salvadoraceae) P.J. Ramoliya, H.M. Patel, A.N. Pandey* Department of Biosciences, Saurashtra University, Rajkot 360005, India Received 21 May 2003; received in revised form 26 April 2004; accepted 8 July 2004
Abstract Effects of salinization of soil on emergence, seedling growth and mineral accumulation of Salvadora persica Linn. (Salvadoraceae) were studied. A mixture of chlorides and sulphates of Na, K, Ca and Mg was added to the soil and salinity was maintained at 4.3, 6.1, 8.4, 10.3, 12.5, 14.9 and 17.2 dS m1. A negative relationship between seedling emergence and salt concentration was obtained. Seedlings did not emerge when soil salinity exceeded 14.9 dS m1. Results suggested that this tree species is salt tolerant at seed germination and seedling stages. Elongation of stem and root was retarded by increasing salt stress. Young roots and stem were most tolerant to salt stress and were followed by leaves and old roots. Leaf tissue exhibited maximum reduction in dry mass production in response to increasing salt stress. However, production of young roots and death of old roots were found to be continuous and plants apparently use this process as an avoidance mechanism to remove excess ions and delay onset of ion accumulation in this tissue. This phenomenon, designated ‘‘fine root turnover’’ is of an importance to the mechanisms of salt tolerance. Plants accumulated Na in roots and were able to regulate transfer of Na ions to leaves. Stem tissues were barrier for translocation of Na from root to leaf. Moreover, K significantly increased in leaf, but decreased in root tissues with increased salinization. Nitrogen content significantly decreased in all tissues (leaf, stem and root) in response to low water treatment and salinization of soil. Phosphorus content significantly decreased, while Ca increased in leaf as soil salinity increased. Changes in elements accumulation pattern and the possible mechanisms for avoidance of Na toxicity in tissues and organism level are discussed. # 2004 Elsevier B.V. All rights reserved. Keywords: Salinization of soil; Salvadora persica; Seedling emergence; Seedling growth; Salt tolerance; Adaptation; Accumulation; Macroand micro-nutrients
1. Introduction * Corresponding author. Tel.: +91 281 2572833/2586419; fax: +91 281 2577633. E-mail address: [email protected], [email protected] (A.N. Pandey).
Salt stress is a world-wide problem and soil salinity is common in arid and semi-arid regions than in humid regions. Salinity is a scourge for agriculture, forestry,
0378-1127/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2004.07.020
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pasture development and other similar practices. An understanding of responses of plants to salinity is of great practical significance. High concentrations of salts have detrimental effects on plant growth (Garg and Gupta, 1997; Mer et al., 2000) and excessive concentrations kill growing plants (Donahue et al., 1983). Many investigators have reported retardation of germination and growth of seedlings at high salinity (Bernstein, 1962; Garg and Gupta, 1997; Ramoliya and Pandey, 2003). However, plant species differ in their sensitivity or tolerance to salts (Brady and Weil, 1996). There are many different types of salts and almost an equally diverse set of mechanisms of avoidance or tolerance. In addition, organs, tissues and cells at different developmental stages of plants exhibit varying degrees of tolerance to environmental conditions (Munns, 1993; Ashraf, 1994). It is reported that soil salinity suppresses shoot growth more than the root growth (Ramoliya and Pandey, 2003; Maas and Hoffman, 1977). However, fewer studies on the effect of soil salinity on root growth have been conducted (Garg and Gupta, 1997). The high salt content lowers osmotic potential of soil water and consequently the availability of soil water to plants. In saline soil, salt induced water deficit is one of the major constraints for plant growth. As soils dry down soil salinity is exacerbated. Frequent droughts are a regular phenomenon in saline deserts. Eventually, responses of roots and shoots of plants to soil salinity should be understood under both wet and dry soil conditions. In addition, many nutrient interactions in salt-stressed plants can occur which may have important consequences for growth. Internal concentrations of major nutrients and their uptake have been frequently studied (e.g. Maas and Grieve, 1987; Cramer et al., 1989), but the relationship between micro-nutrient concentrations and soil salinity is rather complex and remains poorly understood (Tozlu et al., 2000). The knowledge acquired regarding the growth and survival of plants under natural habitat conditions could be useful for: (i) screening of plant species for the afforestation of saline deserts, and also (ii) for understanding the mechanisms which plants use in the avoidance and/ or tolerance of salt stress. Salvadora persica Linn. (Salvadoraceae) is one of the dominant tree species in the Kutch (north–west saline desert) of Gujarat State in India. It also grows successfully in coastal areas as well as in non-saline
and marginal semi-arid central area of Saurashtra region, to the south of Kutch. S. persica is extremely important to local people because of its oil yielding, pharmaceutical, fuel and fodder value and small but edible fruits. However, the potential of this tree species to grow and survive in the saline desert of kutch is not known. The present investigation was carried out: (i) to understand the adaptive features of S. persica, which allow it to grow and survive in saline and arid regions, and (ii) to assess the pattern of macro- and micro-nutrient accumulation within the tissues of this tree species in response to salt stress.
2. Materials and methods 2.1. Study area The present study was carried out at Naliya (238280 N, 688800 E) in Kutch. The soil is a non-calcareous sandy loam containing 70.1% sand, 13.7% silt and 16.2% clay. The available soil-water between the wilting coefficient and field capacity ranged from 7.6% to 22.4%, respectively. The total organic carbon content was 0.6% and pH was 8.1. The electrical conductivity of the soil ranged from 4.3 to 6.1 dS m1. Soil was deficient in nitrogen (0.07%) and phosphorus (0.01%). The Kutch and Saurashtra regions are tropical monsoonic and can be ecoclimatically classified as arid and semi-arid, respectively. The entire area is markedly affected by south-western monsoon which causes the onset of wet season in mid-June, and its retreat by the end of September coincides with a lowering of temperature and gradual onset of winter. Total annual rainfall is about 395 mm at Naliya and about 554 mm in central Saurashtra which occurs totally during the rainy season. Typically, there are three main seasons: summer (April–mid June), monsoon (mid June–September) and winter (November–February). The months of October and March are transition periods between rainy (monsoon) and winter and between winter and summer seasons, respectively. Winters are generally mild and the summers hot. 2.2. Seedling emergence Surface soil (0–10 cm depth) was collected, airdried and passed through a 2 mm mesh screen. Seven
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lots of soil, of 100 kg each, were separately spread, about 50 mm thick, over polyethylene sheets. A mixture of NaCl, KCl, CaCl2, MgCl2, Na2SO4, K2SO4, CaSO4 and MgSO4 in a proportion of 3:3:1:1:1:1:1:1, was then thoroughly mixed with soil to yield electrical conductivities of 6.1, 8.4, 10.3, 12.5, 14.9 and 17.2 dS m1 in the six lots of soil, respectively. The quantities of salt added to the soil are given in the table in Appendix A. There was no addition of salt to the soil of seventh lot which served as control. Electrical conductivity of the control soil was 4.3 dS m1. Soil suspension was prepared in distilled water (1:2 (w/ w)), and electrical conductivity determined by a Systronics digital conductivity meter. Naturally occurring chlorides and sulphates were added to soil to check effects of ion interaction on root uptake. A high proportion of chlorides in salt mixture was maintained as the study area is in proximity to the Arabian Sea and seawater enters and spreads at certain spatially separated locations at its most northern part. Five polyethylene bags for each level of soil salinity were each filled with 2 kg of soil. Tap water was added to the soils to field capacity and soils were then allowed to dry for 6 days. Soils were then raked gently and seeds were sown on 4 July 1999. Bags were kept inside a wire-net cage of 10 m 10 m area which had its top covered by a thick and transparent plastic sheet because it was the rainy season. Ten seeds were sown in each bag at a depth of about 8–12 mm. Immediately after sowing, soils were watered and thereafter watering was carried out on alternate days. Emergence of seedlings was recorded daily over a period of forty days. A linear model was fitted to cumulative percentage seed germination using the expression: Sin1 Hp = b0 + b1x, where Sin1 Hp is the proportion of cumulative seed germination, x is soil salinity and b0 and b1 are constants. Salt concentration at which seed germination was reduced to 50% (SG50) was determined using this model. 2.3. Seedling growth For the growth studies, seedlings of S. persica were grown in Petri dishes from medium sized seeds collected at Naliya in Kutch. Soil of each concentration of salt was filled in to forty open-bottomed cylinders (10 cm diameter 10 cm depth, cut from PVC pipe) and bulk density of the soil was maintained at
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1 g cm3. Volume of a cylinder was 785 cm3, therefore, each cylinder was filled with 785 g soil so that bulk density of soil would be 1 g cm3. Tap water was added to soils up to field capacity (sufficient water to initiate drainage). A high mortality of seedlings was expected with increasing salinity, so on 4 July 1999, single seedlings (with root length varying from 0.5 to 1.5 cm) were planted in soils of 4.3, 6.1 and 8.4 dS m1, two seedlings in soils of 10.3 and 12.5 dS m1 and three seedlings in soils of 14.9 and 17.2 dS m1 conductivity filled within the cylinders. The bottom of each cylinder was fixed with a wire-net so that roots could easily pass through. Cylinders were kept in Petri dishes to enable collection of leachates caused by watering which were returned to the soils. Cylinders with seedlings were kept inside the cage for 20 days for establishment of the seedlings. During this period, seedlings contained in plastic cylinders were watered (to raise the soil moisture to field capacity) on alternate days. The mean maximum temperature in the cage during seedling establishment phase was about 31.9 0.2 8C. About 98%, 96% and 94% seedlings survived on 4.3, 6.1 and 8.4 dS m1 conductivity, respectively and exhibited emergence of the second leaf after 1 week following their transplantation. However, on soils of 10.3, 12.5, 14.9 and 17.1 dS m1 Electrical conductivity, 65%, 58%, 42% and 14% seedlings, respectively, survived and their second leaf sprouted after 2 weeks. Further experiments were not conducted on seedlings grown on soil with 17.2 dS m1 conductivity because seedlings were very weak and seeds did not germinate in soil where salinity exceeded 14.9 dS m1. Seedlings were thinned to only one after emergence of the second leaf. Soil was last watered on 23 July 1999. Thirty-six seedlings in each soil salinity treatment were further selected for two-water treatments. Eighteen seedlings were grown in soil at field capacity (22.4% water: dry weight) and eighteen in soil at 10% water content. For maintaining soil at 10% water content, 25 kg of dry soil was mixed with salt mixture for each level of salinity and spread on polyethylene sheets in the laboratory. Tap water was sprinkled on soils at a ratio of 200 ml water/kg soil. After 2 days, soil was thoroughly mixed and spread for air-drying under a fan. Soil was consistently examined for moisture by rubbing between fingers and its moisture was determined gravimetrically. When soil moisture
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was between 10% and 11%, soil was stored in polyethylene containers to avoid evaporation. Wetting and drying of soil was repeated with modified ratio of water to soil if the expected moisture content was not obtained. Soil moisture was determined on 23 July 1999 before soils were filled in the cylinders and about 10% moisture was recorded for the soil of each concentration of salinity. Each cylinder on 24 July 1999 was placed on top of an identical cylinder filled with soil at similar concentration of salt and maintained at either field capacity (22.4% water: dry weight) or at 10% water content. The junction of upper and lower cylinders was sealed with waterproof adhesive tape. The soil surface in the upper cylinder was covered with aluminium foil to prevent evaporation loss and both the cylinders together were wrapped with polyethylene sheeting. Eighteen replicates for each of the two water treatments, factorialized with six grades of soil (4.3, 6.1, 8.4, 10.3, 12.5 and 14.9 dS m1), were prepared. This gave a total of 216 cylinders, which were arranged in 18 randomized blocks. Fifty days after the cessation of watering, about 40–50% of seedlings at 14.9 dS m1 conductivity and experiencing low water treatment began to wilt and the experiment was terminated. Plants were washed to separate root systems from soil. Morphological characteristics of each seedling were recorded. Shoot height and root length (tap root) were measured. Leaf area was marked out on graph paper. Dry weight of leaves, stems and roots in upper and lower cylinders were determined together with residual water content of the soil. Data recorded for morphological characteristics and dry weight of different components of seedlings were analysed by two-way ANOVA to assess the effect of water treatment and salinity on plant growth. Salt concentration at which dry weight of leaves, stems, upper roots and lower roots of seedlings was reduced by 50% (DW50) was determined by fitting a straight line relationship between the response and salt concentration. 2.4. Mineral analyses Mineral analyses were performed on leaf, stem and root tissues. Plant parts of the seedlings grown in soil at same level of salinity and moisture were pooled separately. Plant samples were ground using mortar
and pestle. Three subsamples of plant tissues were analysed. Total nitrogen was determined by kjeldahl method (Piper, 1944) and phosphorus content estimated by the chlorostannous molybdophosphoric blue colour method in sulfuric acid system (Piper, 1944). Concentrations of Ca, Mg, Na, K, Zn, Fe, Mn and Cu were determined by atomic absorption spectroscopy after triacid (HNO3:H2SO4:HClO4 in the ratio of 10:1:4) digestion. Mineral data were analysed by two-way ANOVA. Correlations and linear regression equations between mineral content and salt concentrations were determined.
3. Results 3.1. Effect of salinization on seedling emergence Seedlings began to emerge 3 days after sowing and 98.0% seedling emergence was achieved over a period of 13 days under control (4.3 dS m1 salinity) conditions (Fig. 1). Seedling emergence in saline soils was recorded on the 4th, 4th, 5th, 6th and 6th days after sowing. Emergence lasted for 13, 12, 12, 11 and 10 days in soils with salinities of 6.1, 8.4 10.3, 12.5 and 14.9 dS m1, respectively, with percent seed germination of 86%, 70%, 42%, 28% and 16%, respectively. Seedlings did not emerge from soils with further increase in salinity. There was a significant reduction in germination of seeds (P < 0.01) with increasing salt stress. A negative relationship between proportion of cumulative seed germination and concentration of salt was obtained according to the following expression: y = 103.3 5.6x (R2Adj = 0.98, P < 0.01), where y is arcsine (8) of proportion of cumulative seed germination and x is salt concentration. 3.2. Effect of water treatment and salinization on leaf expansion and stem and root elongation The low water treatment and increasing salt concentration both significantly reduced (P < 0.01) shoot height and root length of seedlings (Fig. 2). However, the effect of salt was more pronounced under low water treatment. There was a negative linear relationship (r = 0.662 and 0.786 P < 0.01) between shoot height and increasing salt concentration under moist and low water treatments, respectively. A negative
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Fig. 1. Cumulative emergence of seedlings of Salvadora persica in response to soil salinity: 4.3 dS m1 (*); 6.1 dS m1 (~); 8.4 dS m1 (&); 10.3 dS m1 (*); 12.5 dS m1 (~); and 14.9 dS m1 (&).
linear relationship (r = 0.636 and 0.691 P < 0.01) was also obtained for root length and salt concentration under moist and low water treatments, respectively. Nevertheless, roots penetrated the 10 cm thick column of dry and saline subsoils (soils contained in lower cylinders) to their full depth or to a considerable depth. Seedlings began to wilt when soil with 14.9 dS m1 salinity in the upper cylinders above the dry subsoil dried to 7.6% (values for residual soil moisture are not shown). As a result, it appears that S. persica extracts water from highly dry saline soil. Leaf emergence was delayed by increasing salt stress. Further, leaf expansion was significantly reduced (P < 0.01) by increased concentration of salt under both moist and low water treatments, but effects were more pronounced with drier soil. A negative relationship (r = 0.585 and 0.643 P < 0.01) was obtained between leaf area and salt concentration under moist and low water treatments, respectively.
Fig. 2. Effect of salinization of soil under field capacity (&) and low water (&) (10% soil moisture) treatments on elongation of: (A) shoot; (B) root; and (C) expansion of leaf of Salvadora persica seedlings. Symbol represents LSD. In this and Fig. 3, line bars on histogram bars represent the S.E.
3.3. Effect of water treatment and salinization on dry weight Dry weight significantly decreased (P < 0.01) for leaf, stem, shoot (leaf + stem), upper root and total root
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Fig. 3. Effect of salinization of soil under field capacity (&) and low water (&) (10% soil moisture) treatments on dry weight (mg) of: (D) leaf; (E) stem; (F) shoot (leaf + stem); (G) root in upper soil layer; (H) root in lower soil layer; and (I) total root weight of Salvadora persica seedlings. Symbol represents LSD.
in response to low water treatment and increasing concentration of salt in soil (Fig. 3). However, for lower root dry weight reduction was recorded at (P < 0.05) in response to low water treatment and increasing soil salinity. A negative relation was obtained between dry weight of different tissues and salt concentration
(r = 0.494, 0.376, 0.538, 0.367, and 0.412, P < 0.001, for leaf, stem, shoot, upper root and total root, respectively) under moist treatment and (r = 0.547, 0.415, 0.641, 0.472 and 0.559, P < 0.001, for leaf, stem, shoot, upper root and total root, respectively) under drier soil. However, dry weight
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of roots in lower cylinders did not exhibit significant decline in response to increasing concentration of salt in soil under both water treatments. Percent relative weight of tissues of salinized plants compared to those of control plants were computed as (salinized tissue dry weight/control dry weight) 100. Dry weight values of tissues shown in Fig. 3 were used for the calculation of percent relative weight of tissues. Values of percent relative weight varied from 98.3 to 67.0 for young (lower) roots, from 96.0 to 65.7 for stems, from 92.5 to 63.4 for leaves and from 89.2 to 58.6 for old (upper) roots under moist treatment with increasing soil salinity from 6.1 to 14.9 dS m1. Almost similar variations in values of percent relative weight for different components of seedlings were obtained under low water treatment. The salt concentrations in moist soil at which dry weights would be reduced to 50% of control plants (DW50) were 19, 20, and 17 dS m1 for leaf, stem, and old (upper) root tissues, respectively. Root/shoot dry weight ratio was 0.25 under control conditions and moist treatment. It did not change in response to increasing salt stress and also in response to low water treatment.
4. Effect of water treatment and salinization on mineral accumulation 4.1. Potassium and sodium content and K/Na ratio Potassium content (as mg g1 dry weight) significantly increased (P < 0.01) in leaves and stems, while it significantly decreased (P < 0.01) in root tissues in response to low water treatment and increasing soil salinity (Fig. 4). There was a significant positive relationship between K content in leaves and increase in salt concentration (r = 0.738, P < 0.01) under moist treatment. A positive relationship was also recorded for K content in leaves (r = 0.774, P < 0.01) and stems (r = 0.544, P < 0.01) with increasing soil salinity under low water treatment. On the contrary, there was a negative relationship between K content in roots and increase in salt concentration (r = 0.753 and 0.842, P < 0.01 respectively) under moist and low water treatments. Sodium content exhibited a gradual increase in leaves, while it rapidly increased in roots in response to salinization of soil. However, increase of Na content in leaves and roots was more pronounced under low water
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treatment than that under moist treatment. The concentration of Na did not change in stems from that of control in response to low water treatment or increased soil salinity. The K/Na ratio gradually increased in leaves and it did not change in stems, while it significantly decreased (P < 0.01) in roots in response to low water treatment and salinization of soil. There was a significant relationship between reduction of K/Na ratio in roots and increase in salt stress (r = 0.603 and 0.740, P < 0.01, respectively) under moist and low water treatments. 4.2. Nitrogen, phosphorus, calcium and magnesium The concentration of N, K and Ca was much greater than that of P, Mg and Na in all tissues under control, moisture-stress and salt-stress conditions (Fig. 4). However, N content significantly decreased (P < 0.01) in leaves, stems and roots in response to low water treatment and increasing salt concentration in soil. A negative relationship was obtained between N content in different tissues and salt concentration in soil (r = 0.705, P < 0.01 0.458 P < 0.05 and 0.639 P < 0.01 for leaves, stems and roots, respectively) under moist treatment and (r = 0.772, P < 0.01, 0.558, P < 0.05, and 0.700, P < 0.01 for leaves, stems and roots, respectively) under low water treatment. Phosphorus content significantly decreased (P < 0.01) in leaves and stems in response to low water treatment and increase in soil salinity, while P gradually decreased in root tissues. There was a negative relationship between leaf P content and salt concentration (r = 0.479 and 0.496, P < 0.05 respectively, under moist and low water treatments). Concentration of Ca significantly increased in leaves (P < 0.05), while it significantly decreased (P < 0.01) in stems. There was a significant positive relationship between increase in leaf Ca content and increasing salt stress (r = 0.553, P < 0.05 and 0.605, P < 0.05, respectively) under moist and low water treatments. Concentration of Ca in stems gradually declined under moist treatment while it significantly decreased (r = 0.546 P < 0.05) under low water treatment. Reduction in root Ca content with salinization of soil was gradual under both moist and low water treatments. Magnesium content exhibited a gradual decrease in leaves, stems and root tissues in response to low water
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Fig. 4. Effect of salinization of soil under field capacity (*) and low water (*) (10% soil moisture) treatments on the accumulation of nitrogen, phosphorus, potassium, calcium, magnesium, sodium and K/Na ratio in leaf, stem and root tissues of Salvadora persica seedlings. Symbol represents LSD. In this and Fig. 5, bars on symbols represent the S.E.; some error bars are smaller than the symbols.
treatment and increase in salt stress. However, the concentration of P and Mg was lower than that of Na in all the tissues in respect to both low water treatment and salinization of soil.
4.3. Micro-elements There was a significant reduction in the concentration of Zn in leaves (P < 0.01), stems (P < 0.05) and
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Fig. 5. Effect of salinization of soil under field capacity (*) and low water (*) (10% soil moisture) treatments on the accumulation of zinc, copper, manganese and iron in leaf, stem and root tissues of Salvadora persica seedlings. Symbol represents LSD.
roots (P < 0.01) in response to low water treatment (Fig. 5). Reduction in Zn content was also recorded in leaves, stems and root tissues (P < 0.01) in response to increase in salt concentration. A negative relationship was obtained between soil salinity and concentration for Zn in leaves (r = 0.544 and 0.570, P < 0.05) and stems (r = 0.496 and 0.507, P < 0.05) under moist and low water treatments, respectively. There was a gradual decline in Cu content in leaves and stems, while it significantly decreased (P < 0.01) in root tissues in response to low water treatment and salinization of soil. Reduction in Cu content in plant tissues exhibited no relationship with increase in soil salinity. Concentration of Mn did not change in leaves, while it significantly declined (P < 0.01) in stems and roots in response to low water treatment and increase in salt stress. There was a negative relationship between Mn-content in roots and increase in salt concentration (r = 0.912 and 0.939, P < 0.01, respectively) under moist and low water treatments.
Iron content significantly declined in leaves (P < 0.05), stems (P < 0.05) and roots (P < 0.01) in response to low water treatment. There was also a significant reduction in Fe content in all the tissues (P < 0.01) in response to increase in soil salinity. A negative relationship was recorded between soil salinity and concentration for Fe in leaves (r = 0.861 and 0.881, P < 0.01), stems (r = 0.909 and 0.912, P < 0.01) and roots (r = 0.914 and 0.939, P < 0.01) under moist and low water treatments, respectively.
5. Discussion Our earlier work (Mer et al., 2000) indicated that seedling emergence for salt-tolerant barley (Hordeum vulgare) was reduced to 50% (SG50) in soil with salinity of 4.3 dS m1, but for S. persica SG50 was obtained at 10.4 dS m1. This would suggest that this plant species is relatively salt tolerant at seed germi-
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nation. Under field conditions near Naliya and also in a large area of the saline desert of Kutch, maximum soil salinity is found during dry period and minimum during rainy season (wet period) in the year. In general, salinity for 0–10 cm layer of soil varies from 4.3 to 6.1 dS m1. As a result, seeds of S. persica can germinate during rainy season and grow without adverse effect of salinity during post, monsoon period. However, salt concentrations exceeding 14.9 dS m1 salinity were detrimental to seed germination that can be attributed to decreasing osmotic potential of the soil solution. It was observed that seeds began to shrink within a few days and later became non-viable in the soil with high concentration of salt. Although the effects of high salt content on metabolic processes are yet to be fully elucidated, it is reported that salinity reduces protein hydration (Kramer, 1983) and induces changes in the activities of many enzymes (Dubey and Rani, 1990; Garg et al., 1993) in germinating seeds. Reduction in growth of shoot components of S. persica under low water treatment can be attributed to increased matric stress. Kramer (1983) reported that plants subjected to water stress show a general reduction in size and dry matter production. However, root penetration was not restricted by dry soil in the lower cylinders. Further, greater decrease in soil moisture within the upper cylinders under low water treatment than under moist treatment suggests that root extension into the dry subsoil depended on the moisture content in the upper cylinders (values for soil moisture are not shown). Rapid root extension enables the plants to exploit moisture in dry habitats (Etherington, 1987; Pandey and Thakarar, 1997) and is a valuable adaptation. Our results suggest that in dry regions where the available rainfall can wet the surface soil, S. persica seedlings can utilize this moisture for the extension and proliferation of roots into the deeper layers of soil to achieve establishment over the rainy season. Moreover, results are in accordance with the findings of Pandey et al., (1994) for rapid elongation of roots of Prosopis chilensis seedlings in dry habitats. Root growth (upper and lower cylinders’ root weight) was related to the growth of shoots and consequently root/shoot dry weight ratios were equal under the two water treatments. Root/shoot dry weight ratio for S. persica (0.25) was equal to that for aridity and salttolerant seedlings of S. oleoides (0.20), which grows in the same region (Ramoliya and Pandey, 2002).
Reduction in the growth of seedlings was also recorded in response to increasing salt stress. In general, salinity can reduce the plant growth or damage the plants through: (i) osmotic effect (causing water deficit), (ii) toxic effects of ions, and (iii) imbalance of the uptake of essential nutrients. These modes of action may operate on the cellular as well as on higher organizational levels and influence all the aspects of plant metabolism (Kramer, 1983; Garg and Gupta, 1997). Our results for reduction of shoot growth and leaf area development of S. persica with increasing salt concentration are in conformity with the finding of Curtis and Lauchli (1986), who reported that growth of Kenaf (Hibiscus cannabinus) under moderate salt stress was affected primarily through a reduction in elongation of stem and leaf area development. Garg and Gupta (1997) reported that salinity causes reduction in leaf area as well as in rate of photosynthesis which together result in reduced crop growth and yield. Also, high concentration of salt tends to slow down or stop root elongation (Kramer, 1983) and causes reduction in root production (Garg and Gupta, 1997). As a result, water stress and salt stress both reduce the plant growth and their effects are additive. Results for dry weight and relative dry weight of tissues in response to increasing salinity, under moist and low water treatments suggest that dry weight reduction was lowest for young (lower) roots and stem. Salt resistance of tissues can be arranged in the following decreasing order: young roots = stems > leaves > old roots. The concurrent and differential reduction in dry weight of leaves, stems, old roots and young root tissues resulted in constant root/shoot dry weight ratios. The rapid rate of reduction in old roots and the constant root/shoot dry weight ratio suggest that young roots production continued and production of sensitive leaf tissue was seriously reduced by increasing salt stress. The constant root/shoot dry weight ratio, rapid reduction of dry weight of old roots and continuous production of young roots in response to increasing salinity suggest that S. persica plants have a mechanism of old root turnover (loss of old roots followed by subsequent production of new ones) to delay onset of salt stress by indirectly eliminating excess ions through the death of ion saturated old roots. However, in the present study dead and live roots were not quantified, although a few dry and frail lateral roots were observed when the lateral roots were
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spread radially to measure extension of tap roots. Our results are testified by the centuries old practice of farmers in Kutch where they use surface soil from around S. persica trees as manure for their crop fields. Tozlu et al., (2000) obtained death of fine roots of Poncirus trifoliata in response to increasing concentration of NaCl and designated this mechanism as ‘‘fine root turnover’’. Ramoliya and Pandey (2002) reported this mechanism of fine root turnover in S. oleoides which grows in the Kutch region. Moreover, since young roots and stem tissues are salt-resistant, it appears that the plants of S. persica may sequester the salts that they absorb in the roots and stems, thus minimizing the exposure of leaf cells and hence the photosynthetic apparatus to salt. ‘‘Integration in the whole plant’’ is an important aspect of salt tolerance in the glycophytes (Garg and Gupta, 1997). The cation K is essential for cell expansion, osmoregulation and cellular and whole-plant homeostasis (Schachtman et al., 1997). High stomatal K requirement is reported for photosynthesis (Chow et al., 1990). The role of K in response to salt stress is also well documented, where Na depresses K uptake (Fox and Guerinot, 1998). The gradual elevation of Na in leaves and a rapid increase in root tissues of S. persica suggest that there is possibility for exclusion of Na through the process of fine root turnover because high concentration of Na could produce toxic effect to root tissues. Results of Na content in stems which did not change in response to increase in salt concentration suggest that stem tissues were barrier for translocation of Na from roots to leaves. Considering that the stem tissues will be reinforced by growth with time and there is persistence of root turnover, it can be predicted that after seedling stage Na tolerance of plants may increase to a little extent above 14.9 dS m1 salinity which is maximum salt concentration in this experiment. Our conclusion is supported by the fact that in the saline desert of kutch survival of plants of S. persica is greater if they have endured the habitat conditions till seedling stage. Tozlu et al. (2000) reported that in P. trifoliata fine roots played the most important role in Na stress tolerance via indirect ion exclusion through turnover and blocking Na transfer to shoot tissues. Potassium exhibited a rapid decrease in roots while it increased in leaves. These results can be attributed to: (i) transfer of K from roots to leaves, (ii) there
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could have been an exchange of K ions with Na ions in root tissues, and (iii) Na could have directly interfered with k uptake. The pattern of accumulation of K and Na in S. persica conforms to group B and/or group C plants in Marschner’s (1995) classification of plants ability to substitute Na for K. In this classification, Marschner divided plants into four groups, A, B, C and D depending upon whether K is mostly exchangeable with Na. Sodium has a positive effect on growth in A and B plants (mostly salt-tolerant plants). Group C plants contain very little K that can be substituted with Na without a negative effect on growth, and group D plants exhibit no K/Na substitution (salt-sensitive plants). It is reported that uptake mechanisms of both K and Na are similar (Watad et al., 1991; Schroeder et al., 1994). Plants utilize two systems for K acquision, low- and high-affinity uptake mechanisms. Lowaffinity K uptake is not inhibited by Na but the highaffinity process is (Watad et al., 1991; Schroeder et al., 1994). Similarly, Na toxicity in plants is correlated with two proposed Na uptake pathways (Maathuis and Sanders, 1994; Niu et al., 1995). The K and Na profiles of S. persica under salinization suggest that similar mechanism might operate in this species. In general, salinity reduces N accumulation in plants (Feigin, 1985; Garg et al., 1993). An increase in chloride uptake and accumulation is mostly accompanied by a decrease in shoot nitrate concentration (Torres and Bingham, 1973; Garg and Gupta, 1997). The interaction between salinity and P is very complex and there is no clear cut mechanistic explanation for decreased, increased or unchanged P uptake in response to salinization in different species (Grattan and Grieve, 1992). However, it is known that P concentration is related to the rate of photosynthesis, but it decreases the conversion of fixed carbon into starch (Overlach et al., 1993) and therefore decrease of P in leaves will reduce shoot growth. A decreased P concentration in root tissues, on the other hand, strongly stimulates the formation of root hairs and lateral roots in leguminous trees, rape, spinach, tomato and white lupin (Racette et al., 1990). Decreased P in roots may have influenced the increase in root production. Calcium is important during salt stress, e.g. in preserving membrane integrity (Rengel, 1992), signalling in osmoregulation (Mansfield et al., 1990) and influencing K/Na selectivity (Cramer et al., 1987). In the present study, Ca was transferred from roots to
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leaves at high salinities (>8.4 dS m1). The increased Ca content may reduce the toxicity of Na in leaves (Cramer et al., 1987). As a result, Ca fertilizers may mitigate Na toxicity to the plants. Besides the role of Mg in chlorophyll structure and as an enzyme cofactor, another important role of Mg in plants is in the export of photosynthates, which is impaired and leads to enhanced degradation of chlorophyll in Mg deficient source leaves, resulting in increased oxygenase activity of RuBP carboxylase (Marschner and Cakmak, 1989). It is difficult to suggest mechanistic explanations of salinity influence on micro-element concentration due to the relatively smaller differences between control and salinized tissues and the non-linear relationships
between some of the micro-element contents in leaves, stems and root tissues and salt concentrations. It appears that high salinity (>8.4 dS m1) decreased only Fe accumulation at the whole plant level (leaves, stems and root tissues). Other micro-elements remained almost unchanged, but some nutrients were transferred from one tissue to another in response to low water treatment and increasing salt concentration.
Acknowledgement The financial assistance provided by the Ministry of Environment and Forests, New Delhi, India, is gratefully acknowledged.
Appendix A Salt quantities used to prepare soils of different electrical conductivities Electrical conductivity (dS m1)
NaCl [g (100 kg)1]
KCl [g (100 kg)1]
CaCl2 [g (100 kg)1]
MgCl2 [g (100 kg)1]
Na2SO4 [g (100 kg)1]
K2SO4 [g (100 kg)1]
CaSO4 [g (100 kg)1]
MgSO4 [g (100 kg)1]
Total salt [g (100 kg)1]
4.3 6.1 8.4 10.3 12.5 14.9 17.2
0 60 120 180 240 300 360
0 60 120 180 240 300 360
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 240 480 720 960 1200 1440
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Donahue, R.L., Miller, R.W., Shickluna, J.C., 1983. Soils, An Introduction to Soils and Plant Growth, Prentice-Hall, Englewood Cliffs, NJ. Dubey, R.S., Rani, M., 1990. Influence of NaCl salinity on the behaviour of protease, aminopeptidase and carboxyl-peptidase in rice seedlings in relation to salt tolerance. Aust. J. Plant Physiol. 17, 215–224. Etherington, J.R., 1987. Penetration of dry soil by roots of Dactylis glomerata L. clones derived from well drained and poorly drained soils. Funct. Ecol. 1, 19–23. Feigin, A., 1985. Fertilization management of crops irrigated with saline water. Plant Soil. 89, 285–299. Fox, T.C., Guerinot, M.L., 1998. Molecular biology of cation transport in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 669–696. Garg, B.K., Gupta, I.C., 1997. Saline Wastelands Environment and Plant Growth, Scientific Publishers, Jodhpur, India. Garg, B.K., Vyas, S.P., Kathju, S., Lahiri, A.N., Mali, P.C., Sharma, P.C., 1993. Salinity–fertility interaction on growth, mineral composition and nitrogen metabolism of Indian mustard. J. Plant Nutr. 16, 1637–1650.
P.J. Ramoliya et al. / Forest Ecology and Management 202 (2004) 181–193 Grattan, S.R., Grieve, C.M., 1992. Mineral element acquisition and growth response of plants grown in saline environments. Agric. Ecosyst. Environ. 38, 275–300. Kramer, P.J., 1983. Water Relations of Plants, Academic Press, New York. Maas, E.V., Grieve, C.M., 1987. Sodium induced calcium deficiency in salt-stressed corn. Plant Cell Environ. 10, 559–564. Maas, E.V., Hoffman, G.J., 1977. Crop salt tolerance—current assessment. J. Irrig. Drain Div. ASCE 103, 115–134. Maathuis, F.J.M., Sanders, D., 1994. Mechanism of high-affinity potassium uptake in roots of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 91, 9272–9276. Mansfield, T.A., Hetherington, A.M., Atkinson, C.J., 1990. Some aspects of stomatal physiology. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 55–75. Marschner, H., Cakmak, I., 1989. High light intensity enchances chlorosis and necrosis in leaves of zinc, potassium and magnesium deficient bean Phaseolus vulgaris plants. J. Plant Physiol. 134, 308–315. Marschner, H., 1995. Mineral Nutrition of Higher Plants, Academic Press, London. Mer, R.K., Prajith, P.K., Pandya, D.H., Pandey, A.N., 2000. Effect of salts on germination of seeds and growth of young plants of Hordeum vulgare, Triticum aestivum, Cicer arietinum and Brassica juncea. J. Agron. Crop Sci. 185, 209–217. Munns, R., 1993. Physiological processes limiting plant growth in saline soils, some dogmas and hypotheses. Plant Cell Environ. 16, 15–24. Niu, X., Bressan, R.A., Hasegawa, P.M., Pardo, J.M., 1995. Ion homeostasis in NaCl stress environments. Plant Physiol. 109, 735–742. Overlach, S., Diekmann, W., Raschke, K., 1993. Phosphate translocator of isolated guard-cell chloroplasts from Pisum sativum L. transport glucose-6-phosphate. Plant Physiol. 101, 1201–1207. Pandey, A.N., Rokad, M.V., Thakarar, N.K., 1994. Root penetration and survival of Prosopis chilensis and Dalbergia sissoo in dry regions. Proc. Indian Natl. Sci. Acad. 60, 137–142.
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Pandey, A.N., Thakarar, N.K., 1997. Effect of chloride salinity on survival and growth of Prosopis chilensis seedlings. Trop. Ecol. 38, 145–148. Piper, C.S., 1944. Soil and Plant Analysis, Interscience, New York. Racette, S., Louis, I., Torrey, J.G., 1990. Cluster root formation by Gymnostoma papuanum Casuarinaceae in relation to aeration and mineral nutrient availability in water culture. Can. J. Bot. 68, 2564–2570. Ramoliya, P.J., Pandey, A.N., 2002. Effect of increasing salt concentration on emergence, growth and survival of seedlings of Salvadora oleoides (Salvadoraceae). J. Arid Environ. 51, 121–132. Ramoliya, P.J., Pandey, A.N., 2003. Effect of salinization of soil on emergence, growth and survival of seedlings of Cordia rothii. For. Ecol. Manage. 176, 185–194. Rengel, Z., 1992. The role of calcium in salt toxicity. Plant Cell Environ. 15, 625–632. Schachtman, D.P., Kumar, R., Schroeder, J.I., Marsh, E.L., 1997. Molecular and functional characterization of a novel low-affinity cation transporter LCTI in higher plants. Proc. Natl. Acad. Sci. U.S.A. 94, 11079–11084. Schroeder, J.I., Ward, J.M., Gassmann, W., 1994. Perspectives on the physiology and structure of inward-rectifying k channels in higher plants, biophysical implications for k uptake. Annu. Rev. Biophys. Biomol. Struct. 23, 441–471. Torres, B.C., Bingham, F.T., 1973. Salt tolerance of Mexican wheat. I. Effect of NO3 and NaCl on mineral nutrition, growth and grain production of four wheats. Soil Sci. Soc. Am. Proc. 37, 711–715. Tozlu, I., Moore, G.A., Guy, C.L., 2000. Effect of increasing NaCl concentration on stem elongation, dry mass production, and Macro- and micro-nutrient accumulation in Poncirus trifoliata. Aust. J. Plant Physiol. 27, 35–42. Watad, A.A., Reuveni, M., Bressan, R.A., Hasegawa, P.M., 1991. Enhanced net K uptake capacity of NaCl-adapted cells. Plant Physiol. 95, 1265–1269.
Effect of salinization of soil on growth and macro- and micro-nutrient accumulation in seedlings of Salvadora persica (Salvadoraceae) P.J. Ramoliya, H.M. Patel, A.N. Pandey* Department of Biosciences, Saurashtra University, Rajkot 360005, India Received 21 May 2003; received in revised form 26 April 2004; accepted 8 July 2004
Abstract Effects of salinization of soil on emergence, seedling growth and mineral accumulation of Salvadora persica Linn. (Salvadoraceae) were studied. A mixture of chlorides and sulphates of Na, K, Ca and Mg was added to the soil and salinity was maintained at 4.3, 6.1, 8.4, 10.3, 12.5, 14.9 and 17.2 dS m1. A negative relationship between seedling emergence and salt concentration was obtained. Seedlings did not emerge when soil salinity exceeded 14.9 dS m1. Results suggested that this tree species is salt tolerant at seed germination and seedling stages. Elongation of stem and root was retarded by increasing salt stress. Young roots and stem were most tolerant to salt stress and were followed by leaves and old roots. Leaf tissue exhibited maximum reduction in dry mass production in response to increasing salt stress. However, production of young roots and death of old roots were found to be continuous and plants apparently use this process as an avoidance mechanism to remove excess ions and delay onset of ion accumulation in this tissue. This phenomenon, designated ‘‘fine root turnover’’ is of an importance to the mechanisms of salt tolerance. Plants accumulated Na in roots and were able to regulate transfer of Na ions to leaves. Stem tissues were barrier for translocation of Na from root to leaf. Moreover, K significantly increased in leaf, but decreased in root tissues with increased salinization. Nitrogen content significantly decreased in all tissues (leaf, stem and root) in response to low water treatment and salinization of soil. Phosphorus content significantly decreased, while Ca increased in leaf as soil salinity increased. Changes in elements accumulation pattern and the possible mechanisms for avoidance of Na toxicity in tissues and organism level are discussed. # 2004 Elsevier B.V. All rights reserved. Keywords: Salinization of soil; Salvadora persica; Seedling emergence; Seedling growth; Salt tolerance; Adaptation; Accumulation; Macroand micro-nutrients
1. Introduction * Corresponding author. Tel.: +91 281 2572833/2586419; fax: +91 281 2577633. E-mail address: [email protected], [email protected] (A.N. Pandey).
Salt stress is a world-wide problem and soil salinity is common in arid and semi-arid regions than in humid regions. Salinity is a scourge for agriculture, forestry,
0378-1127/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2004.07.020
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pasture development and other similar practices. An understanding of responses of plants to salinity is of great practical significance. High concentrations of salts have detrimental effects on plant growth (Garg and Gupta, 1997; Mer et al., 2000) and excessive concentrations kill growing plants (Donahue et al., 1983). Many investigators have reported retardation of germination and growth of seedlings at high salinity (Bernstein, 1962; Garg and Gupta, 1997; Ramoliya and Pandey, 2003). However, plant species differ in their sensitivity or tolerance to salts (Brady and Weil, 1996). There are many different types of salts and almost an equally diverse set of mechanisms of avoidance or tolerance. In addition, organs, tissues and cells at different developmental stages of plants exhibit varying degrees of tolerance to environmental conditions (Munns, 1993; Ashraf, 1994). It is reported that soil salinity suppresses shoot growth more than the root growth (Ramoliya and Pandey, 2003; Maas and Hoffman, 1977). However, fewer studies on the effect of soil salinity on root growth have been conducted (Garg and Gupta, 1997). The high salt content lowers osmotic potential of soil water and consequently the availability of soil water to plants. In saline soil, salt induced water deficit is one of the major constraints for plant growth. As soils dry down soil salinity is exacerbated. Frequent droughts are a regular phenomenon in saline deserts. Eventually, responses of roots and shoots of plants to soil salinity should be understood under both wet and dry soil conditions. In addition, many nutrient interactions in salt-stressed plants can occur which may have important consequences for growth. Internal concentrations of major nutrients and their uptake have been frequently studied (e.g. Maas and Grieve, 1987; Cramer et al., 1989), but the relationship between micro-nutrient concentrations and soil salinity is rather complex and remains poorly understood (Tozlu et al., 2000). The knowledge acquired regarding the growth and survival of plants under natural habitat conditions could be useful for: (i) screening of plant species for the afforestation of saline deserts, and also (ii) for understanding the mechanisms which plants use in the avoidance and/ or tolerance of salt stress. Salvadora persica Linn. (Salvadoraceae) is one of the dominant tree species in the Kutch (north–west saline desert) of Gujarat State in India. It also grows successfully in coastal areas as well as in non-saline
and marginal semi-arid central area of Saurashtra region, to the south of Kutch. S. persica is extremely important to local people because of its oil yielding, pharmaceutical, fuel and fodder value and small but edible fruits. However, the potential of this tree species to grow and survive in the saline desert of kutch is not known. The present investigation was carried out: (i) to understand the adaptive features of S. persica, which allow it to grow and survive in saline and arid regions, and (ii) to assess the pattern of macro- and micro-nutrient accumulation within the tissues of this tree species in response to salt stress.
2. Materials and methods 2.1. Study area The present study was carried out at Naliya (238280 N, 688800 E) in Kutch. The soil is a non-calcareous sandy loam containing 70.1% sand, 13.7% silt and 16.2% clay. The available soil-water between the wilting coefficient and field capacity ranged from 7.6% to 22.4%, respectively. The total organic carbon content was 0.6% and pH was 8.1. The electrical conductivity of the soil ranged from 4.3 to 6.1 dS m1. Soil was deficient in nitrogen (0.07%) and phosphorus (0.01%). The Kutch and Saurashtra regions are tropical monsoonic and can be ecoclimatically classified as arid and semi-arid, respectively. The entire area is markedly affected by south-western monsoon which causes the onset of wet season in mid-June, and its retreat by the end of September coincides with a lowering of temperature and gradual onset of winter. Total annual rainfall is about 395 mm at Naliya and about 554 mm in central Saurashtra which occurs totally during the rainy season. Typically, there are three main seasons: summer (April–mid June), monsoon (mid June–September) and winter (November–February). The months of October and March are transition periods between rainy (monsoon) and winter and between winter and summer seasons, respectively. Winters are generally mild and the summers hot. 2.2. Seedling emergence Surface soil (0–10 cm depth) was collected, airdried and passed through a 2 mm mesh screen. Seven
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lots of soil, of 100 kg each, were separately spread, about 50 mm thick, over polyethylene sheets. A mixture of NaCl, KCl, CaCl2, MgCl2, Na2SO4, K2SO4, CaSO4 and MgSO4 in a proportion of 3:3:1:1:1:1:1:1, was then thoroughly mixed with soil to yield electrical conductivities of 6.1, 8.4, 10.3, 12.5, 14.9 and 17.2 dS m1 in the six lots of soil, respectively. The quantities of salt added to the soil are given in the table in Appendix A. There was no addition of salt to the soil of seventh lot which served as control. Electrical conductivity of the control soil was 4.3 dS m1. Soil suspension was prepared in distilled water (1:2 (w/ w)), and electrical conductivity determined by a Systronics digital conductivity meter. Naturally occurring chlorides and sulphates were added to soil to check effects of ion interaction on root uptake. A high proportion of chlorides in salt mixture was maintained as the study area is in proximity to the Arabian Sea and seawater enters and spreads at certain spatially separated locations at its most northern part. Five polyethylene bags for each level of soil salinity were each filled with 2 kg of soil. Tap water was added to the soils to field capacity and soils were then allowed to dry for 6 days. Soils were then raked gently and seeds were sown on 4 July 1999. Bags were kept inside a wire-net cage of 10 m 10 m area which had its top covered by a thick and transparent plastic sheet because it was the rainy season. Ten seeds were sown in each bag at a depth of about 8–12 mm. Immediately after sowing, soils were watered and thereafter watering was carried out on alternate days. Emergence of seedlings was recorded daily over a period of forty days. A linear model was fitted to cumulative percentage seed germination using the expression: Sin1 Hp = b0 + b1x, where Sin1 Hp is the proportion of cumulative seed germination, x is soil salinity and b0 and b1 are constants. Salt concentration at which seed germination was reduced to 50% (SG50) was determined using this model. 2.3. Seedling growth For the growth studies, seedlings of S. persica were grown in Petri dishes from medium sized seeds collected at Naliya in Kutch. Soil of each concentration of salt was filled in to forty open-bottomed cylinders (10 cm diameter 10 cm depth, cut from PVC pipe) and bulk density of the soil was maintained at
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1 g cm3. Volume of a cylinder was 785 cm3, therefore, each cylinder was filled with 785 g soil so that bulk density of soil would be 1 g cm3. Tap water was added to soils up to field capacity (sufficient water to initiate drainage). A high mortality of seedlings was expected with increasing salinity, so on 4 July 1999, single seedlings (with root length varying from 0.5 to 1.5 cm) were planted in soils of 4.3, 6.1 and 8.4 dS m1, two seedlings in soils of 10.3 and 12.5 dS m1 and three seedlings in soils of 14.9 and 17.2 dS m1 conductivity filled within the cylinders. The bottom of each cylinder was fixed with a wire-net so that roots could easily pass through. Cylinders were kept in Petri dishes to enable collection of leachates caused by watering which were returned to the soils. Cylinders with seedlings were kept inside the cage for 20 days for establishment of the seedlings. During this period, seedlings contained in plastic cylinders were watered (to raise the soil moisture to field capacity) on alternate days. The mean maximum temperature in the cage during seedling establishment phase was about 31.9 0.2 8C. About 98%, 96% and 94% seedlings survived on 4.3, 6.1 and 8.4 dS m1 conductivity, respectively and exhibited emergence of the second leaf after 1 week following their transplantation. However, on soils of 10.3, 12.5, 14.9 and 17.1 dS m1 Electrical conductivity, 65%, 58%, 42% and 14% seedlings, respectively, survived and their second leaf sprouted after 2 weeks. Further experiments were not conducted on seedlings grown on soil with 17.2 dS m1 conductivity because seedlings were very weak and seeds did not germinate in soil where salinity exceeded 14.9 dS m1. Seedlings were thinned to only one after emergence of the second leaf. Soil was last watered on 23 July 1999. Thirty-six seedlings in each soil salinity treatment were further selected for two-water treatments. Eighteen seedlings were grown in soil at field capacity (22.4% water: dry weight) and eighteen in soil at 10% water content. For maintaining soil at 10% water content, 25 kg of dry soil was mixed with salt mixture for each level of salinity and spread on polyethylene sheets in the laboratory. Tap water was sprinkled on soils at a ratio of 200 ml water/kg soil. After 2 days, soil was thoroughly mixed and spread for air-drying under a fan. Soil was consistently examined for moisture by rubbing between fingers and its moisture was determined gravimetrically. When soil moisture
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was between 10% and 11%, soil was stored in polyethylene containers to avoid evaporation. Wetting and drying of soil was repeated with modified ratio of water to soil if the expected moisture content was not obtained. Soil moisture was determined on 23 July 1999 before soils were filled in the cylinders and about 10% moisture was recorded for the soil of each concentration of salinity. Each cylinder on 24 July 1999 was placed on top of an identical cylinder filled with soil at similar concentration of salt and maintained at either field capacity (22.4% water: dry weight) or at 10% water content. The junction of upper and lower cylinders was sealed with waterproof adhesive tape. The soil surface in the upper cylinder was covered with aluminium foil to prevent evaporation loss and both the cylinders together were wrapped with polyethylene sheeting. Eighteen replicates for each of the two water treatments, factorialized with six grades of soil (4.3, 6.1, 8.4, 10.3, 12.5 and 14.9 dS m1), were prepared. This gave a total of 216 cylinders, which were arranged in 18 randomized blocks. Fifty days after the cessation of watering, about 40–50% of seedlings at 14.9 dS m1 conductivity and experiencing low water treatment began to wilt and the experiment was terminated. Plants were washed to separate root systems from soil. Morphological characteristics of each seedling were recorded. Shoot height and root length (tap root) were measured. Leaf area was marked out on graph paper. Dry weight of leaves, stems and roots in upper and lower cylinders were determined together with residual water content of the soil. Data recorded for morphological characteristics and dry weight of different components of seedlings were analysed by two-way ANOVA to assess the effect of water treatment and salinity on plant growth. Salt concentration at which dry weight of leaves, stems, upper roots and lower roots of seedlings was reduced by 50% (DW50) was determined by fitting a straight line relationship between the response and salt concentration. 2.4. Mineral analyses Mineral analyses were performed on leaf, stem and root tissues. Plant parts of the seedlings grown in soil at same level of salinity and moisture were pooled separately. Plant samples were ground using mortar
and pestle. Three subsamples of plant tissues were analysed. Total nitrogen was determined by kjeldahl method (Piper, 1944) and phosphorus content estimated by the chlorostannous molybdophosphoric blue colour method in sulfuric acid system (Piper, 1944). Concentrations of Ca, Mg, Na, K, Zn, Fe, Mn and Cu were determined by atomic absorption spectroscopy after triacid (HNO3:H2SO4:HClO4 in the ratio of 10:1:4) digestion. Mineral data were analysed by two-way ANOVA. Correlations and linear regression equations between mineral content and salt concentrations were determined.
3. Results 3.1. Effect of salinization on seedling emergence Seedlings began to emerge 3 days after sowing and 98.0% seedling emergence was achieved over a period of 13 days under control (4.3 dS m1 salinity) conditions (Fig. 1). Seedling emergence in saline soils was recorded on the 4th, 4th, 5th, 6th and 6th days after sowing. Emergence lasted for 13, 12, 12, 11 and 10 days in soils with salinities of 6.1, 8.4 10.3, 12.5 and 14.9 dS m1, respectively, with percent seed germination of 86%, 70%, 42%, 28% and 16%, respectively. Seedlings did not emerge from soils with further increase in salinity. There was a significant reduction in germination of seeds (P < 0.01) with increasing salt stress. A negative relationship between proportion of cumulative seed germination and concentration of salt was obtained according to the following expression: y = 103.3 5.6x (R2Adj = 0.98, P < 0.01), where y is arcsine (8) of proportion of cumulative seed germination and x is salt concentration. 3.2. Effect of water treatment and salinization on leaf expansion and stem and root elongation The low water treatment and increasing salt concentration both significantly reduced (P < 0.01) shoot height and root length of seedlings (Fig. 2). However, the effect of salt was more pronounced under low water treatment. There was a negative linear relationship (r = 0.662 and 0.786 P < 0.01) between shoot height and increasing salt concentration under moist and low water treatments, respectively. A negative
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Fig. 1. Cumulative emergence of seedlings of Salvadora persica in response to soil salinity: 4.3 dS m1 (*); 6.1 dS m1 (~); 8.4 dS m1 (&); 10.3 dS m1 (*); 12.5 dS m1 (~); and 14.9 dS m1 (&).
linear relationship (r = 0.636 and 0.691 P < 0.01) was also obtained for root length and salt concentration under moist and low water treatments, respectively. Nevertheless, roots penetrated the 10 cm thick column of dry and saline subsoils (soils contained in lower cylinders) to their full depth or to a considerable depth. Seedlings began to wilt when soil with 14.9 dS m1 salinity in the upper cylinders above the dry subsoil dried to 7.6% (values for residual soil moisture are not shown). As a result, it appears that S. persica extracts water from highly dry saline soil. Leaf emergence was delayed by increasing salt stress. Further, leaf expansion was significantly reduced (P < 0.01) by increased concentration of salt under both moist and low water treatments, but effects were more pronounced with drier soil. A negative relationship (r = 0.585 and 0.643 P < 0.01) was obtained between leaf area and salt concentration under moist and low water treatments, respectively.
Fig. 2. Effect of salinization of soil under field capacity (&) and low water (&) (10% soil moisture) treatments on elongation of: (A) shoot; (B) root; and (C) expansion of leaf of Salvadora persica seedlings. Symbol represents LSD. In this and Fig. 3, line bars on histogram bars represent the S.E.
3.3. Effect of water treatment and salinization on dry weight Dry weight significantly decreased (P < 0.01) for leaf, stem, shoot (leaf + stem), upper root and total root
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Fig. 3. Effect of salinization of soil under field capacity (&) and low water (&) (10% soil moisture) treatments on dry weight (mg) of: (D) leaf; (E) stem; (F) shoot (leaf + stem); (G) root in upper soil layer; (H) root in lower soil layer; and (I) total root weight of Salvadora persica seedlings. Symbol represents LSD.
in response to low water treatment and increasing concentration of salt in soil (Fig. 3). However, for lower root dry weight reduction was recorded at (P < 0.05) in response to low water treatment and increasing soil salinity. A negative relation was obtained between dry weight of different tissues and salt concentration
(r = 0.494, 0.376, 0.538, 0.367, and 0.412, P < 0.001, for leaf, stem, shoot, upper root and total root, respectively) under moist treatment and (r = 0.547, 0.415, 0.641, 0.472 and 0.559, P < 0.001, for leaf, stem, shoot, upper root and total root, respectively) under drier soil. However, dry weight
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of roots in lower cylinders did not exhibit significant decline in response to increasing concentration of salt in soil under both water treatments. Percent relative weight of tissues of salinized plants compared to those of control plants were computed as (salinized tissue dry weight/control dry weight) 100. Dry weight values of tissues shown in Fig. 3 were used for the calculation of percent relative weight of tissues. Values of percent relative weight varied from 98.3 to 67.0 for young (lower) roots, from 96.0 to 65.7 for stems, from 92.5 to 63.4 for leaves and from 89.2 to 58.6 for old (upper) roots under moist treatment with increasing soil salinity from 6.1 to 14.9 dS m1. Almost similar variations in values of percent relative weight for different components of seedlings were obtained under low water treatment. The salt concentrations in moist soil at which dry weights would be reduced to 50% of control plants (DW50) were 19, 20, and 17 dS m1 for leaf, stem, and old (upper) root tissues, respectively. Root/shoot dry weight ratio was 0.25 under control conditions and moist treatment. It did not change in response to increasing salt stress and also in response to low water treatment.
4. Effect of water treatment and salinization on mineral accumulation 4.1. Potassium and sodium content and K/Na ratio Potassium content (as mg g1 dry weight) significantly increased (P < 0.01) in leaves and stems, while it significantly decreased (P < 0.01) in root tissues in response to low water treatment and increasing soil salinity (Fig. 4). There was a significant positive relationship between K content in leaves and increase in salt concentration (r = 0.738, P < 0.01) under moist treatment. A positive relationship was also recorded for K content in leaves (r = 0.774, P < 0.01) and stems (r = 0.544, P < 0.01) with increasing soil salinity under low water treatment. On the contrary, there was a negative relationship between K content in roots and increase in salt concentration (r = 0.753 and 0.842, P < 0.01 respectively) under moist and low water treatments. Sodium content exhibited a gradual increase in leaves, while it rapidly increased in roots in response to salinization of soil. However, increase of Na content in leaves and roots was more pronounced under low water
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treatment than that under moist treatment. The concentration of Na did not change in stems from that of control in response to low water treatment or increased soil salinity. The K/Na ratio gradually increased in leaves and it did not change in stems, while it significantly decreased (P < 0.01) in roots in response to low water treatment and salinization of soil. There was a significant relationship between reduction of K/Na ratio in roots and increase in salt stress (r = 0.603 and 0.740, P < 0.01, respectively) under moist and low water treatments. 4.2. Nitrogen, phosphorus, calcium and magnesium The concentration of N, K and Ca was much greater than that of P, Mg and Na in all tissues under control, moisture-stress and salt-stress conditions (Fig. 4). However, N content significantly decreased (P < 0.01) in leaves, stems and roots in response to low water treatment and increasing salt concentration in soil. A negative relationship was obtained between N content in different tissues and salt concentration in soil (r = 0.705, P < 0.01 0.458 P < 0.05 and 0.639 P < 0.01 for leaves, stems and roots, respectively) under moist treatment and (r = 0.772, P < 0.01, 0.558, P < 0.05, and 0.700, P < 0.01 for leaves, stems and roots, respectively) under low water treatment. Phosphorus content significantly decreased (P < 0.01) in leaves and stems in response to low water treatment and increase in soil salinity, while P gradually decreased in root tissues. There was a negative relationship between leaf P content and salt concentration (r = 0.479 and 0.496, P < 0.05 respectively, under moist and low water treatments). Concentration of Ca significantly increased in leaves (P < 0.05), while it significantly decreased (P < 0.01) in stems. There was a significant positive relationship between increase in leaf Ca content and increasing salt stress (r = 0.553, P < 0.05 and 0.605, P < 0.05, respectively) under moist and low water treatments. Concentration of Ca in stems gradually declined under moist treatment while it significantly decreased (r = 0.546 P < 0.05) under low water treatment. Reduction in root Ca content with salinization of soil was gradual under both moist and low water treatments. Magnesium content exhibited a gradual decrease in leaves, stems and root tissues in response to low water
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Fig. 4. Effect of salinization of soil under field capacity (*) and low water (*) (10% soil moisture) treatments on the accumulation of nitrogen, phosphorus, potassium, calcium, magnesium, sodium and K/Na ratio in leaf, stem and root tissues of Salvadora persica seedlings. Symbol represents LSD. In this and Fig. 5, bars on symbols represent the S.E.; some error bars are smaller than the symbols.
treatment and increase in salt stress. However, the concentration of P and Mg was lower than that of Na in all the tissues in respect to both low water treatment and salinization of soil.
4.3. Micro-elements There was a significant reduction in the concentration of Zn in leaves (P < 0.01), stems (P < 0.05) and
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Fig. 5. Effect of salinization of soil under field capacity (*) and low water (*) (10% soil moisture) treatments on the accumulation of zinc, copper, manganese and iron in leaf, stem and root tissues of Salvadora persica seedlings. Symbol represents LSD.
roots (P < 0.01) in response to low water treatment (Fig. 5). Reduction in Zn content was also recorded in leaves, stems and root tissues (P < 0.01) in response to increase in salt concentration. A negative relationship was obtained between soil salinity and concentration for Zn in leaves (r = 0.544 and 0.570, P < 0.05) and stems (r = 0.496 and 0.507, P < 0.05) under moist and low water treatments, respectively. There was a gradual decline in Cu content in leaves and stems, while it significantly decreased (P < 0.01) in root tissues in response to low water treatment and salinization of soil. Reduction in Cu content in plant tissues exhibited no relationship with increase in soil salinity. Concentration of Mn did not change in leaves, while it significantly declined (P < 0.01) in stems and roots in response to low water treatment and increase in salt stress. There was a negative relationship between Mn-content in roots and increase in salt concentration (r = 0.912 and 0.939, P < 0.01, respectively) under moist and low water treatments.
Iron content significantly declined in leaves (P < 0.05), stems (P < 0.05) and roots (P < 0.01) in response to low water treatment. There was also a significant reduction in Fe content in all the tissues (P < 0.01) in response to increase in soil salinity. A negative relationship was recorded between soil salinity and concentration for Fe in leaves (r = 0.861 and 0.881, P < 0.01), stems (r = 0.909 and 0.912, P < 0.01) and roots (r = 0.914 and 0.939, P < 0.01) under moist and low water treatments, respectively.
5. Discussion Our earlier work (Mer et al., 2000) indicated that seedling emergence for salt-tolerant barley (Hordeum vulgare) was reduced to 50% (SG50) in soil with salinity of 4.3 dS m1, but for S. persica SG50 was obtained at 10.4 dS m1. This would suggest that this plant species is relatively salt tolerant at seed germi-
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nation. Under field conditions near Naliya and also in a large area of the saline desert of Kutch, maximum soil salinity is found during dry period and minimum during rainy season (wet period) in the year. In general, salinity for 0–10 cm layer of soil varies from 4.3 to 6.1 dS m1. As a result, seeds of S. persica can germinate during rainy season and grow without adverse effect of salinity during post, monsoon period. However, salt concentrations exceeding 14.9 dS m1 salinity were detrimental to seed germination that can be attributed to decreasing osmotic potential of the soil solution. It was observed that seeds began to shrink within a few days and later became non-viable in the soil with high concentration of salt. Although the effects of high salt content on metabolic processes are yet to be fully elucidated, it is reported that salinity reduces protein hydration (Kramer, 1983) and induces changes in the activities of many enzymes (Dubey and Rani, 1990; Garg et al., 1993) in germinating seeds. Reduction in growth of shoot components of S. persica under low water treatment can be attributed to increased matric stress. Kramer (1983) reported that plants subjected to water stress show a general reduction in size and dry matter production. However, root penetration was not restricted by dry soil in the lower cylinders. Further, greater decrease in soil moisture within the upper cylinders under low water treatment than under moist treatment suggests that root extension into the dry subsoil depended on the moisture content in the upper cylinders (values for soil moisture are not shown). Rapid root extension enables the plants to exploit moisture in dry habitats (Etherington, 1987; Pandey and Thakarar, 1997) and is a valuable adaptation. Our results suggest that in dry regions where the available rainfall can wet the surface soil, S. persica seedlings can utilize this moisture for the extension and proliferation of roots into the deeper layers of soil to achieve establishment over the rainy season. Moreover, results are in accordance with the findings of Pandey et al., (1994) for rapid elongation of roots of Prosopis chilensis seedlings in dry habitats. Root growth (upper and lower cylinders’ root weight) was related to the growth of shoots and consequently root/shoot dry weight ratios were equal under the two water treatments. Root/shoot dry weight ratio for S. persica (0.25) was equal to that for aridity and salttolerant seedlings of S. oleoides (0.20), which grows in the same region (Ramoliya and Pandey, 2002).
Reduction in the growth of seedlings was also recorded in response to increasing salt stress. In general, salinity can reduce the plant growth or damage the plants through: (i) osmotic effect (causing water deficit), (ii) toxic effects of ions, and (iii) imbalance of the uptake of essential nutrients. These modes of action may operate on the cellular as well as on higher organizational levels and influence all the aspects of plant metabolism (Kramer, 1983; Garg and Gupta, 1997). Our results for reduction of shoot growth and leaf area development of S. persica with increasing salt concentration are in conformity with the finding of Curtis and Lauchli (1986), who reported that growth of Kenaf (Hibiscus cannabinus) under moderate salt stress was affected primarily through a reduction in elongation of stem and leaf area development. Garg and Gupta (1997) reported that salinity causes reduction in leaf area as well as in rate of photosynthesis which together result in reduced crop growth and yield. Also, high concentration of salt tends to slow down or stop root elongation (Kramer, 1983) and causes reduction in root production (Garg and Gupta, 1997). As a result, water stress and salt stress both reduce the plant growth and their effects are additive. Results for dry weight and relative dry weight of tissues in response to increasing salinity, under moist and low water treatments suggest that dry weight reduction was lowest for young (lower) roots and stem. Salt resistance of tissues can be arranged in the following decreasing order: young roots = stems > leaves > old roots. The concurrent and differential reduction in dry weight of leaves, stems, old roots and young root tissues resulted in constant root/shoot dry weight ratios. The rapid rate of reduction in old roots and the constant root/shoot dry weight ratio suggest that young roots production continued and production of sensitive leaf tissue was seriously reduced by increasing salt stress. The constant root/shoot dry weight ratio, rapid reduction of dry weight of old roots and continuous production of young roots in response to increasing salinity suggest that S. persica plants have a mechanism of old root turnover (loss of old roots followed by subsequent production of new ones) to delay onset of salt stress by indirectly eliminating excess ions through the death of ion saturated old roots. However, in the present study dead and live roots were not quantified, although a few dry and frail lateral roots were observed when the lateral roots were
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spread radially to measure extension of tap roots. Our results are testified by the centuries old practice of farmers in Kutch where they use surface soil from around S. persica trees as manure for their crop fields. Tozlu et al., (2000) obtained death of fine roots of Poncirus trifoliata in response to increasing concentration of NaCl and designated this mechanism as ‘‘fine root turnover’’. Ramoliya and Pandey (2002) reported this mechanism of fine root turnover in S. oleoides which grows in the Kutch region. Moreover, since young roots and stem tissues are salt-resistant, it appears that the plants of S. persica may sequester the salts that they absorb in the roots and stems, thus minimizing the exposure of leaf cells and hence the photosynthetic apparatus to salt. ‘‘Integration in the whole plant’’ is an important aspect of salt tolerance in the glycophytes (Garg and Gupta, 1997). The cation K is essential for cell expansion, osmoregulation and cellular and whole-plant homeostasis (Schachtman et al., 1997). High stomatal K requirement is reported for photosynthesis (Chow et al., 1990). The role of K in response to salt stress is also well documented, where Na depresses K uptake (Fox and Guerinot, 1998). The gradual elevation of Na in leaves and a rapid increase in root tissues of S. persica suggest that there is possibility for exclusion of Na through the process of fine root turnover because high concentration of Na could produce toxic effect to root tissues. Results of Na content in stems which did not change in response to increase in salt concentration suggest that stem tissues were barrier for translocation of Na from roots to leaves. Considering that the stem tissues will be reinforced by growth with time and there is persistence of root turnover, it can be predicted that after seedling stage Na tolerance of plants may increase to a little extent above 14.9 dS m1 salinity which is maximum salt concentration in this experiment. Our conclusion is supported by the fact that in the saline desert of kutch survival of plants of S. persica is greater if they have endured the habitat conditions till seedling stage. Tozlu et al. (2000) reported that in P. trifoliata fine roots played the most important role in Na stress tolerance via indirect ion exclusion through turnover and blocking Na transfer to shoot tissues. Potassium exhibited a rapid decrease in roots while it increased in leaves. These results can be attributed to: (i) transfer of K from roots to leaves, (ii) there
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could have been an exchange of K ions with Na ions in root tissues, and (iii) Na could have directly interfered with k uptake. The pattern of accumulation of K and Na in S. persica conforms to group B and/or group C plants in Marschner’s (1995) classification of plants ability to substitute Na for K. In this classification, Marschner divided plants into four groups, A, B, C and D depending upon whether K is mostly exchangeable with Na. Sodium has a positive effect on growth in A and B plants (mostly salt-tolerant plants). Group C plants contain very little K that can be substituted with Na without a negative effect on growth, and group D plants exhibit no K/Na substitution (salt-sensitive plants). It is reported that uptake mechanisms of both K and Na are similar (Watad et al., 1991; Schroeder et al., 1994). Plants utilize two systems for K acquision, low- and high-affinity uptake mechanisms. Lowaffinity K uptake is not inhibited by Na but the highaffinity process is (Watad et al., 1991; Schroeder et al., 1994). Similarly, Na toxicity in plants is correlated with two proposed Na uptake pathways (Maathuis and Sanders, 1994; Niu et al., 1995). The K and Na profiles of S. persica under salinization suggest that similar mechanism might operate in this species. In general, salinity reduces N accumulation in plants (Feigin, 1985; Garg et al., 1993). An increase in chloride uptake and accumulation is mostly accompanied by a decrease in shoot nitrate concentration (Torres and Bingham, 1973; Garg and Gupta, 1997). The interaction between salinity and P is very complex and there is no clear cut mechanistic explanation for decreased, increased or unchanged P uptake in response to salinization in different species (Grattan and Grieve, 1992). However, it is known that P concentration is related to the rate of photosynthesis, but it decreases the conversion of fixed carbon into starch (Overlach et al., 1993) and therefore decrease of P in leaves will reduce shoot growth. A decreased P concentration in root tissues, on the other hand, strongly stimulates the formation of root hairs and lateral roots in leguminous trees, rape, spinach, tomato and white lupin (Racette et al., 1990). Decreased P in roots may have influenced the increase in root production. Calcium is important during salt stress, e.g. in preserving membrane integrity (Rengel, 1992), signalling in osmoregulation (Mansfield et al., 1990) and influencing K/Na selectivity (Cramer et al., 1987). In the present study, Ca was transferred from roots to
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leaves at high salinities (>8.4 dS m1). The increased Ca content may reduce the toxicity of Na in leaves (Cramer et al., 1987). As a result, Ca fertilizers may mitigate Na toxicity to the plants. Besides the role of Mg in chlorophyll structure and as an enzyme cofactor, another important role of Mg in plants is in the export of photosynthates, which is impaired and leads to enhanced degradation of chlorophyll in Mg deficient source leaves, resulting in increased oxygenase activity of RuBP carboxylase (Marschner and Cakmak, 1989). It is difficult to suggest mechanistic explanations of salinity influence on micro-element concentration due to the relatively smaller differences between control and salinized tissues and the non-linear relationships
between some of the micro-element contents in leaves, stems and root tissues and salt concentrations. It appears that high salinity (>8.4 dS m1) decreased only Fe accumulation at the whole plant level (leaves, stems and root tissues). Other micro-elements remained almost unchanged, but some nutrients were transferred from one tissue to another in response to low water treatment and increasing salt concentration.
Acknowledgement The financial assistance provided by the Ministry of Environment and Forests, New Delhi, India, is gratefully acknowledged.
Appendix A Salt quantities used to prepare soils of different electrical conductivities Electrical conductivity (dS m1)
NaCl [g (100 kg)1]
KCl [g (100 kg)1]
CaCl2 [g (100 kg)1]
MgCl2 [g (100 kg)1]
Na2SO4 [g (100 kg)1]
K2SO4 [g (100 kg)1]
CaSO4 [g (100 kg)1]
MgSO4 [g (100 kg)1]
Total salt [g (100 kg)1]
4.3 6.1 8.4 10.3 12.5 14.9 17.2
0 60 120 180 240 300 360
0 60 120 180 240 300 360
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 20 40 60 80 100 120
0 240 480 720 960 1200 1440
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