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Salinity and olive: Growth, salt tolerance, photosynthesis and yield
Agricultural Water Management 78 (2005) 108–121 www.elsevier.com/locate/agwat
Salinity and olive: Growth, salt tolerance, photosynthesis and yield K.S. Chartzoulakis * NAGREF, Institute for Olive Tree and Subtropical Plants, 73100 Chania, Crete, Greece Accepted 1 April 2005 Available online 14 June 2005
Abstract Olive (Olea europaea L.) is a major tree crop in the Mediterranean region and is moderately salt tolerant. Recent studies suggest that olives can be irrigated with water containing 3200 mg/l of salt (ECw of 5 dS/m) producing new growth at leaf Na levels of 0.4–0.5% d.w. Salt tolerance in olives appears to be cultivar-dependent and is likely due to control of net salt import to the shoot. The mechanism is located within the roots and prevents salt translocation, rather than salt absorption. It is probably that K–Na exchange at the plasmalemma is involved in regulating the transport of Na+ to the shoot, while calcium plays a key role in limiting the toxic effects of Na+ on integrity of the plasma membrane in root cells. In addition, osmotic adjustment, stomatal closure and leaf abscission appear to play a role. Low and moderate salinity is associated with reduction of CO2 assimilation rate, stomatal and mesophyll conductance. Salinity reduces the fruit weight and oil content while increases the moisture content of fruits. Total phenol content in the olive oil is not affected by moderate NaCl salinity, while the ratio of unsaturated/saturated fatty acids decreases. # 2005 Elsevier B.V. All rights reserved. Keywords: Salinity; Tolerance mechanisms; Olea europaea; Cultivars; Photosynthesis; Yield; Oil quality
1. Introduction Water scarcity in the Mediterranean basin, especially in countries in arid zone with high rates of population growth, urbanization and industrialization, appears as one of the main factors limiting agricultural development. Within the next 25 years, although irrigated * Tel.: +30 28210 83442; fax: +30 28210 93963. E-mail address: [email protected]. 0378-3774/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.agwat.2005.04.025
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areas will increase, large quantities of fresh water supplies will be diverted from agriculture to meet the growing water demand in the municipal and industrial sectors in the region (Hamdi et al., 1995; Correia, 1999). In order to overcome water shortages and to satisfy the increasing water demand for agricultural development, the use of water of low quality (brackish, reclaimed, drainage) is becoming important in many countries. Recent research developments on salt tolerance of various crops, water, soil and crop management, irrigation and drainage methods will enhance and increase the use of low quality water for irrigation with minimum adverse impacts on yield, soil productivity and environment. The use of saline water is a promising alternative. However, the development of appropriate practices for the use of saline water for irrigation requires an adequate understanding of how salts in the irrigation water affect the soil and plant. Crop type, water quality and soil properties determine to a large extent the management practices required to optimize production. Several examples of successful use of saline water for irrigation can be found in Mediterranean region (Rhoades et al., 1992).
2. Salinity and plant growth Crops and different cultivars of the same crop vary considerably in their tolerance to salinity (Mass, 1986). Most of the available data on the response of the crops to salinity are based on studies assuming standard steady-state conditions. Mass and Hoffman (1977) concluded that crop yield is not reduced until a threshold of salinity is exceeded, according to the following equation: Yr ¼ 100 ðECe tÞs where Yr is the relative crop yield (%), 100 is the maximum yield, ECe is the average salinity of soil saturation extract (dS/m), t is the threshold soil salinity value where yield begins to decline (dS/m), and s is the rate of yield decline per unit increase in ECe. Beyond the threshold level, yield decreases linearly with increasing salinity. The salinity values at zero yield provide an estimate of maximum salinity that plants can tolerate, and is used to calculate the leaching requirements. Salt tolerance is characterized by the values of both the threshold and slope. Salt accumulation in root zone causes the development of an osmotic stress (osmotic effect) and disrupts cell ion homeostasis by inducing inhibition in the uptake of essential nutrients like K+, Ca2+ and NO3 (possibly leading to nutrient deficiency) and accumulation of Na+ and Cl to potentially toxic levels within cells (specific ion effect) (Marschner, 1995; Zhu, 2001). These primary stresses induce the generation of reactive oxygen species (ROS) (Melloni et al., 2003), cause hormonal changes (Munns, 2002), alter carbohydrates metabolism (Gao et al., 1998), reduce the activity of certain enzymes (Munns, 1993) and impair photosynthesis (Loreto et al., 2003). As a consequence of these metabolic modifications, cell division and elongation declines or it may be completely inhibited and cell death is accelerated (Hasegawa et al., 2000). At a whole-plant level the impacts of salinity are reflected through declines in growth, reduction in yield, and in more acute cases, leaf injuries, which can lead to complete defoliation of plants and their
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subsequent desiccation. Actual response to salinity varies with growing conditions including climatic and soil factors, agronomic and irrigation management, crop variety and the sensitivity of crops at different growth stages. Olive (Olea europaea L.) is one of the major tree crops in Mediterranean region, where 97% of the world’s olive oil is produced (COI, 2003). Its cultivation is continuously being extended to irrigated land. Furthermore, in this region salinity is becoming a major problem due to high rates of evaporation and insufficient leaching. In most coastal areas, in which olive is cultivated, the increased need for good quality water for urban use, limits or restricts the use of fresh water for irrigation. On the other hand, in those areas large quantities of low quality water—mostly saline (EC > 2.0 dS/m)—are available, which can and should be used for olive tree irrigation. The objective of this article is to review the existing knowledge of the effect of salinity on olive with particular emphasis on growth, salt tolerance of cultivars, photosynthesis and oil quality.
3. Salinity effects on olive tree 3.1. Salt tolerance Olive is considered as a moderately salt tolerant plant (Rugini and Fedeli, 1990). In comparison with other Mediterranean-grown tree crops, olive is more tolerant than citrus but less tolerant than date palm (Ayers and Westcot, 1976). According to Bernstein (1965) olive growth is reduced only by 10% when the electrical conductivity of the soil saturation extract (ECe) is 4–6 dS/m. This value can be as high as 6–8 dS/m in soils with high calcium status. Recent studies suggest that olive trees can be irrigated with water containing 3200 mg/l of salt (ECw of 5.0 dS/m) with a SAR of 18, producing new growth at leaf Na levels of 0.4–0.5% d.w. (Di Marco, 1985; Al-Saket and Aesheh, 1987; Tattini et al., 1992). Therios and Misopolinos (1988) reported that three-year old olive trees did not suffer salt stress at NaCl concentrations lower than 80 mM (ECw of 8.0 dS/m) during a 90-day culture period. Irrigation water with 137 mM NaCl (ECw of 13.7 dS/m) has been found to be the tolerance limit for olive trees (Rugini and Fedeli, 1990). However, olive trees can tolerate even higher EC values, when NaCl represents a small portion of the soluble salts. The type of salts contained in the irrigation water is also related to the degree of plant damage. Bartolini et al. (1991) irrigating one-year old olive plants, cv Maurino, containing either NaCl or Na2SO4 reported that Na2SO4 was more deleterious to the general growth than NaCl. Taking into account all published information on the effects of salinity on growth and production of olive we can suggest guidelines for the quality of irrigation water for olives (Table 1). A potential and cost effective source for irrigation water in olive-growing areas is the reuse of reclaimed wastewater, which contains essential nutrients for plants, such as nitrogen, phosphorus and potassium. In the island of Crete, Greece the use of such water would increase the irrigated area by 5.3% (Tsagarakis et al., 2001). Tolerance to salt appears to be cultivar-dependent. Genotypic responses of olive to NaCl salinity have not been extensively investigated, and only recently some works have been
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Table 1 Irrigation water quality guidelines for olives Irrigation problem
Degree of problem None
Increasing
Severe
Salinity ECw (dS/m)
<2.5
3–5
>5.5
Specific ion toxicity Sodium (g/l) Chloride (g/l) Boron (ppm)
0.25 0.35 1–2
0.3–1.0 0.4–1.5
>1.2 >1.8
published (Robinson, 1987; Therios and Misopolinos, 1988; Benlloch et al., 1991, 1994; Tattini et al., 1992, 1994; El-Sayed Emtithal et al., 1996; Chartzoulakis et al., 2002a; AlAbsi et al., 2003). The growth of all cultivars tested so far is reduced under salt stress to varying degrees. From published studies on salinity tolerance of young olive cultivars, ‘Pajarero’ ‘Lechino’, Chetoui’ and ‘Chalkidikis’ are considered as moderate sensitive, ‘Cordal’ ‘Manzanillo’, ‘Frantoio’, ‘Koroneiki’, ‘Chemlali’ and ‘Hotjiblanca’ as moderate tolerant, while ‘Kalamata’ ‘Picual’, ‘Lechin de Sevilla’ and ‘Megaritiki’ as tolerant (Therios and Misopolinos, 1988; Benlloch et al., 1991, 1994; Tattini et al., 1992; Chartzoulakis et al., 2002b). A list of olive cultivars tested for salinity tolerance is given in Table 2. However, the tolerance of adult plants grown under field conditions may be different of that obtained with young plants grown in pots. Table 2 Classification of olive cultivars according to their salt-tolerance Resistance
Cultivar
Country
Source
Tolerant
Megaritiki, Lianolia Kerkiras, Kalamata, Kothreiki Frantoio Arbequin˜ a, Picual, Jabaluna Nevadillo, Lechin de Sevilla, Can˜ ivano, Esscarabajuelo Hamed Chemlali
Greece
Therios and Misopolinos (1988), Chartzoulakis et al. (2002a,b) Tattini et al. (1992, 1994) Benlloch et al. (1994), Marin et al. (1995)
Moderately tolerant
Sensitive
Italy Spain
Egypt Tunisia
El-Sayed Emtithal et al. (1996) Bouaziz (1990)
Greece
Therios and Misopolinos (1988), Chartzoulakis et al. (2002a,b) Briccoli Bati et al. (1994), Tattini et al. (1994), Bartolini et al. (1991) El-Sayed Emtithal et al. (1996) Al-Absi et al. (2003)
Amphissis, Koroneiki, Mastoidis, Valanolia, Adramitini Maurino, Coratina, Carolca, Maraiolo
Italy
Aggezi, Toffahi Nabali Muhassan
Egypt Jordan
Chalkidikis, Throubolia, Aguromanaki
Greece
Leccino Bouteillan, Nabal Pajarero, Chetoui, Calego, Cobrancosa, Meski
Italy Egypt Spain
Therios and Misopolinos (1988), Chartzoulakis et al. (2002a,b) Tattini et al. (1994) El-Sayed Emtithal et al. (1996) Benlloch et al. (1994), Marin et al. (1995)
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Salt tolerance in olive cultivars is associated with effective mechanisms of ion exclusion and retention of Na+ and Cl in the root (Tattini et al., 1994; Chartzoulakis et al., 2002b). It is more likely that K–Na exchange at the plasmalemma is involved in regulating the transport of Na+ to the shoot by preventing apoplastic transport into the xylem (Gorham et al., 1985; Storey and Walker, 1999). Specific proteins crossing the plasma membrane mainly regulate the entry of salts into root. K+ channels and other non-selective cation channels are considered responsible for Na+ uptake, while its efflux is mediated by Na+/H+ antiporters (Blumwald et al., 2000). In terms of Cl, members of the ClC family, various non-selective anion channels and Cl/nH+ symporters appear to regulate Cl accumulation into root cells (Tyerman and Skerrett, 1999; White and Broadley, 2001). Although such transporters have not been identified yet in olive we can, however, infer that differences among genotypes in the uptake and accumulation of salts probably reflect differences in the expression, the abundance or the properties of these carriers. Furthermore, the salt tolerance mechanism may be related to the capacity of olive to accumulate salt in the leaf vacuoles (Loreto and Bongi, 1987). Sodium compartmentation into vacuole appears to constitute the most effective way for cells to handle efficiently high concentrations of salts and prevent their toxic effects on the cytoplasm. Na+ compartmentation is regulated by Na+/H+ antiporters (Hasegawa et al., 2000), the activity of which increases with Na+ concentration within plant cells (Ballesteros et al., 1997). The over-expression of genes encoding Na+/H+ antiporters in different plant species induced the tolerance of plants to salinity. 3.2. Plant growth All data published on olive shows that plant growth, (i.e. shoot length, total leaf area, dry weight, root length and rooting ability) is inhibited by moderate and high salinity (Therios and Misopolinos, 1988; Bartolini et al., 1991; Tattini et al., 1992, 1995; Marin et al., 1995; Chartzoulakis et al., 2002a). The extent of reduction showed significant variation according to the duration of salt exposure and the cultivar. Leaf area is more sensitive than total dry
Fig. 1. Percent reduction in leaf area and dry weight of 12 olive cultivars grown at 200 mM/l NaCl for five months. Values are the mean of six replicates S.E.
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weight. In six Greek olive cultivars differing in their salinity tolerance, the effect of salt stress at 200 mM NaCl on total leaf area was greater than that on the total (shoot + root) dry weight (Fig. 1). The decline in leaf growth is the earliest response of glycophytes exposed to salt stress (Munns and Termaat, 1986). Weisman et al. (2004) reported that long-term irrigation with intermediate saline water (4.2 dS/m) did not affect significantly vegetative growth of Barnea olive compared to control (1.2 dS/m). According to Loreto and Bongi (1987) salinity above a certain threshold (Cl concentration higher than 80 mM in total tissue water) alters plant morphology, stomata become less responsive to environmental changes and leaf thickness is reduced. Furthermore, salinity reduces the number of perfect flowers per inflorescence, the viability and germinability of the pollen and fruit set in olives (Therios and Misopolinos, 1988; Cresti et al., 1994). Dry matter partitioning is also affected, since the above ground part of the plant is more affected than that of root at high salinity (100 and 200 mM), resulting in a reduced shoot/root ratio (Therios and Misopolinos, 1988; Tattini et al., 1995; Chartzoulakis et al., 2002b). However, Tattini et al. (1995) reported that the inhibitory effects of salinization on growth of olive cuttings of the salt-tolerant ‘Frantoio’, grown even at 100 mM NaCl, fully recovered reaching values similar to the control, once salinization was relieved, despite the marked accumulation of potentially toxic ions (Na, Cl) in the leaf. More severely stressed plants (200 mM NaCl) recovered to only 60% of the control after four weeks of relief. 3.3. Tissue mineral content Salt tolerance in glycophytes is associated with the ability to prevent the entry and/or translocation of saline ions (mainly Na+ and Cl) from the root zone to aerial parts (Greenway and Munns, 1980; Storey and Walker, 1999). Root sodium and chloride concentration in olive increases with increasing NaCl in the soil (Tattini et al., 1992;
Fig. 2. Sodium concentration (ppm) in roots and leaves of 12 olive cultivars grown at 200 mM/l NaCl for five months.
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Chartzoulakis et al., 2002b). There is an increasing gradient in Na+ and Cl contents from the root to the apical part of the olive tree. Furthermore, large genotypic differences are detected regarding Na+ accumulation in the roots and transport to above ground parts (Fig. 2). At low and moderate salinity most olive cultivars exhibit a sodium exclusion capacity (Tattini et al., 1992; Chartzoulakis et al., 2002b). Ion exclusion and compartmentation at the root level regulates ion concentration in the xylem sap preventing accumulation of potentially toxic ions in the aerial parts. This mechanism seems to work effectively at low and moderate levels of salinity (up to 50 mM NaCl), but it considerably slows the rate of plant growth. The accumulation of Na+ in roots provides a mechanism for olive to cope with salinity in root zone and may indicate the existence of an inhibition mechanism of Na+ transport to leaves. At high salinities in salt sensitive cultivars, Na+ was transported and accumulated to the aerial parts, resulting in toxicity symptoms. The salt-tolerant cultivars have a more efficient mechanism regulating salt translocation to the shoot. The leaf Na+ concentration in the salt tolerant ‘Kalamata’ remained at low level, even at 200 mM NaCl, indicating the existence of an inhibition mechanism of Na+ transport to leaves (Fig. 2). Tattini (1994) reported that the resistance mechanism for salt-tolerant ‘Frantoio’ is probably related to Na+ exclusion and retention by roots and the ability to maintain an appropriate K/Na ratio in actively growing tissues. Differences in lipid composition of root cell membranes may partially explain the different ion-exclusion capacities between cultivars during salt stress (Heimler et al., 1995). Calcium plays a key role in limiting the toxic effects of Na+ on integrity of the plasma membrane in root cells. Excess Na+ displaces Ca2+ from the binding sites at plasma membrane with consequent loss of K/Na selectivity (Cramer et al., 1985). Increasing the Ca/Na ratio in the external solution has been reported to alleviate the effects of salinity on depolarization and selectivity of the plasma membrane (Rinaldelli and Mancuso, 1996). Preferential accumulation of toxic ions in mature leaves is an additional mechanism to prevent excessive salt accumulation in apical leaves (Bongi and Loreto, 1989; Loupassaki et al., 2002). Typical salt toxicity symptoms are dead leaf edge, leaf drop and necrosis of
Fig. 3. Typical salt toxicity symptoms in olive tree.
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stem tip (Fig. 3). Toxicity symptoms appear above 50 mM in salt-sensitive cultivars and become more severe at high salinity levels, while in the salt-tolerant ‘Kalamata’ no toxicity symptoms were observed, even at 200 mM NaCl. Under saline conditions the K+ concentration in many glycophytes is severely reduced (Greenway and Munns, 1980). This is the case for olive, although K+ concentration varies little among cultivars for the same salinity treatment (Bartolini et al., 1991; Tattini et al., 1995; Chartzoulakis et al., 2002b). The greatest decrease in tissue K+ occurs in the root and old leaves, suggesting that olive is able to maintain high K+ levels in young leaves, and this may act as the major monovalent cationic osmoticum in the presence of external salt. The decrease of K+ concentration recorded in olive root, which resulted in a low K/Na ratio, may also provide a mechanism by which olive plant achieve ionic balance following uptake of high Na+ concentrations in roots (Slama, 1986). This mechanism may include the increase of K+ translocation from old to young leaves (Marschner, 1995). Tattini (1994) in a detailed study reported that salt-tolerant ‘Frantoio’ exhibited higher K–Na selectivity than salt-sensitive ‘Leccino’. Furthermore, apical leaves of ‘Frantoio’ showed significantly higher K/Na ratios at all salinity levels than basal leaves, suggesting that basal leaves play a protective role, accumulating the major part of incoming Na, and thus maintaining an appropriate K/Na ratio in actively growing tissues. 3.4. Water relations A decrease in water uptake by salinized olive trees has been reported by Therios and Misopolinos (1988), caused mainly by the decreased osmotic potential in solutions containing NaCl. A detailed analysis of the water relation characteristics of olive leaves under salt stress for salt-tolerant ‘Frantoio’ and salt-sensitive ‘Leccino’ has been reported by Gucci et al. (1997b). The early response of olive to salinity is the reduction of leaf water potential (Cw) and relative water content (RWC), like in most woody crops. However, in olives changes in Cw, RWC and water uptake occur at higher salinities than those causing comparable changes in other fruit trees species (Banus and Primo-Millo, 1992; Gucci et al., 1997b). The decrease in RWC is a result of high salt concentration of the external solution, which caused osmotic stress and dehydration at cellular level. The high bulk modulus of elasticity of olive leaves (LoGullo and Salleo, 1988; Chartzoulakis et al., 1999) and leaf dehydration can explain the substantial drop in Cw during salinity and its ability to recover upon relief of stress. The salt-induced decrease of Cw was accompanied by a decrease of osmotic potential (Cp,) resulting in turgor potential (Cp) values of salinized plants similar or higher than the Cp of the control plants. At 100 mM NaCl the recovery of water potential components is complete on relief of salt stress, but at 200 mM the recovery was lower. Since growth parameters also recovered on relief of stress, it indicates that reductions in the expansion rate of growing cells that occurred during salt stress are not related to changes in turgor of mature leaves. They concluded that osmotic adjustment in olive is mainly achieved by accumulation of inorganic ions, with relatively little energy expenditure. The accumulation of soluble carbohydrates (mainly glucose and mannitol) in response to increasing NaCl concentration of the external medium supports their contribution to osmotic adjustment, while other ions (nitrate, sulfate and phosphate) and amino compounds contributed little to this process. The differences in leaf water relations
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between salt-tolerant ‘Frantoio’ and salt sensitive ‘Leccino’ reflect their differences in the exclusion capacities for Na+ and Cl ions. 3.5. Gas exchange Sclerophyllous olive leaves have a thick cuticle and a constitutively packed mesophyll, which may limit CO2 entry in the chloroplasts and photosynthesis. Under salt stress conditions olive leaves become thicker and more succulent (Bongi and Loreto, 1989). Increasing leaf thickness may further reduce the mesophyll conductance by extending and making more tortuous the CO2 pathway toward the chloroplasts (Evans et al., 1994; Syvertsen et al., 1995). Actually, all published works for olives show photosynthesis reduction under salt stress (Bongi and Loreto, 1989; Tattini et al., 1995; Chartzoulakis et al., 2002b), although the effect of salinity on CO2 assimilation rate varies with the salt concentration to which the plants are exposed and the cultivar. In general, the highest inhibition is observed in olive cultivars with inherently high photosynthesis and stomatal conductance (Loreto et al., 2003). One-year-old plants of six olive cultivars exposed to 200 mM NaCl for five months exhibited a significant decrease in assimilation rate at the end of the experiment. It ranged from 20% for salt-tolerant ‘Kalamata’ to 62% for moderately sensitive ‘Amphissis’ in young leaves (Fig. 4). A decrease in stomatal conductance (gs) precedes changes in photosynthesis in salt-stressed olive plants. Tattini et al. (1995) also found a marked reduction in photosynthesis in olive plants grown at 100 and 200 mM NaCl. However, they reported a full recovery of photosynthesis in 50 and 100 mM salt-stressed plants during the relief period for salt tolerant ‘Frantoio’, accompanied by an increase in stomatal conductance and transpiration. These results indicate that stomatal limitations of photosynthesis are prevalent during the initial stages of salinization. More recently, Loreto et al. (2003) showed that the low chloroplast CO2 concentration set by both low stomatal and mesophyll conductances are the main limitations of photosynthesis in moderately salt-stressed olive. Reduction of photosynthesis under salt stress is attributed to Na and/or Cl in many tree species. Bongi and Loreto (1989) reported that 80 mM of Cl in tissue water is the threshold
Fig. 4. Photosynthesis of six olive cultivars grown at 0 and 200 mM NaCl for six months. Values are means of six replicates S.E.
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for photosynthesis inhibition in salt-stressed olive. However, Tattini et al. (1995) showed that the relationship between CO2 assimilation and Na+ or Cl content in cv Frantoio leaves is poor and changes drastically between salinity and stress relief periods. No thresholds for Na+ or Cl content and photosynthesis were also found in the leaves of six cultivars (Chartzoulakis et al., 2002b). Loreto et al. (2003) concluded that the sensitivity to salt of olive photosynthesis is not dependent on Na+ accumulation, at least when salt accumulation is moderate. These results show that previously reported threshold values are questionable because they are strongly dependent on the cultivar and experimental conditions. 3.6. Yield and oil quality Existing data on the effect of salinity on yield of olive trees are few and in some case contradictory. Generally is accepted that high salinity levels reduce olive tree yield (Gucci and Tattini, 1997a). Bouaziz (1990) did not find any adverse effect of irrigation with brackish water on yield, oil percentage of the fruit and alternate bearing. Klein et al. (1992) reported either an increase of 12% or a decrease of 18% in the yield of Manzanillo trees, irrigated with 4.2 dS/m under field conditions, depending on planting density. When the EC of the irrigation water was 7.5 dS/m oil yield and fresh-fruit yield declined to 74 to 89% and 68 to 83% of the control. Weisman et al. (2004) reported that young Barnea olive trees irrigated with 4.2 dS/m water produced 20% higher yield than those irrigated with 7.5 dS/m. High salinity decreases fruit weight and increases the moisture content of fruits (Klein et al., 1994; Stefanoudaki, 2004). Salinity does not affect (Klein et al., 1994) or reduces oil content of the fruit, although the extent of this reduction changes with cultivar (Zarrouk et al., 1996; Weisman et al., 2004; Stefanoudaki, 2004). Chartzoulakis et al. (2004) reported that irrigation of Koroneiki olives with saline water increased Na+ and Cl concentration in olive fruit, like in other plant tissues. However, fruit Cl and potassium concentration were higher than that in leaves, while fruit Na concentration was lower than that of leaves (Table 3). The additional supply of potassium reduced to some extent the adverse effects of salinity by reducing the transport and accumulation of toxic ions in both leaves and fruits. On the other hand potassium supplement caused a sharp increase of K+ Table 3 Effect of NaCl salinity and K potassium supplement on the concentration of Na, Cl and K in the leaves and fruit of cv ‘Koroneiki’ olive Salinity (mM NaCl)
Leaves (% dw) Na
0 50 100 100 + K 150
0.055 0.685 1.775 0.885 2.125
Fruit (% dw) Cl
a
d c b c a
0.175 0.380 1.135 0.935 2.425
K c c b b a
0.898 0.325 0.120 0.813 0.125
Na a b c a c
0.040 0.572 0.860 0.476 1.116
d c b c a
Cl
K
0.324 d 1.312 c 1.652bc 1.916b 2.516 a
1.084 0.672 0.684 1.656 0.756
b c c a c
a Values represent the mean from four replications. Means within each column separated by different letters are significantly different (P < 0.05, LSD-test).
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concentration in the fruits, resulting in earlier change of fruit color from green to dark and finally fruit maturation (Chartzoulakis et al., 2004). Only a few studies have been carried out on the effect of salinity on olive oil quality. Short-term results showed that total phenol concentration increased in the olive oil produced with high NaCl levels in irrigation water (Stefanoudaki, 2004; Weisman et al., 2004), as has been also reported for water stress (Cresti et al., 1994). Separation of the phenolic compounds by HPLC analysis of the Koroneiki oil extract showed an increasing tendency for the second fraction of the secoiridoid derivatives with salinity levels (Stefanoudaki, 2004). Fatty acid composition of olive oil is also affected by salinity (Zarrouk et al., 1996). Palmitic acid, the major saturated fatty acid as well as the total saturated fatty acids increase with increasing salt concentration in the irrigation water. The ratio of unsaturated/saturated fatty acids is higher in the control and decreases significantly at moderate and high salinity levels (Zarrouk et al., 1996; Stefanoudaki, 2004; Weisman et al., 2004). In addition, the oleic/linoleic acid ratio decreases by increasing the salinity of water used for olive irrigation (Cresti et al., 1994; Stefanoudaki, 2004). These changes may be accounted for the accelerated fruit ripening (Marzouk et al., 1990). In contrast to the above reports, no changes in the fatty acid composition of the oil were found when trees were irrigated with brackish water for 12 years (Bouaziz, 1990).
4. Conclusions Although olive tree cultivation is expanding to many parts of the world during the last decades, its main production is concentrated in the Mediterranean region, where 97% of the world’s olive oil is produced (COI, 2003). Irrigation of olives with saline water will inevitably increase in the future in the Mediterranean due to negative effects of population growth and climate change on the availability and quality of existing fresh water supplies. As a consequence, the risk land salinisation will exacerbate threading the agricultural production particularly in countries with a semi-arid or arid climate. The salt tolerance on olive tree, like most glycophytes, is associated with the restriction of Na+ and/or Cl transport from the root to the shoot. This inclusion/exclusion trait for both Na+ and Cl is heritable (Sykes, 1992), suggesting that breeding and selection for Na+ and Cl excluding genotypes will continue to be a potentially rewarding area of research. Furthermore, attention should be given in the intra-cellular distribution of Na+ and Cl, (levels in the apoplast versus cytoplasm, vacuole), the possibility of ion recirculation as a factor in olive resistance (Na+ removal from the xylem and possible recirculation to the phloem) and the improved understanding of membrane transporter systems for Na+ and Cl. Understanding the mechanisms involved in salt-tolerance of olive tree is crucial to select salt tolerant genotypes or to engineer salt-sensitive genotypes with genetic traits inducing salt tolerance. The characterization of genes that contribute to salt tolerance and the underlying physiological processes could lead to the identification of specific physiological and biochemical markers for salt tolerance in olives. Using the gene transformation technologies for olives, the way is open to manipulate olive salt resistance by insertion of specific resistance genes.
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References Al-Absi, K., Qrunfleh, M., Abu-Sharar, T., 2003. Mechanism of salt tolerance of two olive (Olive europaea L.) cultivars as related to electrolyte concentration and toxicity. Acta Horticult. 618, 281–290. Al-Saket, I.A., Aesheh, I.A., 1987. Effect of saline water on growth of young olive trees. Dirasat 14 (2), 7–17. Ayers, R.S., Westcot, D.W., 1976. Water quality for agriculture. FAO Irrigation and Drainage Paper 29, pp. 1–96. Ballesteros, E., Blumwald, E., Donaire, J.P., Belver, A., 1997. Na+/H+ antiporter activity in tonoplast vesicles isolated from sunflower roots induced by NaCl stress. Physiol. Plantarum 99, 328–334. Banus, J., Primo-Millo, E., 1992. Effects of chloride and sodium on gas exchange parameters and water relations of Citrus plants. Physiol. Plant. 86, 115–123. Bartolini, G., Mazuelos, C., Troncoso, A., 1991. Influence of Na2SO4 and NaCl salts on survival, growth and mineral composition of young olive plants in inert sand culture. Adv. Horticult. Sci. 5, 73–79. Blumwald, E., Aharon, G.S., Apse, M.P., 2000. Sodium transport in plants. Biochim. Biophys. Acta 1465, 140– 151. Benlloch, M., Arboleda, F., Barranco, D., Fernandez-Escobar, R., 1991. Response of young olive trees to sodium chloride and boron excess in irrigation water. HortScience 26 (7), 867–870. Benlloch, M., Marin, L., Fernandez-Escobar, R., 1994. Salt tolerance of various olive varieties. Acta Horticult. 356, 215–217. Bernstein, L., 1965. Salt tolerance of fruit crops. USDA, Agric. Res. Bull. 292 . Bongi, G., Loreto, F., 1989. Gas-exchange properties of salt-stressed olive (Olea europaea L.) leaves. Plant Physiol. 90, 1408–1413. Bouaziz, A., 1990. Behaviour of some olive varieties irrigated with brackish water and grown intensively in the central part of Tunisia. Acta Horticult. 286, 247–250. Briccoli Bati, C., Basta, P., Tocci, C., Turco, D., 1994. Influenza dell’ irrigazione con acqua salmastra su giovani piante di olivo. Olivae 53, 35–38. Chartzoulakis, K., Patakas, A., Bosabalidis, A., 1999. Changes in water relations, photosynthesis and leaf anatomy induced by intermittent drought in two olive cultivars. J. Exp. Envir. Bot. 42 (2), 113–120. Chartzoulakis, K., Loupassaki, M., Androulakis, I., 2002a. Comparative study on NaCl salinity of six olive cultivars. Acta Horticult. 586 (1), 497–502. Chartzoulakis, K., Loupassaki, M., Bertaki, M., Androulakis, I., 2002b. Effects of NaCl salinity on growth, ion content and CO2 assimilation rate of six olive cultivars. Scientia Horticult. 96, 235–247. Chartzoulakis, K., Psarras, G., Vemmos, S., Loupassaki, M., 2004. Effects of salinity and potassium supplement on photosynthesis, water relations and Na, Cl, K and carbohydrate concentration of two olive cultivars. Agric. Res. 27 (1), 75–84. COI (International Olive Oil Council), 2003. The world olive oil market. Olivae 97, 19–21. Correia, F.N., 1999. Water resources in Mediterranean region. Water Intern. 24 (1), 22–30. Cramer, G.R., Lauchli, A., Polito, V.S., 1985. Displacement of Ca2+ by Na+ from the plasmalemma of root cells. Plant Physiol. 79, 207–211. Cresti, M., Ciampolini, F., Tattini, M., Cimato, A., 1994. Effect of salinity on productivity and oil quality of olive (Olea europaea L.) plants. Adv. Horticult. Sci. 8, 211–214. Di Marco, L., 1985. In: Baldini, E., Scaramuzzi, F. (Eds.), Concimazione, in L’Olivo. REDA, Roma. El-Sayed Emtithal, H., El-Said, M.E., El-Sherif, A.H., Sari El-Diem, S.A., 1996. Chemical studies on the salt tolerance of some olive cultivars. Olivae 64, 52–57. Evans, G.R., Von Caemmerer, S., Setchell, B.A., Hudson, G.S., 1994. The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Austr. J. Plant Physiol. 21, 475–495. Gao, Z., Sagi, M., Lips, S.H., 1998. Carbohydrate metabolism in leaves and assimilate partitioning in fruits of tomato (Lycopersicon esculentum L.) as affected by salinity. Plant Sci. 135, 149–159. Gorham, J., Wyn Jones, R.G., McDonnell, G., 1985. Some mechanisms of salt tolerance in crop plants. Plant Soil 89, 15–40. Greenway, H., Munns, R., 1980. Mechanisms of salt tolerance in non-halophytes. Ann. Rev. Plant Physiol. 31, 149–190. Gucci, R., Tattini, M., 1997a. Salinity tolerance in olive. Horticult. Rev. 21, 177–214.
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Gucci, R., Lombardini, L., Tattini, M., 1997b. Analysis of leaf water relations in leaves of two olive (Olea europaea) cultivars differing in tolerance to salinity. Tree Physiol. 17, 13–21. Hamdi, A., Abu-Zeid, M.F., Lacirignola, C., 1995. Water crisis in the Mediterranean: agricultural water demand management. Water Intern. 20 (2), 176–187. Hasegawa, P.M., Bressan, S.A., Zhu, J.K., Bohnert, H.J., 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 463–499. Heimler, D., Tattini, M., Ticci, S., Coradeschi, M.A., Traversi, M.L., 1995. Growth, ion accumulation and lipid composition of two olive genotypes under salinity. J. Plant Nutr. 18, 1723–1734. Klein, I., Ben-Tal, Y., Lavee, S., David, I., 1992. Olive irrigation with saline water (in Hebrew) Volcani Center Report, Bet-Dagan, Israel. Klein, I., Ben-Tal, Y., Lavee, S., De Malach, J., David, I., 1994. Saline irrigation of cv Manzanilo and Uomo di Piccione trees. Acta Hort. 356, 176–218. LoGullo, M.A., Salleo, S., 1988. Different strategies of drought resistance in three Mediterranean sclerophyllus trees growing in the same environmental conditions. New Phytol. 108, 267–276. Loupassaki, M.H., Chartzoulakis, K., Digalaki, N., Androulakis, I., 2002. Effects of salt stress on concentration of nitrogen, phosphorus, potassium, calcium, magnesium and sodium in leaves, shoots and roots of six olive cultivars. J. Plant Nutr. 25 (11), 2457–2482. Loreto, F., Bongi, G., 1987. Control of photosynthesis under salt stress in the olive. In: Prodi, F., Rossi, F., Cristoferi, G. (Eds.), International Conference on Agrometeorology, Fondazione Cesena Agricoltura, Cesena. Loreto, F., Centritto, M., Chartzoulakis, K., 2003. Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant Cell Environ. 26, 595–601. Marin, L., Benlloch, M., Fernandez-Escobar, R., 1995. Screening for olive cultivars for salt tolerance. Scientia Horticult. 64, 113–116. Marschner, H., 1995. Mineral Nutrition of Higher Plants, second ed. Academic Press, London. Marzouk, B., Zarrouk, M., Cherif, A., 1990. Glycerollipid biosynthesis in ripening olive fruits. In: Quin, P.J., Harwood, G.L. (Eds.), Plant Lipid Biochemistry, Structure and Utilization. Portland Press Ltd., London, pp. 228–230. Mass, E.V., Hoffman, G.J., 1977. Crop salt tolerance—current assessment. J. Irrig. Drainage, Div. ASCE 103, 115–134. Mass, E.V., 1986. Salt tolerance of plants. Appl. Agric. Res. 1, 12–26. Melloni, D.A., Oliva, M.A., Martinez, C.A., Cambraia, J., 2003. Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ. Exp. Bot. 49, 69–76. Munns, R., Termaat, A., 1986. Whole plant responses to salinity. Austr. J. Plant Physiol. 13, 143–160. Munns, R., 1993. Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant Cell Environ. 16, 15–24. Munns, R., 2002. Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239–250. Rhoades, J.D., Kandiah, A., Mashali, A. M., 1992. The use of saline waters for crop production. FAO, Irrigation and Drainage Paper, No. 48, Rome, Italy. Rinaldelli, E., Mancuso, S., 1996. Response of young mycorrhizal and non-mycorrhizal plants of olive tree (Olea europaea L.) to saline conditions. I. Short-term electro-physiological and long-term vegetative salt effects. Adv. Horticult. Sci. 10, 126–134. Robinson, F.E., 1987. Growth potential of young olive with high chloride irrigation water. HortScience 22 (3), 509. Rugini, E., Fedeli, E., 1990. Olive (Olea europea L.) as an oilseed crop. In: Bajaj, Y.P.S. (Ed.), Bio-technology in Agriculture and Forestry Legume and Oilseed Crops I, vol.1. Springer, Berlin, pp. 593–641. Slama, F., 1986. Intervention des racines dans le sensibilite ou tolerance a NaCl des plantes cultivees. Agronomie 6, 651–658. Sykes, S.R., 1992. The inheritance of salt exclusion in woody perennial fruit species. Plant Soil 146, 123–129. Syvertsen, J.P., Lloyd, J., McConchie, C., Kriedemann, P.E., Farquhar, G.D., 1995. On the site of biophysical constrains to CO2 diffusion through the mesophyll of hypostomatous leaves. Plant Cell Environ. 18, 149–157. Stefanoudaki, E., 2004. Factors affecting olive oil quality. Ph.D. Thesis, University of Cardiff, UK. Storey, R., Walker, R.R., 1999. Citrus and salinity. Sci. Horticult. 78, 39–81. Tattini, M., Bertoni, P., Caselli, S., 1992. Genotypic responses of olive plants to sodium chloride. J. Plant Nutr. 15 (9), 1467–1485.
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Tattini, M., 1994. Ionic relations of aeroponically grown olive plants during salt stress. Plant Soil 161, 251–256. Tattini, M., Ponzio, C., Coradeschi, M.A., Tafani, R., Traversi, M.L., 1994. Mechanisms of salt tolerance in olive plants. Acta Horticult. 356, 181–184. Tattini, M., Gucci, R., Coradeschi, M.A., Ponzio, C., Everarard, J.D., 1995. Growth, gas exchange and ion content in Olea europaea plants during salinity and subsequent relief. Physiol. Plantarum 95, 203–210. Therios, I.N., Misopolinos, N.D., 1988. Genotypic response to sodium chloride salinity of four major olive cultivars (Olea europea L.) Plant Soil 106, 105–111. Tsagarakis, K.P., Tsoumanis, P., Chartzoulakis, K., Angelakis, A.N., 2001. Water resources status including wastewater treatment and reuse in Greece: related problems and prospectives. Water Intern. 26 (2), 252–258. Tyerman, S.D., Skerrett, I.M., 1999. Root ion channels and salinity. Sci. Horticult. 78, 175–235. Weisman, Z., Itzhak, D., Ben Dom, N., 2004. Optimization of saline water level for sustainable Barnea olive and oil production in desert conditions. Sci. Horticult. 100, 257–266. White, P.J., Broadley, M.R., 2001. Chloride in soils and its uptake and movement within the plant: a review. Ann. Bot. 88, 967–988. Zarrouk, M., Marzouk, B., Ben Miled Daoud, D., Cherif, A., 1996. Oil accumulation in olives and effect of salt on their composition. Olivae 61, 41–45. Zhu, J.K., 2001. Plant salt tolerance. Trends Plant Sci. 6, 66–71.
Salinity and olive: Growth, salt tolerance, photosynthesis and yield K.S. Chartzoulakis * NAGREF, Institute for Olive Tree and Subtropical Plants, 73100 Chania, Crete, Greece Accepted 1 April 2005 Available online 14 June 2005
Abstract Olive (Olea europaea L.) is a major tree crop in the Mediterranean region and is moderately salt tolerant. Recent studies suggest that olives can be irrigated with water containing 3200 mg/l of salt (ECw of 5 dS/m) producing new growth at leaf Na levels of 0.4–0.5% d.w. Salt tolerance in olives appears to be cultivar-dependent and is likely due to control of net salt import to the shoot. The mechanism is located within the roots and prevents salt translocation, rather than salt absorption. It is probably that K–Na exchange at the plasmalemma is involved in regulating the transport of Na+ to the shoot, while calcium plays a key role in limiting the toxic effects of Na+ on integrity of the plasma membrane in root cells. In addition, osmotic adjustment, stomatal closure and leaf abscission appear to play a role. Low and moderate salinity is associated with reduction of CO2 assimilation rate, stomatal and mesophyll conductance. Salinity reduces the fruit weight and oil content while increases the moisture content of fruits. Total phenol content in the olive oil is not affected by moderate NaCl salinity, while the ratio of unsaturated/saturated fatty acids decreases. # 2005 Elsevier B.V. All rights reserved. Keywords: Salinity; Tolerance mechanisms; Olea europaea; Cultivars; Photosynthesis; Yield; Oil quality
1. Introduction Water scarcity in the Mediterranean basin, especially in countries in arid zone with high rates of population growth, urbanization and industrialization, appears as one of the main factors limiting agricultural development. Within the next 25 years, although irrigated * Tel.: +30 28210 83442; fax: +30 28210 93963. E-mail address: [email protected]. 0378-3774/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.agwat.2005.04.025
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areas will increase, large quantities of fresh water supplies will be diverted from agriculture to meet the growing water demand in the municipal and industrial sectors in the region (Hamdi et al., 1995; Correia, 1999). In order to overcome water shortages and to satisfy the increasing water demand for agricultural development, the use of water of low quality (brackish, reclaimed, drainage) is becoming important in many countries. Recent research developments on salt tolerance of various crops, water, soil and crop management, irrigation and drainage methods will enhance and increase the use of low quality water for irrigation with minimum adverse impacts on yield, soil productivity and environment. The use of saline water is a promising alternative. However, the development of appropriate practices for the use of saline water for irrigation requires an adequate understanding of how salts in the irrigation water affect the soil and plant. Crop type, water quality and soil properties determine to a large extent the management practices required to optimize production. Several examples of successful use of saline water for irrigation can be found in Mediterranean region (Rhoades et al., 1992).
2. Salinity and plant growth Crops and different cultivars of the same crop vary considerably in their tolerance to salinity (Mass, 1986). Most of the available data on the response of the crops to salinity are based on studies assuming standard steady-state conditions. Mass and Hoffman (1977) concluded that crop yield is not reduced until a threshold of salinity is exceeded, according to the following equation: Yr ¼ 100 ðECe tÞs where Yr is the relative crop yield (%), 100 is the maximum yield, ECe is the average salinity of soil saturation extract (dS/m), t is the threshold soil salinity value where yield begins to decline (dS/m), and s is the rate of yield decline per unit increase in ECe. Beyond the threshold level, yield decreases linearly with increasing salinity. The salinity values at zero yield provide an estimate of maximum salinity that plants can tolerate, and is used to calculate the leaching requirements. Salt tolerance is characterized by the values of both the threshold and slope. Salt accumulation in root zone causes the development of an osmotic stress (osmotic effect) and disrupts cell ion homeostasis by inducing inhibition in the uptake of essential nutrients like K+, Ca2+ and NO3 (possibly leading to nutrient deficiency) and accumulation of Na+ and Cl to potentially toxic levels within cells (specific ion effect) (Marschner, 1995; Zhu, 2001). These primary stresses induce the generation of reactive oxygen species (ROS) (Melloni et al., 2003), cause hormonal changes (Munns, 2002), alter carbohydrates metabolism (Gao et al., 1998), reduce the activity of certain enzymes (Munns, 1993) and impair photosynthesis (Loreto et al., 2003). As a consequence of these metabolic modifications, cell division and elongation declines or it may be completely inhibited and cell death is accelerated (Hasegawa et al., 2000). At a whole-plant level the impacts of salinity are reflected through declines in growth, reduction in yield, and in more acute cases, leaf injuries, which can lead to complete defoliation of plants and their
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subsequent desiccation. Actual response to salinity varies with growing conditions including climatic and soil factors, agronomic and irrigation management, crop variety and the sensitivity of crops at different growth stages. Olive (Olea europaea L.) is one of the major tree crops in Mediterranean region, where 97% of the world’s olive oil is produced (COI, 2003). Its cultivation is continuously being extended to irrigated land. Furthermore, in this region salinity is becoming a major problem due to high rates of evaporation and insufficient leaching. In most coastal areas, in which olive is cultivated, the increased need for good quality water for urban use, limits or restricts the use of fresh water for irrigation. On the other hand, in those areas large quantities of low quality water—mostly saline (EC > 2.0 dS/m)—are available, which can and should be used for olive tree irrigation. The objective of this article is to review the existing knowledge of the effect of salinity on olive with particular emphasis on growth, salt tolerance of cultivars, photosynthesis and oil quality.
3. Salinity effects on olive tree 3.1. Salt tolerance Olive is considered as a moderately salt tolerant plant (Rugini and Fedeli, 1990). In comparison with other Mediterranean-grown tree crops, olive is more tolerant than citrus but less tolerant than date palm (Ayers and Westcot, 1976). According to Bernstein (1965) olive growth is reduced only by 10% when the electrical conductivity of the soil saturation extract (ECe) is 4–6 dS/m. This value can be as high as 6–8 dS/m in soils with high calcium status. Recent studies suggest that olive trees can be irrigated with water containing 3200 mg/l of salt (ECw of 5.0 dS/m) with a SAR of 18, producing new growth at leaf Na levels of 0.4–0.5% d.w. (Di Marco, 1985; Al-Saket and Aesheh, 1987; Tattini et al., 1992). Therios and Misopolinos (1988) reported that three-year old olive trees did not suffer salt stress at NaCl concentrations lower than 80 mM (ECw of 8.0 dS/m) during a 90-day culture period. Irrigation water with 137 mM NaCl (ECw of 13.7 dS/m) has been found to be the tolerance limit for olive trees (Rugini and Fedeli, 1990). However, olive trees can tolerate even higher EC values, when NaCl represents a small portion of the soluble salts. The type of salts contained in the irrigation water is also related to the degree of plant damage. Bartolini et al. (1991) irrigating one-year old olive plants, cv Maurino, containing either NaCl or Na2SO4 reported that Na2SO4 was more deleterious to the general growth than NaCl. Taking into account all published information on the effects of salinity on growth and production of olive we can suggest guidelines for the quality of irrigation water for olives (Table 1). A potential and cost effective source for irrigation water in olive-growing areas is the reuse of reclaimed wastewater, which contains essential nutrients for plants, such as nitrogen, phosphorus and potassium. In the island of Crete, Greece the use of such water would increase the irrigated area by 5.3% (Tsagarakis et al., 2001). Tolerance to salt appears to be cultivar-dependent. Genotypic responses of olive to NaCl salinity have not been extensively investigated, and only recently some works have been
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Table 1 Irrigation water quality guidelines for olives Irrigation problem
Degree of problem None
Increasing
Severe
Salinity ECw (dS/m)
<2.5
3–5
>5.5
Specific ion toxicity Sodium (g/l) Chloride (g/l) Boron (ppm)
0.25 0.35 1–2
0.3–1.0 0.4–1.5
>1.2 >1.8
published (Robinson, 1987; Therios and Misopolinos, 1988; Benlloch et al., 1991, 1994; Tattini et al., 1992, 1994; El-Sayed Emtithal et al., 1996; Chartzoulakis et al., 2002a; AlAbsi et al., 2003). The growth of all cultivars tested so far is reduced under salt stress to varying degrees. From published studies on salinity tolerance of young olive cultivars, ‘Pajarero’ ‘Lechino’, Chetoui’ and ‘Chalkidikis’ are considered as moderate sensitive, ‘Cordal’ ‘Manzanillo’, ‘Frantoio’, ‘Koroneiki’, ‘Chemlali’ and ‘Hotjiblanca’ as moderate tolerant, while ‘Kalamata’ ‘Picual’, ‘Lechin de Sevilla’ and ‘Megaritiki’ as tolerant (Therios and Misopolinos, 1988; Benlloch et al., 1991, 1994; Tattini et al., 1992; Chartzoulakis et al., 2002b). A list of olive cultivars tested for salinity tolerance is given in Table 2. However, the tolerance of adult plants grown under field conditions may be different of that obtained with young plants grown in pots. Table 2 Classification of olive cultivars according to their salt-tolerance Resistance
Cultivar
Country
Source
Tolerant
Megaritiki, Lianolia Kerkiras, Kalamata, Kothreiki Frantoio Arbequin˜ a, Picual, Jabaluna Nevadillo, Lechin de Sevilla, Can˜ ivano, Esscarabajuelo Hamed Chemlali
Greece
Therios and Misopolinos (1988), Chartzoulakis et al. (2002a,b) Tattini et al. (1992, 1994) Benlloch et al. (1994), Marin et al. (1995)
Moderately tolerant
Sensitive
Italy Spain
Egypt Tunisia
El-Sayed Emtithal et al. (1996) Bouaziz (1990)
Greece
Therios and Misopolinos (1988), Chartzoulakis et al. (2002a,b) Briccoli Bati et al. (1994), Tattini et al. (1994), Bartolini et al. (1991) El-Sayed Emtithal et al. (1996) Al-Absi et al. (2003)
Amphissis, Koroneiki, Mastoidis, Valanolia, Adramitini Maurino, Coratina, Carolca, Maraiolo
Italy
Aggezi, Toffahi Nabali Muhassan
Egypt Jordan
Chalkidikis, Throubolia, Aguromanaki
Greece
Leccino Bouteillan, Nabal Pajarero, Chetoui, Calego, Cobrancosa, Meski
Italy Egypt Spain
Therios and Misopolinos (1988), Chartzoulakis et al. (2002a,b) Tattini et al. (1994) El-Sayed Emtithal et al. (1996) Benlloch et al. (1994), Marin et al. (1995)
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Salt tolerance in olive cultivars is associated with effective mechanisms of ion exclusion and retention of Na+ and Cl in the root (Tattini et al., 1994; Chartzoulakis et al., 2002b). It is more likely that K–Na exchange at the plasmalemma is involved in regulating the transport of Na+ to the shoot by preventing apoplastic transport into the xylem (Gorham et al., 1985; Storey and Walker, 1999). Specific proteins crossing the plasma membrane mainly regulate the entry of salts into root. K+ channels and other non-selective cation channels are considered responsible for Na+ uptake, while its efflux is mediated by Na+/H+ antiporters (Blumwald et al., 2000). In terms of Cl, members of the ClC family, various non-selective anion channels and Cl/nH+ symporters appear to regulate Cl accumulation into root cells (Tyerman and Skerrett, 1999; White and Broadley, 2001). Although such transporters have not been identified yet in olive we can, however, infer that differences among genotypes in the uptake and accumulation of salts probably reflect differences in the expression, the abundance or the properties of these carriers. Furthermore, the salt tolerance mechanism may be related to the capacity of olive to accumulate salt in the leaf vacuoles (Loreto and Bongi, 1987). Sodium compartmentation into vacuole appears to constitute the most effective way for cells to handle efficiently high concentrations of salts and prevent their toxic effects on the cytoplasm. Na+ compartmentation is regulated by Na+/H+ antiporters (Hasegawa et al., 2000), the activity of which increases with Na+ concentration within plant cells (Ballesteros et al., 1997). The over-expression of genes encoding Na+/H+ antiporters in different plant species induced the tolerance of plants to salinity. 3.2. Plant growth All data published on olive shows that plant growth, (i.e. shoot length, total leaf area, dry weight, root length and rooting ability) is inhibited by moderate and high salinity (Therios and Misopolinos, 1988; Bartolini et al., 1991; Tattini et al., 1992, 1995; Marin et al., 1995; Chartzoulakis et al., 2002a). The extent of reduction showed significant variation according to the duration of salt exposure and the cultivar. Leaf area is more sensitive than total dry
Fig. 1. Percent reduction in leaf area and dry weight of 12 olive cultivars grown at 200 mM/l NaCl for five months. Values are the mean of six replicates S.E.
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weight. In six Greek olive cultivars differing in their salinity tolerance, the effect of salt stress at 200 mM NaCl on total leaf area was greater than that on the total (shoot + root) dry weight (Fig. 1). The decline in leaf growth is the earliest response of glycophytes exposed to salt stress (Munns and Termaat, 1986). Weisman et al. (2004) reported that long-term irrigation with intermediate saline water (4.2 dS/m) did not affect significantly vegetative growth of Barnea olive compared to control (1.2 dS/m). According to Loreto and Bongi (1987) salinity above a certain threshold (Cl concentration higher than 80 mM in total tissue water) alters plant morphology, stomata become less responsive to environmental changes and leaf thickness is reduced. Furthermore, salinity reduces the number of perfect flowers per inflorescence, the viability and germinability of the pollen and fruit set in olives (Therios and Misopolinos, 1988; Cresti et al., 1994). Dry matter partitioning is also affected, since the above ground part of the plant is more affected than that of root at high salinity (100 and 200 mM), resulting in a reduced shoot/root ratio (Therios and Misopolinos, 1988; Tattini et al., 1995; Chartzoulakis et al., 2002b). However, Tattini et al. (1995) reported that the inhibitory effects of salinization on growth of olive cuttings of the salt-tolerant ‘Frantoio’, grown even at 100 mM NaCl, fully recovered reaching values similar to the control, once salinization was relieved, despite the marked accumulation of potentially toxic ions (Na, Cl) in the leaf. More severely stressed plants (200 mM NaCl) recovered to only 60% of the control after four weeks of relief. 3.3. Tissue mineral content Salt tolerance in glycophytes is associated with the ability to prevent the entry and/or translocation of saline ions (mainly Na+ and Cl) from the root zone to aerial parts (Greenway and Munns, 1980; Storey and Walker, 1999). Root sodium and chloride concentration in olive increases with increasing NaCl in the soil (Tattini et al., 1992;
Fig. 2. Sodium concentration (ppm) in roots and leaves of 12 olive cultivars grown at 200 mM/l NaCl for five months.
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Chartzoulakis et al., 2002b). There is an increasing gradient in Na+ and Cl contents from the root to the apical part of the olive tree. Furthermore, large genotypic differences are detected regarding Na+ accumulation in the roots and transport to above ground parts (Fig. 2). At low and moderate salinity most olive cultivars exhibit a sodium exclusion capacity (Tattini et al., 1992; Chartzoulakis et al., 2002b). Ion exclusion and compartmentation at the root level regulates ion concentration in the xylem sap preventing accumulation of potentially toxic ions in the aerial parts. This mechanism seems to work effectively at low and moderate levels of salinity (up to 50 mM NaCl), but it considerably slows the rate of plant growth. The accumulation of Na+ in roots provides a mechanism for olive to cope with salinity in root zone and may indicate the existence of an inhibition mechanism of Na+ transport to leaves. At high salinities in salt sensitive cultivars, Na+ was transported and accumulated to the aerial parts, resulting in toxicity symptoms. The salt-tolerant cultivars have a more efficient mechanism regulating salt translocation to the shoot. The leaf Na+ concentration in the salt tolerant ‘Kalamata’ remained at low level, even at 200 mM NaCl, indicating the existence of an inhibition mechanism of Na+ transport to leaves (Fig. 2). Tattini (1994) reported that the resistance mechanism for salt-tolerant ‘Frantoio’ is probably related to Na+ exclusion and retention by roots and the ability to maintain an appropriate K/Na ratio in actively growing tissues. Differences in lipid composition of root cell membranes may partially explain the different ion-exclusion capacities between cultivars during salt stress (Heimler et al., 1995). Calcium plays a key role in limiting the toxic effects of Na+ on integrity of the plasma membrane in root cells. Excess Na+ displaces Ca2+ from the binding sites at plasma membrane with consequent loss of K/Na selectivity (Cramer et al., 1985). Increasing the Ca/Na ratio in the external solution has been reported to alleviate the effects of salinity on depolarization and selectivity of the plasma membrane (Rinaldelli and Mancuso, 1996). Preferential accumulation of toxic ions in mature leaves is an additional mechanism to prevent excessive salt accumulation in apical leaves (Bongi and Loreto, 1989; Loupassaki et al., 2002). Typical salt toxicity symptoms are dead leaf edge, leaf drop and necrosis of
Fig. 3. Typical salt toxicity symptoms in olive tree.
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stem tip (Fig. 3). Toxicity symptoms appear above 50 mM in salt-sensitive cultivars and become more severe at high salinity levels, while in the salt-tolerant ‘Kalamata’ no toxicity symptoms were observed, even at 200 mM NaCl. Under saline conditions the K+ concentration in many glycophytes is severely reduced (Greenway and Munns, 1980). This is the case for olive, although K+ concentration varies little among cultivars for the same salinity treatment (Bartolini et al., 1991; Tattini et al., 1995; Chartzoulakis et al., 2002b). The greatest decrease in tissue K+ occurs in the root and old leaves, suggesting that olive is able to maintain high K+ levels in young leaves, and this may act as the major monovalent cationic osmoticum in the presence of external salt. The decrease of K+ concentration recorded in olive root, which resulted in a low K/Na ratio, may also provide a mechanism by which olive plant achieve ionic balance following uptake of high Na+ concentrations in roots (Slama, 1986). This mechanism may include the increase of K+ translocation from old to young leaves (Marschner, 1995). Tattini (1994) in a detailed study reported that salt-tolerant ‘Frantoio’ exhibited higher K–Na selectivity than salt-sensitive ‘Leccino’. Furthermore, apical leaves of ‘Frantoio’ showed significantly higher K/Na ratios at all salinity levels than basal leaves, suggesting that basal leaves play a protective role, accumulating the major part of incoming Na, and thus maintaining an appropriate K/Na ratio in actively growing tissues. 3.4. Water relations A decrease in water uptake by salinized olive trees has been reported by Therios and Misopolinos (1988), caused mainly by the decreased osmotic potential in solutions containing NaCl. A detailed analysis of the water relation characteristics of olive leaves under salt stress for salt-tolerant ‘Frantoio’ and salt-sensitive ‘Leccino’ has been reported by Gucci et al. (1997b). The early response of olive to salinity is the reduction of leaf water potential (Cw) and relative water content (RWC), like in most woody crops. However, in olives changes in Cw, RWC and water uptake occur at higher salinities than those causing comparable changes in other fruit trees species (Banus and Primo-Millo, 1992; Gucci et al., 1997b). The decrease in RWC is a result of high salt concentration of the external solution, which caused osmotic stress and dehydration at cellular level. The high bulk modulus of elasticity of olive leaves (LoGullo and Salleo, 1988; Chartzoulakis et al., 1999) and leaf dehydration can explain the substantial drop in Cw during salinity and its ability to recover upon relief of stress. The salt-induced decrease of Cw was accompanied by a decrease of osmotic potential (Cp,) resulting in turgor potential (Cp) values of salinized plants similar or higher than the Cp of the control plants. At 100 mM NaCl the recovery of water potential components is complete on relief of salt stress, but at 200 mM the recovery was lower. Since growth parameters also recovered on relief of stress, it indicates that reductions in the expansion rate of growing cells that occurred during salt stress are not related to changes in turgor of mature leaves. They concluded that osmotic adjustment in olive is mainly achieved by accumulation of inorganic ions, with relatively little energy expenditure. The accumulation of soluble carbohydrates (mainly glucose and mannitol) in response to increasing NaCl concentration of the external medium supports their contribution to osmotic adjustment, while other ions (nitrate, sulfate and phosphate) and amino compounds contributed little to this process. The differences in leaf water relations
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between salt-tolerant ‘Frantoio’ and salt sensitive ‘Leccino’ reflect their differences in the exclusion capacities for Na+ and Cl ions. 3.5. Gas exchange Sclerophyllous olive leaves have a thick cuticle and a constitutively packed mesophyll, which may limit CO2 entry in the chloroplasts and photosynthesis. Under salt stress conditions olive leaves become thicker and more succulent (Bongi and Loreto, 1989). Increasing leaf thickness may further reduce the mesophyll conductance by extending and making more tortuous the CO2 pathway toward the chloroplasts (Evans et al., 1994; Syvertsen et al., 1995). Actually, all published works for olives show photosynthesis reduction under salt stress (Bongi and Loreto, 1989; Tattini et al., 1995; Chartzoulakis et al., 2002b), although the effect of salinity on CO2 assimilation rate varies with the salt concentration to which the plants are exposed and the cultivar. In general, the highest inhibition is observed in olive cultivars with inherently high photosynthesis and stomatal conductance (Loreto et al., 2003). One-year-old plants of six olive cultivars exposed to 200 mM NaCl for five months exhibited a significant decrease in assimilation rate at the end of the experiment. It ranged from 20% for salt-tolerant ‘Kalamata’ to 62% for moderately sensitive ‘Amphissis’ in young leaves (Fig. 4). A decrease in stomatal conductance (gs) precedes changes in photosynthesis in salt-stressed olive plants. Tattini et al. (1995) also found a marked reduction in photosynthesis in olive plants grown at 100 and 200 mM NaCl. However, they reported a full recovery of photosynthesis in 50 and 100 mM salt-stressed plants during the relief period for salt tolerant ‘Frantoio’, accompanied by an increase in stomatal conductance and transpiration. These results indicate that stomatal limitations of photosynthesis are prevalent during the initial stages of salinization. More recently, Loreto et al. (2003) showed that the low chloroplast CO2 concentration set by both low stomatal and mesophyll conductances are the main limitations of photosynthesis in moderately salt-stressed olive. Reduction of photosynthesis under salt stress is attributed to Na and/or Cl in many tree species. Bongi and Loreto (1989) reported that 80 mM of Cl in tissue water is the threshold
Fig. 4. Photosynthesis of six olive cultivars grown at 0 and 200 mM NaCl for six months. Values are means of six replicates S.E.
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for photosynthesis inhibition in salt-stressed olive. However, Tattini et al. (1995) showed that the relationship between CO2 assimilation and Na+ or Cl content in cv Frantoio leaves is poor and changes drastically between salinity and stress relief periods. No thresholds for Na+ or Cl content and photosynthesis were also found in the leaves of six cultivars (Chartzoulakis et al., 2002b). Loreto et al. (2003) concluded that the sensitivity to salt of olive photosynthesis is not dependent on Na+ accumulation, at least when salt accumulation is moderate. These results show that previously reported threshold values are questionable because they are strongly dependent on the cultivar and experimental conditions. 3.6. Yield and oil quality Existing data on the effect of salinity on yield of olive trees are few and in some case contradictory. Generally is accepted that high salinity levels reduce olive tree yield (Gucci and Tattini, 1997a). Bouaziz (1990) did not find any adverse effect of irrigation with brackish water on yield, oil percentage of the fruit and alternate bearing. Klein et al. (1992) reported either an increase of 12% or a decrease of 18% in the yield of Manzanillo trees, irrigated with 4.2 dS/m under field conditions, depending on planting density. When the EC of the irrigation water was 7.5 dS/m oil yield and fresh-fruit yield declined to 74 to 89% and 68 to 83% of the control. Weisman et al. (2004) reported that young Barnea olive trees irrigated with 4.2 dS/m water produced 20% higher yield than those irrigated with 7.5 dS/m. High salinity decreases fruit weight and increases the moisture content of fruits (Klein et al., 1994; Stefanoudaki, 2004). Salinity does not affect (Klein et al., 1994) or reduces oil content of the fruit, although the extent of this reduction changes with cultivar (Zarrouk et al., 1996; Weisman et al., 2004; Stefanoudaki, 2004). Chartzoulakis et al. (2004) reported that irrigation of Koroneiki olives with saline water increased Na+ and Cl concentration in olive fruit, like in other plant tissues. However, fruit Cl and potassium concentration were higher than that in leaves, while fruit Na concentration was lower than that of leaves (Table 3). The additional supply of potassium reduced to some extent the adverse effects of salinity by reducing the transport and accumulation of toxic ions in both leaves and fruits. On the other hand potassium supplement caused a sharp increase of K+ Table 3 Effect of NaCl salinity and K potassium supplement on the concentration of Na, Cl and K in the leaves and fruit of cv ‘Koroneiki’ olive Salinity (mM NaCl)
Leaves (% dw) Na
0 50 100 100 + K 150
0.055 0.685 1.775 0.885 2.125
Fruit (% dw) Cl
a
d c b c a
0.175 0.380 1.135 0.935 2.425
K c c b b a
0.898 0.325 0.120 0.813 0.125
Na a b c a c
0.040 0.572 0.860 0.476 1.116
d c b c a
Cl
K
0.324 d 1.312 c 1.652bc 1.916b 2.516 a
1.084 0.672 0.684 1.656 0.756
b c c a c
a Values represent the mean from four replications. Means within each column separated by different letters are significantly different (P < 0.05, LSD-test).
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concentration in the fruits, resulting in earlier change of fruit color from green to dark and finally fruit maturation (Chartzoulakis et al., 2004). Only a few studies have been carried out on the effect of salinity on olive oil quality. Short-term results showed that total phenol concentration increased in the olive oil produced with high NaCl levels in irrigation water (Stefanoudaki, 2004; Weisman et al., 2004), as has been also reported for water stress (Cresti et al., 1994). Separation of the phenolic compounds by HPLC analysis of the Koroneiki oil extract showed an increasing tendency for the second fraction of the secoiridoid derivatives with salinity levels (Stefanoudaki, 2004). Fatty acid composition of olive oil is also affected by salinity (Zarrouk et al., 1996). Palmitic acid, the major saturated fatty acid as well as the total saturated fatty acids increase with increasing salt concentration in the irrigation water. The ratio of unsaturated/saturated fatty acids is higher in the control and decreases significantly at moderate and high salinity levels (Zarrouk et al., 1996; Stefanoudaki, 2004; Weisman et al., 2004). In addition, the oleic/linoleic acid ratio decreases by increasing the salinity of water used for olive irrigation (Cresti et al., 1994; Stefanoudaki, 2004). These changes may be accounted for the accelerated fruit ripening (Marzouk et al., 1990). In contrast to the above reports, no changes in the fatty acid composition of the oil were found when trees were irrigated with brackish water for 12 years (Bouaziz, 1990).
4. Conclusions Although olive tree cultivation is expanding to many parts of the world during the last decades, its main production is concentrated in the Mediterranean region, where 97% of the world’s olive oil is produced (COI, 2003). Irrigation of olives with saline water will inevitably increase in the future in the Mediterranean due to negative effects of population growth and climate change on the availability and quality of existing fresh water supplies. As a consequence, the risk land salinisation will exacerbate threading the agricultural production particularly in countries with a semi-arid or arid climate. The salt tolerance on olive tree, like most glycophytes, is associated with the restriction of Na+ and/or Cl transport from the root to the shoot. This inclusion/exclusion trait for both Na+ and Cl is heritable (Sykes, 1992), suggesting that breeding and selection for Na+ and Cl excluding genotypes will continue to be a potentially rewarding area of research. Furthermore, attention should be given in the intra-cellular distribution of Na+ and Cl, (levels in the apoplast versus cytoplasm, vacuole), the possibility of ion recirculation as a factor in olive resistance (Na+ removal from the xylem and possible recirculation to the phloem) and the improved understanding of membrane transporter systems for Na+ and Cl. Understanding the mechanisms involved in salt-tolerance of olive tree is crucial to select salt tolerant genotypes or to engineer salt-sensitive genotypes with genetic traits inducing salt tolerance. The characterization of genes that contribute to salt tolerance and the underlying physiological processes could lead to the identification of specific physiological and biochemical markers for salt tolerance in olives. Using the gene transformation technologies for olives, the way is open to manipulate olive salt resistance by insertion of specific resistance genes.
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