Irrigation of Mediterranean crops with saline water: from physiology to management practices

Irrigation of Mediterranean crops with saline water: from physiology to management practices

Agriculture, Ecosystems and Environment 106 (2005) 171–187 Irrigation of Mediterranean crops with saline water: from phy...

349KB Sizes 7 Downloads 179 Views

Agriculture, Ecosystems and Environment 106 (2005) 171–187

Irrigation of Mediterranean crops with saline water: from physiology to management practices N.V. Paranychianakisa, K.S. Chartzoulakisb,* a

NAGREF, Institute for Agricultural Research, 71307 Iraklio, Crete, Greece NAGREF, Institute for Olives and Subtropical Plants, 73100 Chania, Crete, Greece


Abstract Salinity is currently one of the most severe abiotic factors limiting agricultural production. The high rates of population growth and global warming are expected to further exacerbate the threat of salinity, especially in areas with a semi-arid climate as in the Mediterranean region. Salinity affects plant performance through the development of osmotic stress and disruption of ion homeostasis, which in turn cause metabolic dysfunctions. Particular emphasis is given on the impacts of salinity on photosynthesis because of its potential restrictions on plant growth and yield. The inhibition of photosynthesis under low to moderate salinity stress appear to be mainly attributed to diffusional limitations (stomatal and mesophyll conductance), even for salt-sensitive fruit trees such as citrus trees. In contrast, biochemical limitations to photosynthesis appear to occur only when stress becomes heavy. A thorough understanding of the mechanisms conferring salt tolerance is therefore essential under the expected climatic change, as it will enable the selection of salt-tolerant genotypes and the adoption of appropriate practices to alleviate salinity impacts on agricultural production. In fruit trees, salt tolerance is mainly associated with their ability to restrict salt accumulation in the leaves. Cell features of specific tissues, morphological factors and water-use efficiency regulate salt accumulation in the shoot. Furthermore, most fruit trees display a rapid osmotic adjustment in response to salinity, which is mainly attributed to the accumulation of inorganic ions and carbohydrates. Little information is available about the ability of horticultural crops to detoxify reactive oxygen species and to synthesize compatible solutes and hence on the potential contribution of these mechanism to induce salt tolerance in horticultural crops. # 2004 Elsevier B.V. All rights reserved. Keywords: Climate change; Horticultural crops; Mechanisms of salt tolerance; Photosynthesis; Water resources

1. Introduction Water demand is increasing worldwide due to fast population growth rates, improvement in living * Corresponding author. Tel.: +30 821 97142; fax: +30 821 93963. E-mail address: [email protected] (K.S. Chartzoulakis).

standards, expansion of irrigation schemes and global warming (IPCC, 1996; UN Population Division, 1994). In regions affected by water scarcity such as the Mediterranean basin, water supplies are already degraded, or subjected to degradation processes, which worsen the shortage of water (Chartzoulakis et al., 2001; Attard et al., 1996). Reduced water supplies induce restrictions on

0167-8809/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2004.10.006


N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

water uses and allocation policies among different user sectors. In such regions, the competition for scarce water resources among users will inevitably reduce the supplies of freshwater available for crop irrigation. As a consequence, agriculture will increasingly be forced to utilize marginal waters such as brackish water or reclaimed effluent to meet its increasing demands, which in turn increases the risks of soil salinization and yield reduction. Accumulation of salts in root zone affects plant performance through the development of a water deficit and the disruption of ion homeostasis (Zhu, 2001; Munns, 2002). These stresses change hormonal status and impair basic metabolic processes (Loreto et al., 2003; Munns, 2002) resulting in inhibition of growth and reduction in yield (Maas, 1993; Prior et al., 1992; Paranychianakis et al., 2004a). Depressed photosynthesis has been suggested to be responsible for at least part of the growth and yield reduction (Prior et al., 1992; Munns, 2002). Despite the vast number of studies dealing with the impacts of salinity on photosynthesis of horticultural crops, most of them fail to quantify the nature of photosynthetic limitations. Stomatal closure, arising from the osmotic component of salinity, has been reported to be primarily responsible for photosynthesis inhibition in some studies (Paranychianakis et al., 2004b; Ban˜ uls and PrimoMillo, 1995). Reductions in mesophyll conductance due to salinity-induced anatomical changes in leaves have also been suggested to contribute in photosynthesis inhibition in citrus (Citrus sp.) (RomeroAranda et al., 1998), grapevines (Vitis vinifera) (Gibberd et al., 2003; Downton, 1977) and olive trees (Olea europea) (Bongi and Loreto, 1989; Loreto et al., 2003). Other studies have found strong correlations between salt accumulation, in particular Cl, and photosynthesis reduction (Lloyd et al., 1989; Walker et al., 1981; Chartzoulakis et al., 2002), implying that non-stomatal factors dominate in photosynthesis inhibition. In fact, such correlations do not represent cause–effect relationships, bringing into question the contribution of nonstomatal limitations. Identifying the nature of nonstomatal limitations of photosynthesis under stress conditions is currently an active area of photosynthesis research (Medrano et al., 2002; Centritto et al., 2003). Estimations based on the model of Farquhar

et al. (1980) suggest a reduction of Rubisco activity even at moderate salinity levels (Loreto et al., 2003; Rivelli et al., 2002), while in vitro assays show that reductions in Rubisco activity and content occur only under severe salt stress (Delfine et al., 1999). However, Centritto et al. (2003) showed that estimates of photosynthetic capacity based on A– Ci curves without removing diffusional limitations could lead to incorrect interpretations of the actual limitations of photosynthesis. In order to cope with salinity stress plants trigger a variety of mechanisms, which differentiate substantially among plant species or genotypes. These mechanisms operate in a coordinated manner both at a cellular and a whole-plant level. In horticultural crops, salt tolerance is associated with their ability to restrict salt accumulation in leaves (Mullins et al., 1996; White and Broadley, 2001). Damage in fruit trees is closely associated with Cl accumulation, thus genotypes with enhanced ability to restrict Cl entry into shoots generally show a higher tolerance (Antcliff et al., 1983; Ban˜ uls et al., 1997; Storey and Walker, 1999). Salt accumulation in shoot depends on cell features (Tester and Davenport, 2003), morphological factors (Moya et al., 1999), transpiration rate (Moya et al., 2003) and water-use efficiency (Gibberd et al., 2003). The most horticultural crops show a rapid osmotic adjustment in response to salinity which is attributed to inorganic ions and soluble carbohydrates (Walker et al., 1981; Gucci et al., 1997; Lloyd et al., 1990), while a limited number of studies deal with their ability to synthesize compatible solutes (Lloyd et al., 1990). Findings from annual crops show that genotypes with effective antioxidant systems show a superior performance in saline environments. However, relatively little information is available about the ability of horticultural crops to detoxify reactive oxygen species. Arbona et al. (2003) found that ‘Carrizo’ citrange, a salt-sensitive rootstock, possesses an efficient defense system against ROS generation. However, the change in salt tolerance of certain genotypes in different areas (Maas, 1993) and the inability of salt-tolerant cells to generate tolerant plants (Tester and Davenport, 2003) show that our knowledge for the factors induce salinity tolerance at a whole-plant level is incomplete.

N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

2. Salinity and climate change in Mediterranean region Soil salinization is one of the most severe causes of yield reduction in modern agriculture. On a worldwide basis, salinity has already affected approximately 80 million ha of arable land (Ghassemi et al., 1995) and still continues to increase (FAOSTAT, statistics database, Other estimates are considerably higher and indicate that up to 50% of all irrigated land may be salt-affected (Flowers, 1999). Irrigation with low-quality water and/or improper management practices are the principal causes of land salinization in the Mediterranean. 2.1. Current situation Even today many Mediterranean countries including Egypt, Libya, Tunisia, Algeria, Morocco, Syria, Malta and the Lebanon exhibit water availability below the threshold of 1000 m3/person/year (Table 1). In addition, lower availability than the benchmark of water scarcity is also observed in certain regions


within countries such as Spain, Greece and Italy, although on average they exceed the 1000 m3/person/ year threshold (UN Population Division, 1994). Pressure on the limited water resources in such areas is steadily increasing due to both increasing population and living standards. Furthermore, the water quality of existing groundwater is deteriorating due to its overexploitation, which favors sea intrusion into aquifers. Problems of sea intrusion are currently encountered in coastal areas of Italy, Spain, Greece and North Africa (Aru, 1996; Chartzoulakis et al., 2001). In order to overcome water scarcity many countries have adopted the use of marginal water and in particular, for irrigation (Oron et al., 2002). This coupled with their adverse climatic conditions make the Mediterranean region more vulnerable to salinization. In fact salinization in the Mediterranean basin is currently a serious problem. The salt-affected areas today amount to some 16 million ha or 25% of total irrigated land. However, detailed information about each country remains scarce. This situation may deteriorate in the future due to the effects of climate change on the precipitation, evaporation, runoff and soil moisture storage. As a consequence, the existing

Table 1 Population and freshwater availability for 1990, 2025 and 2050 in the Mediterranean countries (UN Population Division, 1994) Country

1990 Population (in thousands)

Albania Algeria Cyprus Egypt France Greece Israel Italy Jordan Lebanon Libya Malta Morocco Palestine Portugal Spain Syria Tunisia Turkey Yugoslavia

2025 Availability (m3/inh.year)

Population (in thousands)

2050 Availability (m3/inh.year)

Population (in thousands)

Availability (m3/inh.year)

3289 24935 702 56132 56718 10238 4660 57023 4259 2555 4545 354 24334

6385 690 1282 1046 3262 5763 461 3279 308 1949 1017 85 1151

4668 45475 927 97301 61247 9868 7808 52324 12039 4424 12885 422 40650

4499 378 971 605 3021 5979 275 3574 109 1126 359 71 689

5265 55674 1006 117398 60475 8591 8927 43630 16874 5189 19109 439 47858

3989 309 895 502 3059 6868 241 4286 78 960 242 68 585

9868 39272 12348 8080 56098 22945

6688 2826 2089 540 3619 11549

9685 37571 33505 13209 90937 24582

6815 2954 770 328 2232 10780

9140 31765 47212 15607 106284 24441

7221 3494 546 279 1910 10842


N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

problems of water scarcity and quality will worsen and countries in the southern and eastern Mediterranean will be most affected. 2.2. Mediterranean and climate change Various models have been developed to predict climate change (IPCC, 1996). They predict an increase in mean temperature, and changes in the amounts and patterns of precipitation. However, considerable uncertainty exists about the extent of these changes. Wingley (1992) predicted that a doubling of the CO2 concentrations over the Mediterranean region could cause warming of about 3.5 8C by the latter half of the 21st century. Based on the runs of different transient models, Rosenzweig and Tubiello (1997) estimated that the temperature will rise by 1.4–2.6 8C by 2020. It has also been predicted that by 2100 temperatures could have risen by up to 2.5–3 8C over the Mediterranean sea, 3–4 8C over coastal areas and 4–4.5 8C over inland areas reaching its maximum value, approximately 5.5 8C above Morocco (Cubasch et al., 1996). With regards to precipitation, the situation remains rather complicated. This is due to the inability of global circulation models to predict accurately regional rainfall (Palutikof and Wigley, 1996). However, there is a consensus that a decrease of precipitation will occur in the part of Mediterranean south of 40–458N and an increase in precipitation will occur north of it (IPCC, 1996). 2.3. Effects of climatic change on water resources availability and quality Higher temperatures and population growth will increase the demands for water in most Mediterranean countries. Moreover, higher rates of evaporation would cause rises in salt concentration in surface water bodies, while rises in sea level would favor sea intrusion into aquifers to coastal areas. It is estimated that 1 m rise in the sea level will reduce water in the main reservoir in Malta by 40% (Attard et al., 1996), while in France, the salinity in the Vaccares is expected to increase significantly (Corre, 1996). Problems of sea intrusion would be further exacerbated in response to higher demand.

Under these conditions, freshwater resources available for agriculture will decline quantitatively and qualitatively. Water demands for irrigation are projected to rise, bringing increased competition between agriculture and other users. Therefore, the use of lower-quality supplies will inevitably be practiced for irrigation purposes in order to maintain an economically viable agriculture. Many southern and eastern countries of the Mediterranean (Algeria, Cyprus, Morocco, Tunisia) have already experienced a long drought. In these countries, the growth and yield of crops were markedly reduced resulting in financial consequences to their national economies.

3. Plant response to salinity Salt accumulation in root zone causes the development of osmotic stress and disrupts cell ion homeostasis by inducing both the inhibition in uptake of essential nutrients as K+, Ca2+ and NO3 and the accumulation of toxic levels of Na+ and Cl. In addition, ROS can be generated (Zhu, 2001). These stresses cause hormonal changes (Munns, 2002), alter carbohydrate 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 and dysfunctions, cell division and elongation decline or it may be completely inhibited and cell death is accelerated. At a whole-plant level, the impacts of salinity are reflected through declines in growth, reductions in yield and, in more acute cases, leaf injuries are developed which can lead to the complete defoliation of plants and their subsequent desiccation. Munns (1993) suggested a two-phase model to explain the response of plant growth to salinity. During the first phase, growth reduction is ascribed to the development of a water deficit, which prevails immediately after the application of salinity treatments. The second phase is due to accumulation of salts in the shoot at toxic levels. This phase takes time to develop depending on the intensity of stress and plant tolerance to salinity. Under field conditions, however, plant response to salinity may appreciably deviate from this model. The gradual increase in soil salinity in that case may result in a concurrent occurrence of both osmotic and ionic effects of

N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

salinity. Furthermore, the composition of irrigation water and the salt tolerance of the crop may affect the contribution of each component in growth reduction. During irrigation with waters of a high ECw value but with relatively low concentrations of Na+ and Cl, the osmotic component will prevail over the ionic. In such cases, drought-tolerant species will display a better performance. In contrast, when water with high concentrations of Na+ and Cl is used for irrigation of salt-sensitive crops or genotypes, the ionic component will dominate. Although field studies did not enable us the possibility to distinguish between osmotic and ionic effects of salinity on performance of horticultural crops it is most probable that the osmotic component prevails in such conditions. Declines in growth rate of Soultanina grapevines, planted in large pots and grown under field conditions, were correlated with corresponding reductions in predawn leaf water potential (Cpd) (Fig. 1) indicating that osmotic effect of salinity was the main cause of growth reduction. Exposure of citrus genotypes to salinity treatments of different composition (40 mM Na+, Cl or NaCl) and

Fig. 1. Growth rate (A) and predawn leaf water potential variation (B) in vines irrigated with recycled water and freshwater during the 1998 growing season.


isotonic solution of nutrients showed that growth reduction was mainly due to the osmotic effect. In ‘Macrophylla’ however ionic effects were also detected (Ruiz et al., 1999). Generally, yield is reduced by salinity to a lesser extent than growth. Although some relationships have been established to describe the response of yield to salinity, based on single studies or the compilation of data from many studies (Maas and Hoffman, 1977; Maas, 1993; Shalhevet and Levy, 1990), yield losses often dramatically deviates from those predicted by models. Possible causes are differences in salt tolerance among genotypes or rootstocks, cumulative effects of salinity on plant performance over the years, soil type, environmental conditions and applied management practices.

4. Salt stress and photosynthesis 4.1. Photosynthesis and growth Whether decreased photosynthesis is the cause of growth reduction due to a lower availability of assimilates to growing sinks remains a matter of controversy (Munns, 2002). This may be due to: (a) an inability of single leaf photosynthesis to reflect net carbon gain at a whole-plant level, (b) a divergent response to salinity among plant species or genotypes and (c) differences in the length of exposure and the intensity of salt stress. In the sort-term hormonal signals arising from abscisic acid, biosynthesis appear to dominate in growth reduction over water deficit, ionic imbalances or decreased production of assimilates and that response appears to be uniform for both annual species and horticultural crops. This is supported by the greater sensitivity of growth reduction either to salt or water stress than photosynthesis (Paranychianakis, 2001). In the long-term, however, reduced availability of carbohydrates may contribute in growth reduction. Except the reductions in photosynthesis rate, salinityinduced leaf senescence and abscission and the inability of plants to produce new leaves may result in assimilates starvation. The growth of salt-stressed citrus recovered after the application of Ca2+ a response ascribed to ameliorative effects of Ca2+, on leaf abscission and hence, on the maintenance of


N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

assimilate utilization by growing tips. Gao et al. (1998) found reduced activity of the enzyme acid invertase in salt-stressed tomato plants, which may have inhibited growth through the limited sucrose utilization. In addition, assimilates’ accumulation in leaves of salt-stressed grapevines and olives (Walker et al., 1981; Downton and Loveys, 1981; Tattini et al., 1996) resulting either from impairments in carbohydrate metabolism or for osmotic adjustment may result in feedback repression on the Calvin cycle causing a further reduction in photosynthesis and hence in growth.

greater photosynthetic leaf area (Romero-Aranda et al., 1998). Reductions in net assimilation rate per unit of leaf area were strongly correlated with depressed growth implying that reduced production of assimilates has a significant role in growth inhibition under saline conditions (Lovelock and Ball, 2002). In addition, the lower starch content measured at the end of growing season in the tissues of grapevines irrigated with saline effluent (Table 2) further supports the hypothesis that inadequate supplies of assimilates contribute to growth reduction (Paranychianakis, 2001). Reduced supplies of starch in grapevines are also reported by Prior et al. (1992). This is especially crucial for horticultural crops since assimilates availability in old wood affects the following season growth and the potential for yield. More concrete evidence for the possible involvement of reduced assimilates on growth inhibition of salt-treated plants is provided by plants grown under elevated CO2 (Mavrogianopoulos et al., 1999; Maggio et al., 2002). The stimulation of growth of salt-stressed plants grown under a CO2 environment implies that salinityinduced reduction of photosynthesis reduces growth through its effects on assimilates production. It is not only net gain of carbon, but also the availability of assimilates to growing sinks that may affect its potential utilization for growth. Assimilates in salt-treated plants may be preferentially directed for osmotic adjustment, biosynthesis of compatible solutes, repair of the salinity-caused damage and the maintenance of basic metabolic processes at the expense of growth. Thus, despite the increases in leaf carbohydrates which is a common response of saltstressed plants (Gao et al., 1998; Walker et al., 1981), growth may eventually be limited due to the reduced availability of assimilates to growing sinks. Alterations in the activity of specific enzymes may reduce

4.2. Photosynthesis and salinity Reduction in photosynthesis of horticultural crops grown in saline environments can be attributed to reductions in stomatal or mesophyll conductance and biochemical limitations. The relative contribution of these limitations remains obscure and often contrasting. This may due to the technical constrains when assessing biochemical limitations, to difficulties to separate between the osmotic and ionic effects of salinity or to differences among species or genotypes. Thus, findings suggest either Na+ and/or Cl toxicities (Ban˜ uls and Primo-Millo, 1992; Fisarakis et al., 2001; Ban˜ uls et al., 1997; Lloyd et al., 1990) or stomatal closure (Paranychianakis et al., 2004b; Ban˜ uls and Primo-Millo, 1995) as the main causes of photosynthesis reduction on horticultural crops. 4.2.1. Stomatal limitations The strong correlations between leaf Cl and/or + Na content and photosynthesis rate as well as the maintenance of turgor in salt-stressed plants have led in the conclusion that biochemical limitations dominate in the reduction of photosynthesis in saltstressed fruit trees. However, these correlations do not

Table 2 The effects of water quality on root, trunk and stems content of soluble carbohydrates and starch (adapted from Paranychianakis, 2001) Organs

Carbohydrates (% dw)

Starch (% dw)

Recycled water


Recycled water


Roots (<2 mm) Roots (>2 mm) Trunk Stems

2.13 1.68 2.24 2.67 b

1.86 1.66 2.26 2.99 a

9.93 8.16 6.50 5.41

11.43 9.98 6.82 5.93

b b b b

Any two means not followed by the same letter are significantly different at P < 0.05 with Tukey’s significant difference.

a a a a

N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187


reduction. Likewise, leaf gas exchange of citrus was not affected by foliar application of NaCl even until leaf burns began to develop (Romero-Aranda and Syvertsen, 1996).

Fig. 2. Relationship between photosynthesis (Pn) and predawn leaf water potential for grapevines irrigated with recycled water (open circles) and freshwater (filled squares) (adapted from Paranychianakis et al., 2004b).

represent cause–effect relationships. In addition, it is now widely accepted that stomatal closure is not due to turgor loss, but it is a highly regulated response to salinity (Munns, 1993). Abscisic acid biosynthesis and its transfer to shoots, and the accumulation of carbohydrates, K+, Ca2+ and Cl in guard cells are involved in stomatal closure (Robinson et al., 1997; Talbott and Zeiger, 1998). The same relationships between Cpd and gas exchange found for salt-stressed and non-stressed grapevines imply that decreased photosynthesis is attributed to stomatal closure arising from the osmotic component of salinity (Fig. 2) (Paranychianakis et al., 2004b). A significant correlation between stomatal conductance and leaf water potential in salt-treated citrus was also reported by Ban˜ uls and Primo-Millo (1995). Based on the lack of significant effect of salinity on midday leaf water potential (Cmd), Walker et al. (1997) attributed the decline of photosynthesis rather to an ion imbalance than to Cl toxicity or to water deficit development. However, Cmd is not as reliable a parameter as Cpd for assessing plant water status and it is consistent with the absence of any significant effect of salinity on Cmd of grapevines despite the significant reduction on Cpd (Paranychianakis et al., 2004b). The rapid recovery of photosynthesis after the relief of salt stress despite leaf salt content remaining unchanged or even slightly increasing (Walker et al., 1981; Fisarakis et al., 2001; Tattini et al., 1995) provides further evidence that stomatal limitations dominate in photosynthesis

4.2.2. Mesophyll limitations Both water and salt stress may cause changes in leaf anatomy, which in turn can reduce the diffusion of CO2 to chloroplasts. Decreases in mesophyll conductance of salt-stressed fruit trees resulting from increases in leaf thickness, reductions in intercellular air spaces and the lower volume/area ratio of cells have been associated with decreased photosynthesis (Bongi and Loreto, 1989; Downton, 1977; RomeroAranda et al., 1998). These anatomical changes appear to be genotype-dependent (Romero-Aranda et al., 1998; Loreto et al., 2003). A recent study on olive trees revealed that the sensitivity of photosynthesis to salts was higher for cultivars with inherently higher rates of photosynthesis (Loreto et al., 2003). This effect cannot be explained either by the observed reduction of photochemical efficiency or by changes in Rubisco activity of salt-stressed leaves. The strong relationship between photosynthesis and mesophyll conductance or high CO2 drawn-down (Fig. 3), found both in cultivars with inherently low photosynthesis and in salt-stressed plants of all cultivars, suggests that the low CO2 chloroplast concentration is the limiting factor of photosynthesis in olive trees. These findings

Fig. 3. Relationship between photosynthesis and CO2 draw-down from ambient (Ca) to the chloroplast (Cc) concentration (adapted from Loreto et al., 2003). Different symbols represent different olive cultivars.


N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

indicate that salinity impacts on photosynthesis can be reversed if the conductance to CO2 diffusion is restored. This observation is of great importance with respect to climate change. In fact, these results predict a better performance for salt-stressed plants in a CO2rich world. 4.2.3. Biochemical limitations Photosynthesis versus Ci curves have been widely used to separate the biochemical from stomatal limitations of photosynthesis. These curves often show a decrease in apparent carboxylation efficiency and hence on Rubisco activity even at moderate salinity levels (Rivelli et al., 2002; Loreto et al., 2003). However, such effects may due to technical constraints as was recently shown in leaves of salt-treated olive trees (Centritto et al., 2003). In that study the preconditioning of salt-treated leaves to very low CO2 to force the opening of stomata removed limitations that implied biochemical impairment of photosynthesis. These findings are in agreement with those of in vitro assays which indicate that Rubisco content and activity remain unchanged at moderate salinity levels (Walker et al., 1981; Delfine et al., 1999). Likewise, Medrano et al. (2002) investigating the potential contribution of biochemical limitations to photosynthesis reduction in water-stressed plants found a similar relationship to that of Rubisco activity assessed in vitro and gs when Pn–Ci curves were converted to Pn–Cc and the apparent carboxylation efficiency was recalculated. In addition, Rubisco is maintained in excess in plant leaves since it may serve for N storage. Thus, slight reductions in Rubisco content may not limit photosynthetic capacity. Quick et al. (1991) found that photosynthesis was reduced only 6% when Rubisco was decreased by 60% in tobacco plants. The lower contents of Rubisco were compensated for by an increase in its activation (60–100%), increases in its substrates, and a decrease of its product. 4.3. Effects of salinity on photosynthesis under climate change The concentration of CO2 in the atmosphere is increasing and is expected to double by the end of the century. Plants grown under elevated CO2 environments show higher photosynthesis, reduced stomatal

conductance and improved water-use efficiency (Drake et al., 1997). Thus, the performance of horticultural crops grown under saline conditions may be improved. Little information is available for the performance of salt-stressed plants under conditions of elevated CO2. Mavrogianopoulos et al. (1999) reported that atmospheric CO2 concentrations of 800 and 1200 ppm stimulated photosynthesis in melons by 75 and 120%, respectively, in a range of salinity levels. In another study, enhanced rates of photosynthesis in response to a doubling of the atmospheric CO2 concentration were observed when plants exposed to salinity levels of 25% seawater (Ball et al., 1997). However, further increases in salinity level were not resulted in differences in photosynthesis between CO2-enriched and non-enriched plants implying that biochemical limitations may prevail at higher salinity levels. The increased rates of photosynthesis that are observed under increased concentrations of CO2 may be responsible for the better performance of salttreated tomato plants grown at 900 ppm compared to those at 400 ppm. Plants grown at elevated CO2 exhibited a 60% greater threshold value for salinity tolerance (Maggio et al., 2002). However, all the above studies concentrate on the effects of increased CO2 concentrations on plants grown in saline environments without taking into consideration the concurrent changes in temperature and the ozone effects that may appreciably change their performance. Thus, more information is needed to model the performance of salinity-suffering crops with respect to occurring climatic changes.

5. Mechanisms of salt tolerance To cope with salinity plants trigger divergent mechanisms that operate at a cellular and a whole-plant level allowing their adaptation and survival in saline environments. Differences in the mechanisms plants posses determine their performance under saline conditions. This review mainly focuses on the processes regulating tolerance at a whole-plant level such as salt uptake and transport to the shoot, but some information is also given for mechanisms operating at a cellular level such as osmoregulation, compartmentation of salts and ROS scavenging.

N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

5.1. Salt uptake and transport In fruit species salinity tolerance has been associated with their ability to restrict salts accumulation in the shoot and particularly Cl. Thus, leaf Cl content has been widely used as a criterion for rating genotypes according to their ability to tolerate salinity (Antcliff et al., 1983; Storey and Walker, 1999). The extent of salt accumulation in the shoot is determined by the processes regulating net uptake rate, loading to and reabsorption from the xylem, and preferential distribution in particular organs or tissues. 5.1.1. Salt net uptake Net accumulation of salts into root is the result of the balance between influx and efflux. These processes are mainly regulated by ion channels and transporters since the symplastic pathway appears to dominate for both Na+ and Cl entry (Tester and Davenport, 2003). 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). In fruit trees such carriers have not been identified yet, however, it can be inferred that differences among genotypes or rootstocks in the uptake and accumulation of salts (Chartzoulakis et al., 2002; Moya et al., 2003; Romero-Aranda et al., 1998; Walker et al., 1997) probably reflect differences in the expression, the abundance or the properties of these carriers. In addition, the rate of salt uptake by fruit trees is dependent on their concentration in soil solution (Moya et al., 2003; Storey, 1995) and morphological factors such as the size of root system and root to shoot ratio (Moya et al., 1999). 5.1.2. Root to shoot transport Another control of salt accumulation in the shoot can occur by minimizing salts’ efflux to the xylem or by maximizing their reabsorption from the xylem at the root or the stem. This means that parenchyma cells have completely different properties from root cortical cells since they need to maximize influx and minimize efflux (Tester and Davenport, 2003). The mechanisms,


which regulate the removal of salts from xylem sap are not fully understood. Differences in the xylem Na+ and Cl concentration assessed in citrus rootstocks (Zekri and Parsons, 1990; Walker et al., 1993b) may imply differences in the rates of salt loading to xylem or in the mechanisms they posses to reabsorb them back to xylem. The increased accumulation of salts in leaves of Etrog citron rootstock with increasing transpiration in contrast to Rangpur lime rootstock in which salt accumulation was not affected by transpiration rate (Storey, 1995) may also imply differences in these mechanisms among these rootstocks. The results of this study also reveals the existence of a feedback regulation of Cl transport to shoot for Rangpur lime rootstock which is probably modulated by leaf Cl content. Similarly, Elgazzar et al. (1965) found that the shoot of Trifoliate orange was more effective to restrict the transport of 22Na+ to leaves compared to the Rough lemon. Furthermore, the ability of citrus to reabsorb Na+ is highly depended on salt concentration of the xylem sap (Elgazzar et al., 1965). Preferential accumulation of both Na+ and Cl in the root has been often associated with lower salt accumulation in the shoot. However, recent studies question the contribution of this mechanism to induce salt tolerance in the long-term or at high salinity levels. Irrigation of grapevines with saline effluent did not result in differences in Na+ accumulation in roots (Fig. 4) at the end of the season compared to freshwater-irrigated vines, while only slight differences were assessed in the case of Cl. Significant differences among citrus rootstocks to sequester salts in roots were found only when irrigated with 30 and 60 mM NaCl, but these differences were eliminated when salinity treatment increased to 90 mM NaCl (Garcia-Sanchez et al., 2002). Similar results were reported for olive trees by Chartzoulakis et al. (2002). These studies indicate that sequestration of salts in root can prevent salinity stress only at low salinity levels or in the short-term. Apart from differences in cell properties of different tissues to control salt uptake and translocation in the shoot, morphological factors may also exert an important role. Moya et al. (1999) found that manipulation of the root to shoot ratio by applying root pruning and defoliation affected Cl accumulation in the shoot. Increases in the root to shoot ratio and


N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

Fig. 4. Na+ distribution in the different organs of grapevines irrigated with recycled (open bars, EC: 1.9 dS/m, Na+: 264 mg/l, Cl: 436 mg/l) vs. freshwater (solid bars, EC: 0.6 dS/m, Na+: 72 mg/l, Cl: 118 mg/l) (adapted from Paranychianakis, 2001). Bars without letters imply nonsignificant differences.

reductions in leaf biomass favored Cl accumulation in the shoot. 5.1.3. Distribution of salts within shoot Preferential allocation of both Na+ and Cl in old leaves is crucial for salinity tolerance in glycophytes. This may due to the rapid growth rates of young leaves and the low transpiration rate. It is also possible that salts are preferentially removed from sap moving to actively growing organs (Tester and Davenport, 2003). Marschner (1995) reported that 22Na+ which moved out from source leaf did not reach into growing regions of the roots or the shoot. It should be stressed, however, that genotype and the intensity or the duration of stress could substantially alter the pattern of salts distribution within the shoot. Vines grafted on 41B rootstock showed a preferential accumulation of Na+ to old leaves independent of salt availability, while vines grafted on 1103P and 110R did not show any differentiation in the allocation of Na+ with leaf age (Fig. 4) (Paranychianakis, unpublished data). In the same study Cl distribution with leaf age did not change in leaves of vines irrigated with saline effluent in contrast to those irrigated with freshwater (Fig. 5) implying that there is a threshold content for leaves to sequester Cl. After this threshold concentration is

exceeded Cl is translocated uniformly in the younger leaves. Moreover, salt distribution may change within a given leaf. Preferential accumulation of Na+ to leaf epidermical cells has been observed (Karley et al., 2000). Such an allocation pattern for Na+ is of paramount importance for maintaining photosynthetic efficiency of mesophyll cells.

Fig. 5. Distribution of Cl in leaves of different age according to its availability in irrigation water (adapted from Paranychianakis, 2001). Bars without letters imply non-significant differences.

N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

5.2. Intercellular compartmentation There is of substantial number of studies in the literature showing that neither Na+ nor Cl contents in leaves is related to salt tolerance. This lack of correlation probably results from differential ability of various plant species or genotypes to distribute salts within cell organelles. Sodium compartmentation into vacuole appears to constitute the most effective mechanism of plant cells to handle efficiently high concentrations of salts and to prevent their toxic effects on cytoplasm. Na+ compartmentation is regulated by Na+/H+ antiporters (Hasegawa et al., 2000). The overexpression of genes encoding Na+/H+ antiporters in different plant species induced the tolerance of plants to salinity. Zhang and Blumwald (2001) reported that tomato plants (Lycopersicum solanum) overexpressing an Arabidopsis vacuolar Na+/H+ antiporter were able to grow and produce fruits even at concentrations of 200 mM NaCl. Leaf Na+ and Cl contents reached values of 20-fold to those of wild-type plants. 5.3. Osmotic adjustment Accumulation of solutes is a universal response of stressed plants grown. Enhanced levels of osmolytes in certain taxonomic groups such as xerophytes and halophytes, known for their outstanding ability to withstand adverse environmental conditions, imply their crucial role in plant adaptation and survival in water-deficient environments. Accumulation of solutes results in osmotic adjustment favoring water absorption and retention, which may maintain plant growth and photosynthesis. Most horticultural crops display a rapid osmotic adjustment in response to salinity, which is ascribed mainly to ions and/or carbohydrates accumulation (Downton and Loveys, 1981; Lloyd et al., 1990; Ban˜ uls and Primo-Millo, 1992; Gucci et al., 1997). Relative little information is available for the ability of these species to accumulate compatible solutes. Compatible solutes apart from their contribution in osmotic adjustment may have a protective role in protein structure and photosynthesis. They probably act as osmoprotectants and ROS scavengers. Engineering plant species with genes inducing the biosynthesis of compatible solutes such as D-ononitol or sorbitol has been


associated with higher rates of photosynthesis (Sheveleva et al., 1997; Gao et al., 2001). Citrus accumulate mainly proline and proline betaine and it is dependent on genotype (Lloyd et al., 1990; Ban˜ uls and Primo-Millo, 1992; Walker et al., 1993a, 1993b), however, the contribution of these solutes in conferring salt tolerance and photosynthesis of citrus remains questionable (Lloyd et al., 1989). Apparently, more research should be conducted on this field to elucidate the role of compatible solutes in conferring salt tolerance in horticultural crops. 5.4. Reactive oxygen species scavenging The generation of ROS in salt-stressed plants is mainly induced from pathways alternative to photosynthesis and photorespiration, from photosynthetic apparatus and from mitochondrial respiration and may result in peroxidation of membrane lipids, oxidation of proteins and disruption of PSII (Mittler, 2002; Zhu, 2001; Nishiyama et al., 2001). Thus, plants with more effective antioxidant systems will display a superior performance in saline environments. Little information is available about the extent that ROS may contribute to salinityinduced damage in horticultural crops. Differences in the salt tolerance between two mulberry genotypes (Morrus alba L.) were associated with differences in the activity of enzymes involved in ROS detoxification (Subhakar et al., 2001). ‘Carrizo’ citrange, sensitive to salinity rootstock, responded to salt-induced oxidative stress by increasing enzymatic and non-enzymatic antioxidant defense proportionally to the intensity of stress resulting in low levels of malondialdehyde content (Arbona et al., 2003).

6. Management practices In order to mitigate the impacts of the use of lowquality waters on the productivity of agricultural crops, intense management practices should be adopted. These practices can be separated into three distinct categories: (a) irrigation management strategies, (b) plant cultural practices and (c) the selection of salt-tolerant genotypes.


N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

6.1. Irrigation practices Irrigation management practices aim for the efficient use of saline water. This can be achieved by maintaining salt accumulation in the root zone at levels lower than the threshold values. Above these values, a reduction of yield is observed. Such practices are: (a) proper irrigation scheduling, (b) efficient leaching of salts, (c) selection of irrigation method and (d) establishing artificial drainage. 6.1.1. Irrigation scheduling The term ‘irrigation scheduling’ includes both the estimation of the irrigation requirements of the given crop and the application of the appropriate irrigation intervals. The establishment of an appropriate irrigation schedule under saline water irrigation is much more complicated than when freshwater is applied, due to limited or completely absent information on the wateruse of salt-stressed plants. Critical questions that arise are if the salinity changes the consumptive use of irrigated plants and what are the leaching requirements (LR) that should be included in the crop water demands for waters of variable quality. Successful irrigation with low-quality water requires relationships that relate yield to water consumption. To establish such relationships, two different approaches can be used. Field experimentation, which is an expensive and timeconsuming procedure, or the use of mathematical models to describe the soil-water–crop system. Plant growth response under saline irrigation is a function of the salts’ concentration in soil solution, in particular Na+ and Cl, and the matrix potential of the soil. Thus, maintaining adequate soil-water availability is essential to restrict the damage of salt accumulation. This can be achieved by increasing irrigation frequency. After irrigation, soil moisture content is high and the salt concentration or osmotic pressure of the soil solution approaches their minimal values. 6.1.2. Irrigation method Irrigation method applied for saline irrigation may have a great influence on salt accumulation and distribution in the soil profile and hence on crop production. Sprinkler irrigation with saline water may cause injury if applied to plants with high rates of foliar salt absorption, and the injury risk is greater if

irrigation is practiced during the daytime when the evaporation rate is high. Trickle or drip irrigation is recommended as it keeps the soil moisture continuously high at the root zone, maintaining a low salt concentration level. Common problems associated with drip irrigation are the need to remove the accumulating salts from the wetting front and the avoidance of drippers clogging. The use of subsurface drip irrigation (SDI) appears to be an ideal method for irrigation with saline water. Irrigation of pears (Prunus sp.) with saline water (ECw = 4.4 dS/m) through SDI increased yield compared to surface drip irrigation (Oron et al., 2002). In addition, the depth that emitters are located appears to be a critical parameter since it affects salt distribution in the root zone and therefore the intensity of stress. 6.1.3. Leaching requirements The amount of water (in terms of a fraction of the applied water) that must be applied in excess to the crop in order to control salts is referred to as ‘leaching requirements’ (LR) and can be calculated, for drip irrigation, from the following formula (Ayers and Westcot, 1985): LR ¼

ECw 5ECe  ECw


where ECw is the electrical conductivity (dS/m) of the irrigation water and ECe the electrical conductivity (dS/m) of the saturation extract. ECe is the average soil salinity tolerated by the crop. Depending on the crop and the salinity of the water and soil, a 15–20% leaching fraction is commonly recommended. 6.1.4. Establishing artificial drainage When saline water is used for irrigation, existing drainage problems greatly complicate water management for salinity control. Temporary or permanent high water tables (1.5 m or less) make the control of salts difficult since their leaching is ineffective. A more effective way for controlling the salinity problems associated with a high water table is to establish artificial drainage. 6.2. Cultural practices Cultural practices may dramatically improve the performance of crops grown in saline environments. In

N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

this section, emphasis is given to practices such as the application of water or soil amendments, improved fertilization schedule and other miscellaneous practices. 6.2.1. Water or soil amendments Soil permeability problems can be prevented or corrected by using soil or water amendments. Improved soil permeability can be achieved if either the sodium in the irrigation water is lowered or the calcium and magnesium concentration will increase. However, at present there are no economically viable processes for removing salts from irrigation water. Chemicals can be added to the soil or irrigation water to increase calcium concentration and to improve the sodium/calcium ratio. Gypsum, sulfur or sulfuric acid are the most commonly used soil amendments, while gypsum, sulfuric acid and sulfur dioxide are used as water amendments. Rates of gypsum application to soil commonly range from 2 to 20 ton/ha, but amounts as high as 40 ton/ha can be used in areas with extremely high sodium content. Mulching may also be beneficial on saline soils since it reduces evaporation from the soil surface and/or encourages downward flux of soil water. 6.2.2. Improved fertilization schedule Inhibition of the uptake of essential nutrients by salinity may result in severe reductions in yield, depending on plant species. Supplemental fertilization, particularly of K+, Ca2+, NO3 and in some cases micronutrients, lead to a recovery of physiological parameters and stimulates growth (Cramer and Nowak, 1992; Marschner, 1995; Zhu, 2001). In addition, application of K+ and Ca2+ may also improve plant performance by reducing the uptake of salts (Romero-Aranda et al., 1998).


6.2.3. Miscellaneous practices The introduction of arbuscular mycorrhizae has been found to improve the performance of plants grown in saline environments (Ruiz-Lozano et al., 1996). The beneficial effects of arbuscular mycorrhizae are associated with improved nutrition and better water absorption (Ruiz-Lozano and Azco´ n, 1995). The better performance of salt-treated Lactuca sativa plants inoculated with arbuscular mycorrhizae was associated with increased photosynthesis and water-use efficiency (Ruiz-Lozano et al., 1996). Other techniques, like the foliar application of polyamines or glycine betaine, appear also to provide promising results for their commercial application in the future to improve the performance of salt-stressed plants. 6.3. Salt tolerance of different plant species and genotypes The selection of plant-tolerant plant species or genotypes is a common practice to reduced losses of yield under saline conditions. Threshold values of salinity tolerance for citrus, grapevines and olive trees are given in Table 3. Declines in water quality below the threshold values reported in Table 3 do not preclude their potential use for irrigation of the considered crops, however the adoption of both intense management practices and the use of salttolerant genotypes is recommended to maintain crop productivity in acceptable levels and to ensure land sustainability. It should be stressed, however, that the threshold values reported in Table 3 is indicative since they may considerably vary among different cultivars or rootstocks (Antcliff et al., 1983; Storey and Walker, 1999; Chartzoulakis et al., 2002). A classification of various genotypes of citrus, grapevines and olives is shown in Table 4 based on published studies.

Table 3 Potential use of such resources for citrus, grapevines and olive trees irrigation Water classification

TDS (ppm)

EC (dS/m)


Threshold EC (dS/m)

Freshwater Slightly brackish Brackish Moderately saline Saline Highly saline

<500 500–1000 1000–2000 2000–5000 5000–10000 10000–35000

<0.6 0.6–1.5 1.5–3.0 3.0–8.0 8.0–15.0 15.0–45.0

Citrus Grapevines Olives

1.1–1.4 1.4–3.0 1.8–2.5


N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

Table 4 Salt tolerance rating of various cultivars and rootstocks of citrus, grapevines and olives Tolerant genotypes Citrus Grapevines Olives

Sunki mandarin, Cleopatra mandarin, Rangpur lime Ramsey, Dogridge, French Colombard Picual, Canivano, Jabaluna, Nevadillo, Ardequina, Frantoio, Kalamata, Lianolia Kerkiras, Megaritiki, Korthreiki

Moderately tolerant genotypes Citrus Sampson tangelo, Rough lemon, Sour orange, Ponkan mandarin Grapevines 110R, 1103P, 140R, Chenin Blanc, Grenache, Soultanina Olives Chorruo, Changlot Real, Verdial de velez, Gordal Sevillana, Oblonga, Blanqueta, Alameno, Manzanillo, Redondil, Hojiblanca, Canivano Negro, Zorzariega, Picudo, Coratina, Maraiolo, Maurino, Koroneiki, Mastoidis, Amphisis, Valanolia, Adramitini Sensitive genotypes Citrus Grapevines Olives

Troyer citrange, Trifoliate orange, Rusk citrange, Sweet orange 41B, SO4, Muscat of Alexandria, Barbera, Ribier Pajarero, Chetoui, Calego, Cobancosa, Meski, Leccino, Throumbolia, Chondrolia Chalkidikis, Agouromanaki

Salt tolerance in each category is comparative for the given crop and does not imply similar salt tolerance among the different crops.

Furthermore, in woody plants salt tolerance of a given genotype can display significant variations from one area to another. Such variations have been reported for citrus (Maas, 1993) and grapevines (Downton, 1977; Antcliff et al., 1983; Arbabzadeh and Dutt, 1987). Causes responsible for this variation are differences in environmental factors (soil fertility, soil physical conditions and climatic factors) which are met from one region to another and plant genetic diversity.

7. Conclusions and future research needs Population growth and global warming will substantially impact the availability and quality of existing freshwater supplies. As a consequence, the risk of land salinization will further threaten agricultural production, particularly in areas with a semiarid or arid climate. However, more detailed studies are needed to quantify the temporal and spatial effects of climate change on water resources. Such information is of paramount importance to adopt appropriate management practices to minimize the salinization of agricultural land and the impacts of salinity on crops’ productivity. Decreased photosynthesis may represent a serious constrain for current’s season growth and yield. In addition, the lower amounts of assimilates in permanent organs of perennial plants may be

responsible for the progressive decline in their performance and their reduced fertility. Diffusional limitations appear to dominate in photosynthesis reduction at low to moderate salinity levels even for plant species sensitive to salinity. This implies that the performance of salt-stressed plants will be improved from the expected increase in CO2 concentration. However, results of plants growing under elevated CO2 environments are limited and often confusing. The situation becomes even more complex if we take into account the concurrent increase in temperature and the reductions in the availability of water resources and nutrients. Since global warming is expected to increase the salt-affected land, the need for a thorough understanding of the mechanisms determining salt tolerance in plants becomes more crucial in order to maintain agricultural production within economically viable levels. Despite the exciting progress, which has been performed the last decade in terms of the identification of genes inducing salinity tolerance, signaling and biochemical adjustments as well as the mechanisms operating at a whole-plant level, our knowledge is incomplete. This is confirmed by the differential response to salinity of a given genotype in different areas and by the inability of salt-tolerant cells to generate tolerant plants. Therefore, a better understanding of the interactions among genetic traits, climatic conditions and management practices is required.

N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

References Antcliff, A.J., Newman, H.P., Barret, H.C., 1983. Variation in chloride accumulation in some American species of grapevine. Vitis 22, 357–362. Arbabzadeh, F., Dutt, G., 1987. Salt tolerance of grape rootstocks, under greenhouse conditions. Am. J. Enol. Vitic. 38, 95–101. Arbona, V., Flors, V., Jacas, J., Garcia-Agustin, P., Gomez-Gadenas, A., 2003. Enzymatic and non-enzymatic antioxidant responses of Carrizo citrange, a salt sensitive Citrus rootstock, to different levels of salinity. Plant Cell Physiol. 44, 388–394. Aru, A., 1996. The Rio Santa Lucia site: an integrated study of desertification. In: Brandt, C.J., Thornes, J.B. (Eds.), Mediterranean Desertification and Land Use. Wiley, Chichester, UK, pp. 189–206. Attard, D.J., Axiak, V., Borg, S., Cachia, J., de Bono, G., Lanfranco, E., Micallef, R.E., Mifsud, J., 1996. Implications of expected climatic changes for Malta. In: Jeftic, L., Keckes, S., Pernetta, J. (Eds.), Climate Change and the Mediterranean, vol. 2. Arnold, UK, pp. 322–430. Ayers, R.S., Westcot, D.W., 1985. Irrigation water quality. In: Pettygrove, G.S., Asano, T. (Eds.), Irrigation with Reclaimed Municipal Wastewater – A Guidance Manual. Lewis Publishers. Ball, M.C., Cochrane, M.J., Rawson, H.M., 1997. Growth and water use of the mangroves Rhizophora apiculata and R. stylosa in response to salinity and humidity under ambient and elevated concentrations of atmospheric CO2. Plant Cell Environ. 20, 1158–1166. Ban˜ uls, 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. Ban˜ uls, J., Primo-Millo, E., 1995. Effects of salinity on some Citrus scion-rootstock combinations. Ann. Bot. 76, 97–102. Ban˜ uls, J., Serna, M.D., Legaz, F., Talon, M., Primo-Millo, E., 1997. Growth and gas exchange parameters of Citrus plants stressed with different salts. J. Plant Physiol. 150, 194–199. Blumwald, E., Aharon, G.S., Apse, M.P., 2000. Sodium transport in plants. Biochim. Biophys. Acta 1465, 140–151. Bongi, G., Loreto, F., 1989. Gas exchange properties of salt-stressed olive (Olea europaea L.) leaves. Plant Physiol. 90, 1408–1416. Centritto, M., Loreto, F., Chartzoulakis, K., 2003. The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings. Plant Cell Environ. 26, 585–594. Chartzoulakis, K., Loupassaki, M., Bertaki, M., Androulakis, I., 2002. Effects of NaCl salinity on growth, ion content and CO2 assimilation rate of six olive cultivars. Sci. Hortic. 96, 235–247. Chartzoulakis, K.S., Paranychianakis, N.V., Angelakis, A.N., 2001. Water resources management in the island of Crete, Greece with emphasis on the agricultural use. Water Policy 3, 193–205. Corre, J.J., 1996. Implications des changements climatiques etude de cas:Le Golfe du Lion (France). In: Jeftic, L., Milliman, J.D., Sestini, G. (Eds.), Climatic Change and the Mediterranean. Edward Arnold, London, pp. 328–427. Cramer, G.R., Nowak, R.S., 1992. Supplemental manganese improves the relative growth, net assimilation and photosynthetic rates of salt-stressed barley. Physiol. Plant. 84, 600–605.


Cubasch, U., von Storch, H., Waszkewitz, J., Zorita, E., 1996. Estimates of climate change in southern Europe derived from dynamical climate model output. Clim. Res. 7, 129– 149. Delfine, S., Alvino, A., Villani, M.C., Loreto, F., 1999. Restrictions to CO2 conductance and photosynthesis in spinach leaves recovering from salt stress. Plant Physiol. 119, 1101–1106. Downton, W.J.S., 1977. Photosynthesis in salt stressed grapevines. Aust. J. Plant Physiol. 4, 183–192. Downton, W.J.S., Loveys, B.R., 1981. Abscisic acid content and osmotic relations of salt-stressed grapevine leaves. Aust. J. Plant Physiol. 8, 443–448. Drake, A.M., Gonzalez-Meler, M., Long, S.P., 1997. More efficient plants: a consequence of rising atmospheric CO2. Annu. Rev. Plant Physiol. Mol. Biol. 48, 607–637. Elgazzar, A., Wallace, A., Hemaidan, N., 1965. Sodium distribution in rough lemon and trifoliate orange seedlings. Soil Sci. 99, 387– 391. Farquhar, G.D., von Caemmerer, S., Berry, J.A., 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90. Fisarakis, I., Chartzoulakis, K., Stavrakas, D., 2001. Response of Sultana vines (V. vinifera L.) on six rootstocks to NaCl salinity exposure and recovery. Agric. Water Manage. 51, 13– 27. Flowers, T.J., 1999. Salinisation and horticultural production. Sci. Hortic. 78, 1–4. 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. Gao, M., Tao, R., Miura, K., Dandekar, A.M., Sugiura, A., 2001. Transformation of Japanese persimmon (Diospyros kaki Thunb.) with apple cDNA encoding NADP-dependent sorbitol-6-phosphate dehydrogenase. Plant Sci. 160, 837–845. Garcia-Sanchez, F., Jifon, J.L., Carvajal, M., Syvertsen, J.P., 2002. Gas exchange, chlorophyll, nutrient contents in relation to Na+ and Cl accumulation in Sunburst mandarin grafted in different rootstocks. Plant Sci. 162, 705–712. Ghassemi, F., Jakeman, A.J., Nix, H.A., 1995. Salinization of Land and Water Resources: Human Causes, Extent Management and Case Studies. UNSW Press/CAB International, Sydney, Australia/Wallingford, UK. Gibberd, M.R., Walker, R.R., Condon, G.A., 2003. Whole-plant transpiration efficiency of Sultana grapevine grown under saline conditions is increased through the use of Cl-excluding rootstock. Funct. Plant Biol. 30, 643–652. Gucci, R., Lombardini, L., Tattini, M., 1997. Analysis of leaf water relations in leaves of two olive (Olea europea) cultivars differing in tolerance to salinity. Tree Physiol. 17, 13–21. 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. IPCC, 1996. Houghton, J.T., Meira Filho, L.B., Callander, B.A., Harris, N., Kattenberg, A., Maskell, K. (Eds.), Climate Change 1995: The Science of Climate Change. Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge.


N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187

Karley, A.J., Leigh, R.A., Sanders, D., 2000. Differential ion accumulation and ion fluxes in the mesophyll and epidermis of barley. Plant Physiol. 122, 835–844. Lloyd, J., Kriedemann, P.E., Aspinall, D., 1989. Comparative sensitivity of Prior Lisbon lemon and Valencia orange trees to foliar sodium and chloride concentrations. Plant Cell Environ. 12, 529–540. Lloyd, J., Kriedemann, P.E., Aspinall, D., 1990. Contrasts between Citrus species in response to salinisation: an analysis of photosynthesis and water relations for different rootstock scion combinations. Physiol. Plant. 78, 236–246. Loreto, F., Centritto, M., Chartzoulakis, K., 2003. Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant Cell Environ. 26, 595–601. Lovelock, C.E., Ball, M.C., 2002. Influence of salinity on photosynthesis of halophytes. In: Lauchli, A., Lutge, U. (Eds.), Salinity: Environment–Plants–Molecules. Kluwer Academic Publishers, pp. 315–340. Maas, E.V., 1993. Salinity and citriculture. Tree Physiol. 12, 195– 216. Maas, E.V., Hoffman, G.J., 1977. Crop salt tolerance: current assessment. J. Irrig. Drain. Div. 103, 115–134. Maggio, A., Dalton, F.N., Piccinni, G., 2002. The effects of elevated carbon dioxide on static and dynamic indices for tomato salt tolerance. Eur. J. Agron. 16, 197–206. Marschner, H., 1995. Mineral Nutrition of Higher Plants, 2nd ed. Academic Press, London. Mavrogianopoulos, G.N., Spanakis, J., Tsikalas, P., 1999. Effect of carbon dioxide enrichment and salinity on photosynthesis and yield in melon. Sci. Hortic. 79, 51–63. Medrano, H., Escalona, J.M., Bota, J., Gulias, J., Flexas, J., 2002. Regulation of photosynthesis to progressive drought: stomatal conductance as a reference parameter. Ann. Bot. 89, 895– 905. Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405–410. Moya, J.L., Go´ mez-Cadenas, A., Primo-Millo, E., Talon, M., 2003. Chloride absorption in salt-sensitive Carrizo citrange and salttolerant Cleopatra mandarin citrus rootstocks is linked to water use. J. Exp. Bot. 54, 825–833. Moya, J.L., Primo-Millo, E., Talon, M., 1999. Morphological factors determining salt tolerance in citrus seedlings: the shoot to root ratio modulates passive root uptake of chloride ions and their accumulation in leaves. Plant Cell Environ. 22, 1425– 1433. Mullins, M.G., Bouquet, A., Williams, L.E., 1996. Biology of Grapevine, 3rd ed. Press Syndicate of the University of Cambridge, Cambridge, p. 239. 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. Nishiyama, Y., Yamamoto, H., Allakhverdiev, S.I., Inaba, M., Yokota, A., Murata, N., 2001. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J. 20, 5587–5594.

Oron, G., DeMalach, Y., Gillerman, L., David, I., Lurie, S., 2002. Effect of water salinity and irrigation technology on yield and quality of pears. Biosyst. Eng. 81, 237–247. Palutikof, J.P., Wigley, T.M.L., 1996. Developing climate change scenarios for the Mediterranean region. In: Jeftic, L., Keckes, S., Pernetta, J.C. (Eds.), Climatic Change and the Mediterranean, vol. 2. Edward Arnold, London, pp. 27– 55. Paranychianakis, N.V., 2001. Influence of rootstock, irrigation level and recycled water on the growth, nutrition and physiology of Soultanina grapevines. Ph.D. Thesis. Agricultural University of Athens, pp. 202. Paranychianakis, N.V., Aggelides, S., Angelakis, A.N., 2004a. Influence of rootstock, irrigation level and recycled water on the growth and yield of Soultanina grapevines. Agric. Water Manage. 69, 13–27. Paranychianakis, N.V., Chartzoulakis, K.S., Angelakis, A.N., 2004b. Influence of rootstock, irrigation level and recycled water on water relations and gas exchange of Soultanina grapevines. Environ. Exp. Bot. 52, 185–198. Prior, L.D., Grieve, A.M., Slavish, P.G., Gullis, P.R., 1992. Sodium chloride and soil texture interactions in irrigated field grown Sultana grapevines. II. Plant mineral content, growth and physiology. Aust. J. Agric. Res. 43, 1067–1084. Quick, W.P., Schurr, U., Scheibe, R., Schultze, E.D., Rodermel, S.R., Bogorad, L., Stitt, M., 1991. Decreased ribulose-1,5-biphosphate carboxylase-oxygenase in transgenic tobacco transformed with antisense rdcS: impacts on photosynthesis in ambient growth conditions. Planta 183, 542–554. Rivelli, A.R., Lovelli, S., Perniola, M., 2002. Effects of salinity on gas exchange, water relations and growth of sunflower (Helianthus annuus). Funct. Plant Biol. 29, 1405–1415. Robinson, M.F., Viery, A.A., Sanders, D., Mansfiels, T.A., 1997. How can stomata contribute to salt tolerance. Ann. Bot. 80, 387– 393. Romero-Aranda, R., Moya, J.L., Tadeo, F.R., Legaz, F., PrimoMillo, E., Talon, M., 1998. Physiological and anatomical disturbances induced by chloride salts in sensitive and tolerant citrus: beneficial and detrimental effects of cations. Plant Cell Environ. 21, 1243–1253. Romero-Aranda, R., Syvertsen, J.P., 1996. The influence of foliar applied urea nitrogen and saline solutions on net gas exchange of Citrus leaves. J. Am. Soc. Hortic. Sci. 121, 501– 506. Rosenzweig, C., Tubiello, F.N., 1997. Impacts of global climate change on Mediterranean agriculture: current methodologies and future directions. An introductory essay. Mitigation Adaptation Strategies for Global Change 1, 219–232. Ruiz, D., Martinez, V., Cerda, A., 1999. Demarcating specific ion (NaCl, Cl, Na) and osmotic effects in the response of two citrus rootstocks to salinity. Sci. Hortic. 80, 213–224. Ruiz-Lozano, J.M., Azco´ n, R., 1995. Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol. Plant. 95, 472–478. Ruiz-Lozano, J.M., Azco´ n, R., Go´ mez, M., 1996. Alleviation of salt stress by arbuscular mycorrhizal Glomus species in Lactuca sativa plants. Physiol. Plant. 98, 767–772.

N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187 Shalhevet, J., Levy, Y., 1990. Citrus trees. In: Stewart, B.A., Nielsen, D.R. (Eds.), Irrigation of Agricultural Crops. American Society of Agronomy, Madison, WI, pp. 951–986. Sheveleva, E., Chmara, W., Bohnert, H.J., Jensen, R.G., 1997. Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L.. Plant Physiol. 115, 1211– 1219. Storey, R., 1995. Salt tolerance, ion relations and the effect of root medium on the response of citrus to salinity. Aust. J. Plant. Phys. 22, 101–114. Storey, R., Walker, R.R., 1999. Citrus and salinity. Sci. Hortic. 78, 39–81. Subhakar, C., Lakshmi, A., Giridarakumar, S., 2001. Changes in the antioxidant efficacy in two high yielding genotypes of mulberry (Morrus alba L.) under NaCl salinity. Plant Sci. 161, 613–619. Talbott, L.D., Zeiger, E., 1998. The role of sucrose in guard cell osmoregulation. J. Exp. Bot. 49, 329–337. Tattini, M., Gucci, R., Coradeschi, M.A., Ponzio, C., Everard, J.D., 1995. Growth, gas exchange and ion content in Olea europaea plants during salinity stress and subsequent relief. Physiol. Plant. 95, 203–210. Tattini, M., Gucci, R., Romani, A., Baldi, A., Everard, J.D., 1996. Changes in non-structural carbohydrates in olive (Olea europea) leaves during root zone salinity stress. Physiol. Plant. 98, 117– 124. Tester, M., Davenport, P., 2003. Na+ tolerance and Na+ transport in higher plants. Ann. Bot. 91, 503–527. Tyerman, S.D., Skerrett, I.M., 1999. Root ion channels and salinity. Sci. Hortic. 78, 175–235. UN Population Division, 1994. World population prospects (sustaining water: an update). The 1994 Revision. The UN, New York.


Walker, R.P., Torokfalvy, E., Scott, N.S., Kriedemann, P.E., 1981. An analysis of photosynthetic response to salt treatment in Vitis vinifera. Aust. J. Plant Physiol. 8, 359–374. Walker, R.R., Blackmore, D.H., Clingeleffer, P.R., Iakono, F., 1997. Effect of salinity and Ramsey rootstock on ion concentrations and carbon dioxide assimilation in leaves of drip-irrigated, fieldgrown grapevines (Vitis vinifera L. cv. Sultana). Aust. J. Grape Wine Res. 3, 66–74. Walker, R.R., Blackmore, D.H., Sun, Q., 1993a. Carbon dioxide assimilation and foliar ion concentrations in leaves of lemon (Citrus limon L.) trees irrigated with NaCl or Na2SO4. Aust. J. Plant Physiol. 20, 173–185. Walker, R.R., Munns, R., Tonnet, M.L., 1993b. Xylem chloride and sodium concentrations of salt treated citrus plants. In: Beilby, M.J., Walker, N.A., Smith, J.R. (Eds.), Membrane Transport in Plants and Fungi. University of Sydney, Sydney, pp. 490– 494. 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. Wingley, T.M.L., 1992. Future climate of the Mediterranean Basin with particular emphasis on changes in precipitation. In: Jeftic, L., Milliman, J.D., Sestini, G. (Eds.), Climatic Change and the Mediterranean. Arnold, London, pp. 15–44. Zekri, M., Parsons, L.R., 1990. Response of split-root Sour orange seedlings to NaCl and polyethylene glycol stresses. J. Exp. Bot. 41, 35–40. Zhang, H.X., Blumwald, E., 2001. Transgenic salt tolerant tomato plants accumulate salt in the foliage but not in fruits. Nat. Biotechnol. 19, 765–768. Zhu, J.K., 2001. Plant salt tolerance. Trends Plant Sci. 6, 66–71.