irrigation of mediterranean crops with saline water: from physiology to management practices

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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,*

aNAGREF, Institute for Agricultural Research, 71307 Iraklio, Crete, GreecebNAGREF, 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).

0167-8809/$ – see front matter # 2004 Elsevier B.V. All rights reserved

doi:10.1016/j.agee.2004.10.006

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

.

N.V. Paranychianakis, K.S. Chartzoulakis / Agriculture, Ecosystems and Environment 106 (2005) 171–187172

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 hormo-

nal 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 sug-

gested 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 respon-

sible for photosynthesis inhibition in some studies

(Paranychianakis et al., 2004b; Banuls and Primo-

Millo, 1995). Reductions in mesophyll conductance

due to salinity-induced anatomical changes in leaves

have also been suggested to contribute in photo-

synthesis inhibition in citrus (Citrus sp.) (Romero-

Aranda 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 correla-

tions do not represent cause–effect relationships,

bringing into question the contribution of non-

stomatal limitations. Identifying the nature of non-

stomatal limitations of photosynthesis under stress

conditions is currently an active area of photosynth-

esis 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 sub-

stantially 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; Banuls 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), tran-

spiration rate (Moya et al., 2003) and water-use

efficiency (Gibberd et al., 2003). The most horti-

cultural 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 root-

stock, 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) 171–187 173

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, http://apps.fao.org/cgi-bin/nph-dp.pl). 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 Mediterra-

nean.

2.1. Current situation

Even today many Mediterranean countries includ-

ing 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

Table 1

Population and freshwater availability for 1990, 2025 and 2050 in the M

Country 1990 2025

Population

(in thousands)

Availability

(m3/inh.year)

Population

(in thousan

Albania 3289 6385 4668

Algeria 24935 690 45475

Cyprus 702 1282 927

Egypt 56132 1046 97301

France 56718 3262 61247

Greece 10238 5763 9868

Israel 4660 461 7808

Italy 57023 3279 52324

Jordan 4259 308 12039

Lebanon 2555 1949 4424

Libya 4545 1017 12885

Malta 354 85 422

Morocco 24334 1151 40650

Palestine

Portugal 9868 6688 9685

Spain 39272 2826 37571

Syria 12348 2089 33505

Tunisia 8080 540 13209

Turkey 56098 3619 90937

Yugoslavia 22945 11549 24582

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 popula-

tion 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 saliniza-

tion. 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

editerranean countries (UN Population Division, 1994)

2050

ds)

Availability

(m3/inh.year)

Population

(in thousands)

Availability

(m3/inh.year)

4499 5265 3989

378 55674 309

971 1006 895

605 117398 502

3021 60475 3059

5979 8591 6868

275 8927 241

3574 43630 4286

109 16874 78

1126 5189 960

359 19109 242

71 439 68

689 47858 585

6815 9140 7221

2954 31765 3494

770 47212 546

328 15607 279

2232 106284 1910

10780 24441 10842

http://apps.fao.org/cgi-bin/nph-dp.pl


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 8Cby 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 exacer-

bated 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 devel-

opment 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 treat-

ments. 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


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, salinity-

induced 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


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 (Mavrogiano-

poulos et al., 1999; Maggio et al., 2002). The

stimulation of growth of salt-stressed plants grown

under a CO2 environment implies that salinity-

induced 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 salt-

stressed plants (Gao et al., 1998; Walker et al., 1981),

growth may eventually be limited due to the reduced

availability of assimilates to growing sinks. Altera-

tions in the activity of specific enzymes may reduce

Table 2

The effects of water quality on root, trunk and stems content of soluble

Organs Carbohydrates (% dw)

Recycled water Freshw

Roots (<2 mm) 2.13 1.86

Roots (>2 mm) 1.68 1.66

Trunk 2.24 2.26

Stems 2.67 b 2.99 a

Any two means not followed by the same letter are significantly differen

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 carbohy-

drate metabolism or for osmotic adjustment may result

in feedback repression on the Calvin cycle causing a

further reduction in photosynthesis and hence in

growth.

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 contrast-

ing. 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

(Banuls and Primo-Millo, 1992; Fisarakis et al., 2001;

Banuls et al., 1997; Lloyd et al., 1990) or stomatal

closure (Paranychianakis et al., 2004b; Banuls and

Primo-Millo, 1995) as the main causes of photo-

synthesis 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 salt-

stressed fruit trees. However, these correlations do not

carbohydrates and starch (adapted from Paranychianakis, 2001)

Starch (% dw)

ater Recycled water Freshwater

9.93 b 11.43 a

8.16 b 9.98 a

6.50 b 6.82 a

5.41 b 5.93 a

t at P < 0.05 with Tukey’s significant difference.


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 Paranychia-

nakis et al., 2004b).

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.

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 correla-

tion between stomatal conductance and leaf water

potential in salt-treated citrus was also reported by

Banuls 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

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).

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 con-

ductance 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; Romero-

Aranda 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


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 CO2-

rich 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 environ-

ments 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 condi-

tions 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 salt-

treated 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 perfor-

mance. 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 perfor-

mance 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.


5.1. Salt uptake and transport

In fruit species salinity tolerance has been

associated with their ability to restrict salts accumula-

tion 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� concentra-

tion 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 differ-

ences 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 transloca-

tion 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


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 non-

significant differences.

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.

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.


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; Banuls 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 osmoprotec-

tants 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; Banuls

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 photo-

synthetic apparatus and from mitochondrial respira-

tion 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 salinity-

induced damage in horticultural crops. Differences

in the salt tolerance between two mulberry geno-

types (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 enzy-

matic and non-enzymatic antioxidant defense pro-

portionally 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 low-

quality 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 strate-

gies, (b) plant cultural practices and (c) the selection of

salt-tolerant genotypes.


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 water-

use 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 time-

consuming 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 avail-

ability 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 continu-

ously 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(1)

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 manage-

ment 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


this section, emphasis is given to practices such as the

application of water or soil amendments, improved

fertilization schedule and other miscellaneous prac-

tices.

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 fertiliza-

tion, 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).

Table 3

Potential use of such resources for citrus, grapevines and olive trees irrig

Water classification TDS (ppm) EC (dS/m

Freshwater <500 <0.6

Slightly brackish 500–1000 0.6–1.5

Brackish 1000–2000 1.5–3.0

Moderately saline 2000–5000 3.0–8.0

Saline 5000–10000 8.0–15

Highly saline 10000–35000 15.0–45

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 mycor-

rhizae are associated with improved nutrition and

better water absorption (Ruiz-Lozano and Azcon,

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 salt-

tolerant 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.

ation

) Crop Threshold EC (dS/m)

Citrus 1.1–1.4

Grapevines 1.4–3.0

Olives 1.8–2.5

.0

.0


Table 4

Salt tolerance rating of various cultivars and rootstocks of citrus, grapevines and olives

Tolerant genotypes

Citrus Sunki mandarin, Cleopatra mandarin, Rangpur lime

Grapevines Ramsey, Dogridge, French Colombard

Olives 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 Troyer citrange, Trifoliate orange, Rusk citrange, Sweet orange

Grapevines 41B, SO4, Muscat of Alexandria, Barbera, Ribier

Olives 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 agri-

cultural production, particularly in areas with a semi-

arid or arid climate. However, more detailed studies

are needed to quantify the temporal and spatial effects

of climate change on water resources. Such informa-

tion 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 under-

standing 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 under-

standing of the interactions among genetic traits,

climatic conditions and management practices is

required.


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