InTechOpen uses cookies to offer you the best online experience. By continuing to use our site, you agree to our Privacy Policy.

Agricultural and Biological Sciences » "Responses of Organisms to Water Stress", book edited by Sener Akıncı, ISBN 978-953-51-0933-4, Published: January 16, 2013 under CC BY 3.0 license. © The Author(s).

# Comparison Between the Water and Salt Stress Effects on Plant Growth and Development

By Alexandre Bosco de Oliveira, Nara Lídia Mendes Alencar and Enéas Gomes-Filho
DOI: 10.5772/54223

Article top

## Overview

Figure 1. Effects of salt stress on plants (reproduced from [21]).

Figure 2. Physiological and molecular basis of drought stress tolerance (adapted from [8, 26]).

Figure 3. Adaptive responses of plants to salt stress (reproduced from [28]).

Figure 4. Water and salt stress tolerance mechanisms in plants (adapted from [31]).

Figure 5. Causes of irrigation salinity (reproduced from [35]).

Figure 6. Some physiological and biochemical perturbations in plants caused by fluctuations in abiotic environments [12].

Figure 7. Change in plant physiology as consequence to salinity adapted from [40].

Figure 8. Growth responses to salt stress from [6].

Figure 9. Salinity effects on relationship between percent germination and time after water addition at low, moderate and high salinity, modified from [46].

Figure 10. Effect of NaCl increasing on the growth on shoot dry mass in different halophytes. Solid lines represents dicotyledonous species; broken lines, monocotyledonous species. (♦)Suaeda maritima (35 d), (∎) Thellungiella halophila (14 d); (▲ ) Disphyme australe (60 d); ( *) Puccinellia peisonis (42 d); (●) Distichlis spicata (21 d). (Modified from 49)

Figure 11. Epidermis front view of the leaves of Atriplex nummularia Lindl. grown in sodic saline soil under different water regimes: (a) 35%; (b) 55%; (c) 75; (d) 95% of FC. Vesicular trichome consisting of stalk cell surmounted by a vesicular cell (f–g) and stomata (h). sc: stalk cell; vc: vesicular cell; dr: drusa; st: stoma. Bar: 50 μm (a–d), 25 μm (e–h). Modified from [55]

Figure 12. Plant responses to water stress from 82

# Comparison Between the Water and Salt Stress Effects on Plant Growth and Development

Alexandre Bosco de Oliveira1, Nara Lídia Mendes Alencar1, 2 and Enéas Gomes-Filho1, 3

## 1. Introduction

Abiotic stress limits crop productivity [1], and plays a major role in determining the distribution of plant species across different types of environments. Abiotic stress and its effects on plants in both natural and agricultural settings is a topic that is receiving increasing attention because of the potential impacts of climate change on rainfall patterns and temperature extremes, salinization of agricultural lands by irrigation, and the overall need to maintain or increase agricultural productivity on marginal lands. In the field, a plant may experience several distinct abiotic stresses either concurrently or at different times through the growing season [2].

In reference [3] are showed some common examples of the abiotic stresses a plant may encounter which include a decreased availability of water, extremes of temperature including freezing, decreased availability of essential nutrients from the soil (or conversely the build-up of toxic ions during salt stress), excess light (especially when photosynthesis is restricted) or increased hardness of the soil that restricts root growth.

In the face of a global scarcity of water resources and the increased salinization of soil and water, abiotic stress is already a major limiting factor in plant growth and will soon become even more severe as desertification covers more and more of the world's terrestrial area. Plants are often subjected to periods of soil and atmospheric water deficits during their life cycle. Moreover, the faster-than-predicted change in global climate [4] and the different available scenarios for climate change suggest an increase in aridity for the semiarid regions of the globe. Together with overpopulation, this will lead to an overexploitation of water resources for agriculture purposes and increased constraints on plant growth and survival aid, therefore, on realizing crop yield potential [5]. Thus, if a single abiotic stress is to be identified as the most common in limiting the growth of crops worldwide, it most probably is low water supply [1].

Like the water stress, salinity is one of the major severe abiotic factors affecting crop growth and productivity [6]. Salt’s negative effects on plant growth have initially been associated with the osmotic stress component caused by decreases in soil water potential and, consequently, restriction of water uptake by roots.

The literature shows that drought and salinity are already widespread in many regions. Therefore, in reference [7] the authors have presented that in world where population growth exceeds food supply, agricultural and plant biotechnologies aimed at overcoming severe environmental stresses need to be fully implemented.

### 1.1. Plant stress definitions

The term stress is most often used subjectively and with various meanings. The physiological definition and appropriate term for stress are referenced as responses to different situations. The flexibility of normal metabolism allows the development of responses to environmental changes, which fluctuate regularly and predictably over daily and seasonal cycles [8]. Thus, stress plays a pivotal role in determining interaction outcomes because it strongly influences the strength of underlying positive and negative interactions.

Stress is defined as any external abiotic (heat, water, salinity) or biotic (herbivore) constraint that limits the rate of photosynthesis and reduces a plant’s ability to convert energy to biomass [9]. The strength of positive interactions increases with increasing stress except at the most extreme levels. In contrast, the strength of negative interactions is either unrelated to stress and remains consistently high, or alternatively, decreases with increasing stress [10].

Environmental stress could be defined in plants as any change in growth condition(s), within the plant’s natural habitat, that alters or disrupts its metabolic homeostasis. Such change(s) in growth condition requires an adjustment of metabolic pathways, aimed at achieving a new state of homeostasis, in a process that is usually referred to as acclimation [11]. However, the concept of plant stress is often used imprecisely, and stress terminology can be confusing, so it is useful to start our discussion with some definitions. Stress is usually defined as an external factor that exerts a disadvantageous influence on the plant. In most cases, stress is a measured in relation to plant survival, crop yield, growth (biomass accumulation), or the primary assimilation processes (CO2 and mineral uptake), which are related to overall growth. In addition, the concept of stress is intimately associated with that of stress tolerance, which is the plant’s fitness to cope with an unfavourable environment. In the literature the term stress resistance is often used interchangeably with stress tolerance, although the latter term is preferred [12].

According with the literature [13], changes in strength of these underlying processes drive shifts between competition and facilitation. The stress gradient hypothesis (SGH) predicts that facilitation and competition vary inversely along stress gradients with facilitation more frequent and stronger when stress is high and competition more frequent and stronger when stress is low. The SGH also predicts that the strongest facilitation should occur with competitive species at the upper limits of their stress tolerance while the strongest competition should occur with stress tolerant species located at their ecological optimum.

Shifts in the structure of interaction outcomes, i.e. a shift from competition to facilitation, along stress gradients are likely to have profound implications for community stability [14, 15]. Community compositional instability can be defined as changes in species abundances that drive directional changes in community composition. There is growing evidence that changes in the structure of species interactions can reduce such stability [16].

In both natural and agricultural conditions, plants are frequently exposed to environmental stresses. In [17] the work presents how some environmental factors, such as air temperature, can become stressful in just a few minutes; others, such as soil water content, may take days to weeks, and factors such as soil mineral deficiencies can take months to become stressful.

### 1.2. Concepts and consequences of water and salt stress on plants

Water-deficit stress can be defined as a situation in which plant water potential and turgor are reduced enough to interface with normal functions. Water stress is considered to be a moderate loss of water, which leads to stomatal closure and limitation of gas exchange. Desiccation is a much more extensive loss of water that can potentially lead to gross disruption of metabolism and cell structure and eventually to the cessation of enzyme catalyzing reactions. Water stress is characterized by reduction of water content, turgor, total water potential, wilting, closure of stomata, and decrease in cell enlargement and growth. Severe water stress may result in arrest of photosynthesis, disturbance of metabolism, and finally death [8, 18].

The term ‘salinity’ refers to the presence in soil and water of electrolytic mineral solutes in concentrations that are harmful to many agricultural crops. Except along seashores, saline soils seldom occur in humid regions, thanks to the net downward percolation of fresh water though the soil profile, brought about by the excess of rainfall compared with evapotranspiration. In arid regions, on the other hand, there may be periods of no net downward percolation and hence no effective leaching, so salts can accumulate in the soil. Hence the combined effect of meager rainfall, high evaporation, the presence of salt-bearing sediments, and – in many places, particularly river valleys and other low-lying areas – the occurrence of shallow, brackish groundwater which gives rise to saline soils [19].

Salinity in soil or water is one of the major stresses and, especially in arid and semi-arid regions, can severely limit crop production. The Figure 1 is showing that deleterious effects of salinity on plant growth are associated with low osmotic potential of soil solution (water stress), nutritional imbalance, specific ion effect (salt stress), or a combination of these factors [20].

### Figure 1.

Effects of salt stress on plants (reproduced from [21]).

### 1.3. Mechanisms of acclimation or adaptation to water and salt stress

Drought and soil salinity are among the most damaging abiotic stresses affecting today’s agriculture. It is understandable that plants are under periodic water stress because of the unpredictable nature of rainfall. Salt stress may also occur in areas where soils are naturally high in salts and/or where irrigation, hydraulic lifting of salty underground water, or invasion of seawater in coastal areas brings salt to the surface soil that plants inhabit. Plants have evolved mechanisms that allow them to perceive the incoming stresses and rapidly regulate their physiology and metabolism to cope with them. Very often such regulations and responses include feed-forward mechanisms for stress reduction that are in addition to the responses that are seen after stresses have caused irreversible damage to physiological functions. A good example of such a feed-forward mechanism the ability of plants to regulate their water loss through partial closure of stomata and/or reduced leaf development, long before there is a substantial loss of their leaf turgor or some irreversible damage to inner membrane systems. [22-24].

In this way, talking specific about water deficit, the physiological responses of plants to water stress include leaf wilting, a reduction in leaf area, leaf abscission, and the stimulation of root growth by directing nutrients to the underground parts of the plants. Plants are more susceptible to drought during flowering and seed development (the reproductive stages), as plant’s resources are deviated to support root growth. In addition, abscisic acid (ABA), a plant stress hormone, induces the closure of leaf stomata (microscopic pores involved in gas exchange), thereby reducing water loss through transpiration, and decreasing the rate of photosynthesis. These responses improve the water-use efficiency of the plant on the short term [25]. The Figure 2 reveals physiological, biochemical and molecular responses to this abiotic stress in plants. It is very important highlight that most of these responses are similar in salt-stressed plants.

### Figure 2.

Physiological and molecular basis of drought stress tolerance (adapted from [8, 26]).

In salt-stressed plants, in addition to osmotic effects it is also affected by toxic damages as function of nutritional disequilibrium and high salt levels uptake for plants. Thus, salinity inhibition of plant growth is the result of osmotic and ionic effects and the different plant species have developed different mechanisms to cope with these effects [6]. The osmotic adjustment, i. e., reduction of cellular osmotic potential by net solute accumulation, has been considered an important mechanism to salt and drought tolerance in plants. This reduction in osmotic potential in salt stressed plants can be a result of inorganic ion (Na+, Cl-, and K+) and compatible organic solute (soluble carbohydrates, amino acids, proline, betaines, etc) accumulations [27]. However these changes are only any few initial responses of many others occurred from salt-stressed seedlings. For instance this behavior, in the Figure 3 has been showed a schematic summary of the stresses that plants suffer under high salinity growth condition and the corresponding responses that plants use in order to survive these detrimental effects.

### Figure 3.

Adaptive responses of plants to salt stress (reproduced from [28]).

## 2. Water stress x salt stress effects on plant growth and development

Plant responses to drought and salinity are complexes and involve adaptive changes and/or deleterious effects. The decrease in the water potential occurred in both abiotic stresses results in reduced cell growth, root growth and shoot growth and also causes inhibition of cell expansion and reduction in cell wall synthesis [29]. According these authors, drought (likely to salinity) affects the regular metabolism of the cell such as carbon-reduction cycle, light reactions, energy charge and proton pumping and leads to the production of toxic molecules.

The literature has affirmed that plant responses to salt and water stress have much in common. For example, according reference [30], salinity reduces the ability of plants to take up water, and this quickly causes reductions in growth rate, along with a suite of metabolic changes identical to those caused by water stress. Therefore, most mechanisms were development by plants to tolerate abiotic stresses like water deficit and salinity, which are schematically showed in Figure 4.

#### Figure 4.

Water and salt stress tolerance mechanisms in plants (adapted from [31]).

### 2.1. Salinity and water deficit problem in arid and semi-arid regions

Arid and semiarid regions of the world such as Brazilian’s Northeast, mostly faces with inadequate, irregular and erratic nature of rainfall. Moreover, according [3], in the field, drought can cause a number of plant stresses including temperature, light and nutrient stresses. However, the stress component that defines drought is a decrease in the availability of soil water. For [32], in addition with recurrent drought lack of efficient use of scarcely available water amplified the impact of water scarcity in agricultural production and productivity. These authors affirm the reduction of agricultural production results from a combination of many factors, such as crop management, crop genetics and biotic stress. Therefore, limited and irregular rainfall directly and indirectly leads to low production levels and consequently food insecurity in developing regions of the world such as Brazilian’s semiarid. In addition, [33] have related it is widely recognized that land use–cover changes, such as desertiﬁcation in arid and semiarid regions and deforestation in tropical zones, may exert an inﬂuence on regional or even global environmental change by changing the hydrological cycle and surface energy balance.

Looking for avoid the water stress and to improve the productivity at arid and semiarid regions generally adopt the use of irrigation, principally the drip. In this way, drip irrigation has the potential to increase crop yields with less water and it can maintain relatively constant soil water content over time near the drip lines. However, [34] have related a disadvantage of drip irrigation is that salt accumulates near the periphery of the wetted area. According them, this salt accumulation can be a matter of concern if the emitter placement does not coincide reasonably well with the location of the plant row, particularly for crops that are sensitive or moderately sensitive to soil salinity.

### 2.2. Salinity in soil is increased by the water deficit and aridity conditions

In arid regions, there may be periods of no net downward percolation and hence no effective leaching, so salts can accumulate in the soil. In reference [19], the combined effect of meager rainfall, high evaporation, the presence of salt-bearing sediments, and – in many places, particularly river valleys and other low-lying areas – the occurrence of shallow, brackish groundwater which gives rise to saline soils. In addition, the irrigation has been one of the major practices that more contributes with the soil salinization, like showed in Figure 5.

### Figure 5.

Causes of irrigation salinity (reproduced from [35]).

Less obvious than the appearance of naturally saline soils, but perhaps more insidious, is the inadvertent induced salination of originally productive soils, caused by human intervention. Irrigation waters generally contain appreciable quantities of salts. (For example: even with relatively good-quality irrigation water containing no more than 0.3 kg salts m3, applying 10,000 mm water per season would add as much as 3 000 kg salts ha-1 per year!) Crop plants normally extract water from the soil while leaving most of the salt behind. Unless leached away (continuously or intermittently), such salts sooner or later begin to hinder crop growth [19].

These deleterious effects previously showed caused by salinization can be managed by changed farm management practices. In [30] has been indicated in irrigated agriculture, better irrigation practices, such as drip irrigation, to optimize use of water can be employed. In rain-fed agriculture, this researcher suggest practices such as rotation of annual crops with deep-rooted perennial species may restore the balance between rainfall and water use, thus preventing rising water tables bringing salts to the surface. All such practices will rely on a high degree of salt tolerance, not only of the perennial species used to lower a saline water table, but also of the crops to follow, as some salt will remain in the soil.

### 2.3. Salt stress and irrigation and bad water uses

Irrigation water quality can have a profound impact on crop production. In reference [36], the work affirms that all irrigation water contains dissolved mineral salts, but the levels and composition of the salts vary depending on the source of the irrigation water. Salinity from irrigation can occur over time wherever irrigation occurs, since almost all water (even natural rainfall) contains some dissolved salts. When the plants use the water, the salts are left behind in the soil and eventually begin to accumulate. Since soil salinity makes it more difficult for plants to absorb soil moisture, these salts must be leached out of the plant root zone by applying additional water. This water in excess of plant needs is called the leaching fraction [37].

Salination from irrigation water is also greatly increased by poor drainage and use of saline water for irrigating agricultural crops. Therefore, inefficient or bad irrigation water and drainage systems are a major cause of excess leakage and increase the risk of salinity and waterlogging in irrigation areas. Poor water distribution on paddocks results in some areas being under-irrigated, causing salts to accumulate (where watertables are high) and other areas being over-irrigated and waterlogged. Groundwater mounds can develop under irrigation areas as a result of leakage from inefficient systems and restrictive layers. This puts pressure on the regional groundwater system forcing saline groundwater into waterways. Irrigating with saline water adds salt to the soil and increases the need for applying more irrigation water to leach salts past the plant root zone [38].

From studies of FAO [39] we can affirm that prevention and reclamation of salt-affected soils require an integrated management approach, including consideration of socioeconomic aspects, monitoring & maintenance of irrigation schemes and reuse and/or safe disposal of drainage water. Implementation of efﬁcient irrigation and drainage systems and good farming practices can prevent and, in some cases, reverse salinization. If appropriate management practices are not applied in time, it may be necessary to take the land out of production altogether. Moreover, actions to fight or mitigate salinization can be implemented by local institutions and research stations, while research and technology transfer can play a crucial role in providing tools, setting up management strategies or spreading water-saving techniques.

### 2.4. Growth and plant development affected by multiple stresses as water and salt stress

Plant growth can be limited by water deficit and by excess water. Water deficit occurs in most natural and agricultural habitats and is caused mainly by intermittent to continuous periods without precipitation. Excess water occurs as the result of flooding or soil compaction [12].

When plant cells experience water deficit, cellular dehydration occurs, this promotes reductions of cell turgor (Ψp) and cell volume. It is also associated with the water potential (Ψw) of the apoplast becoming more negative than that of the symplast. Cellular dehydration could causes ion concentration reaching cytotoxic levels [12].

Water deficit not only decreases turgor pressure, but also decreases wall extensibility and increase yield threshold. The water deficit effects on yield threshold are presumably involved in complex structural changes of the cell wall that may not be readily reversed after relief of water deficit [12].

### Figure 6.

Some physiological and biochemical perturbations in plants caused by fluctuations in abiotic environments [12].

Salinity can have similar aspects to water stress in plant growth, except for the addition of ion cytotoxicity, which appears with salt excess in soil. [12].

The toxicity of high Na+ and Cl- in the cytosol is due to their specific ion effects. High salt concentrations, outside the cell, can result in osmotic stress. Once in the cytosol, however, certain ions act specifically, either singly or in combination, affecting whole plant because ions move to the shoot in the transpiration stream [6].

The increase of solutes on root medium, mainly the ions, can promote a reduction of water absorption by plant root system, contributing to reduction of root conductivity. As consequence, the plant absorbs less water, and if the transpiration rate is higher than water absorption rate, and the result is a water deficit, which could result in photosynthetic rate reduction and growth rate reduction [40]. According to the figure below, salt stress effects in timescale alters initially, absorption of water and nutrients, and membranes permeability [41].

### Figure 7.

Change in plant physiology as consequence to salinity adapted from [40].

These previous changes reflect in nutritional and hydric balance of plants and promote changes in metabolism, in hormonal balance, gas exchange and ROS production. All these changes undertake cell expansion and division, vegetative and reproductive growth and acceleration of leaf senescence, which result in plant death [12].

An important strategy to avoid ion toxicity is the accumulation of ions during osmotic adjustment in vacuoles, where the ions are kept out of contact with cytosolic enzymes or organelles. Many halophytes utilize vacuolar compartmentalization of Na+ and Cl- to facilite osmotic adjustment that sustain or enhances growth in saline environments. When ions are compartmentalized in vacuoles, at the same time other solutes must accumulate in the cytoplasm to maintain water potential equilibrium within the cell, as example of these compatible solutes, can be cited the quaternary ammonium compounds, sugar alcohols, quaternary ammonium compounds (QACs) and tertiary sulfonium compounds (TSCs) [12].

According to [6], the growth responses to salinity stress occurs in two phases: a rapid and intense response to the increase in external osmotic pressure related to NaCl increase in the medium, which contribute to a stronger reduction in growth. Followed, it can be observed, a slower response due to toxic ion accumulation in tissues (Ionic phase), which is related to a severe toxicity in leaves, represented in most of times by chlorosis and can be originated necrosis in these tissues (See figure 8). Leaf injury and death is probably due to the high salt load in the leaf that exceeds the capacity of salt compartmentation in the vacuoles, causing salt to build up in the cytoplasm to toxic leaves [6,30]. These responses vary strongly between genotypes, salinity levels, soil and other abiotic factors [6].

### Figure 8.

Growth responses to salt stress from [6].

Plants undergo characteristic changes from the time salinity stress is imposed until they reach maturity [30]. Salinity inhibition of plant growth is the result of osmotic and ionic effects and the different plant species have developed different mechanisms to cope with these effects [30]. The plant responses to salinity are different between the species, the salt levels and also depends of the time exposition. In the table below could be observed the plant response to salinity at different time scales [Table modified from 30].

### Table 1.

Water and salt-specific effects on plant growth

As can be observed in this table, in the first few seconds or minutes, it has been observed that cells lose water or shrink. When the hours are passing, cells regain the original volume but cell elongation is reduced, contributing to lower rates of leaf and root growth. After some days, cell elongation and cell division promote alterations in leaf size appearance [30]. In plants, with high salt absorption, the oldest plants become senescent, and some leaves can dead. After months, differences between months, with high and low salt uptake become very pronounced, with a large amount o leaf injury and complete death in some cases if the salinity level is high enough [30].

The tolerance or plant response to salt can vary with cultivars, the plant age and growth stage, environmental conditions, cultural practices, irrigation management, soil fertility, and the intensity or other plant stress. Another, stress factor is wind that can be injurious to plants as salt. When the two are combined near the ocean, plants suffer even greater damage. Some crassulaceae and succulent plants are highly salt and wind tolerant, in different way, moderate salt tolerant plants of soil salinity usually tolerate light salt spray but should not be used in exposed locations [42].

The comparative effect of salinity and water stress on growth was analyzed in Jatropha curcas seedlings. The plants subject to water stress, through the exposition to PEG, showed higher restrictions in leaf growth compared to the salt-stressed ones. Moreover, only the PEG treatment caused a pronounced effect on leaf membrane integrity. Since the plants subjected to mild water and salt stresses showed a rapid and almost complete recovery, these physiological alterations could represent a set of adaptive mechanisms employed by J. curcas to cope with these stressful conditions [43].

Pinus seed germination was evaluated in different conditions: water stress simulated by PEG agent experiments, salt stress using sodium chloride (NaCl) and diluted sea water, associated to different temperatures (heat stress). Seed germination and the activities of the main enzymes involved in Pinus seed reserve utilization (glyoxylate cycle enzymes) decreased with increasing PEG, NaCl and seawater concentrations. In addition, the seawater treatment was the less severe on seed germination. As regard to heat treatments, the maximum germination percentage (80%) was obtained at 80°C and short exposure time (3 min) [44].

Another study involving water and salt stress effects on plant growth was verified in Tamarisk (Tamarix chinensis Lour.) seedlings, where it was observed that the water supply and salt content had interactive effects on Tamarisk biomass, while interactive effects of the both stress had no influence in biomass allocation. This parameter was more affected by water supply, which implied that the balance between soil water availability and atmospheric evaporative demand defined the biomass allocation [45].

Salinity affects both vegetative and reproductive plant development, which promotes negative implications depending on the harvested organ, stem, leaf, root, shoot, fruit, fiber or grain [46]. Salinity generally reduces shoot growth more than root growth and can reduce the flowering and increase sterility. Considering the salt-tolerance importance from an agronomic or horticulturist perspective is based on the yield of the harvestable organ, relative to that in non-stressed environments, understanding how salinity affects vegetative and reproductive development is important for developing management strategies that can minimize stress at critical times [46]. Salinity stress could delay germination, although most plants are tolerant and there may be no difference in the percentage of germinated seeds.

### Figure 9.

Salinity effects on relationship between percent germination and time after water addition at low, moderate and high salinity, modified from [46].

Helianthus annuus seed germination was evaluated using treatment to overcome salt and drought stress during germination. In this study, it was verified that seeds subjected to salinity and water stress showed reduced germination in both conditions [47]. Germination, root and shoot length were higher in NaCl than PEG conditions, but mean germination time and abnormal germination percentage were lower in these conditions [47]. The authors concluded that germination inhibition at the same water potential of NaCl and PEG resulted from osmotic effect rather than salt toxicity, in addition it was observed that hydropriming increased germination and seedling growth under salt and drought stresses [47]. Another study with germination approached salt and water stress on seed germination and early embryo growth in two cultivars of sweet sorghum. In this study, it was observed that salt stress prolonged the germination time. Shoot and root growth was adversely affected by water stress (PEG), whereas the effect of salt stress was less relevant [48].

### 2.5. Salt tolerant plants “Halophytes” and water stress tolerant plants

Halophytes are plants that can survive and reproduce in environments with high salt concentration (200 mM NaCl), these plants constitute about 1% of the world’s flora. Halophytes can be classified as “natural” and plants that tolerate salt but do not normally live in saline conditions [49]. Other classifications of halophytes are based on the characteristics of naturally saline habitats [49] or the chemical composition of the shoots (‘physiotypes’, [50] or the ability to secrete ions (recreto-halophytes, [51]).

The effect of salinity on growth varies amongst halophytes, which can be observed in figure bellow for different species [49]. According this figure, Sueada maritima was the specie that could growth in the highest NaCl concentration, however the best condition was around 40 mM NaCl. The most affected specie was Thellungiella halophila, which showed stronger growth reduction from 200 mM NaCl. In addition, it can be highlighted that dicotyledonous species showed higher tolerance to NaCl than monocotyledonous species, except for T. halophila [49].

### Figure 10.

Effect of NaCl increasing on the growth on shoot dry mass in different halophytes. Solid lines represents dicotyledonous species; broken lines, monocotyledonous species. (♦)Suaeda maritima (35 d), (∎) Thellungiella halophila (14 d); (▲ ) Disphyme australe (60 d); ( *) Puccinellia peisonis (42 d); (●) Distichlis spicata (21 d). (Modified from 49)

The salt requirement by halophyte during their growth and development were evaluated in two halophytic species (Inula crithmoides L. and Plantago crassifolia Forssk.) and a maritime dune species (Medicago marina L.) [52]. In this study was observed that growth parameters results showed that all three species grew much better on the salt-free and nutrient-rich substrates, peat and garden soil, than on saline soil and dune sand. These results indicate that salts are not necessarily required for development of halophytic species, and suggest that limitation of water and nutrients, rather than soil salinity per se, are the most important restrictive factors for plant growth in saline habitat [52].

Studies involving extreme dicotyledonous halophytes show that optimal growth in the presence of low or moderate salt concentrations; on the other hand, this stimulatory effect is not commonly detected in monocotyledonous halophytes, nor in other salt-tolerant dicots, which grow best in the absence of salt [53]. The salt tolerance degree usually varies among halophytes and, for a specific species, also at different developmental stages [53], but inhibition of plant growth is always observed at sufficiently high salinity levels, in all investigated taxa [52, 53].

Tamarix chinensis that is used as a windbreak for preventing desertification and erosion in arid areas and potential bio-energy resources for marginal land utilization [54], was evaluated with relation to salt and water stress on biomass and photosynthetic characteristic. In this study was observed that soil salt increment had no significant effect on biomass allocation of T. chinensis seedlings [45], while water deficit significantly favoured root biomass accumulation [45].

In study about growth parameters and anatomical changes in the halophyte Atriplex nummularia Lindl, it was observed that the height, diameter and fresh and leaf dry biomass, stems and roots were sensitive to soil moisture. Moreover, anatomical changes in the vesicular trichomes of the leaves were detected with water soil variations and druse formed by deposition of sodium chloride within cells [Figure from 55]. A low water content in the oil is related to small average diameters and volumes of the epidermal vesicles [55].

### Figure 11.

Epidermis front view of the leaves of Atriplex nummularia Lindl. grown in sodic saline soil under different water regimes: (a) 35%; (b) 55%; (c) 75; (d) 95% of FC. Vesicular trichome consisting of stalk cell surmounted by a vesicular cell (f–g) and stomata (h). sc: stalk cell; vc: vesicular cell; dr: drusa; st: stoma. Bar: 50 μm (a–d), 25 μm (e–h). Modified from [55]

In another study also with A. nummularia was observed that leaves display a most prominent osmotic adjustment than roots. In addition, it has been also concluded that Na+ and Cl− ions are the major components to the overall osmotic adjustment, in both salt-untreated and treated leaves but in untreated roots the K+ is the major component [56]. For Atriplex allimus, the decrease in fresh weight might be attributed to the decrease in water content. Moreover, the decrease in photosynthesis could result from a decrease in stomatal conductance, which corresponds to a protective mechanism against water loss to improve water use efficiency [57]. The A. allimus could tolerate NaCl and drought through decreasing growth, reducing gas exchange parameters to improve water use efficiency. In another study with halophytes, it was verified the effect of salinity and soil drying on nutrient uptake and growth of Spartina alterniflora in a simulated tidal system [58]. This study demonstrated that high salinity associated with drought decreased survival to 71%, Furthermore, leaf chlorosis and browning occurred in plants subjected to increased salinity and drought conditions, which can demonstrated that drought may magnify the adverse effects of salinity on plant nutrient status [58]. Some plants can develop a lot of mechanisms to support water deficit, as example the development of internal water deficit, which can be important for some crops such as coffee and mango in order to trigger phenological events such as flower bud release. Additionally, it has been know that for a tropical environment the range of evaporative demand on average is higher than that of temperate zones. This implies that leaf water status changes much more diurnally in tropical trees than in many temperate trees or annuals, and leaf water deficits may occur under the high evaporative demand even without any soil water shortage, such as in banana, cocoa, coffee, papaya, and tea [59].

The development of thick cuticular membranes generally is interpreted as an adaptation to drought with regard to the formation of an efficient transpiration barrier. The capacity of Teucrium chamaedrys in maintaining a low but still measurable stomatal conductance under drought stress at maximum light intensity can be interpreted as a mechanism to adjust leaf temperature below the heat resistance limit by transpiration cooling [60].

Jatropha curcas L. is a biodiesel crop that is resistant to drought stress, and the tolerance of Jatropha curcas seedlings to NaCl was evaluated through some ecophysiological analyses. This study showed that the negative NaCl effects on J. curcas crop, are mainly due to Cl- and /or Na+ toxicity and to a nutritional imbalance caused by increase in Na+/ K+. Moreover, the osmotic effect on salinity in this species is very pronounced, probably due to strong control of leaf transpiration, which reduces water loss [61].

The NaCl differential tolerance of different maize genotypes were evaluated through some growth and physiological parameters and it was concluded that the SDM/RDM ratios, leaf Na+ content or leaf soluble organic solute content had no relation with salt tolerance. On the other hand, Na+ and soluble organic solute accumulation in roots due to salinity appeared to play an important role in the acclimation of maize genotypes, being that these characteristics could be used as physiological markers to salinity [62].

### 2.6. Studies involving adaptations or acclimations of tropical plants to water and and salt stress

Plants under salt stress can occasionally tolerate alterations in the environmental conditions. Salt tolerance in plants is determinate by multiple biological traits that will determine their water retentions and/ or acquisition capacity in safeguarding photosynthetic functions and ion homeostasis. The plant ability of eliminating free radical under salinity and water stress using active osmolytes, usually demand a lot of energy. Many plant species that are salt tolerant to salt stress show the ability to produce and accumulate osmoprotectants [63].

Water deficit and saline soils of the Brazilian semi-arid northeastern region are limiting factors and most of the times negatively affect the plant development. Mimosa tenuiflora popular known as Jurema preta is a small, multiple use tree that is widely distributed in environments with severe water stress. In this study, it was verified that Jurema preta seeds germination showed more sensitive to NaCl than to water stress, and due to the stronger germination reduction in this condition, this species can be classified as a glycophyte [64].

The water relations in six adult species of Caatinga, a typical vegetation from Brazilian semi-arid, in the middle of the dry season. Based on results, the trees were classified into four groups: (I) Mimosa caesalpiniifolia had low leaf water potential (Ψw) at predawn and no significant decrease at midday; (II) Caesalpinia pyramidalis and Auxemma oncocalyx had low Ψw at predawn and significant decrease at midday. For these species the recuperation of water status at night may have been sufficient for maintaining stomata open during the day; (III) Caesalpinia ferrea and Calliandra spinosa had relatively high Ψw at predawn and a significant decrease at midday. They might also have deeper root systems; and (IV) Tabebuia caraiba with the highest Ψw at predawn and no significant decrease at midday, possibly indicating a combination of good stomatal control of water loss and a deeper root system [77].

In relation to commom bean plants, mild water deficit affected the photochemical apparatus in these plants, probably due to by down-regulation since plants did not show photoinhibition. The photochemical apparatus of A222 and A320 genotypes was more sensitive to drought stress. On the other hand, even after 10 d of water withholding, the maximum efficiency of photosystem 2 was not affected, what suggest efficiency of the photoprotection mechanisms [78].

The seasonal variations of physiological aspects of caatinga species demonstrated the high levels of water potential, even in the dry period, a situation in which commonly occurs water stress due to absence of soil water. It is related to water potential decrease during the absence of water in soil. The fluorescence data showed that the photosynthetic states were good with no apparent deficiency of water. In addition, it was verified that the survival strategies of these species to water deficit are efficient and result from a highly complex evolution [79].

In a study with Vigna unguiculata, an important crop largely cultivated in warm and hot lands, it were evaluated some photosynthetical parameters and metabolic changes in cowpea under water stress and recovery treatments. In this study it was verified that decreased CO2 assimilation rates during water stress were largely dependent on stomatal closure, which reduced available internal CO2 and restricted water loss through transpiration [80]. Additionally, the alterations in carbohydrate metabolism showed an accumulation of soluble sugars in water-stressed leaves, which also persisted in rewatering plants for 1 day. The authors conclude that a transient end-product inhibition of photosynthesis, contributing to a minor non-stomatal limitation during stress and recovery initial phase [80].

In relation to Phaseolus vulgaris, the mild water stress effects on photosynthetic parameters and water potential were analyzed in five common bean. The stomatal conductance and net photosynthetic rate were significantly reduced in all genotypes due to the water deficit [81]. Mild water deficit affected the photochemical apparatus in bean genotypes probably by down-regulation since plants did not show photoinhibition. It was also interesting in this study, that even after 10 d of water withholding, the maximum efficiency of photosystem 2 was not affected, what suggest efficiency of the photoprotection mechanisms [81].

In the figure below, it is resumed long-term or acclimations responses to drought stress and short-term responses that reach the plant perceive the water stress and develop the following responses against this condition [82]. The majority of traits related to plant drought adaptations, as example root size and depth, hydraulic conductivity and seed storage reserves are associated to plant development and structure and are constitutive rather than stress induced. In addition, a large part of drought plants resistance to drought and its ability to get rid of to excess radiation. The natural mechanisms responsible to leaf photoprotection, especially to related to thermal dissipation and oxidative stress. Plants can also endure water drought conditions by avoiding tissue dehydration, while maintaining tissue water potential as high as possible, or tolerating lower water potential. Dehydration avoidance is usually observed in annual and perennial plants, which has been associated to proper characteristics as example: capacity to minimize water loss and maximize water uptake [82]. The water loss could be done by stomata closer, reducing light absorbance by leaf or through reflectance increasing due to the development of a trichome layer, or by decresing of leaf surface with reduced growth or by shedding of young by old leaves. On the other hand, the maximizing water could be reaching by increasing in root system, which is resulting of alteration in allocation of plant sources [82].

### Figure 12.

Plant responses to water stress from 82

## 3. Conclusion

Among the great number of abiotic stress affecting plants, drought and salinity are the most severe and stronger ones that limit plant growth and crop productivity in agriculture worldwide. These stress could have damages exceeding the sum of that attributed to all other natural disasters, and when they happen together promoted devastating changes in plants subjected to them. Plant responses to drought and salt stresses have much in common, the water limitations in water stress is very difficult to plant tolerate and maintain its normal growth and development. Salt stress occurs from both osmotic stress due to low water potentials and salt-specific effects, for this beyond the water restrictions, salt-stressed plants have to develop conditions to tolerate the toxic effects caused by ion accumulation, which could affect all aspects of plant metabolism. In the first view, we could speculate that salt stress in plants are more severe than water stress, by the fact that the first condition show two components, however, it is early to conclude this. This is because studies on the comparative physiology of plants to water and salt stress are few, and it is necessary perform more studies involving different plant species, as cultivate and as native, subjected at the same time to both stress to conclude what is the most severe for plant growth and development. Moreover, the development of new tools and strategies to evaluate the combination of water and salt stress on plant are also necessary, but the perspectives in relation to the better understanding of how some plants could tolerate, escape, acclimate and adaptate to these severe abiotic stresses. This knowledge could have the support of studies involving since molecular (genomics and proteomics tools) aspects as ecotype researches (isotopes, imagging) and this combination will allow the faster comprehension of plant perfomance in different environments, as well the brinding of genotype and phenotype gap.

## Acknowledgements

The authors would like to thank National Institute of Science and Technology Salinity (CNPq/MCT/Brazil) for the fellowships and financial support.

## References

1 - Araus JL, Slafer GA, Reynolds MP, Royo C. Plant breeding and drought in C-3 cereals: what should we breed for? Annals of Botany 2002;89(7) 925-940.
2 - Tester M, Bacic A. Abiotic stress tolerance in grasses. From model plants to crop plants. Plant Physiology 2005;137(3) 791–793.
3 - Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK. Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal 2006;45(4) 523-539.
4 - Intergovernmental Panel on Climate Change (2007). http://www.ipcc.ch. Accessed 25 October 2007.
5 - Passioura JB. The drought environment: physical, biological and agricultural perspectives. Journal of Experimental Botany 2007;58(2) 113–117.
6 - Munns R, Tester M. Mechanisms of salinity tolerance. Annual Review of Plant Biology 2008;59(1) 651-681.
7 - Vinocur B, Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Current Opinion in Biotechnology 2005;16(2) 123-132.
8 - Shao HB, Chu LY, Jaleel CA, Zhao CX. Water-deficit stress-induced anatomical changes in higher plants. Comptes Rendus Biologies 2008;54(3) 215–225.
9 - Grime JP. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist 1977;111(7) 1169–1194.
10 - Gaucherand S, Liancourt P, Lavorel S. Importance and intensity of competition along a fertility gradient and across species. Journal of Vegetation Science 2006;17(4) 455-464.
11 - Mittler R. Abiotic stress, the field environment and stress combination. Trends in Plant Science 2006;11(1) 11-19.
12 - Taiz L, Zeiger E. Plant Physiology. Sunderland: Sinauer Associates, 2009.
13 - Liancourt P, Callaway RM, Michalet R. Stress tolerance and competitive-response ability determine the outcome of biotic interactions. Ecology 2005;86(6) 1611-1618.
14 - Ives AR, Carpenter SR. Stability and Diversity of Ecosystems. Science 2007;317(5834) 58-62.
15 - Butterfield BJ. Effects of facilitation on community stability and dynamics: synthesis and future directions. Journal of Ecology 2009;97(6) 1192-1201.
16 - Villarreal-Barajas T., Martorell C. Species-specific disturbance tolerance, competition and positive interactions along an anthropogenic disturbance gradient. Journal of Vegetation Science 2009;20(6) 1027-1040
17 - Boyer JS. Plant productivity and environment. Science 1982;218(4571) 443-448.
18 - Amarjit KN, Kumari S, Sharma DR. In vitro selection and characterization of water-stress tolerant cultures of bell pepper. Indian Journal of Plant Physiology 2005;10(1) 14-19.
19 - Hillel D. Salinity; Management. In: Hillel D, Hatfield JH, Powlson DS, Rosenzweig C, Scow KM, Singer MJ, Sparks DL. (Eds.) Encyclopedia of Soils in the Environment. London: Elsevier/Academic Press; 2005. p.435-442.
20 - Ashraf M., Harris PJC. Potential biochemical indicators of salinity tolerance in plants. Plant Science 2004;166(1) 3-16.
21 - Evelin H, Kapoor R, Giri B. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Annals of Botany 2009;104(7) 1263-1280.
22 - Cowan IR. Water use and optimization of carbon assimilation. In: Lang OL, Nobel PS, Osmond CB, Ziegler H. (Eds.) Physiological plant ecology. II. Water relations and carbon assimilation. Berlin: Springer-Verlag; 1982. p.589–613.
23 - Davies WJ, Zhang J. Root signals and the regulation of growth and development of plants in drying soil. Annual Review of Plant Physiology and Plant Molecular Biology 1991; 42(1) 55–76.
24 - Zhang J, Jia W, Yang J, Ismail AM. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Research 2006; 97(1) p.111-119.
25 - Waseem M, Ali A, Tahir M, Nadeem MA, Ayub M, Tanveer A, Ahmad R, Hussain M. Mechanism of drought tolerance in plant and its management through different methods. Continental Journal of Agricultural Science 2011;5(1) 10-25.
26 - Reddy AR, Chiatanya KV, Vivekanandan M. Drought induced responses of photosynthesis and antioxidant metabolism in higher plants. Journal of Plant Physiology 2004;161(11) 1189–1202.
27 - Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Molecular Biology 2000;51(1) 463-499.
28 - Horie T, Karahara I, Katsuhara M. Salinity tolerance mechanisms in glycophytes: An overview with the central focus on rice plants. The Rice Journal 2012;5(1) 1-18.
29 - Chaitanya KY, Sundar D, Jutur PP, Reddy AR. Water stress effects on photosynthesis in different mulberry cultivars. Plant Growth Regulation 2003;40(1) 75-80.
30 - Munns R. Comparative physiology of salt and water stress. Plant, Cell and Environment 2002;25(2) 239–250.
31 - Mahajan S, Tuteja N. Cold, salinity and drought stresses: An overview. Archives of Biochemistry and Biophysics 2005;444(2) 139-158.
32 - Yihun Y, Shultz B, Haile AM, Erkossa T. Agricultural Productivity Optimization in water scarce Semi-Arid Region of Ethiopia. Delft: UNESCO‐IHE; 2010.
33 - Wang Q,
34 - Takahashi H. A Land surface water deficit model for an arid and semiarid region: Impact of desertification on the water deficit status in the Loess Plateau, China. Journal of Climate 1999;12(1) 244-257.
35 - Hanson B, May D. Drip irrigation salinity management for row crops. Oakland: University of California; 2011.
36 - Slinger D, Tenison K. Salinity Glove Box Guide: NSW Murray & Murrumbidgee Catchments. New South Wales: NSW Department of Primary Industries; 2007.
37 - Grattan SR. Irrigation water salinity and crop production. Oakland: University of California; 2002.
38 - Edwards CA, Bohlen PJ. Biology and ecology of earthworms, London: Chapman & Hall; 1996.
39 - Podmore C. Irrigation salinity – causes and impacts. Primefact 2009;937(1) 1-4.
40 - FAO - Food and Agriculture Organization of the United Nations. Management of irrigation induced induced salt-affected soils. Rome: CISEAU, IPTRID, AGLL and FAO ; 1996. http://www.fao.org (accessed 07 August 2012).
41 - Prisco JT. Alguns aspectos da fisiologia do ‘’ stress salino. Revista Brasileira de Botânica 1980, 3: 85-94.
42 - Prisco JT, Gomes-Filho E. Fisiologia e bioquímica do estresse salino em plantas. In : Gheyi HR, Dias NS, Lacerda FC. Manejo da Salinidade na Agricultura : Estudos Básicos e Aplicados (Eds). Expressão Gráfica e Editora : Fortaleza, INCTSal, 478p, 2010.
43 - Benzona N, Hensley D, Yogi J, Tavares J, Rauch F, Iwata R, Kellison M, Wong M, and Patti C. Salt and wind tolerance of landscape plants for Hawai’i. Cooperative Extension Service, Landscape 2009; 13 : 1-9.
44 - Silva EN, Ribeiro RV, Ferreira-Silva SL, Viégas RA, Silveira JAG. Comparative effects of salinity and water stress on photosynthesis, water relations and growth of Jatropha curcas plants. Journal of Arid Environments 2010; 74(10): 1-8.
45 - Sidari M, Mallamacci C, Muscolo A. Drought, salinity and heat differently affect seed germination of Pinus pinea. Journal of Forest Research 2008; 13:326–330.
46 - Wang W, Wang R, Yuan Y, Du N, Guo W. Effects of salt and water stress on plant biomass and photosynthetic characteristics of Tamarisk (Tamarix chinensis Lour.) seedlings. African Journal of Biotechnology 2011; 10: 17981-1789.
47 - Läuchli A, Grattan SR. Plant growth and development under salinity stress. In Jenkis MA, Hasegawa PM, Jain SM (Eds). Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops. California: Springer; 2007. p. 1-32.
48 - Kayaa MD, Okçu G, Atak M, Çıkılı Y, Kolsarıcı O. Seed treatments to overcome salt and drought stress during germination in sunflower (Helianthus annuus L.). European Journal Agronomy 2006; 24: 291–295.
49 - Patanè C, Saita A, Sortino O. Comparative effects of salt and water stress on seed germination and early embryo growth in two cultivars of sweet sorghum. Journal Agronomy and Crop Science 2012, 1-8.
50 - Flowers TJ, Colmer TD. Salinity tolerance in halophytes. New Phytologist 2008; 179: 945–963.
51 - Albert R, Pfundner G, Hertenberger G, Kastenbauer T, Watzka M. The physiotype approach to understanding halophytes and xerophytes. In: Breckle S-W, Schweizer B, Arndt U, eds. Ergebnisse weltweiter ökologischer Forschung. Stuttgart, Germany: Verlag Günter Heimbach, 2000; p. 69–87.
52 - Breckle SW. Salinity, halophytes and salt affected natural ecosystems. In: Läuchli A, Lüttge U, eds. Salinity: environment–plants–molecules. Dordrecht, the Netherlands: Kluwer Academic Publishers; 2002. p. 53–77.
53 - Grigore MN, Villanueva M, Boscaiu M, Vicente O. Do Halophytes Really Require Salts for Their Growth and Development? An Experimental Approach. Notulae Scientia Biologicae 2012; 4(2):23-29.
54 - Vicente O, Boscaiu M, Naranjo MA, Estrelles E, Bellés JM, Soriano P. Responses to salt stress in the halophyte Plantago crassifolia (Plantaginaceae). Journal of Arid Environments, 2004; 58:463-481.
55 - Li XY, Zhang XM, He XY, Zeng FJ, Thomas FM, Foetzki A. Drought stress and irrigation effects on water relations of Tamarix ramosissima in the Qira Oasis. Acta Phytoecologica Sinica Chinese, 2004; 28(5): 644-650.
56 - Souza ER, Freire MBGS, Cunha KPV, Nascimento CWA, Ruiz HA, Teixeira MA. Biomass, anatomical changes and osmotic potential in Atriplex nummularia Lindl. cultivated in sodic saline soil under water stress. Environmental and Experimental Botany, 2012; 82: 20– 27.
57 - Silveira JAG, Araújo SAM, Lima JPMS, Viégas RA. Roots and leaves display contrasting osmotic adjustment mechanisms in response to NaCl-salinity in Atriplex nummularia. Environmental and Experimental Botany, 2009; 66: 1–8.
58 - Mamdouh M, Nemat A, Abdel-Hamid A, Mamdouh MS, Abu-Alnaga AZ, Nada RM, Reham M. Physiological aspects of tolerance in Atriplex halimus L. to NaCl and drought. Acta Physiologia Plantarum 2011; 33:547–557.
59 - Brown CE, Pezeshki SR, DeLauneb RD. The effects of salinity and soil drying on nutrient uptake and growth of Spartina alterniflora in a simulated tidal system. Environmental and Experimental Botany 2006; 58: 140–148.
60 - Da Matta F. Ecophysiology of tropical tree crops: an introduction. Brazilian Journal of Plant Physiology 2007; 19: 239-244.
61 - Burghardta M, Burghardta A, Gall J, Rosenbergerb C, Riedererb M. Ecophysiological adaptations of water relations of Teucrium chamaedrys L. to the hot and dry climate of xeric limestone sites in Franconia (Southern Germany). Flora 2008; 203: 3–13.
62 - Díaz-López, L.; Gimeno, V.; Lidón, V.; Simón, I.; Martínez, V.; García-Sánchez, F. The tolerance of Jatropha curcas seedling to NaCl: An ecophysiological analyses. Plant Physiology and Biochemistry 2012; 54: 34-24.
63 - Azevedo-Neto AD, Prisco JT, Enéas-Filho J, Lacerda CF, Silva JV, Costa PHA. Effects of salt stress on plant growth, stomatal reponse and solute accumulation of different maize genotypes. Brazilian Journal of Plant Physiology 2004; 16(1): 31-38.
64 - Esteves BS, Suzuki MS. Salinity effects on plants. Oecologia Brasilica 2008; 12 (4): 662-679.
65 - Bakke IA, Freire ALO, Bakke OA, Andrade AP, Bruno ALO. Water and sodium chloride effects on Mimosa tenuiflora (WILLD.) poiret seed germination. Caatinga 2006; 19(3): 261-267.
66 - Gondim FA, Gomes-Filho E, Lacerda CF, Prisco JT, Azevedo Neto AD, Marques EC. Pretreatment with H2O2 in maize seeds: effects on germination and seedling acclimation to salt stress. Brazilian Journal of Plant Physiology 2010; 22(2): 103-112.
67 - Silva EN, Silveira JAG, Rodrigues CRF, Lima CS, Viégas RA. Contribuição de solutos orgânicos e inorgânicos no ajustamento osmótico de pinhão-manso submetido à salinidade. Pesquia agropecuária brasileira 2009; 44(5): 437-445.
68 - Freitas VS, Alencar NLM, Lacerda CF, Prisco JT, Gomes-Filho E. Changes in physiological and biochemical indicators associated with salt tolerance in cotton, sorghum and cowpea. African Journal of Biochemistry Research 2011; 5(8): 264-271.
69 - Praxedes SC, Lacerda CF, DaMatta FM, Prisco JT, Gomes-Filho E. Salt tolerance is associated with differences in accumulation, biomass allocation and photosynthesis in cowpea cultivars. Journal of Agronomy and Crop Sceince 2010; 196: 193-204.
70 - Costa PHA, Silva JV, Bezerra MA, Enéas-Filho J, Prisco JT, Gomes-Filho E. Growth and organic and inorganic solute contents in NaCl-stressed cultivars of Vigna unguiculata. Revista Brasileira de Botânica 2003; 26 (3): 289-297.
71 - Marques EC, Freitas VS, Bezerra MA, Prisco JT, Gomes-Filho E. Effects of salt stress on germination, emergence and establishment of dwarf-cashew seedling. Revista Ciência Agronômica 2010; 42 (4): 993-999.
72 - Bezerra MA, Lacerda CF, Gomes-Filho E, Abreu CEB, Prisco JT. Physiology of cashew plants grown under adverse conditions. Brazilian Journal of Plant Physiology 2007; 19 (4): 449-461.
73 - Ferreira-Silva SL, Silveira JAG, Voigt EL, Soares LSP, Viégas RA. Changes in physiological indicators associated with salt tolerance in two contrasting cashew rootstocks. Brazilian Journal of Plant Physiology 2008; 20 (1): 51-59.
74 - Abreu CEB, Bezerra MA, Enéas-Filho J, Prisco JT, Gomes-Filho E. Physiological and biochemical changes occurring in dwarf-cashew seedlings subjected to salt stress. Brazilian Journal of Plant Physiology 2008; 20 (2): 105-118.
75 - Alvarez-Pizarro JC, Alencar NLM, Prisco JT, Gomes-Filho E. Salt-induced changes on H+-ATPase activity, sterol and phospholipid content and lipid peroxidation of root plasma membrane from dwarf- cashew (Anacardium occidentale L.) seedlings. Plant Growth Regulation 2009; 59 (2): 125-135.
76 - Lima MA, Bezerra MA, Gomes-Filho E, Pinto CM, Enéas-Filho J. Gas exchange in leaves of sun and shade of cashew in different water regimes. Revista Ciência Agronômica 2010; 41 (4): 654-663.
77 - Amorim AV, Gomes-Filho E, Bezerra MA, Prisco JT, Lacerda CF. Physiologic responses of precocious dwarf cashew at different levels of salinity. Revista Ciência Agronômica 2010; 41(1): 113-121.
78 - Dombroski LD, Praxedes SC, Freitas RMO, Pontes FM. Water relations of Caatinga trees in the dry season. South African Journal of Botany 2011; 77: 430–434.
79 - Santos MG, Ribeiro RV, Machado EC, Pimentel C. Photosynthetic parameters and leaf water potential of five common bean genotypes under mild water deficit. Biologia Plantarum 2009, 53(2): 229-236.
80 - Trovão DMB, Fernandes PD, Andrade LA, Dantas-Neto J. Seazonal variations of physiological aspects of Caatinga species. Revista Brasileira de Engenharia Agrícola Ambiental 2007, 11(3): 307–311.
81 - Souza RP, Machado EC, Silva JAB, Lagôa AMMA, Silveira JAG. Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environmental and Experimental Botany 2004, 51: 45–56.
82 - Santos MG, Ribeiro RV, Machado EC, Pimentel C. Photosynthetic parameters and leaf water potential of five common bean genotypes under mild water deficit. Biologia Plantarum 2009, 53 (2): 229-236.
83 - Chaves MM, Maroco JP, Pereira JS. Understanding plant responses to drought-from genes to whole plant. Functional Plant Biology 2003, 30: 239-264.