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Int. J. Biosci. 2014

RESEARCH PAPER OPEN ACCESS

Influence of drought stress on photosynthetic enzymes,

chlorophyll, protein and relative water content in crop plants

Alireza Sobhkhizi, Mahdiyeh fadai Rayni, Hossein Badie Barzin, Mohsen Noori*

Higher Educational Complex of Saravan, Iran

Key words: Drought tolerance, Reactive oxygen species, Leaf water content.

http://dx.doi.org/10.12692/ijb/5.7.89-100

Article published on October 06, 2014

Abstract

Water deficit/drought affects every aspect of plant growth and the yield modifying the anatomy, morphology,

physiology, biochemistry and finally the productivity of crop. Water is an important factor in agricultural and

food production yet it is a highly limited resource and is becoming increasingly more important over time for

optimal crop production. While decreased Rubisco activity may not be the cause of photosynthetic reduction

during water stress, its down-regulation may still be important because it could preclude a rapid recovery upon

rewatering. Chlorophyll is one the major chloroplast components for photosynthesis and relative chlorophyll

content has a positive relationship with photosynthetic rate. Water stress causes deceleration of cell enlargement

and thus reduces stem lengths by inhibiting inter nodal elongation and also checks the tillering capacity of

plants. The importance of root system in acquiring water has long been recognized. Influence of drought stress

on Photosynthetic enzymes, Chlorophyll, Protein and Relative water content in crop plants.

* Corresponding Author: Mohsen Noori 1366.nouri@gmail.com

International Journal of Biosciences | IJB |

ISSN: 2220-6655 (Print) 2222-5234 (Online)

http://www.innspub.net

Vol. 5, No. 7, p. 89-100, 2014

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Int. J. Biosci. 2014

Introduction

At present in consequence of global climate changes a

progressive increase of the average annual

temperature of the earth results in the development

of some stress factors. This leads to the significant

decrease of the productivity of agricultural plants in

regions having water deficit. Modern biotechnological

methods have been used now to investigate

molecular- genetic bases of drought resistance to

create cultures tolerant to drought and high

temperature (Raines, 2006). water stress is major

harmful factor in arid and semi-arid regions

worldwide (Ranjana et al., 2006) that limits the area

under cultivation and yield of crops. Drought is

observed in irrigated areas due to insufficient supply

of water and canal closure (Hafeez et al., 2003).

Water deficit/drought affects every aspect of plant

growth and the yield modifying the anatomy,

morphology, physiology, biochemistry and finally the

productivity of crop (Jones et al., 2003; Hafiz et al.,

2004). Stress is the result of complex interactions

between plants and the environment. In natural

conditions the effect of only one stress factor without

interaction with others does not occur. Many

environmental factors in isolation may not cause

stress, but in different combinations they can create

stress conditions for plants (Slováková, 2007).

Motivation and aims of the study is influence of

drought stress on Photosynthetic enzymes,

Chlorophyll, Protein and Relative water content in

crop plants.

Matherials and methods

This paper is a review article of the literature search

on ISI, Scopus and the Information Center of Jahad

and MAGIRAN SID is also abundant. Search library

collection of books, reports, proceedings of the

Congress was also performed. All efforts have been

made to review articles and abstracts related to

internal and external validity.

Result and discussion

Water resource management

Water is an important factor in agricultural and food

production yet it is a highly limited resource and is

becoming increasingly more important over time for

optimal crop production (O’Shaughnessy et al., 2011;

Wang et al., 2012). Therefore, research on irrigation

and water management has focused on crop yield

responses to water supply (Chen et al., 2010 a;

Köksal, 2011). The use of remote sensing for irrigation

practices, water resource management, and disease

and insect management has been largely investigated

(Ozdogan, 2011; Elmetwalli et al., 2012).

Fig. 1. Summary of the main effects of water stress

on the photosynthetic parameters of C4 leaves.

Stomatal and non-stomatal factors are indicated by

dashed and continuous lines, respectively. The (–)

sign indicates an effect in the opposite direction. The

term leakiness (Φ) is defined as the fraction of CO2

fixed by PEPC which leaks out of the bundle sheath.

Photosynthetic enzymes

Photosynthesis is the oldest and the most important

biochemical process on the Earth. It is a unique

process on the Earth and its result is the production

of organic substances and oxygen. Photosynthesis is a

process used by plants and other organisms to

convert light energy, normally from the sun, into

chemical energy and is very sensitive to drought

(Brestič, 2001). The data on water stress induced

regulation of the activity of photosynthetic enzymes

other than Rubisco are scarce. Thimmanaik et al.

(2002) studied the activity of several photosynthetic

enzymes under progressive water stress in two

different cultivars of Morus alba. Unlike Rubisco,

which is highly stable and resistant to water stress,

the activity of some enzymes involved in the

regeneration of ribulose-1,5-bisphosphate (RuBP) are

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Int. J. Biosci. 2014

progressively impaired from very early stages of water

stress. Thus, these results present the possibility that

some enzymes involved in the regeneration of RuBP

could play a key regulatory role in photosynthesis

under water stress. During water stress induced by

polyethilenglycole, Rubisco activity significantly

increased in young potato leaves, while decreased in

mature leaves (Bussis et al., 1998). But NADP-

GAPDH and PRK activities have been decreased and

this change became faster in the course of drought.

While decreased Rubisco activity may not be the

cause of photosynthetic reduction during water stress,

its down-regulation may still be important because it

could preclude a rapid recovery upon rewatering

(Ennahli and Earl, 2005). Similarly, some reports

have shown strong drought-induced reductions of

Rubisco activity per unit leaf area (Maroco et al.,

2002) and per mg showed that the decrease of

Rubisco activity in vivo was not connected with the

protein content. It occurs because of CO2

concentration decrease in the carboxylation center in

consequence of the partly closing of stomata (Flexas

et al., 2006). But it is known, that enzyme regulation

occurs not only in transcription, but also in

posttranscriptional level. Activities of the tested

enzymes are regulated by light as well as by the

concentration of photosynthetic metabolites (Raines,

2006).

Fig. 2. Physiological mechanisms induced by water stress.

Modern investigations of genotypes differing in their

drought tolerance

Modern investigations of genotypes differing in their

drought tolerance within the same species and among

the ancestors of crops may serve as a marker in

obtaining more productive genotypes. Photosynthetic

CO2 assimilation in C3-plants is affected by

environmental variables including temperature, CO2

concentration and water availability. Of these

variables, water is the main biotic factor limiting

plant productivity in many regions of the world

(Chaves et al., 2002).

Chlorophyll

Chlorophyll is one the major chloroplast components

for photosynthesis and relative chlorophyll content

has a positive relationship with photosynthetic rate.

Chen et al.( 2007) noted that assessment of pigment

content has become an effective means of monitoring

plant growth and estimating photosynthetic

productivity while Fillella et al.(1995) reported that

remote estimates of pigment concentration provides

an improved evaluation of the spatial and temporal

dynamics of plant stress. Chlorophyll concentration

has been known as an index for evaluation of source

therefore a decrease of this can be consideration of a

non-stomata limiting factor in the drought stress

conditions. Chlorophyll concentration has been

known as an index for evaluation of source (Herzog,

1986), therefore decrease of this can be consideration

as a nonstomata limiting factor in the drought stress

conditions. There are reports about decrease of

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chlorophyll in the drought stress conditions

(Majumdar et al, 1981; Mayoral et al, 1981; Kuroda et

al, 1990) Also, it is reported that chlorophyll content

of resistant and sensitive cultivars to drought and

thermal stress reduced. But resistant cultivar to

drought and thermal stress conditions had high

chlorophyll content (Sairam et al, 1997). Other

reports have represented that drought stress did not

have effect on chlorophyll concentration

(Kulshreshtha et al, 1987). According to Maxwell and

Johnson (2000) the measurement of chlorophyll

fluorescence in situ is a useful tool to evaluate the

tolerance of the photosynthetic apparatus to

environmental stress which reduces the maximum

efficiency of PSII photochemistry. It is used to

determine how light use efficiency for photosynthesis

occurs at the cellular level. It can also be used to

estimate the activity of the thermal energy dissipation

in photosystem II which protects photosystems from

the adverse effects of light and heat stress.

Fig. 3. Schematic overview of a common System Biology approach to study abiotic stress responses in plants.

Primary responses of plants to water deficit

Water is a necessary factor in life and it influences the

existence of plants and realization of their life cycle.

One of the primary responses of plants to water

deficit is stomata closure,which minimizes water loss

(Carmo-Silvia, 2012). Plants wither and close stomata

to limit transpiration and prevent more loss of water.

Drought as abiotic stress is multidimensional in

nature (Rahman, 2012).

Fig. 4.Water and salt stress tolerance mechanisms in plants.

Reactive oxygen species

Stress factors such as drought trigger common

reactionsmin plants and lead to cellular damages

mediated by reactive oxygen species (ROS).

According to Price and Hendry (1991) who studied

the role of oxygen radicals in different grasses

exposed to drought, water deficit stress causes an

overall inhibition of protein synthesis, inactivation of

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Int. J. Biosci. 2014

several chloroplast enzymes, impairment of electron

transport, increased membrane permeability, and

increased activity of the H2O2 scavenger system.

Antioxidative enzymes such as superoxide dismutase

(SOD), ascorbate peroxidase (APX) and catalase

(CAT) play an important role against drought stress

(Apel and Hirt, 2004; Habibi and Hajiboland, 2011).

Drought resistance

Water stress can affect photosynthesis directly by

causing changes in plant metabolism or indirectly by

limiting the amount of CO2 available for fixation

(Lawlor and Cornic, 2002). Drought resistance of a

plant is related to its ability to maintain higher

relative water content in the leaves under water

stress. Many changes in gene expression occur in

plants growing under limited water conditions (Bray,

2002). Provisional stresses existing in the

intermediate stages of growth has a negative impact

on the plant growth, but the plants that have a higher

tolerance to dryness and after solving the stress can

improve and rectify the losses, will indicate the lowest

reduction in the function (Daneshian et al, 2009).

Protein

Water stress is reported to inhibit the incorporation

of amino acids into proteins and to cause a decrease

in the protein content of the tissues. Water deficit

impedes protein synthesis at the ribosomal level:

some proteins are apparently formed and inactivated

quickly whereas others appear to be relatively stable.

Studies on sunflower by Rao et al. (1987) showed that

water deficit reduces seed protein content. Protein

content, particularly soluble protein usually falls to

about 40-60% of the initial content as the water

deficit becomes intense in drought sensitive plants.

Dry matter accumulation

Dry matter accumulation is a result of assimilate flow

from the resource organs to the storing organs. Dry

matter accumulation is initially set by the storages

themselves. The effect of the resource is not often

direct, but it is through storing organs formation and

it is indirect. Although the speed of assimilate

transferring is depended on the transferring path, but

the transferring path has the least effect in setting the

distribution of dry matter of the plant (Marcelis,

1996). The available water for the plants is one of the

most important factors limiting the potential function

of agriculture in the semidry regions (Dogdalen et al.

2006, Stone et al. 2001). The increasing water

shortage is the most important issue in many

countries in the world (Zurat et al. 2004) and the

limits of the availability of the water for irrigation

needs fundamental changes in the irrigation

management or application of methods in which the

water resources are preserved better (Dogdalen et al.

2006).

Models that adequately simulate the effects of water

stress on yield

Models that adequately simulate the effects of water

stress on yield can be valuable tools in irrigation

management. These models can be used to optimize

the allocation of irrigation water between different

crops and or the distribution of water during the crop

season (Bryant et al., 1992; Cabelguenne et al., 1995;

Cabel guenne et al., 1997; Howell et al., 1989; Stewart

et al., 1975; Wenda and Hanks, 1981). Complete

testing of a model is needed before it can be used for

irrigation planning in a particular area. This will

ensure that the model correctly simulates the main

physiological processes that affect crop yield under

water stress. Among the models that can be used for

this task, a distinction can be made between crop

growth simulation models, which simulate main

processes of crop growth (leaf area growth, biomass

production and partition), such as CERES-maize

(Jones and Kiniry, 1986), Crop Syst (Stockle et al.,

1994), EPIC (Williams et al., 1984), GOSSYM (Reddy

et al., 1997), and SUCROS (Penning de Vries and Van

Laar, 1982), and those models that do not explicitly

simulate crop growth but that have been developed

for irrigation planning. CROPWAT (Smith, 1992) is

the best known among the latter.

Ion uptake due water stress

Since nutrient uptake is closely linked to water soil

status, it is expected that, decline of available soil

moisture might decrease the diffusion rate of

94 Sobhkhizi et al.

Int. J. Biosci. 2014

nutrients from soil matrix to roots. Evidence of

decreased ion uptake due water stress effect was

attributed to the reduction in root absorption power

(Aldesuquy et al., 2012). Decreasing water availability

under drought generally results in limited total

nutrient uptake and their diminished tissue

concentrations in crop plants. An important effect of

water deficit is on the acquisition of nutrients by the

root and their transport to shoots. Lowered

absorption of the inorganic nutrients can result from

interference in nutrient uptake and the unloading

mechanism, and reduced transpirational flow (Garg,

2003; McWilliams, 2003). However, plant species

and genotypes of a species may vary in their response

to mineral uptake under water stress. In general,

moisture stress induces an increase in N, a definitive

decline in P and no definitive effects on K (Garg,

2003). Transpiration is inhibited by drought, as

shown for beech (Peuke et al., 2002), but this may

not necessarily affect nutrient uptake in a similar

manner. Influence of drought on plant nutrition may

also be related to limited availability of energy for

assimilation of NO−3 /NH+4 , PO43− and SO4 2−: they

must be converted in energy-dependent processes

before these ions can be used for growth and

development of plants (Grossman and Takahashi,

2001). As nutrient and water requirements are closely

related, fertilizer application is likely to increase the

efficiency of crops in utilizing available water. This

indicates a significant interaction between soil

moisture deficits and nutrient acquisition. Studies

show a positive response of crops to improved soil

fertility under arid and semi-arid conditions.

Currently, it is evident that crop yields can be

substantially improved by enhancing the plant

nutrient efficiency under limited moisture supply

(Garg, 2003). It was shown that N and K uptake was

hampered under drought stress in cotton

(McWilliams, 2003). Likewise, P and PO3− contents in

the plant tissues diminished under drought, possibly

because of lowered PO4 3−mobility as a result of low

moisture availability (Peuke and Rennenberg, 2004).

In drought-treated sunflower, the degree of stomatal

opening of K+-applied plants initially indicated

quicker decline. However, at equally low soil water

potential, diffusive resistance in the leaves of

K+applied plants remained lower than those receiving

no K+ (Lindhauer et al., 2007). However root growth

and potential root hydraulic conductance have been

found to increase with inoculation (Pereyra, et al.,

2006) who reported that inoculation is accompanied

by biochemical changes in roots which, in turn,

promote plant-growth and tolerance to water stress.

Presumably, increased root growth would lead to a

greater volume of soil explored and hence a greater

potential reservoir of soil water. It is also possible that

inoculation enables the plant to better withstand

drought conditions due to its role in energy storage

and protein formation. Thus, under such drought

condition and continuous decrease in nutrient uptake

of the soils the importance use of seed inoculation has

been indicated by Damodar et al., (1999).

Leaf water content

Leaf water content is a useful indicator of plant water

balance since it expresses the relative amount of

water present on the plant tissues (Yamasaki and

Dillenburg, 1999). The species adapted better to dry

environments have higher relative water content at

given water potential. Water deficit also causes leaf

water potential and rates of elongation to decline

more rapidly in rice than in maize or sorghum so that

dry matter accumulation and nutrient uptake decline

or cease. Leaf dehydration can be minimized by

decreasing evapotranspiration or by increasing water

absorption from the drying soil (Chaves et al., 2003).

Shoot and root growth

Water stress causes deceleration of cell enlargement

and thus reduces stem lengths by inhibiting inter

nodal elongation and also checks the tillering capacity

of plants. The importance of root system in acquiring

water has long been recognized. A prolific root system

can confer the advantage to support accelerated plant

growth during the early crop growth stage and extract

water from shallow soil layers that is otherwise easily

lost by evaporation in legumes (Johansen et al.,

1992). Differences in root length could confer

tolerance to drought by some varieties. Greater plant

fresh and dry weights under water deficit conditions

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Int. J. Biosci. 2014

are desirable characters. A common adverse effect of

water deficit on crop plants is the reduction in fresh

and dry biomass production. However some

genotypes shows better stress tolerance than the

others. Studies by Mohammadian et al. (2005)

showed that mild water stress affected the shoot dry

weight while shoot dry weight was greater than root

dry weight loss under severe stress in sugar beet

genotypes. Wullschleger et al. (2005) reported a

decrease in the root dry weight under mild and severe

water stress in populous species.

Stomata characteristics

Epidermis tissues have three types of main cells

include epidermal cells, guard cells with their

subsidiary cells and trichomes or leaf hairs (Munir et

al., 2011). In most species, frequency of stomata in

the lower epidermis are more than the upper

epidermis (Muradoglu and Gundogdu, 2011). Traits

of leaf epidermal tissue such as stomata size and

shape as well as form of trichomes are valuable in

taxonomy and identification of plant genera and

species (Munir et al., 2011, Scatena et al., 2005;

Dickison, 2000). Anatomical traits such as high

stomatal density, a reduction of stomata size and

deeply developed stomata can be used for

identification of xerophytic plants (Martins and Zieri,

2003, Belhadj et al., 2007). Stomata characteristics

such as frequency and dimensions are greatly affected

by type of species and environmental factors (Munir

et al., 2011, XueJun and XinShi, 2000).

Environmental stresses such as water stress most

effects on leaf traits (XueJun and XinShi, 2000).

Breeding program

In developing a breeding program to improve the

drought resistance of a crop plant it is necessary to

gain knowledge concerning the genetics and

physiology of tolerance mechanisms (Clarke &

Townley-Smith, 1984; Inoue et al., 2004). Yield is the

principle selection index used under drought stress

conditions. If we had known how to select for high

yield potential using criteria other than grain yield,

perhaps results could have been achieved by way of

enhanced total plant productivity rather than just by

changing the production ratio (Blum, 2005). The

identification of physiological traits responsible for

drought tolerance should be considered in the

breeding program, because grain yield and drought

resistance are controlled at independent genetic loci

(Morgan, 1984). Therefore, the use of physiological

traits as an indirect selection would be important in

augmenting yield-based selection procedures.

Selection efficiency could be improved if particular

physiological and/or morphological attributes related

to yield under a stress environment could be

identified and employed as selection criteria for

complementing traditional plant breeding (Acevedo,

1991). These morpho physiological traits should be

highly heritable, greatly correlated with stress

tolerance and can be easily assessed. A range of traits

has been suggested that could be utilized to increase

selection efficiency and used as indirect selection for

improving yield under stress conditions.

Proline content

However it is reported that proline content in

resistant wheat cultivars was more than in sensitive

cultivar under the drought and salinity stress (kao,

1981). Also accumulation of proline has been reported

under the drought stress in another various crops

such as chick pea (cicer arietinum), (Ayerb & Tenori,

1998) corn (zea mays), (Serraj & Sinclair, 2002) and

peanut (Arachis hypogaea ) (Smith et al, 2002). Ten

& Hollaran ; (1982) expressed that the crops under

the stress, accumulate the most amount of free

proline in their leaves tissue by studying of changes

and correlation of proline accumulation in spring

wheat cultivars and comparison of performed

experiments by another researchers . Increasing of

proline amount due to drought stress has reported in

another researches (Heuer , 1994; Safarnejad et al,

1996; Mattioni , 1997 ; Sharpe &Verslues , 1999; ;

Staden et al , 1999; Serraj & Sinclair, 2002;Safarnejad

,2004).

Relative water content (RWC)

The difference of relative water content (RWC) has

been reported as 18.6 and 21.8 percent for most

resistant and most sensitive genotypes to drought

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Int. J. Biosci. 2014

stress in 2years of experiment. (Merah, 2001). In

studies that performed on 4 cultivars of bread wheat,

RWC reduced to 43 percent (from 88% to 45%) by

moisture stress (Siddique et al, 2000). (Mationn et al,

(1989) represented a similar report as regards a drop

in the amount of RWC in tolerant and sensitive

cultivars of barley.

Evaporation from leaves

Fuchs and Tanner (1966) reported that it is well-

known from energy balance considerations that leaf

temperature varies with evaporation from leaves and

hence is a function of stomata conductance (Jones,

1999). Leaf temperature is a physiological trait that

can be used for monitoring plant water status

(Jimenez-Bello et al., 2011). In general, water stress

causes stomata closure in plants, and this leads to

higher leaf temperature (Sdoodee, Kaewkong, 2006).

References

Acevedo E. 1991. Improvement of winter cereal

crops in Mediterranean environments. Use of yield,

morphological and physiological traits. In Acevedo, E.

(ed): Physiology-Breeding of Winter Cereals for

Stressed Mediterranean Environments. Journal of

Plant Physiology 55, 273– 305.

http://dx.doi.org/10.1002/j.20500416.2008.tb0030

0.x

Aldesuquy HS, Abbas MA, Abo- Hamed SA,

Elhakem AH, Alsokari SS. 2012. Glycine betaine

and salicylic acid induced modification in

productivity of two different cultivars of wheat grown

under water stress. Journal of Stress Physiology &

Biochemistry 8(2), 72-89.

http://dx.doi.org/10.2135/cropsci2002.1996

Alexieva V, Sergiev I, Mapelli S, Karanov E.

2001. The effect of drought and ultraviolet radiation

on growth and stress markers in pea and wheat. Plant

Cell Environ. 24, 1337–1344.

http://dx.doi.org/10.2135/cropsci1997.0011183X003

700010038x

Al-Ghamdi A. 2009. Evaluation of oxidative stres

tolerance in two wheat (Triticum aestivum L.)

cultivars in response to drought. International

Journal of Agriculture and Biology 1, 7-12.

http://dx.doi.org/10.1016/S0308-521X(01)00023-3.

Amjad MK, Jabran SI, Awan AA, Ehsanullah

M. 2011. Morpho-physiological diversity and its

implications for improving drought tolerance in grain

sorghum at different growth stages. AJCS. 5(3), 308-

317.

http://dx.doi.org/10.1006/anbo.1999.1076

Apel K, Hirt H. 2004. Reactive oxygen species:

Metabolism, oxidative stress and signal transduction.

Pakistan Journal of Biological Sciences 55, 373–399.

http://dx.doi.org/10.1002/(SICI)1521-186X

Arora A, Sairam RK, Srivastava GC. 2002.

Oxidative stress and antioxidative system in plants.

Current Science 82, 1227-1238.

http://dx.doi.org/10.1002/ffj.1562

Asseng S, Foster I, Turner NC. 2011 The impact

of temperature variability on wheat yields, Glob.

Change Biol. 17, 997–1012.

http://dx.doi.org/10.1016/j.foodchem.2006.07.051

Ayerbe L, Tenorio JL. 1998. Turgor maintenance,

osmostic adjustment and soluble sugar and proline

accumulation in 49 pea cultivars in response to water

stress. Field crop Research 59, 225-235.

http://dx.doi.org/10.1016/S0308-521X(01)00023-3

Bakalova S, Nedeva D, Mckee J. 2008 protein

profiles in wheat seedlings subjected to dehydration

stress. Applied ecology and environmental research

6(2), 37- 48.

http://dx.doi.org/10.1002/(SICI)10991026(199801/0

2)13:1<1::AID-FFJ672>3.0.CO;2-4

Belhadj S, Derridj A, Moriana A, Gijon MDC,

Mevy JP, Gauquelin T. 2011 Comparative analysis

of stomatal characters in eight wild atlas pistachio

populations (Pistacia atlantica Desf.; Anacardiaceae).

International Research Journal of Plant Science.

97 Sobhkhizi et al.

Int. J. Biosci. 2014

2(3), 060-069.

http://dx.doi.org/10.1071/P9930639

Bernstein L, Francois LE. 1973. Comparisons of

drip, furrow, and sprinkler irrigation. Soil Sci. 115,

73- 86.

http://dx.doi.org/10.3390/12122567

Blum A. 2005. Drought resistance, water-use

efficiency, and yield potential – are they compatible,

dissonant, or mutually exclusive. Pakistan Journal of

Biological Sciences 56, 1159–1168.

http://dx.doi.org/10.1017/S0960258500004141

Bohnert HJ, Sheveleva E, 1998. Plant stress

adaptations—making metabolism move. Curr Opin

Plant Biol. 1, 267–274.

http://dx.doi.org/10.1002/ffj.1328

Boote KJ, Allen LH, Prasad PVV, Baker JT,

Gesch RW, Synder AM. 2005. Pan D.Elevated

temperature and CO2 impacts on pollination,

reproductive growth and yield of several globally

important crops, J. Agric. Meteorol. 60, 469–474.

http://dx.doi.org/10.1080/22297928.2000.1064826

9

Borrell AK, Hammer GL, Henzell RG. 2000.

Does maintaining green leaf area in sorghum improve

yield under drought. Dry matter production and yield.

Crop Science 40, 1037- 1048.

http://dx.doi.org/10.1002/cbdv.201000249

Borsani O, Valpuesta V, Botella MA. 2001.

Evidence for a role of salycylic acid in the oxidative

damage generated by NaCl and osmotic stress in

Arabidopsis seedling, Plant Physiol. 14, 110- 124.

http://dx.doi.org/10.1016/j.foodchem.2005.09.054

Bousba R, Djekoun A, Benbelkacem AE,

Kacem NS. 2011. Osmoregulation et osmoprotection

des cellules foliaires de blé dur (Triticum durum Desf)

sous condition de deficit hydrique 12, 134-147.

http://dx.doi.org/10.1081/PLN-120017665

Bousba R, Ykhlef N, Djekoun A. 2009. Water

use efficiency and flag leaf photosynthetic in response

to water deficit of durum wheat (Trticum durum

Desf).World Journal of Agricultural Sciences 5, 609 -

616.

http://dx.doi.org/10.2134/agronj2002.1530

Boyer JS. 1970. Leaf enlargement and metabolic

rates in corn, soybean, and sunflower at various leaf

water potentials. Plant Physiol. 46, 233-235.

http://dx.doi.org/10.1016/j.indcrop.2006.07.004

Boyer JS. 1982. Plant productivity and environment.

218, 443-448.

http://dx.doi.org/10.2135/cropsci1997.0011183X003

700010038x

Bray EA. 2002. Classification of genes differentially

expressed during water-deficit stress in Arabidopsis

thaliana: an analysis using microarray and

differential expression data. Field Crops Research.

89, 803-811.

http://dx.doi.org/10.1016/j.eja.2005.10.006

Bryant KJ, Benson VW, Kiniry JR, Williams

JR, Lace well RD. 1992. Simulating corn yield

response to irrigation timings: Validation of the EPIC

model Plant Cell Environ. 5, 237–242.

http://dx.doi.org/10.1017/S0960258500003032

Bussis D, Kauder F, Heineke D. 1998.

Acclimation of potato plants to polyethylene

glycolinduced water deficit. J. Exp. Bot. 49, 1349-

1360.

http://dx.doi.org/10.2478/v10247-012-0042-6

Caspari HW, Hossein M, Chalmers DJ. 1994.

Water use, growth, and fruit yield of ‘Hosui’ Asian

pears under deficit irrigation. J. Am. Soc. Hort. Sci.

119, 383--388.

http://dx.doi.org/10.1016/j.eja.2005.10.006

Cattivellia L, Rizza F, Badeck FW,

Mazzucotelli E, Mastrangelo AM. 2008. Drought

tolerance improvement in crop plants: An integrated

98 Sobhkhizi et al.

Int. J. Biosci. 2014

view from breeding to genomics, Drought tolerance

improvement in crop plants: An integrated view from

breeding to genomics, Field Crops Res. 105, 1–14.

http://dx.doi.org/10.1017/S0960258500003032

Challinor AJ, Wheeler TW, Slingo M. 2005.

Simulation of the impact of high temperature stress

on the yield of an annual crop, Agr. Forest Meteorol.

135, 180–189.

http://dx.doi.org/10.1017/S0960258500004141

Chaves MM, Maroco JP, Pereira JS. 2003.

Understanding plant responses to drought – from

genes to the whole plant. Funct. Plant Biol. 30, 239-

264.

http://dx.doi.org/10.1071/P9930639

Chaves MM. 1991 Effects of water deficits on carbon

assimilation. J. Exp. Bot. 42, 1–16.

http://dx.doi.org/10.2135/cropsci1992.0011183X003

200030033x

Chen L, Wang X. 2003. Features and functions of

plant moisture induced protein. Biology Teaching.

23(3), 503–508.

http://dx.doi.org/10.1093/aob/77.6.591

Cornic G. 2000. Drought stress inhibits

photosynthesis by decreasing stomatal aperture – not

by affecting ATP synthesis. Trends Plant Sci. 5, 187–

188.

http://dx.doi.org/10.1016/S0308-521X(01)00023-3

Crisosto CH, Johnson JG, Luza GM. 1994.

Irrigation regimes affect fruit soluble solids

concentration and rate of water loss of ‘O’Henry’

peaches. HortScience 29, 1169--1171.

http://dx.doi.org/10.2478/v10247-012-0052-4

Dai ZY, Ku MSB, Edwards GE. 1995. C4

photosynthesis. The effects of leaf development on

the CO2-concentrating mechanism and

photorespiration in maize. Plant Physiol. 107, 815–

825.

http://dx.doi.org/10.1006/anbo.1999.1076

Dash S, Mohanty N. 2001. Evaluation of assays for

the analysis of thermo tolerance and recovery

potentials of seedlings of wheat (Triticum aestivum

L.) cultivars. J. Plant Phys. 158, 1153-165.

http://dx.doi.org/10.4141/cjps94-012

Davies WJ, Hartung W. 2004. Has extrapolation

from biochemistry to crop functioning worked to

sustain plant production under water scarcity? In:

Proceeding of the 4th International Crop Science

Congress. 11, 34-54.

http://dx.doi.org/10.1016/j.eja.2005.08.001

English MJ, Musick JT, Murty VV. 1990. Deficit

irrigation. In: Hoffman, G.J., Howell, T.A., Solomon,

K.H. (Eds.), Management of Farm Irrigation System.

American Society of Agricultural Engineers, St.

Joseph 12, 631–663P.

http://dx.doi.org/10.1016/S0074-7696(08)62489-4

Ennahli S, Earl H. 2005. Physiological limitations

to photosynthetic carbon assimilation in cotton under

water stress. Crop Sci. 45, 2374- 2382.

http://dx.doi.org/10.1104/p.109.2.499

Lynch DR, Foroud N, Kozub GC, Farries BC.

1995. The effect of moisture stress at three growth

stages on the yield components of yield and

processing quality of eight potato cultivars. Am.

Potato J. 72, 375–386.

http://dx.doi.org/10.2135/cropsci2003.2135

Nouri A, Etminan JA. 2011. Assessment of yield,

yield related traits and drought tolerance of durum

wheat genotypes (Triticum turjidum var. durum

Desf.). Aus. J. Crop Sci. 5, 8-16.

http://dx.doi.org/10.1016/S0014-5793(00)01822-6

Nyachiro JM, Briggs KG, Hoddinott J,

Johnson-Flanagan AM. 2001. Chlorophyll

content, chlorophyll fluorescence and water deficit in

spring wheat, Cereal Res. Commun. 29, 135– 142.

http://dx.doi.org/10.2135/cropsci2002.1996

Ommen OE, Donnelly A, Vanhoutvin S, van

99 Sobhkhizi et al.

Int. J. Biosci. 2014

Oijen M, Manderscheid R. 1999. Chlorophyll

content of spring wheat flag leaves grown under

elevated CO2 concentrations and other

environmental stresses within the ESPACE-wheat

project. Eur. J. Agron. 10, 197-203.

http://dx.doi.org/10.1017/S0960258599000057

Ozkur O, Ozdemir F, Bor M, Turkan I. 2009.

Physiochemical and antioxidant responses of

theperennial xerophyte Capparis ovata Desf. To

drought. Environmental and Experimental Botany.

66, 487–492.

http://dx.doi.org/10.1002/(SICI)1521-186X

Pattanagul W, Madore MA. 1999. Water deficit

affects on raffinose family oligosaccharide

metabolism. 15, 34- 65.

http://dx.doi.org/10.1109/27.842898

Simova LV, Vassileva T, Petrova N. 2006.

Proteolytic activity in wheat leaves during drought

stress and recovery. Gen. Appl. Plant Physiol. Special

Issue. 22, 91-100.

http://dx.doi.org/10.1081/PLN-120017665

Singh PK, Mishra AK, Imtiyaz M. 1991. Moisture

stress and the water use efficiency of mustard.

Agricultural Water Management. 20, 245–253.

http://dx.doi.org/10.2134/agronj2002.1530

Stewart CR. 1981. Proline accumulation:

Biochemical aspects. In: Paleg LG, Aspinall D (Eds),

Physiology and Biochemistry of drought resistance in

plants. 12, 243-251.

http://dx.doi.org/10.2135/cropsci1997.0011183X003

700010038x

Stitt M., Schulze E. 1994. Does Rubisco controls

the rate of photosynthesis and plant growth? An

exercise in molecular ecophysiology. Plant Cell

Environ. 17, 465-487.

http://dx.doi.org/10.1016/j.indcrop.2006.07.004

Thimmanaik S, Giridara KS, Jyothsna KG,

Surnyanarayana N, Sudhakar C.

2002.Photosynthesis and the enzymes of

photosynthetic carbon reduction cycle in mulberry

during water stress and recovery. Photosynth. 40,

233-236.

http://dx.doi.org/10.1016/S0308-521X(01)00023-3

Tsakiris G, Pangalou D, Vangelis H. 2007.

Regional Drought Assessment based on the

Reconnaissance Drought Index (RDI), Water Resour.

Manag 21, 821–833.

http://dx.doi.org/10.2478/v10247-012-0042-6

Turner LB. 1991. The effect of water stress on the

vegetative growth of white clover (Trifolium repens

L.): Comparison of long-term water deficit and short-

term developing water stress. J. Exp. Bot. 42, 311-

316.

http://dx.doi.org/10.1016/j.eja.2005.10.006

Vendruscolo AC, Schuster M, Pileggi CA,

Scapim HBC, Molinari CJ, Marur C. 2007.

Stressinduced synthesis of proline confers tolerance

to water deficit in transgenic wheat. J. Plant Physiol.

164(10), 1367-1376.

http://dx.doi.org/10.1017/S0960258500003032

Vergara R, VerdeF, Pitto L, Loschiavo F, Terzi

M. 1990. Reversible variations in the methylation

pattern of carrot DNA during somatic embryogenesis.

Plant Cell Rep. 8, 697– 700.

http://dx.doi.org/10.1017/S0960258500004141

Wample RL, Farrar S. 1983. Yield and quality of

furrow and trickle irrigated hop (Humulus lupulus L.)

in Washington state. Agric. Water Manage. 7, 457-

470.

http://dx.doi.org/10.1071/P9930639

Wang JH, Geng LH, Zhang CM. 2012. Research

on the weak signal detecting technique for crop water

stress based on wavelet denoising. Advanced

Materials Research. 22, 424– 425.

http://dx.doi.org/10.1016/j.indcrop.2006.07.004

Watling JR, Press MC. 1997. How is the

100 Sobhkhizi et al.

Int. J. Biosci. 2014

relationship between the C4 cereal Sorghum bicolor

and the C3 root hemi-parasites Striga hermonthica

and Striga asiatica affected by elevated CO2? Plant

Cell Environ. 20, 1292–1300.

http://dx.doi.org/10.2135/cropsci1992.0011183X003

200030033x

Wierenga PJ, Hendrickx J. 1985. Yield and

quality of trickle-irrigated chile peppers. Agric. Water

Manage. 9, 339-356.

http://dx.doi.org/10.1093/aob/77.6.591

Witcombe, JR, Hollington PA, Howarth CJ,

Reader S, Steele KA. 2008. Breeding for abiotic

stresses for sustainable agriculture, Philos. T. R. Soc.

B. 363, 703–716.

Wong SC. 1979. Elevated atmospheric partial

pressure of CO2 and plant growth. I. Interactions of

nitrogen nutrition and photosynthetic capacity in C3

and C4 plants. Oecologia. 44, 68–74.

http://dx.doi.org/10.2478/v10247-012-0052-4

XueJun D, XinShi Z. 2000 Special stomatal

distribution in Sabina vulgaris in relation to its

survival in a desert environment. Trees. 14, 369-375.

http://dx.doi.org/10.2478/v10247-012-0042-6

Yancy PH, Clark ME, Hand SC, Bowlus RD,

Somero GN. 1982. Living with water stress:

evolution of osmolyte systems, Science. 217, 1214–

1223.

http://dx.doi.org/10.1016/S0308-521X(01)00023-3

Yordanov I, Velikova V, Tsonev T. 2003. Plant

responses to drought and stress tolerance. Bulg. J.

Plant Physiol. 13, 187-206.

http://dx.doi.org/10.1006/anbo.1999.1076

Zhang H, Wang X, You M, Liu C. 1999. Water-

yield relations and water use efficiency of winter

wheat in the North China Plain. Irrigation Science.

19, 37–45.

http://dx.doi.org/10.4141/cjps94-012

Ziska LH, Bunce JA. 1997. Influence of increasing

carbon dioxide concentration on the photosynthetic

and growth stimulation of selected C4 crops and

weeds. Photosynth Res. 54, 199–208.

http://dx.doi.org/10.1016/j.eja.2005.08.001

Zlatev Z, Stoyanov Z. 2005. Effect of water stress

on leaf water relations of young bean plans. J. Central

Eur. Agric. 6(1), 5-14.

http://dx.doi.org/10.1016/S0074-7696(08)62489-4

Zwart SJ, Bastiaanssen WGM, 2004. Review of

measured crop water productivity values for irrigated

wheat, rice, cotton and maize. Agric. Water Manage.

69, 115-133.

http://dx.doi.org/10.1017/S0960258500004141