Ecophysiology and Responses of Plants under Salt Stress || Role of Nitric Oxide in Improving Plant Resistance Against Salt Stress

413P. Ahmad et al. (eds.), Ecophysiology and Responses of Plants under Salt Stress, DOI 10.1007/978-1-4614-4747-4_15, © Springer Science+Business Media, LLC 2013

15.1 Introduction

Soil salinity is a serious threat to global crop production (Zhu 2001 ) . More than 20% of cultivated land is affected by salinity worldwide (Zhu 2001 ; Rengasamy 2006 ) and owing to climate change, the area under salinity is expected to increase (Wassmann et al. 2009 ) .

Salinity imposes both osmotic stress and ionic toxicity to plants disturbing the activities of cytosolic enzymes thereby causing nutritional disorders (Hernández et al. 1993, 1995 ; Serrano and Rodriguez 2002 ; Zhu 2003 ; Valderrama et al. 2006 ) and oxidative damage (Xiong and Zhu 2002 ; Xiong et al. 2002 ) . Overproduction of reactive oxygen species (ROS) such as hydroxyl radical ( • OH), single oxygen (O

2 1 ),

superoxide (O 2 – ), hydrogen peroxide (H

2 O

2 ) and alkoxy radicals (RO) under salinity

cause oxidative damage (Xiong and Zhu 2002 ; Xiong et al. 2002 ).

M. Farooq Institute of Plant Nutrition , Justus-Liebig-University , Heinrich-Buff-Ring 26-32, D-35392 Giessen , Germany

Department of Agronomy , University of Agriculture , Faisalabad 38040 , Pakistan

The UWA Institute of Agriculture , The University of Western Australia , Crawley , WA 6009 , Australia

K.H.M. Siddique (*) The UWA Institute of Agriculture , The University of Western Australia , Crawley , WA 6009 , Australia e-mail: [email protected]

S. Schubert Institute of Plant Nutrition , Justus-Liebig-University , Heinrich-Buff-Ring 26-32, D-35392 Giessen , Germany

Chapter 15 Role of Nitric Oxide in Improving Plant Resistance Against Salt Stress

Muhammad Farooq , Kadambot H.M. Siddique , and Sven Schubert

414 M. Farooq et al.

Nitric oxide (NO), an important bioactive molecule, is involved in the regulation of various physiological and biochemical processes in plants such as seed germination (Kopyra and Gwóźdź 2003 ; Arasimowicz and Floryszak-Wieczorek 2007 ) , plant growth (Durner and Klessig 1999 ; Arasimowicz and Floryszak-Wieczorek 2007 ) , stomatal oscillations (Neill et al. 2002 ; Bright et al. 2006 ) , plant maturation and senescence (Leshem et al. 1998 ; Guo and Crawford 2005 ; Arasimowicz and Floryszak-Wieczorek 2007 ) .

Nitric oxide is synthesized through both enzymatic and non-enzymatic reactions (Bethke et al. 2004 ) , however its synthesis increases substantially under salinity. For instance, upon exposure to salt stress, endogenous level of NO was signi fi cantly increased in olive ( Olea europaea L.; Valderrama et al. 2007 ) , sun fl ower ( Helianthus annuus L.; David et al. 2010 ) and Arabidopsis ( Arabidopsis thaliana (L.) Heynh; Zhao et al. 2007a ; Qiao et al. 2009 ) . Through its involvement in the electron trans-port chain during respiration (Zottini et al. 2002 ) , NO modulates the antioxidant defense system scavenging ROS under salinity in plants (Table 15.1 ; Kopyra and Gwóźdź 2003 ; Molassiotis et al. 2010 ) . NO also helps to maintain a high K + /Na + ratio in the cytosol (Table 15.1 ; Ruan et al. 2004 ; Siddiqui et al. 2011 ) through increased expression of plasma membrane and/or tonoplast H + -ATPase and H + -PPase under salinity (Zhao et al. 2004 ; Shi et al. 2007 ) . Furthermore, NO triggers accumulation of organic osmolytes and compatible solutes, like proline, soluble sugars (Table 15.1 ; Guo et al. 2009 ) , so as to maintain cell turgor and regulate water acquisition.

In this chapter, the role of NO in improving resistance against salinity in plants is being discussed through different methods.

15.2 Osmoregulation and Osmoprotection

Salinity causes osmotic stress which affects tissue water contents and water uptake in plants. Seed germination is the fi rst step in the ontogeny of plants. Germination starts by water imbibition and ends with radical protrusion through resumption of metabolism (Bewleyl 1997 ) . Owing to salinity-induced osmotic stress, seed germi-nation signi fi cantly decreases under salinity (Misra and Dwivedi 2004 ) leading to poor crop stand establishment (Almansouri et al. 2001 ) . However, NO application signi fi cantly increases germination and stand establishment in several crops under salinity (Table 15.2 ; Kopyra and Gwóźdź 2003 ; Li et al. 2005 ; Zheng et al. 2009 ) .

In yellow lupin ( Lupinus luteus L.), salinity signi fi cantly suppressed germina-tion, nonetheless seed treatment with sodium nitroprusside (SNP), the NO donor, triggered germination under salinity (Kopyra and Gwóźdź 2003 ) . Similarly, in the succulent shrub suaeda ( Suaeda salsa (L.) Pall.), a halophyte, NO stimulated seed germination under salinity stress (Li et al. 2005 ) . Pre-sowing seed treatment with 0.1 and 0.2 mM NO signi fi cantly improved the germination of rice ( Oryza sativa L.) genotypes under salinity (Habib et al. 2010 ) . Likewise in wheat ( Triticum aestivum L.),

41515 Role of Nitric Oxide in Improving Plant Resistance Against Salt Stress

Table 15.1 Mechanisms of nitric-oxide-induced salinity resistance in different plant species

NO-mediated effect Plant species References

Increased expression of tonoplast H + -ATPase and Na + /H + antiporter gene

Maize Zhang et al. ( 2006, 2007a )

Increased germination rate and root growth Lupin Kopyra and Gwóźdź ( 2003 )

Survival of more green leaf tissue, and increased quantum yield for photosystem II

Rice Uchida et al. ( 2002 )

Expression of plasma membrane H + -ATPase resulting in increased K + /Na + ratio

Reed Zhao et al. ( 2004 )

Decreased Na + accumulation in cytosol Maize Zhang et al. ( 2004 ) Increased K + content in cytosol Wheat Ruan et al. ( 2004 ) Decreased Na + content with simultaneous

increase in K + content Seashore mallow Guo et al. ( 2009 )

Increased activity of catalase, superoxide dismutase, peroxidase and ascorbate peroxidase

Seashore mallow Guo et al. ( 2009 )

Increased activity of enzymatic (superoxide dismutase, guaiacol peroxidase, catalase, ascorbate peroxidase) and non-enzymatic (ascorbate, reduced glutathione) antioxidants

Tomato Wu et al. ( 2011 )

Increased proline accumulation Seashore mallow Guo et al. ( 2009 ) Wheat Ruan et al. ( 2002 ) Tomato Wu et al. ( 2011 )

Increased accumulation of soluble sugars Tomato Wu et al. ( 2011 ) Increased accumulation of putrescine, spermine

and spermidine Cucumber Fan et al. ( 2012 )

Increased activity of catalase, superoxide dismutase, dehydroascorbate reductase and ascorbate peroxidase, guaiacol peroxidase and glutathione reductase, and increased expression of plasma membrane and tonoplast H + -ATPase and H + -PPase

Cucumber Shi et al. ( 2007 )

Increased activity of catalase and superoxide dismutase, decrease in contents of malondialdehyde and hydrogen peroxide, and increased K + /Na + ratio

Wheat Zheng et al. ( 2009 )

Increased activity of superoxide dismutase, peroxidase and ascorbate peroxidase and proline accumulation, and decrease in contents of malondialdehyde

Mustard Zeng et al. ( 2011 )

through improved water imbibition and metabolism, seed soaking in SNP solution increased the germination rate as well as coleoptile and radicle growth (Zheng et al. 2009 ) . Apart from the accumulation of ions in vacuoles, plants synthesize low-molecular-mass organic compounds, the compatible solutes, which help to regulate turgor and water acquisition under osmotic stress (Yancey et al. 1982 ; Bohnert et al. 1995 ; Hasegawa et al. 2000 ) . Several osmolytes including glycine-betaine, sugar alcohols, soluble sugars, proline, trehalose, polyols, etc., have been


Table 15.2 In fl uence of externally-applied nitric oxide on germination, and some morphological characteristics under salinity in different plant species

Plant species Salinity level NO treatment

Increase over salinity control Reference

Yellow lupin 100 mM NaCl 100 m M SNP 88% increase in germination

Kopyra and Gwóźdź ( 2003 )

Cucumber 100 mM NaCl 50 m M SNP 52% increase in shoot dry weight

Shi et al. ( 2007 )

Cucumber 100 mM NaCl 50 m M SNP 48% increase in root dry weight

Shi et al. ( 2007 )

Suaeda (brown seeds)

800 mM NaCl 50 m M SNP 62% increase in germination

Li et al. ( 2005 )

Suaeda (brown seeds)


Li et al. ( 2005 )

Suaeda (black seeds)


Li et al. ( 2005 )

Suaeda (black seeds)


Li et al. ( 2005 )

Wheat 300 mM NaCl 100 m M SNP 20% increase in germination

Zheng et al. ( 2009 )

Wheat 300 mM NaCl 100 m M SNP 18% increase in coleoptiles dry weight

Zheng et al. ( 2009 )

Tomato (cv. Hufan148)

100 mM NaCl 100 m M SNP 11% increase in shoot dry weight

Wu et al. ( 2011 )


100 mM NaCl 100 m M SNP 31% increase in shoot dry weight

Wu et al. ( 2011 )


100 mM NaCl 100 m M SNP 13% increase in root dry weight

Wu et al. ( 2011 )


100 mM NaCl 100 m M SNP 40% increase in root dry weight

Wu et al. ( 2011 )

Rice 100 mM NaCl 1 m M SNP 21% increase in surviving green parts

Uchida et al. ( 2002 )

Rice 100 mM NaCl 10 m M SNP 17% increase in surviving green parts

Uchida et al. ( 2002 )

Cucumber 50 mM NaCl 100 m M SNP 41% increase in plant height

Fan et al. (2012)

Cucumber 50 mM NaCl 100 m M SNP 67% increase in plant fresh weight

Fan et al. (2012)

Cucumber 50 mM NaCl 100 m M SNP 50% increase in plant dry weight

Fan et al. (2012)

Cucumber 100 mM NaCl 50 m M SNP 50% increase in shoot dry weight

Shi et al. ( 2007 )

Cucumber 100 mM NaCl 50 m M SNP 33% increase in root dry weight

Shi et al. ( 2007 )

Mustard 150 mM NaCl 100 m M SNP 51% increase in relative water contents

Zeng et al. ( 2011 )


reported to accumulate in various plant species under salinity and drought (Yancey et al. 1982 ; Bohnert et al. 1995 ; Hasegawa et al. 2000 ; Farooq et al. 2009 ) . In addition to their role in the maintenance of water balance in plant tissues, these osmolytes also act as osmoprotectants; for instance, proline scavenges free radicals (Chen and Murata 2000 ) .

NO stimulates cytosolic synthesis of proline; for example, exogenous applica-tion of SNP signi fi cantly increased cytosolic proline accumulation in seashore mal-low ( Kosteletzkya virginica L.), conferring salinity resistance (Guo et al. 2009 ) . Moreover NO application have found to increase proline accumulation in wheat, that scavenges ROS and stabilize the structure of the macromolecule (Ruan et al. 2002 ) . Likewise in tomato ( Lycopersicom esculentum Mill.), same treatment has shown to improve the accumulation of proline as well as soluble sugars under salt stress (Wu et al. 2011 ) . Another study on tomato showed that exogenous NO signi fi cantly ameliorated the salinity induced decrease in photosynthetic pigments rate of photosynthesis (Wu et al. 2010 ) .

15.3 Ion Homeostatis

In cytosol, a high K + /Na + ratio is vital for normal cell functioning. However, signi fi cant enhancement of Na + uptake under salinity disrupts the physiological and biochemical activities in plant cells by disturbing K + /Na + ratio that, eventually leads to death of cell, tissue or organ (Adams et al. 1992 ) . Reduced Na + uptake, improved K + uptake and compartmentation of absorbed Na + are strategies for plants to cope with salinity-induced damages in this regard.

NO regulates these strategies responsible for salinity resistance in plants. Salt-inducible enzyme Na + /H + antiporter is involved in removal of Na + from cytosol and/or its vacuolar compartmentation (Niu et al. 1993 ; Michelet and Boutry 1995 ; Apse et al. 1999 ; Chen et al. 2010 ) . NO signi fi cantly increases the activity of vacuolar H + -ATPase and H + -Ppase – the driving forces for Na + /H + exchange (Zhang et al. 2007a ) . In maize ( Zea mays L.), for instance, exogenous application of NO substan-tially increased the activity of tonoplast H + -ATPase and Na + /H + antiport facilitating Na + compartmentation (Zhang et al. 2006, 2007a ) . In seashore mallow, however, NO application signi fi cantly decreased Na + contents and simultaneously increased K + contents in shoots under salt stress.

In the calluses of reed ( Phragmites communis Trin . ), NO application increased the expression of the plasma membrane H + -ATPase, leading to a high K + /Na + ratio in the cytosol (Zhao et al. 2004 ) . Similarly in calluses from poplar ( Populus euphratica L.), NO induced salt resistance by improving plasma membrane H + -ATPase activity that increased the K + /Na + ratio (Zhang et al. 2007b ) . In another study on maize, NO increased K + accumulation in roots, leaves and sheaths, and simultaneously decreased Na + accumulation contributing to salt resistance (Zhang et al. 2004 ) . However in wheat, NO did not affect Na + content but K + content signi fi cantly increased thus increasing the K + /Na + ratio in roots of wheat seedling under salinity (Ruan et al. 2004 ) .


Exogenous application of SNP alleviated the salinity induced injury by maintaining a higher K + /Na + ratio and an increased plasma membrane H + -ATPase activity in cal-lus of wild type Arabidopsis but not in callus of ethylene-insensitive mutant inetr1-3 (Wang et al. 2009 ) .

Several experiments using NO donors and inhibitors indicated plasma membrane H + -ATPase and vacuolar H + -ATPase and H + -PPase dependent increase in K + /Na + ratio in the cytosol. Therefore NO serves as a signal for inducing salt resistance in plants (Zhao et al. 2004 ; Zhang et al. 2006 ; Shi et al. 2007 ) .

15.4 Antioxidative Defense System

Salinity-induced osmotic stress triggers the synthesis of reactive oxygen species (ROS) (Abogadallah 2010 ) . Besides oxidative damage to lipids (Fridovich 1986 ; Wise and Naylor 1987 ) , proteins and nucleic acids (Fridovich 1986 ; Imlay and Linn 1988 ) , these cytotoxic ROS may also disrupt normal metabolism in plants (Farooq et al. 2009 ). However, NO substantially ameliorates oxidative stress damage by act-ing as an antioxidant, stimulating production of enzymatic and non-enzymatic anti-oxidants as well as osmoprotectants (Beligni et al. 2002 ; Guo et al. 2009 ; Tanou et al. 2009a ; Molassiotis et al. 2010 ) .

In mustard ( Brassica juncea L.), NO application signi fi cantly increased the activity of superoxide dismutase (SOD), peroxidase (POD) and ascorbate peroxi-dase (APX), to prevent oxidative damage as indicated by the reduced value of malondialdehyde (MDA) (Zeng et al. 2011 ) . Likewise in seashore mallow, exoge-nous application of NO increased the activity of catalase (CAT), SOD, POD and APX protecting plants from oxidative damage under salinity (Guo et al. 2009 ) . Whereas in bitter orange ( Citrus aurantium L.) trees, root pre-treatment with NO increased the activity of SOD, CAT, APX and glutathione reductase (GR), pro-moted maintenance of cellular redox homeostasis and mitigated oxidative damage under salt stress (Tanou et al. 2009a ) . This induction of the antioxidant system helps to resist salinity stress (Tanou et al. 2009a ) . Exogenous application of NO protected chickpea ( Cicer arietinum L.) plants from salinity-induced oxidative damage through increased activity of antioxidant enzymes including SOD, CAT, APX, GR and dehydro-ascorbate reductase (DHAR) and higher ratios of glutathione/glutathi-one disul fi de and ascorbate/dehydroascorbate (Sheokand et al. 2010 ) . Similarly the exogenous application of NO signi fi cantly increased in the activity of antioxidant enzymes (superoxide dismutase, catalase, ascorbate peroxidase) in rice, thus increasing the resistance against salinity (Uchida et al. 2002 ) .

NO can also act as an antioxidant to protect plants from oxidative damage (Beligni et al. 2002 ) . In wheat, NO application substantially enhanced the activity of SOD and CAT (Ruan et al. 2002 ) . Whereas in tomato, exogenous application of NO improved the antioxidant enzymes SOD, guaiacol peroxidase, CAT, APX, non-enzymatic antioxidant ascorbate and reduced glutathione under salinity thus help-ing to alleviate salt-induced oxidative damage (Wu et al. 2011 ) .


15.5 Regulation of Signalling and Plant Hormones

Upon exposure to salinity stress, endogenous level of certain plant hormones such as abscisic acid (ABA) and cytokinins increase substantially (Thomas et al. 1992 ; Aldesuquy 1998 ; Vaidyanathan et al. 1999 ) . Increased endogenous level of these hormones modulate salinity resistance in plants; for instance, ABA alters salt-stress-induced genes (de Bruxelles et al. 1996 ) regulating salinity resistance in plants (Gupta et al. 1998 ) .

The protective role of NO during salinity-induced osmotic stress is dosage-dependent (Kopyra and Gwóźdź 2003 ) . At low concentrations, the mechanism of NO in leaf water control is ABA-dependent but at high concentrations, NO can maintain leaf water by inducing stomatal closure independent of ABA accumula-tion (Xing et al. 2004 ) .

NO mediates ABA signalling in guard cells to regulate stomatal oscillations; however with reduced endogenous NO, the degree of ABA-induced stomatal clo-sure decreases (Neill et al. 2002 ) . Exogenous NO application af fi rms its involve-ment in stomatal regulation in dose-dependent manner. For instance, externally-applied NO decreased the rate of transpiration through ABA-induced stomatal closure in several plant species including broad bean ( Vicia faba L.), salpichroa ( Salpichroa organifolia L.) and Tradescantia spp. (Garcia-Mata and Lamattina 2001 ) . Nevertheless, application of NO inhibitors reverses NO-induced stomatal closure thus af fi rming its involvement in this process (Bright 2006 ) .

15.6 Molecular Mechanism

Physiological and metabolic adaptations to salinity at the cellular level have led to the identi fi cation of several genes responsible for salt resistance in plants (Shinozaki et al. 1998 ) . NO is also involved in the expression of certain genes under salinity (Chen et al. 2010 ) . For example, expression of NtGRAS1 , new member of the GRAS gene family was induced by NO application in tobacco ( Nicotiana tabacum L.). NtGRAS1 regulated the transcription of genes involved in salinity resistance in plants (Czikkel and Maxwell 2007 ) .

Chen et al. ( 2010 ) reported that owing to NO-induced expression of the HA1 and SOS1 , salt secretion and net Na + ef fl ux in salt glands was increased in mangrove plant ( Avicennia marina (Forssk.) Vierh.) resulting in increased salinity resistance. Furthermore, increase in Na + sequestration into the vacuoles of the epidermis and hypodermal cells by NO-induced expression of VHA-c1 and NHX1 genes also con-fers salinity resistance in mangrove plant (Chen et al. 2010 ) .

The protein kinases family is also involved in NO-mediated signaling cascades under salt stress. For example in tobacco cell suspensions exposed to salt stress, the osmotic stress-activated protein kinase ( NtOSAK ) activated by NO gets interacted with glyceraldehyde-3-phosphate dehydrogenase (GAPDH), the enzyme involved in glycolysis to provide energy and carbon molecules (Wawer et al. 2010 ) .


In a recent proteomic study on citrus ( Citrus aurantium L.), Tanou et al. ( 2009a ) provided a global survey of the proteins controlled by salinity. Root pre-treatment with SNP prior to imposing salt stress reversed many of the NaCl-responsive proteins. These SNP/NaCl responsive proteins-mainly involved in photosynthesis (corresponding to enzymes of Calvin-Benson cycle), defense mechanism and energy/glycolysis are potentially important for salt resistance as these may exert a NO-mediated effect by acclimating citrus plants before the actual experience of salt stress. In another proteomic study on citrus, NO application modi fi ed accumulation levels of leaf S-nitrosylated proteins and decreased protein carbonylation (Tanou et al. 2009b ) . In maize, however NO application induced G-protein-associated pro-tein accumulation (Bai et al. 2011 ) .

Arabidopsis mutant Atnoa1 , with an impaired in vivo NOS activity and low endogenous NO level, is more sensitive to salinity than its wild type (Zhao et al. 2007a ) . However, exogenous NO application to Atnoa1 improved salinity resistance by mitigating salinity-induced oxidative damage (Zhao et al. 2007b ) .

15.7 Conclusion and Future Perspective

Nitric oxide, a small ubiquitous molecule, modulates an array of physiological and biochemical processes in plants. In plants, NO improves salinity resistance through production of osmolytes and speci fi c proteins controlling water fl ux, ion homeosta-sis and antioxidant defense system scavenging free radicals. NO also regulates hor-monal balance to improve salt resistance in plants.

Experimental evidence in supporting the above roles for NO has been obtained through the application of either gaseous NO or NO donors. However, different NO donors may release different molecular species of NO, which may have distinct effects on plants under salt stress; these differential effects should be monitored. Despite the exponential growth in NO research in plants under abiotic stresses, there is a need for much more – given the essential roles of NO in plant growth and devel-opment under salinity. Integration of NO functions with plant metabolism, growth and development, especially with plant hormones should be examined in more detail. A deeper understanding of the NO-induced transcription factors, regulating genes, the products of the major stress responsive genes and cross talk between dif-ferent signaling components should also investigated.

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Ecophysiology and Responses of Plants under Salt Stress || Role of Nitric Oxide in Improving Plant Resistance Against Salt Stress