Plant Acclimation to Environmental Stress || Physiological Role of Nitric Oxide in Plants Grown Under Adverse Environmental Conditions

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  • 269N. Tuteja and S. Singh Gill (eds.), Plant Acclimation to Environmental Stress,DOI 10.1007/978-1-4614-5001-6_11, Springer Science+Business Media New York 2013


    ABA Abscisic acid APX Ascorbate peroxidase AsA Ascorbic acid ATP Adenosine triphosphate CAT Catalase CDPK Calcium-dependent protein kinase cGMP Cyclic guanosine monophosphate cPTIO 2-(4-Carboxyphenyl)-4,4,5,5-tetramethylimidazoline-l-oxyl-3-oxide COX Cytochrome c oxidase DHA Dehydroascorbate DHAR Dehydroascorbate reductase ETC Electron transport chain GAP Glycerinaldehyde-3-phosphate GPX Glutathione peroxidase GR Glutathione reductase

    M. Hasanuzzaman Laboratory of Plant Stress Responses , Department of Applied Biological Science, Kagawa University , Miki-cho , Kita-gun , Kagawa 761-0795 , Japan

    Department of Agronomy , Sher-e-Bangla Agricultural University , Dhaka 1207 , Bangladesh e-mail:

    S. Singh Gill Stress Physiology and Molecular Biology Lab , Centre for Biotechnology, MD University , Rohtak 124 001 , India

    M. Fujita (*) Laboratory of Plant Stress Responses , Department of Applied Biological Science, Kagawa University , Miki-cho , Kita-gun , Kagawa 761-0795 , Japan e-mail:

    Chapter 11 Physiological Role of Nitric Oxide in Plants Grown Under Adverse Environmental Conditions

    Mirza Hasanuzzaman, Sarvajeet Singh Gill, and Masayuki Fujita

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    GS Glutathione synthase GSH Reduced glutathione GSNO S -nitrosoglutathione GSSG Oxidized glutathione GST Glutathione S -transferase IAA Indole-3-acetic acid JA Jasmonic acid LNNA N w -nitro l -arginine LOOH Lipid hydroperoxides MAPK Mitogen-activated protein kinase MDA Malondialdehyde MDHA Monodehydroascorbate MDHAR Monodehydroascorbate reductase NADH Nicotinamide adenine dinucleotide NADPH Nicotinamide adenine dinucleotide phosphate NADPH

    ox NADPH oxidases

    NiR Nitrite reductase NO Nitric oxide NOHA N-hydroxyarginine NOS Nitric oxide synthase NR Nitrate reductase PA Polyamine PAL Phenylalanine ammonia-lyase PCD Programmed cell death PEG Polyethylene glycol POX Peroxidases RNS Reactive nitrogen species ROOH Organic hydroperoxides ROS Reactive oxygen species RWC Relative water content SA Salicylic acid SAM S -adenosyl methionine SNAP S -nitroso- N -acetylpenicillamine SNP Sodium nitroprusside TFBS Transcription factor binding sites XDH Xanthine dehydrogenase XOR Xanthine oxidoreductase g -ecs g -Glutamylcysteine synthetase

    1 Introduction

    By 2050, the worlds population will have increased by a third and demand for agricultural products will rise by 70% (Noble and Ruaysoongnern 2010 ) . In meet-ing future food production demands without consuming more land, it is necessary

  • 27111 Physiological Role of Nitric Oxide in Plants Grown Under Adverse

    to boost up the yield of crop. However, due to rapid climate changes crop plants are suffering from different adverse conditions, termed as abiotic stress. Abiotic stresses, particularly salinity, drought, temperature extremes, ooding, toxic metals, high-light intensity, UV-radiation, herbicides, and ozone, are the major causes of yield loss in cultivated crops worldwide and pose major threats to agriculture and food security (Rodrguez et al. 2005 ; Acquaah 2007 ) . Abiotic stress leads to a series of morphological, physiological, biochemical, and molecular changes that adversely affect plant growth and productivity (Wang et al. 2001 ) . However, the rapidity and ef ciency of these responses may be decisive for the viability of the given species. Plants are only able to survive under such stressful conditions if they are able to perceive the stimulus, generate and transmit signals, and initiate various physiologi-cal and biochemical changes (Bohnert and Jensen 1996 ) . Abiotic stresses can also lead to oxidative stress through the increase in reactive oxygen species (ROS), including singlet oxygen ( 1 O 2 ), superoxide (O 2 ), hydrogen peroxide (H 2 O 2 ), and hydroxyl radicals (OH), all of which are highly reactive and may cause cellular damage through oxidation of lipids, proteins, and nucleic acids (Apel and Hirt 2004 ; Gill and Tuteja 2010 ) .

    Exploring suitable crop improvements or ways to alleviate stress is one of the tasks of plant biologists. Nitric oxide (NO) is a highly reactive, membrane-perme-able free radical which was previously considered to be a highly toxic compound (Gordge 1998 ) . The discovery and elucidation of its biological functions in the 1980s came as a surprise. NO was named Molecule of the Year in 1992 by the journal Science, a NO Society was founded, and a scienti c journal, Nitric Oxide, devoted entirely to NO, was created (Delledonne 2005 ) . Its emission from plants has been reported several years ago in soybean plants (Klepper 1979 ) . Later, in vivo and in vitro nitrate reductase (NR)-dependent NO production has been found in other plants such as sun ower and maize (Rockel et al. 2002 ) . However, the dis-covery of NOs signaling role in cardiovascular system regulation has changed the paradigm concerning its cytotoxicity (Korhonen et al. 2005 ) . The biological func-tions of NO have gradually been elucidated. NO can provoke both bene cial and harmful effects in plant cells (Hasanuzzaman et al. 2010 ) . This dual role probably depends on the local concentration of NO as an effect of the rate of synthesis, trans-location, effectiveness of removal of this reactive nitrogen species, as well as its ability to directly interact with other molecules and signals (Arasimowicz and Floryszak-Wieczorek 2007 ) .

    In plant system, many possible sources work together for the production or syn-thesis of NO which depends on the plant species, plant organs, environmental con-ditions, and the signal pathway in the plant (Neill et al. 2002a ) . Recently, different groups reviewed the sources of NO in plant (Popova and Tuan 2010 ; Baudouin 2011 ; Misra et al. 2011a ) . It can be produced non-enzymatically or enzymatically through cytosolic nitrate reductase (NR), plasma membrane nitrite reductase (NiR), nitric oxide synthase (NOS) and xanthine dehydrogenase (XDH), etc.

    Research on NO in plants has gained considerable attention in recent years mainly due to its function in plant growth and development and as a key signaling molecule in different intracellular processes. Nitric oxide now can be designated as a jack-of-all-trades molecule which regulates plant cell responses under physiological conditions

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    throughout the life cycle of plants (Yemets et al. 2011 ) . As reviewed in several recent reports (Besson-Bard et al. 2008 ; Wilson et al. 2008 ; Leitner et al. 2009 ; Hao and Zhang 2010 ; Corpas et al. 2011 ; Mazid et al. 2011a, b ; Siddiqui et al. 2011 ; Wimalasekera et al. 2011 ) , NO production has been associated with a number of physiological situa-tions in plants. These cover the entire lifespan of the plant and include germination (rov et al. 2011 ) , root development (Yemets et al. 2011 ) , nodulation (del Giudice et al. 2011 ; Meilhoc et al. 2011 ) , control of stomatal movements (Hancock et al. 2011 ; He et al. 2011 ) , owering (Khurana et al. 2011 ) , pollen tube growth (rov et al. 2011 ) , and leaf senescence (Prochzkov and Wilhelmov 2011 ) .

    Recently, NO has emerged as an important signaling molecule and antioxidant. NO triggers many kinds of redox-regulated (defense-related) gene expressions, directly or indirectly, to establish plant stress tolerance (Polverari et al. 2003 ; Sung and Hong 2010 ) . Several recent reports indicated that the application of exogenous NO donors confers tolerance to various abiotic stresses like salinity (Hasanuzzaman et al. 2011a ) , drought (Bai et al. 2011 ) , high temperature (Hossain et al. 2010b ) , chilling (Liu et al. 2011 ) , toxic metals (Xiong et al. 2010 ) , ooding (Gupta et al. 2011 ) , high-light intensity (Xu et al. 2010c ) , UV-B radiation (Kim et al. 2010 ) , and elevated ozone (Ahlfors et al. 2009 ) . It was also suggested that NO, itself, possesses antioxidant properties and might act as a signal in activating ROS-scavenging enzyme activities under various abiotic stresses (Palavan-Unsal and Arisan 2009 ; Hao and Zhang 2010 ; Mazid et al. 2011a ; Siddiqui et al. 2011 ) . Several lines of study have shown that the protective effect of NO against abiotic stress is closely related to the NO-mediated reduction of ROS in plants (Beligni and Lamattina 1999a ; Wang and Yang 2005 ; Hao and Zhang 2010 ; Corpas et al. 2011 ) .

    In this chapter, we discuss recent progress in understanding the function of NO in plant responses and tolerance to abiotic stresses and in plant development. The physiological and biochemical mechanisms of NO-induced abiotic stress tolerance and the translation of signal transduction into cellular responses towards stress tol-erance are the foci of this review.

    2 Nitric Oxide Synthesis/Production in Plants

    In plant system, many possible sources work together for the production or synthe-sis of NO which depends on the plant species, plant organs, environmental condi-tions, and the signal pathway in the plant (Neill et al. 2002a ) . Recently, different groups reviewed the sources of NO in plant (Popova and Tuan 2010 ; Baudouin 2011 ; Misra et al. 2011a ); Fig. 11.1 .

    Higher plants can react both to the atmospheric or soil NO and they are also able to emit substantial amounts of NO (Durner and Klessig 1999 ) . In the atmosphere, nitri cation/denitri cation cycles provide NO as a by-product of N 2 O oxidation into the atmosphere. Nitri cation of NH 4 + is the primary source of N 2 emitted to the atmosphere, where it oxidizes to NO and NO 2 (Wojtaszek 2000 ) . In plant, NO can be formed both enzymatically and non-enzymatically (Fig. 11.1 ).

  • 27311 Physiological Role of Nitric Oxide in Plants Grown Under Adverse

    Production of NO from NO 2 is a common non-enzymatic phenomenon which occurs at low pH compartments (Igamberdiev et al. 2010 ) . In this case, NO 2 can dismutate to NO and NO 3 (Sthr and Ullrich 2002 ) . The generation in vitro of NO by the reaction of H 2 O 2 (1050 mM) and l -arginine (1020 mM) at pH 7.4 and 37 C has been reported by Nagase et al . (Nagase et al. 1997 ) . The non-enzymatic synthesis of NO has also been demonstrated by Gotte et al . ( 2002 ) , with short-time kinetics, by shock waves treatment of solutions containing 1 mMH 2 O 2 and 10 mM l -arginine. Beligni et al. (Beligni et al. 2002 ) obtained the NO synthesis in barley aleurone cells as reduction of NO 2 by AsA at acidic pH. Light-mediated reduction of NO 2 by carotenoids was also proposed as another non-enzymatic mechanism of NO formation (Cooney et al. 1994 ) .

    There are several enzymes in plants that may produce NO. The key enzymes involved in the production of NO in plants are: cytosolic nitrate reductase (NR; EC, plasma membrane nitrite reductase (NiR, EC., nitric oxide syn-thase (NOS; EC, and xanthine dehydrogenase (XDH; EC One of the major origin of NO production in plants, however, is probably through the action of NADPH-dependent NR which provided the rst known mechanism to make NO in plants. This enzyme can generate NO from NO 2 with NAD(P)H as electron donor and the catalysis site is probably the molybdenum cofactor (Moco) (Yamasaki et al. 1999 ; Rockel et al. 2002 ; Crawford 2006 ; Ferreira and Cataneo 2010 ) ; Fig 11.1 ). This is the only enzyme whose NO-producing activity has been con rmed both in vivo and in vitro (Courtois et al. 2008 ; Kaiser et al. 2002 ) . In plant cells, NO 2 can be accumulated when the photosynthetic activity is inhibited or under anaerobic conditions (Lamattina et al. 2003 ; Rockel et al. 2002 ) . Production of NO, dependent on NR activity, was recorded in many cultivated plants such as in Ccucumis sativus (de la Haba et al. 2001 ) , Helianthus annuus , Zea mays (Rockel et al. 2002 ) , Triticum aestivum (Xu and Zhao 2003 ) , Nicotiana tabacum (Planchet

    Fig. 11.1 Different mechanisms of NO synthesis/production in plant

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    et al. 2005 ) , and Medicago truncatula (Horchani et al. 2011 ) . Recently, a number of plant studies provided evidence for the role of NR in NO synthesis in plant (Moreau et al. 2010 ) . It has been reported that NR is responsible for NO production during stomatal closure (Desikan et al. 2002 ; Bright et al. 2006 ; Neill et al. 2008 ) , in response to defense elicitors (Shi and Li 2008 ; Srivastava et al. 2009 ; Wu et al. 2009 ) , under abiotic stress (Sang et al. 2008 ) , and during developmental processes (Kolbert et al. 2008 ; Seligman et al. 2008 ) .

    Another enzyme that can generate NO is NiR by which plants synthesize NO from NO 2 . Nitric oxide production in plants by NiR has been observed in several plant species, viz., Helianthus annuus (Rockel et al. 2002 ) , Glycine max (Delledonne et al. 1998 ) , and Chlamydomonas reinhardtii (Sakihama et al. 2002 ) . A plasma membrane-bound, root-speci c enzyme, NO 2 -NO oxidoreductase (Ni-NOR), using cytochrome c as an electron donor in vivo and having a comparatively reduced pH optimum is reported by Sthr and Stremlau (Sthr and Stremlau 2006 ) . Recently, Gupta and Kaiser ( 2010 ) showed the NO 2 -dependent NO production in plant cells under anoxic condition, which is localized in and mediated by the electron transport chain in the mitochondrial membranes.

    Nitric oxide synthase is another enzyme for NO synthesis in plants, whose activ-ity in higher plants was rst reported by Cueto et al. ( 1996 ) as well as Ninnemann and Maier ( 1996 ) by using the method of conversion of arginine, the substrate of NOS, into citrulline. Since last 20 years, there have been an increasing number of reports showing the presence of NOS activity in plants similar, to a certain extent, to mammalian NOS (del Ro et al. 2004 ) . Later, NOS-like activity in plants has been detected widely. Corpas et al. ( 2006 ) showed arginine-dependent NOS activity, which was dependent on the plant organ and its developmental stage. The enzy-matic oxidation of l -arginine to yield NO and l -citrulline has been reported in extracts...


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