Heavy metal toxicity in plants and the potential NO-releasing novel techniques as the impending mitigation alternatives

Environmental pollutants like heavy metals are toxic, persistent, and bioaccumulative in nature. Contamination of agricultural fields with heavy metals not only hampers the quality and yield of crops but also poses a serious threat to human health by entering the food chain. Plants generally cope with heavy metal stress by regulating their redox machinery. In this context, nitric oxide (NO) plays a potent role in combating heavy metal toxicity in plants. Studies have shown that the exogenous application of NO donors protects plants against the deleterious effects of heavy metals by enhancing their antioxidative defense system. Most of the studies have used sodium nitroprusside (SNP) as a NO donor for combating heavy metal stress despite the associated concerns related to cyanide release. Recently, NO-releasing nanoparticles have been tested for their efficacy in a few plants and other biomedical research applications suggesting their use as an alternative to chemical NO donors with the advantage of safe, slow and prolonged release of NO. This suggests that they may also serve as potential candidates in mitigating heavy metal stress in plants. Therefore, this review presents the role of NO, the application of chemical NO donors, potential advantages of NO-releasing nanoparticles, and other NO-release strategies in biomedical research that may be useful in mitigating heavy metal stress in plants. Graphical Abstract Heavy metal toxicity reduces plant growth and productivity. Since traditionally used NO donors do not provide a sustained NO-release, therefore heavy metal toxicity can be mitigated by novel NO-delivery techniques.

[1]  Linchuan Fang,et al.  A global meta-analysis of heavy metal(loid)s pollution in soils near copper mines: Evaluation of pollution level and probabilistic health risks. , 2022, The Science of the total environment.

[2]  C. K. Kim,et al.  Phytohormonal Regulation Through Protein S-Nitrosylation Under Stress , 2022, Frontiers in Plant Science.

[3]  Jingzi Beiyuan,et al.  Phytoremediation of potentially toxic elements (PTEs) contaminated soils using alfalfa (Medicago sativa L.): A comprehensive review. , 2022, Chemosphere.

[4]  Shruti Gupta,et al.  N-Nitrosomelatonin, as efficient nitric oxide donor and transporter in Arabidopsis seedlings. , 2021, Nitric oxide : biology and chemistry.

[5]  A. Seabra,et al.  Nitric-oxide releasing chitosan nanoparticles towards effective treatment of cutaneous leishmaniasis. , 2021, Nitric oxide : biology and chemistry.

[6]  A. Pande,et al.  NO Network for Plant–Microbe Communication Underground: A Review , 2021, Frontiers in Plant Science.

[7]  K. Tsuchida,et al.  Osmotic stress in banana is relieved by exogenous nitric oxide , 2021, PeerJ.

[8]  Li‐Li Li,et al.  Advanced nitric oxide donors: chemical structure of NO drugs, NO nanomedicines and biomedical applications. , 2021, Nanoscale.

[9]  A. Shah,et al.  Synergistic effects of nitric oxide and silicon on promoting plant growth, oxidative stress tolerance and reduction of arsenic uptake in Brassica juncea. , 2021, Chemosphere.

[10]  M. Yacoub,et al.  Nitric Oxide Releasing Hydrogel Nanoparticles Decreases Epithelial Cell Injuries Associated With Airway Reopening , 2021, Frontiers in Bioengineering and Biotechnology.

[11]  Pingfan Zhou,et al.  Application of Nanoparticles Alleviates Heavy Metals Stress and Promotes Plant Growth: An Overview , 2020, Nanomaterials.

[12]  P. Ahmad,et al.  Nitric oxide donor, sodium nitroprusside, mitigates mercury toxicity in different cultivars of soybean. , 2020, Journal of hazardous materials.

[13]  D. Lin,et al.  A new strategy using nanoscale zero-valent iron to simultaneously promote remediation and safe crop production in contaminated soil , 2020, Nature Nanotechnology.

[14]  A. Hassanein,et al.  Sodium Nitroprusside Mitigates the Inhibitory Effect of Salt and Heavy Metal Stress on Lupine Yield and Downregulates Antioxidant Enzyme Activities , 2020 .

[15]  G. S. Shekhawat,et al.  Nitric oxide induced Cd tolerance and phytoremediation potential of B. juncea by the modulation of antioxidant defense system and ROS detoxification , 2020, Biometals : an international journal on the role of metal ions in biology, biochemistry, and medicine.

[16]  Alexander T. Williams,et al.  Control of systemic inflammation through early nitric oxide supplementation with nitric oxide releasing nanoparticles , 2020, Free Radical Biology and Medicine.

[17]  Y. Wan,et al.  The fate of arsenic in rice plants (Oryza sativa L.): Influence of different forms of selenium. , 2020, Chemosphere.

[18]  Marco Pieroni Nitric oxide-releasing cyclodextrins as biodegradable antibacterial scaffolds: a patent evaluation of US2019343869(A1) , 2020, Expert opinion on therapeutic patents.

[19]  D. Chauhan,et al.  Regulation of ascorbate-glutathione cycle by exogenous nitric oxide and hydrogen peroxide in soybean roots under arsenate stress. , 2020, Journal of hazardous materials.

[20]  A. Sofo,et al.  Nitric Oxide Cooperates With Auxin to Mitigate the Alterations in the Root System Caused by Cadmium and Arsenic , 2020, Frontiers in Plant Science.

[21]  Jin-Wook Yoo,et al.  Nitric Oxide-Releasing S-Nitrosoglutathione-Conjugated Poly(Lactic-Co-Glycolic Acid) Nanoparticles for the Treatment of MRSA-Infected Cutaneous Wounds , 2020, Pharmaceutics.

[22]  Z. Ren,et al.  Light-triggered NO-releasing nanoparticles for treating mice with liver fibrosis , 2020, Nano Research.

[23]  Megha D. Bhatt,et al.  Application of Nanoparticles in Overcoming Different Environmental Stresses , 2020 .

[24]  H. Samet Alleviation of cobalt stress by exogenous sodium nitroprusside in iceberg lettuce , 2020, Chilean journal of agricultural research.

[25]  E. Koomen,et al.  Change in National Dosing Advice of Nitroprusside After Potentially Fatal Cyanide Intoxication , 2020, SN Comprehensive Clinical Medicine.

[26]  Kai Yang,et al.  Near-Infrared Light-Responsive Nitric Oxide Delivery Platform for Enhanced Radioimmunotherapy , 2020, Nano-Micro Letters.

[27]  S. Mikhalovsky,et al.  Nanosized copper(ii) oxide/silica for catalytic generation of nitric oxide from S-nitrosothiols. , 2020, Journal of materials chemistry. B.

[28]  D. Piacentini,et al.  Nitric oxide alleviates cadmium- but not arsenic-induced damages in rice roots. , 2020, Plant physiology and biochemistry : PPB.

[29]  Z. Yi,et al.  Copper-Based Metal-Organic Framework as A Controllable Nitric Oxide-Releasing Vehicle for Enhanced Diabetic Wound Healing. , 2020, ACS applied materials & interfaces.

[30]  A. Seabra,et al.  Effects of copper oxide nanoparticles on growth of lettuce (Lactuca sativa L.) seedlings and possible implications of nitric oxide in their antioxidative defense , 2020, Environmental Monitoring and Assessment.

[31]  Qianjun He,et al.  Strategies for engineering advanced nanomedicines for gas therapy of cancer , 2020, National science review.

[32]  W. Liao,et al.  Roles of nitric oxide in heavy metal stress in plants: Cross-talk with phytohormones and protein S-nitrosylation. , 2020, Environmental pollution.

[33]  H. Hamidi,et al.  Relationship of Sodium Nitroprusside with Growth and Antioxidant Enzymes of Canola under Lead Stress , 2020 .

[34]  A. Seabra,et al.  Nitric Oxide-Releasing Nanomaterials and Skin Infections , 2020 .

[35]  Y. Hotta,et al.  Review of a Potential Novel Approach for Erectile Dysfunction: Light-Controllable Nitric Oxide Donors and Nanoformulations. , 2020, Sexual medicine reviews.

[36]  A. Seabra,et al.  Nitric oxide-loaded chitosan nanoparticles as an innovative antileishmanial platform. , 2019, Nitric oxide : biology and chemistry.

[37]  P. Ahmad,et al.  Sodium nitroprusside (SNP) improves tolerance to arsenic (As) toxicity in Vicia faba through the modifications of biochemical attributes, antioxidants, ascorbate-glutathione cycle and glyoxalase cycle. , 2019, Chemosphere.

[38]  R. Stolf-Moreira,et al.  Effects of nitric oxide-releasing nanoparticles on neotropical tree seedlings submitted to acclimation under full sun in the nursery , 2019, Scientific Reports.

[39]  L. Tamás,et al.  Reactive oxygen species, auxin and nitric oxide in metal-stressed roots: toxicity or defence , 2019, BioMetals.

[40]  C. Kaya,et al.  Alleviating effect of nitric oxide on oxidative stress and antioxidant defence system in pepper (Capsicum annuum L.) plants exposed to cadmium and lead toxicity applied separately or in combination , 2019, Scientia Horticulturae.

[41]  L. M. Sandalio,et al.  Role of nitric oxide in plant responses to heavy metal stress: exogenous application versus endogenous production. , 2019, Journal of experimental botany.

[42]  Shi-Weng Li,et al.  Nitric oxide donor improves adventitious rooting in mung bean hypocotyl cuttings exposed to cadmium and osmotic stresses , 2019, Environmental and Experimental Botany.

[43]  Ashwani Kumar Thukral,et al.  Nitric oxide-mediated regulation of oxidative stress in plants under metal stress: a review on molecular and biochemical aspects. , 2019, Physiologia plantarum.

[44]  M. Gu,et al.  Nitric oxide acts as an antioxidant and inhibits programmed cell death induced by aluminum in the root tips of peanut (Arachis hypogaea L.) , 2019, Scientific Reports.

[45]  Z. Hussain,et al.  Enhancement of storability and antioxidant systems of sweet cherry fruit by nitric oxide-releasing chitosan nanoparticles (GSNO-CS NPs). , 2019, Food chemistry.

[46]  A. Sebastian,et al.  Cadmium and sodium adsorption properties of magnetite nanoparticles synthesized from Hevea brasiliensis Muell. Arg. bark: Relevance in amelioration of metal stress in rice. , 2019, Journal of hazardous materials.

[47]  B. Yun,et al.  Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress , 2019, Environmental and Experimental Botany.

[48]  L. M. Sandalio,et al.  Reactive oxygen and nitrogen species as key indicators of plant responses to Cd stress , 2019, Environmental and Experimental Botany.

[49]  Daniel C W Tsang,et al.  Effect of metal oxide nanoparticles on amino acids in wheat grains (Triticum aestivum) in a life cycle study. , 2019, Journal of environmental management.

[50]  M. Nabaei,et al.  Interactive Effect of Melatonin and Sodium Nitroprusside on Seed Germination and Seedling Growth of Catharanthus roseus under Cadmium Stress , 2019, Russian Journal of Plant Physiology.

[51]  J. Akhtar,et al.  EFFECT OF EXOGENOUS APPLICATION OF SALICYLIC ACID AND SODIUM NITROPRUSSIDE ON MAIZE UNDER SELENIUM STRESS , 2019 .

[52]  S. Arora,et al.  Nanotechnological Interventions for Improving Plant Health and Productivity , 2019, Plant Biotechnology: Progress in Genomic Era.

[53]  J. B. Barroso,et al.  S-nitrosothiols function during abiotic stress in plants. , 2019, Journal of experimental botany.

[54]  Min Wang,et al.  Anti-CD24 antibody-nitric oxide conjugate (ANC) selectively and potently suppresses hepatic carcinoma. , 2019, Cancer research.

[55]  Hanan Ahmed Hashem,et al.  Nitric oxide enhances the adaptive responses of lupine plants against heavy-metal stress , 2018, Australian Journal of Crop Science.

[56]  Meetu Gupta,et al.  Nitric oxide confronts arsenic stimulated oxidative stress and root architecture through distinct gene expression of auxin transporters, nutrient related genes and modulates biochemical responses in Oryza sativa L. , 2018, Environmental pollution.

[57]  H. Tian,et al.  Dual Intratumoral Redox/Enzyme‐Responsive NO‐Releasing Nanomedicine for the Specific, High‐Efficacy, and Low‐Toxic Cancer Therapy , 2018, Advanced materials.

[58]  F. J. Corpas,et al.  Assessing Nitric Oxide (NO) in Higher Plants: An Outline , 2018 .

[59]  A. Sepehri,et al.  Titanium Dioxide Nanoparticles and Sodium Nitroprusside Alleviate the Adverse Effects of Cadmium Stress on Germination and Seedling Growth of Wheat (Triticum aestivum L.) , 2018 .

[60]  Yuanjie Dong,et al.  Effects of exogenous nitric oxide on cadmium toxicity and antioxidative system in perennial ryegrass , 2018 .

[61]  C. Liu,et al.  The investigation of the alleviated effect of copper toxicity by exogenous nitric oxide in tomato plants , 2018 .

[62]  H. Kermanian,et al.  Effects of exogenous salicylic acid and sodium nitroprusside on α-tocopherol and phytochelatin biosynthesis in zinc-stressed safflower plants , 2018 .

[63]  S. Mehmood,et al.  Nitric oxide induces rice tolerance to excessive nickel by regulating nickel uptake, reactive oxygen species detoxification and defense-related gene expression. , 2018, Chemosphere.

[64]  J. Oliveira,et al.  Oxidative stress triggered by arsenic in a tropical macrophyte is alleviated by endogenous and exogenous nitric oxide , 2018, Brazilian Journal of Botany.

[65]  P. Onianwa,et al.  Bioaccumulation of heavy metals in soil and selected food crops cultivated in Kogi State, north central Nigeria , 2017, Environmental Systems Research.

[66]  J. Vangronsveld,et al.  Reciprocal Interactions between Cadmium-Induced Cell Wall Responses and Oxidative Stress in Plants , 2017, Front. Plant Sci..

[67]  A. P. Schwab,et al.  Uptake, Accumulation, and in Planta Distribution of Coexisting Cerium Oxide Nanoparticles and Cadmium in Glycine max (L.) Merr. . , 2017, Environmental science & technology.

[68]  Fangbai Li,et al.  Silica nanoparticles alleviate cadmium toxicity in rice cells: Mechanisms and size effects. , 2017, Environmental pollution.

[69]  S. Singh,et al.  Nitric oxide mediated transcriptional modulation enhances plant adaptive responses to arsenic stress , 2017, Scientific Reports.

[70]  D. Ampasala,et al.  Alleviation of nickel toxicity in finger millet (Eleusine coracana L.) germinating seedlings by exogenous application of salicylic acid and nitric oxide , 2017 .

[71]  R. Weller,et al.  Chitosan nanoparticles for nitric oxide delivery in human skin. , 2017, MedChemComm.

[72]  Yajun Wang,et al.  Near‐Infrared Laser‐Triggered Nitric Oxide Nanogenerators for the Reversal of Multidrug Resistance in Cancer , 2017 .

[73]  Z. Qian,et al.  MRI-guided and ultrasound-triggered release of NO by advanced nanomedicine. , 2017, Nanoscale.

[74]  O. Sadeghipour Nitric oxide increases Pb tolerance by lowering Pb uptake and translocation as well as phytohormonal changes in cowpea (Vigna unguiculata (L.) Walp.) , 2017 .

[75]  F. J. Corpas,et al.  Characterization of the galactono-1,4-lactone dehydrogenase from pepper fruits and its modulation in the ascorbate biosynthesis. Role of nitric oxide☆ , 2017, Redox biology.

[76]  A. Seabra,et al.  Nitric oxide-releasing nanoparticles: synthesis, characterization, and cytotoxicity to tumorigenic cells , 2017, Journal of Nanoparticle Research.

[77]  P. Ahmad,et al.  Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato , 2017, Protoplasma.

[78]  A. Seabra,et al.  Nitric oxide-releasing chitosan nanoparticles alleviate the effects of salt stress in maize plants. , 2016, Nitric oxide : biology and chemistry.

[79]  Kyung-Min Kim,et al.  Nitric Oxide Responsive Heavy Metal-Associated Gene AtHMAD1 Contributes to Development and Disease Resistance in Arabidopsis thaliana , 2016, Frontiers in plant science.

[80]  Hong Jae Lee,et al.  pH-Responsive mineralized nanoparticles as stable nanocarriers for intracellular nitric oxide delivery. , 2016, Colloids and surfaces. B, Biointerfaces.

[81]  O. Dhankher,et al.  Nitric Oxide Alleviated Arsenic Toxicity by Modulation of Antioxidants and Thiol Metabolism in Rice (Oryza sativa L.) , 2016, Front. Plant Sci..

[82]  S. Arora,et al.  Zinc sulfide nanoparticle mediated alterations in growth and anti-oxidant status of Brassica juncea , 2016, Biologia.

[83]  Qianjun He,et al.  X-ray Radiation-Controlled NO-Release for On-Demand Depth-Independent Hypoxic Radiosensitization. , 2015, Angewandte Chemie.

[84]  M. Simontacchi,et al.  Plant Survival in a Changing Environment: The Role of Nitric Oxide in Plant Responses to Abiotic Stress , 2015, Front. Plant Sci..

[85]  Amedea B Seabra,et al.  State of the art, challenges and perspectives in the design of nitric oxide-releasing polymeric nanomaterials for biomedical applications. , 2015, Biotechnology advances.

[86]  R. Kohli,et al.  Exogenous Nitric Oxide (NO) Interferes with Lead (Pb)-Induced Toxicity by Detoxifying Reactive Oxygen Species in Hydroponically Grown Wheat (Triticum aestivum) Roots , 2015, PloS one.

[87]  Yanjie Wang,et al.  Effects of nitric oxide on alleviating cadmium stress in Typha angustifolia , 2015, Plant Growth Regulation.

[88]  A. Seabra,et al.  Evaluation of the effects of nitric oxide-releasing nanoparticles on plants , 2015 .

[89]  M. Fujita,et al.  Interactive effects of nitric oxide and glutathione in mitigating copper toxicity of rice (Oryza sativa L.) seedlings , 2015, Plant signaling & behavior.

[90]  K. Shah,et al.  Evidences for suppression of cadmium induced oxidative stress in presence of sulphosalicylic acid in rice seedlings , 2015, Plant Growth Regulation.

[91]  K. Shah,et al.  Evidences for reduced metal-uptake and membrane injury upon application of nitric oxide donor in cadmium stressed rice seedlings. , 2014, Plant physiology and biochemistry : PPB.

[92]  G. Loake,et al.  Nitric oxide function in plant biology: a redox cue in deconvolution. , 2014, The New phytologist.

[93]  M. Fujita,et al.  Exogenous sodium nitroprusside and glutathione alleviate copper toxicity by reducing copper uptake and oxidative damage in rice (Oryza sativa L.) seedlings , 2014, Protoplasma.

[94]  R. Chari,et al.  Antibody-drug conjugates: an emerging concept in cancer therapy. , 2014, Angewandte Chemie.

[95]  Dongsik Park,et al.  A platform for nitric oxide delivery. , 2014, Journal of materials chemistry. B.

[96]  S. Liu,et al.  Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass , 2014, Biologia Plantarum.

[97]  H. Chakrapani,et al.  Nitroreductase-activated nitric oxide (NO) prodrugs. , 2013, Bioorganic & medicinal chemistry letters.

[98]  J. Durner,et al.  Nitric oxide, antioxidants and prooxidants in plant defence responses , 2013, Front. Plant Sci..

[99]  H. Kermanian,et al.  Exogenous nitric oxide (as sodium nitroprusside) ameliorates arsenic-induced oxidative stress in watercress (Nasturtium officinale R. Br.) plants , 2013 .

[100]  M. Rehmani,et al.  Effect of Nitric Oxide on Alleviating Cadmium Toxicity in Rice (Oryza sativa L.) , 2013 .

[101]  G. S. Shekhawat,et al.  Nitric oxide (NO) in alleviation of heavy metal induced phytotoxicity and its role in protein nitration. , 2013, Nitric oxide : biology and chemistry.

[102]  H. Chakrapani,et al.  INDQ/NO, a bioreductively activated nitric oxide prodrug. , 2013, Organic letters.

[103]  M. Fujita,et al.  Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system , 2013, Ecotoxicology.

[104]  N. Tuteja,et al.  Importance of nitric oxide in cadmium stress tolerance in crop plants. , 2013, Plant physiology and biochemistry : PPB.

[105]  P. Carter,et al.  Antibody-drug conjugates in cancer therapy. , 2013, Annual review of medicine.

[106]  H. Akbari,et al.  GERMINATION AND SEEDLING GROWTH OF WHEAT , 2013 .

[107]  W. Xiufeng,et al.  EXOGENOUS APPLICATION OF SODIUM NITROPRUSSIDE ALLEVIATED CADMIUM INDUCED CHLOROSIS, PHOTOSYNTHESIS INHIBITION AND OXIDATIVE STRESS IN CUCUMBER , 2013 .

[108]  M. Rai,et al.  Nano carriers for nitric oxide delivery and its potential applications in plant physiological process: A mini review , 2013, Journal of Plant Biochemistry and Biotechnology.

[109]  Maojun Xu,et al.  Lead-induced nitric oxide generation plays a critical role in lead uptake by Pogonatherum crinitum root cells. , 2012, Plant & cell physiology.

[110]  M. Terrile,et al.  Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. , 2012, The Plant journal : for cell and molecular biology.

[111]  S. Arora,et al.  Gold-nanoparticle induced enhancement in growth and seed yield of Brassica juncea , 2012, Plant Growth Regulation.

[112]  P. Tchounwou,et al.  Heavy metal toxicity and the environment. , 2012, Experientia supplementum.

[113]  Angela Feechan,et al.  S-nitrosylation of NADPH oxidase regulates cell death in plant immunity , 2011, Nature.

[114]  Ing Chia Phang,et al.  The protective effect of sodium nitroprusside (SNP) treatment on Arabidopsis thaliana seedlings exposed to toxic level of Pb is not linked to avoidance of Pb uptake. , 2011, Ecotoxicology and environmental safety.

[115]  W. Kaiser,et al.  Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. , 2011, The New phytologist.

[116]  H. Zhang,et al.  Effects of the nitric oxide donor sodium nitroprusside on antioxidant enzymes in wheat seedling roots under nickel stress , 2010, Russian Journal of Plant Physiology.

[117]  Huahua Wang,et al.  Nitrate reductase-dependent nitric oxide production is involved in aluminum tolerance in red kidney bean roots , 2010 .

[118]  N. Durán,et al.  Nitric oxide-releasing vehicles for biomedical applications , 2010 .

[119]  A. Kumari,et al.  Nitric oxide induced alleviation of toxic effects of short term and long term Cd stress on growth, oxidative metabolism and Cd accumulation in Chickpea , 2010 .

[120]  Han Lu,et al.  Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall , 2009, Planta.

[121]  Jeremy S. Webb,et al.  Nitric oxide‐mediated dispersal in single‐ and multi‐species biofilms of clinically and industrially relevant microorganisms , 2009, Microbial biotechnology.

[122]  P. Taylor,et al.  S-Nitrosylation of AtSABP3 Antagonizes the Expression of Plant Immunity* , 2009, Journal of Biological Chemistry.

[123]  K. Dietz,et al.  The relationship between metal toxicity and cellular redox imbalance. , 2009, Trends in plant science.

[124]  Karolina M. Pajerowska-Mukhtar,et al.  Plant Immunity Requires Conformational Charges of NPR1 via S-Nitrosylation and Thioredoxins , 2008, Science.

[125]  Jide Tian,et al.  Design, synthesis, and antihepatocellular carcinoma activity of nitric oxide releasing derivatives of oleanolic acid. , 2008, Journal of medicinal chemistry.

[126]  R. Kohli,et al.  Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots , 2008 .

[127]  L. Lamattina,et al.  Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. , 2007, The Plant journal : for cell and molecular biology.

[128]  M. Perazzolli,et al.  S-Nitrosylation of Peroxiredoxin II E Promotes Peroxynitrite-Mediated Tyrosine Nitration[W][OA] , 2007, The Plant Cell Online.

[129]  N. Rana,et al.  Cadmium induced oxidative stress influence on glutathione metabolic genes of Camellia sinensis (L.) O. Kuntze , 2007, Environmental toxicology.

[130]  Jianhua Zhang,et al.  Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. , 2007, The New phytologist.

[131]  Mingui Zhao,et al.  Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. , 2007, The New phytologist.

[132]  D. Abdelkader Role of Nitric Oxide, Glutathione and Sulfhydryl Groups in Zinc Homeostasis in Plants , 2007 .

[133]  J. Polacco,et al.  Nitric Oxide Functions as a Positive Regulator of Root Hair Development , 2006, Plant signaling & behavior.

[134]  You-Sheng Wang,et al.  Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. , 2005, Plant & cell physiology.

[135]  C. Kao,et al.  Nitric oxide reduces Cu toxicity and Cu-induced NH4+ accumulation in rice leaves. , 2005, Journal of plant physiology.

[136]  M. Benavides,et al.  Nitric oxide protects sunflower leaves against Cd-induced oxidative stress , 2005 .

[137]  N. Taniguchi,et al.  Nitric oxide donors : for pharmaceutical and biological applications , 2005 .

[138]  P. Wang,et al.  Sialated diazeniumdiolate: a new sialidase-activated nitric oxide donor. , 2004, Organic letters.

[139]  M. Wójcik,et al.  Phytochelatin synthesis and cadmium localization in wild type of Arabidopsis thaliana , 2004, Plant Growth Regulation.

[140]  C. Kao,et al.  Cadmium toxicity is reduced by nitric oxide in rice leaves , 2004, Plant Growth Regulation.

[141]  E. Gwóźdź,et al.  Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus , 2003 .

[142]  Brian W. Smith,et al.  Heavy Metal in Fertilizers: Considerations for Setting Regulations , 2002 .

[143]  P. Wang,et al.  Glycosylated diazeniumdiolates: a novel class of enzyme-activated nitric oxide donors , 2001 .

[144]  K. M. Davies,et al.  Esterase-sensitive nitric oxide donors of the diazeniumdiolate family: in vitro antileukemic activity. , 2000, Journal of medicinal chemistry.

[145]  Simon C Watkins,et al.  Targeting nitric oxide (NO) delivery in vivo. Design of a liver-selective NO donor prodrug that blocks tumor necrosis factor-alpha-induced apoptosis and toxicity in the liver. , 1997, Journal of medicinal chemistry.

[146]  J. Nriagu,et al.  Quantitative assessment of worldwide contamination of air, water and soils by trace metals , 1988, Nature.

[147]  J. C. Norris,et al.  In vivo release of cyanide from sodium nitroprusside. , 1987, British journal of anaesthesia.