Molecular Mechanisms of Nitric Oxide (NO) Signaling and Reactive Oxygen Species (ROS) Homeostasis during Abiotic Stresses in Plants
Abstract
:1. Introduction
2. Nitric Oxide (NO) Signaling under Abiotic Stresses
2.1. NO and Drought Stress
2.1.1. NO and ROS-Mediated Oxidative Stress
2.1.2. NO and Stomatal Closure during Drought
2.1.3. NO and Drought-Responsive Genes
2.2. NO and Metal/Metalloid Stress
2.2.1. Cadmium Stress
2.2.2. Copper Stress
2.2.3. Arsenic Stress
2.2.4. Zinc Stress
2.2.5. Other Heavy Metal Stresses (Lead, Chromium, Mercury)
2.3. NO and Salinity Stress
3. Conclusions and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- He, M.; He, C.Q.; Ding, N.Z. Abiotic stresses: General defenses of land plants and chances for engineering multi stress tolerance. Front. Plant Sci. 2018, 9, 1771. [Google Scholar] [CrossRef] [Green Version]
- Wani, S.H.; Kumar, V.; Shriram, V.; Sah, S.K. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop. J. 2016, 4, 162–176. [Google Scholar] [CrossRef] [Green Version]
- Fancy, N.N.; Bahlmann, A.; Loake, G.J. Nitric oxide function in plant abiotic stress. Plant Cell Environ. 2016, 40, 462–472. [Google Scholar] [CrossRef] [PubMed]
- Nakashima, K.; Ito, Y.; Yamaguchi-Shinozaki, K. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 2009, 149, 88–95. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mittler, R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002, 7, 405–410. [Google Scholar] [CrossRef]
- Lindermayr, C.; Durner, J. Interplay of reactive oxygen species and nitric oxide: Nitric oxide coordinates reactive oxygen species homeostasis. Plant Physiol. 2015, 167, 1209–1210. [Google Scholar] [CrossRef] [Green Version]
- Vranova, E.; Inze, D.; Breusegem, F.V. Signal transduction during oxidative stress. J. Exp. Bot. 2002, 53, 1227–1236. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Furchgott, R.F.; Zawadzki, J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980, 288, 373–376. [Google Scholar] [CrossRef]
- Gillespie, J.S.; Liu, X.; Martin, W. The effects of L-arginine and NG-monomethyl L-arginine on the response of the rat ano-coccygeus muscle to NANC nerve stimulation. Br. J. Pharmacol. 1989, 98, 1080–1082. [Google Scholar] [CrossRef] [Green Version]
- Grün, S.; Lindermayr, C.; Sell, S.; Durner, J. Nitric oxide and gene regulation in plants. J. Exp. Bot. 2006, 57, 507–516. [Google Scholar] [CrossRef] [Green Version]
- Schmidt, H.H.; Walter, U. NO at work. Cell 1994, 78, 919–925. [Google Scholar] [CrossRef]
- Siddiqui, M.H.; Al-Whaibi, M.H.; Basalah, M.O. Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 2011, 248, 447–455. [Google Scholar] [CrossRef] [PubMed]
- Wink, D.A.; Mitchell, J.B. Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 1998, 25, 434–456. [Google Scholar] [CrossRef]
- Klepper, L. Nitric oxide (NO) and nitrogen dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos. Environ. 1979, 13, 537–542. [Google Scholar] [CrossRef]
- Beligni, M.V.; LaMattina, L. Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 2000, 210, 215–221. [Google Scholar] [CrossRef] [PubMed]
- García-Mata, C.; Lamattina, L. Abscisic acid (ABA) inhibits light-induced stomatal opening through calcium- and nitric oxide-mediated signaling pathways. Nitric Oxide 2007, 17, 143–151. [Google Scholar] [CrossRef]
- Takahashi, S.; Yamasaki, H. Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. FEBS Lett. 2002, 512, 145–148. [Google Scholar] [CrossRef] [Green Version]
- Sadhu, A.; Moriyasu, Y.; Acharya, K.; Bandyopadhyay, M. Nitric oxide and ROS mediate autophagy and regulate Alternaria alternata toxin-induced cell death in tobacco BY-2 cells. Sci. Rep. 2019, 9, 8973. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Crawford, N.M.; Guo, F.-Q. New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci. 2005, 10, 195–200. [Google Scholar] [CrossRef]
- He, Z.L.; Yang, X.E.; Stoffella, P.J. Trace elements in agroecosystems and impacts on the environment. J. Trace Elem. Med. Biol. 2005, 19, 125–140. [Google Scholar] [CrossRef]
- Rather, B.A.; Mir, I.R.; Masood, A.; Anjum, N.A.; Khan, N.A. Nitric oxide pre-treatment advances seed germination and alle-viates copper-induced photosynthetic inhibition in indian mustard. Plants 2020, 9, 776. [Google Scholar] [CrossRef]
- Creus, C.M.; Graziano, M.; Casanovas, E.M.; Pereyra, M.A.; Simontacchi, M.; Puntarulo, S.; Barassi, C.A.; LaMattina, L. Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 2005, 221, 297–303. [Google Scholar] [CrossRef]
- Pagnussat, G.C.; Lanteri, M.L.; Lombardo, M.C.; Lamattina, L. Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol. 2004, 135, 279–286. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Correa-Aragunde, N.; Lombardo, C.; LaMattina, L. Nitric oxide: An active nitrogen molecule that modulates cellulose synthesis in tomato roots. New Phytol. 2008, 179, 386–396. [Google Scholar] [CrossRef]
- Guo, F.-Q.; Crawford, N.M. Arabidopsis Nitric Oxide Synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 2005, 17, 3436–3450. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wani, K.I.; Zehra, A.; Choudhary, S.; Naeem, M.; Khan, M.M.A.; Castroverde, C.D.M.; Aftab, T. Mechanistic insights into strigolactone biosynthesis, signaling, and regulation during plant growth and development. J. Plant Growth Regul. 2020, 1–17, 1–17. [Google Scholar] [CrossRef]
- Lamattina, L.; García-Mata, C.; Graziano, M.; Pagnussat, G. Nitric oxide: The versatility of an extensive signal molecule. Annu. Rev. Plant Biol. 2003, 54, 109–136. [Google Scholar] [CrossRef]
- Koshland, D.E., Jr. The molecule of the year. Science 1992, 58, 1861–1862. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hamurcu, M.; Khan, M.K.; Pandey, A.; Ozdemir, C.; Avsaroglu, Z.Z.; Elbasan, F.; Omay, A.H.; Gezgin, S. Nitric oxide regulates watermelon (Citrullus lanatus) responses to drought stress. 3 Biotech 2020, 10, 494. [Google Scholar] [CrossRef]
- De Sousa, L.F.; de Menezes-Silva, P.E.; Lourenço, L.L.; Galmés, J.; Guimarães, A.C.; da Silva, A.F.; Farnese, F.D.S. Improving water use efficiency by changing hydraulic and stomatal characteristics in soybean exposed to drought: The involvement of nitric oxide. Physiol. Plant 2020, 168, 576–589. [Google Scholar] [CrossRef]
- Farouk, S.; Al-Huqail, A.A. Sodium nitroprusside application regulates antioxidant capacity, improves phytopharma-ceutical production and essential oil yield of marjoram herb under drought. Ind. Crop. Prod. 2020, 158, 113034. [Google Scholar] [CrossRef]
- Sahay, S.; Khan, E.; Gupta, M. Nitric oxide and abscisic acid protects against PEG-induced drought stress differentially in Brassica genotypes by combining the role of stress modulators, markers and antioxidants. Nitric Oxide 2019, 89, 81–92. [Google Scholar] [CrossRef]
- Hasanuzzaman, M.; Nahar, K.; Rahman, A.; Inafuku, M.; Oku, H.; Fujita, M. Exogenous nitric oxide donor and arginine provide protection against short-term drought stress in wheat seedlings. Physiol. Mol. Biol. Plants 2018, 24, 993–1004. [Google Scholar] [CrossRef] [PubMed]
- Majeed, S.; Nawaz, F.; Naeem, M.; Ashraf, M.Y. Effect of exogenous nitric oxide on sulfur and nitrate assimilation pathway enzymes in maize (Zea mays L.) under drought stress. Acta Physiol. Plant 2018, 40, 206. [Google Scholar] [CrossRef]
- Yagci, S.; Yildirim, E.; Yildirim, N.; Shams, M.; Agar, G. Nitric oxide alleviates the effects of copper-induced DNA methylation, genomic instability, LTR retrotransposon polymorphism and enzyme activity in lettuce. Plant Physiol. Rep. 2019, 24, 289–295. [Google Scholar] [CrossRef]
- Pető, A.; Lehotai, N.; Feigl, G.; Tugyi, N.; Ördög, A.; Gémes, K.; Kolbert, Z. Nitric oxide contributes to copper tolerance by in-fluencing ROS metabolism in Arabidopsis. Plant Cell Rep. 2013, 32, 1913–1923. [Google Scholar] [CrossRef]
- Dong, Y.; Xu, L.; Wang, Q.; Fan, Z.; Kong, J.; Bai, X. Effects of exogenous nitric oxide on photosynthesis, antioxidative ability, and mineral element contents of perennial ryegrass under copper stress. J. Plant Interact. 2013, 9, 402–411. [Google Scholar] [CrossRef] [Green Version]
- Khairy, A.I.H.; Oh, M.J.; Lee, S.M.; Kim, D.S.; Roh, K.S. Nitric oxide overcomes Cd and Cu toxicity in in vitro-grown tobacco plants through increasing contents and activities of rubisco and rubisco activase. Biochim. Open 2016, 2, 41–51. [Google Scholar] [CrossRef] [Green Version]
- Hu, Y.; You, J.; Liang, X. Nitrate reductase-mediated nitric oxide production is involved in copper tolerance in shoots of hulless barley. Plant Cell Rep. 2014, 34, 367–379. [Google Scholar] [CrossRef] [PubMed]
- He, L.; Wang, X.; Feng, R.; He, Q.; Wang, S.; Liang, C.; Yan, L.; Bi, Y. Alternative pathway is involved in nitric oxide-enhanced tolerance to cadmium stress in barley roots. Plants 2019, 8, 557. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nabaei, M.; Amooaghaie, R. Nitric oxide is involved in the regulation of melatonin-induced antioxidant responses in Catharanthus roseus roots under cadmium stress. Botany 2019, 97, 681–690. [Google Scholar] [CrossRef]
- Piacentini, D.; Ronzan, M.; Fattorini, L.; Della Rovere, F.; Massimi, L.; Altamura, M.M.; Falasca, G. Nitric oxide alleviates cadmium-but not arsenic-induced damages in rice roots. Plant Physiol. Biochem. 2020, 151, 729–742. [Google Scholar] [CrossRef] [PubMed]
- Li, S.-W.; Li, Y.; Leng, Y.; Zeng, X.-Y.; Ma, Y.-H. Nitric oxide donor improves adventitious rooting in mung bean hypocotyl cuttings exposed to cadmium and osmotic stresses. Environ. Exp. Bot. 2019, 164, 114–123. [Google Scholar] [CrossRef]
- Ahmad, P.; Ahanger, M.A.; Alyemeni, M.N.; Wijaya, L.; Alam, P. Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma 2018, 255, 79–93. [Google Scholar] [CrossRef]
- Ahmad, A.; Khan, W.U.; Shah, A.A.; Yasin, N.A.; Naz, S.; Ali, A.; Tahir, A.; Batool, A.I. Synergistic effects of nitric oxide and silicon on promoting plant growth, oxidative stress tolerance and reduction of arsenic uptake in Brassica juncea. Chemosphere 2021, 262, 128384. [Google Scholar] [CrossRef] [PubMed]
- Singh, R.; Parihar, P.; Prasad, S.M. Interplay of Calcium and nitric oxide in improvement of growth and arsenic-induced toxicity in mustard seedlings. Sci. Rep. 2020, 10, 6900. [Google Scholar] [CrossRef] [Green Version]
- Praveen, A.; Pandey, A.; Gupta, M. Protective role of nitric oxide on nitrogen-thiol metabolism and amino acids profiling during arsenic exposure in Oryza sativa L. Ecotoxicology 2020, 29, 825–836. [Google Scholar] [CrossRef]
- Farnese, F.S.; Oliveira, J.A.; Paiva, E.A.; Menezes-Silva, P.E.; da Silva, A.A.; Campos, F.V.; Ribeiro, C. The involvement of nitric oxide in integration of plant physiological and ultrastructural adjustments in response to arsenic. Front. Plant Sci. 2017, 8, 516. [Google Scholar] [CrossRef] [Green Version]
- Namdjoyan, S.; Kermanian, H.; Soorki, A.A.; Tabatabaei, S.M.; Elyasi, N. Interactive effects of salicylic acid and nitric oxide in alleviating zinc toxicity of Safflower (Carthamus tinctorius L.). Ecotoxicology 2017, 26, 752–761. [Google Scholar] [CrossRef]
- Tripathi, D.K.; Mishra, R.K.; Singh, S.; Singh, S.; Singh, V.P.; Singh, P.K.; Pandey, A.C. Nitric oxide ameliorates zinc oxide nano-particles phytotoxicity in wheat seedlings: Implication of the ascorbate-glutathione cycle. Front. Plant Sci. 2017, 8, 1. [Google Scholar] [CrossRef]
- Kaya, C. Nitric oxide improves high zinc tolerance in maize plants. J. Plant Nutr. 2015, 39, 2072–2078. [Google Scholar] [CrossRef]
- Becana, M.; Dalton, D.A.; Moran, J.F.; Iturbe-Ormaetxe, I.; Matamoros, M.A.; Rubio, M.C. Reactive oxygen species and antiox-idants in legume nodules. Physiol. Plant 2000, 109, 372–381. [Google Scholar] [CrossRef] [Green Version]
- Foyer, C.H.; Lelandais, M.; Kunert, K.J. Photooxidative stress in plants. Physiol. Plant 1994, 92, 696–717. [Google Scholar] [CrossRef]
- Huang, H.; Ullah, F.; Zhou, D.-X.; Yi, M.; Zhao, Y. Mechanisms of ROS regulation of plant development and stress responses. Front. Plant Sci. 2019, 10, 800. [Google Scholar] [CrossRef] [PubMed]
- Sandalio, L.M.; Romero-Puertas, M.C. Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. Ann. Bot. 2015, 116, 475–485. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schippers, J.H.; Foyer, C.; van Dongen, J. Redox regulation in shoot growth, SAM maintenance and flowering. Curr. Opin. Plant Biol. 2016, 29, 121–128. [Google Scholar] [CrossRef] [PubMed]
- Decros, G.; Baldet, P.; Beauvoit, B.; Stevens, R.; Flandin, A.; Colombié, S.; Pétriacq, P. Get the balance right: ROS homeostasis and redox signalling in fruit. Front. Plant Sci. 2019, 10, 1091. [Google Scholar] [CrossRef] [PubMed]
- Muñoz, P.; Munné-Bosch, S. Photo-oxidative stress during leaf, flower and fruit development. Plant Physiol. 2018, 176, 1004–1014. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, H.-T.; Wan, Z.-Y.; Li, S.; Zhang, Y. Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 2014, 26, 2007–2023. [Google Scholar] [CrossRef] [Green Version]
- Gan, L.; Wu, X.; Zhong, Y. Exogenously applied nitric oxide enhances the drought tolerance in hulless barley. Plant Prod. Sci. 2015, 18, 52–56. [Google Scholar] [CrossRef] [Green Version]
- Arasimowicz-Jelonek, M.; Floryszak-Wieczorek, J.; Kubiś, J. Interaction between polyamine and nitric oxide signaling in adaptive responses to drought in cucumber. J. Plant Growth Regul. 2009, 28, 177–186. [Google Scholar] [CrossRef]
- Santisree, P.; Bhatnagar-Mathur, P.; Sharma, K.K. NO to drought-multifunctional role of nitric oxide in plant drought: Do we have all the answers? Plant Sci. 2015, 239, 44–55. [Google Scholar] [CrossRef] [PubMed]
- Kolbert, Z.; Bartha, B.; Erdei, L. Generation of nitric oxide in roots of Pisum sativum, Triticum aestivum and Petroselinum crispum plants under osmotic and drought stress. Acta Biol. Szeged. 2005, 49, 13–16. [Google Scholar]
- Filippou, P.; Bouchagier, P.; Skotti, E.; Fotopoulos, V. Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ. Exp. Bot. 2014, 97, 1–10. [Google Scholar] [CrossRef]
- Gayatri, G.; Agurla, S.; Raghavendra, A.S. Nitric oxide in guard cells as an important secondary messenger during stomatal closure. Front. Plant Sci. 2013, 4, 425. [Google Scholar] [CrossRef] [Green Version]
- Fan, Q.J.; Liu, J.H. Nitric oxide is involved in dehydration/drought tolerance in Poncirus trifoliata seedlings through regulation of antioxidant systems and stomatal response. Plant Cell Rep. 2012, 31, 145–154. [Google Scholar] [CrossRef]
- Besson-Bard, A.; Astier, J.; Rasul, S.; Wawer, I.; Dubreuil-Maurizi, C.; Jeandroz, S.; Wendehenne, D. Current view of nitric oxide-responsive genes in plants. Plant Sci. 2009, 177, 302–309. [Google Scholar] [CrossRef]
- Palmieri, M.C.; Sell, S.; Huang, X.; Scherf, M.; Werner, T.; Durner, J.; Lindermayr, C. Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: A bioinformatics approach. J. Exp. Bot. 2008, 59, 177–186. [Google Scholar] [CrossRef] [Green Version]
- Chen, P.; Chen, J.; Sun, M.; Yan, H.; Feng, G.; Wu, B.; Zhang, X.; Wang, X.; Huang, L. Comparative transcriptome study of switchgrass (Panicum virgatum L.) homologous autopolyploid and its parental amphidiploid responding to consistent drought stress. Biotechnol. Biofuels 2020, 13, 170. [Google Scholar] [CrossRef]
- Nabi, R.B.S.; Tayade, R.; Hussain, A.; Kulkarni, K.P.; Imran, Q.M.; Mun, B.-G.; Yun, B.-W. Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress. Environ. Exp. Bot. 2019, 161, 120–133. [Google Scholar] [CrossRef]
- Bartels, D. Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr. Comp. Biol. 2005, 45, 696–701. [Google Scholar] [CrossRef]
- Miller, G.; Suzuki, N.; Ciftci-Yilmaz, S.; Mittler, R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 2010, 33, 453–467. [Google Scholar] [CrossRef]
- Hasanuzzaman, M.; Hossain, M.A.; da Silva, J.A.T.; Fujita, M. Plant response and tolerance to abiotic oxidative stress: Anti-oxidant defense is a key factor. In Crop Stress and Its Management: Perspectives and Strategies; Springer: Dordrecht, The Netherlands, 2012; pp. 261–315. [Google Scholar]
- Seki, M.; Narusaka, M.; Abe, H.; Kasuga, M.; Yamaguchi-Shinozaki, K.; Carninci, P.; Hayashizaki, Y.; Shinozaki, K. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 2001, 13, 61–72. [Google Scholar] [CrossRef] [Green Version]
- Neill, S.J.; Barros, R.; Bright, J.; Desikan, R.; Hancock, J.; Harrison, J.; Morris, P.; Ribeiro, D.; Wilson, I.D. Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot. 2008, 59, 165–176. [Google Scholar] [CrossRef] [Green Version]
- Shao, R.; Wang, K.; Shangguan, Z. Cytokinin-induced photosynthetic adaptability of Zea mays L. to drought stress associated with nitric oxide signal: Probed by ESR spectroscopy and fast OJIP fluorescence rise. J. Plant Physiol. 2010, 167, 472–479. [Google Scholar] [CrossRef]
- Asai, S.; Ohta, K.; Yoshioka, H. MAPK Signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 2008, 20, 1390–1406. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shi, H.; Ye, T.; Zhu, J.-K.; Chan, Z. Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J. Exp. Bot. 2014, 65, 4119–4131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.; Hou, Z.-H.; Liu, G.-H.; Hou, L.-X.; Liu, X. Hydrogen sulfide may function downstream of nitric oxide in ethylene-induced stomatal closure in Vicia faba L. J. Integr. Agric. 2012, 11, 1644–1653. [Google Scholar] [CrossRef]
- Zhang, A.; Jiang, M.; Zhang, J.; Ding, H.; Xu, S.; Hu, X.; Tan, M. 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. New Phytol. 2007, 175, 36–50. [Google Scholar] [CrossRef]
- Shan, C.; Zhang, S.; Ou, X. The roles of H2S and H2O2 in regulating AsA-GSH cycle in the leaves of wheat seedlings under drought stress. Protoplasma 2018, 255, 1257–1262. [Google Scholar] [CrossRef]
- Zandalinas, S.I.; Balfagón, D.; Arbona, V.; Gómez-Cadenas, A. Modulation of antioxidant defense system is associated with combined drought and heat stress tolerance in Citrus. Front. Plant Sci. 2017, 8, 953. [Google Scholar] [CrossRef] [Green Version]
- Wu, J.; Zhang, J.; Li, X.; Xu, J.J.; Wang, L. Identification and characterization of a PutCu/Zn-SOD gene from Puccinellia tenuiflora (Turcz.) Scribn. et Merr. Plant Growth Regul. 2016, 79, 55–64. [Google Scholar] [CrossRef]
- Farooq, M.; Basra, S.M.A.; Wahid, A.; Cheema, Z.A.; Cheema, M.A.; Khaliq, A. Physiological role of exogenously applied gly-cinebetaine to improve drought tolerance in fine grain aromatic rice (Oryza sativa L.). J. Agron. Crop Sci. 2008, 194, 325–333. [Google Scholar] [CrossRef]
- Murata, Y.; Mori, I.C.; Munemasa, S. Diverse stomatal signaling and the signal integration mechanism. Annu. Rev. Plant Biol. 2015, 66, 369–392. [Google Scholar] [CrossRef]
- Van Meeteren, U.; Kaiser, E.; Malcolm Matamoros, P.; Verdonk, J.C.; Aliniaeifard, S. Is nitric oxide a critical key factor in ABA-induced stomatal closure? J. Exp. Bot. 2020, 71, 399–410. [Google Scholar] [CrossRef]
- Lawson, T.; Blatt, M.R.; Yu, L.; Shi, D.; Li, J.; Kong, Y.; Yu, Y.; Chai, G.; Hu, R.; Wang, J.; et al. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol. 2014, 164, 1556–1570. [Google Scholar] [CrossRef] [Green Version]
- García-Mata, C.; Gay, R.; Sokolovski, S.; Hills, A.; Lamattina, L.; Blatt, M.R. Nitric oxide regulates K+ and Cl- channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc. Natl. Acad. Sci. USA 2003, 100, 11116–11121. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sokolovski, S.; Hills, A.; Gay, R.; Garcia Mata, C.; Lamattina, L.; Blatt, M.R. Protein phosphorylation is a prerequisite for in-tracellular Ca2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. Plant J. 2005, 43, 520–529. [Google Scholar] [CrossRef] [PubMed]
- Huang, A.-X.; She, X.-P.; Cao, B.; Zhang, B.; Mu, J.; Zhang, S.-J. Nitric oxide, actin reorganization and vacuoles change are involved in PEG 6000-induced stomatal closure in Vicia faba. Physiol. Plant 2009, 136, 45–56. [Google Scholar] [CrossRef] [PubMed]
- Ning, P.; Wang, J.; Zhou, Y.; Gao, L.; Wang, J.; Gong, C. Adaptational evolution of trichome in Caragana korshinskii to natural drought stress on the Loess Plateau, China. Ecol. Evol. 2016, 6, 3786–3795. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Desikan, R.; Last, K.; Harrett-Williams, R.; Tagliavia, C.; Harter, K.; Hooley, R.; Hancock, J.T.; Neill, S.J. Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J. 2006, 47, 907–916. [Google Scholar] [CrossRef]
- Correa-Aragunde, N.; Graziano, M.; Chevalier, C.; Lamattina, L. Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J. Exp. Bot. 2006, 57, 581–588. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, J.; Yang, H.; Mu, J.; Lu, T.; Peng, J.; Deng, X.; Kong, Z.; Bao, S.; Cao, X.; Zuo, J. Nitric oxide regulates protein methylation during stress responses in plants. Mol. Cell 2017, 67, 702–710.e4. [Google Scholar] [CrossRef] [PubMed]
- Stamler, J.S. Redox signaling: Nitrosylation and related target interactions of nitric oxide. Cell 1994, 78, 931–936. [Google Scholar] [CrossRef]
- Radi, R. Nitric oxide, oxidants, and protein tyrosine nitration. Proc. Natl. Acad. Sci. USA 2004, 101, 4003–4008. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feng, X.; Liu, W.; Cao, F.; Wang, Y.; Zhang, G.; Chen, Z.-H.; Wu, F. Overexpression of HvAKT1 improves drought tolerance in barley by regulating root ion homeostasis and ROS and NO signaling. J. Exp. Bot. 2020, 71, 6587–6600. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.C.; Li, Y.H.; Yuan, H.M.; Zhang, B.L.; Zhai, S.; Lu, Y.T. WD40-REPEAT 5a functions in drought stress tolerance by regu-lating nitric oxide accumulation in Arabidopsis. Plant Cell Environ. 2017, 40, 543–552. [Google Scholar] [CrossRef] [PubMed]
- Khan, M.; Imran, Q.M.; Shahid, M.; Mun, B.G.; Lee, S.U.; Khan, M.A.; Yun, B.W. Nitric oxide-induced AtAO3 differentially reg-ulates plant defense and drought tolerance in Arabidopsis thaliana. BMC Plant Biol. 2019, 19, 602. [Google Scholar] [CrossRef]
- Chen, F.; Hu, Y.; Vannozzi, A.; Wu, K.; Cai, H.; Qin, Y.; Mullis, A.; Lin, Z.; Zhang, L. The WRKY Transcription Factor Family in Model Plants and Crops. Crit. Rev. Plant Sci. 2017, 36, 311–335. [Google Scholar] [CrossRef]
- Gao, Y.; Liu, J.; Yang, F.; Zhang, G.; Wang, D.; Zhang, L.; Ou, Y.; Yao, Y. The WRKY transcription factor WRKY8 promotes resistance to pathogen infection and mediates drought and salt stress tolerance in Solanum lycopersicum. Physiol. Plant. 2019, 168, 98–117. [Google Scholar] [CrossRef]
- Ahammed, G.J.; Li, X.; Mao, Q.; Wan, H.; Zhou, G.; Cheng, Y. The SlWRKY81 transcription factor inhibits stomatal closure by attenuating nitric oxide accumulation in the guard cells of tomato under drought. Physiol. Plant. 2021, 172, 885–895. [Google Scholar] [CrossRef] [PubMed]
- Tchounwou, P.B.; Yedjou, C.G.; Patlolla, A.K.; Sutton, D.J. Heavy metal toxicity and the environment. NIH 2012, 101, 133–164. [Google Scholar] [CrossRef] [Green Version]
- Shallari, S.; Schwartz, C.; Hasko, A.; Morel, J. Heavy metals in soils and plants of serpentine and industrial sites of Albania. Sci. Total Environ. 1998, 209, 133–142. [Google Scholar] [CrossRef]
- Harvey, L.J.; McArdle, H.J. Biomarkers of copper status: A brief update. Br. J. Nutr. 2008, 99, S10–S13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stern, B.R. Essentiality and toxicity in copper health risk assessment: Overview, update and regulatory considerations. Toxicol. Environ. Health A 2010, 73, 114–127. [Google Scholar] [CrossRef]
- Shahid, M.; Dumat, C.; Khalid, S.; Niazi, N.K.; Antunes, P.M.C. Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. Rev. Environ. Contam. Toxicol. 2016, 241, 73–137. [Google Scholar] [CrossRef]
- Sanz-Fernández, M.; Rodríguez-Serrano, M.; Sevilla-Perea, A.; Pena, L.; Mingorance, M.D.; Sandalio, L.M.; Romero-Puertas, M.C. Screening Arabidopsis mutants in genes useful for phytoremediation. J. Hazard. Mater. 2017, 335, 143–151. [Google Scholar] [CrossRef]
- Cui, B.; Pan, Q.; Clarke, D.; Villarreal, M.O.; Umbreen, S.; Yuan, B.; Shan, W.; Jiang, J.; Loake, G.J. S-nitrosylation of the zinc finger protein SRG1 regulates plant immunity. Nat. Commun. 2018, 9, 4226. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Romero-Puertas, M.C.; Terrón-Camero, L.C.; Peláez-Vico, M.Á.; Olmedilla, A.; Sandalio, L.M. Reactive oxygen and nitrogen species as key indicators of plant responses to Cd stress. Environ. Exp. Bot. 2019, 161, 107–119. [Google Scholar] [CrossRef]
- Loix, C.; Huybrechts, M.; Vangronsveld, J.; Gielen, M.; Keunen, E.; Cuypers, A. Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants. Front. Plant Sci. 2017, 8, 1867. [Google Scholar] [CrossRef] [Green Version]
- Souri, Z.; Karimi, N.; de Oliveira, L.M. Antioxidant enzymes responses in shoots of arsenic hyperaccumulator, Isatis cappadocica Desv., under interaction of arsenate and phosphate. Environ. Technol. 2018, 39, 1316–1327. [Google Scholar] [CrossRef]
- Terrón-Camero, L.C.; Peláez-Vico, M.Á.; Del-Val, C.; Sandalio, L.M.; Romero-Puertas, M.C. Role of nitric oxide in plant responses to heavy metal stress: Exogenous application versus endogenous production. J. Exp. Bot. 2019, 70, 4477–4488. [Google Scholar] [CrossRef] [PubMed]
- Sahay, S.; Gupta, M. An update on nitric oxide and its benign role in plant responses under metal stress. Nitric Oxide 2017, 67, 39–52. [Google Scholar] [CrossRef] [PubMed]
- Beligni, M.V.; Lamattina, L. Nitric oxide: A non-traditional regulator of plant growth. Trends Plant Sci. 2001, 6, 508–509. [Google Scholar] [CrossRef]
- Ismael, M.A.; Elyamine, A.M.; Moussa, M.G.; Cai, M.; Zhao, X.; Hu, C. Cadmium in plants: Uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 2019, 11, 255–277. [Google Scholar] [CrossRef]
- Verbruggen, N.; Hermans, C.; Schat, H. Mechanisms to cope with arsenic or cadmium excess in plants. Curr. Opin. Plant Biol. 2009, 12, 364–372. [Google Scholar] [CrossRef] [PubMed]
- Besson-Bard, A.; Gravot, A.; Richaud, P.; Auroy, P.; Duc, C.; Gaymard, F.; Taconnat, L.; Renou, J.-P.; Pugin, A.; Wendehenne, D. Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol. 2009, 149, 1302–1315. [Google Scholar] [CrossRef] [Green Version]
- Connolly, E.L.; Fett, J.; Guerinot, M.L. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 2002, 14, 1347–1357. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Graziano, M.; Lamattina, L. Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. Plant J. 2007, 52, 949–960. [Google Scholar] [CrossRef]
- Zafari, S.; Sharifi, M.; Chashmi, N.A.; Mur, L. Modulation of Pb-induced stress in Prosopis shoots through an interconnected network of signaling molecules, phenolic compounds and amino acids. Plant Physiol. Biochem. 2016, 99, 11–20. [Google Scholar] [CrossRef] [Green Version]
- Per, T.S.; Masood, A.; Khan, N.A. Nitric oxide improves S-assimilation and GSH production to prevent inhibitory effects of cadmium stress on photosynthesis in mustard (Brassica juncea L.). Nitric Oxide 2017, 68, 111–124. [Google Scholar] [CrossRef]
- Khator, K.; Saxena, I.; Shekhawat, G.S. Nitric oxide induced Cd tolerance and phytoremediation potential of B. juncea by the modulation of antioxidant defense system and ROS detoxification. BioMetals 2021, 34, 15–32. [Google Scholar] [CrossRef] [PubMed]
- Kaya, C.; Ashraf, M.; Alyemeni, M.N.; Ahmad, P. Responses of nitric oxide and hydrogen sulfide in regulating oxidative defence system in wheat plants grown under cadmium stress. Physiol. Plant 2019, 168, 345–360. [Google Scholar] [CrossRef] [PubMed]
- Dong, Y.J.; Chen, W.F.; Liu, F.Z.; Wan, Y.S. Physiological responses of peanut seedlings to exposure to low or high cadmium concentration and the alleviating effect of exogenous nitric oxide to high cadmium concentration stress. Plant Biosyst. Int. J. Deal. All Asp. Plant Biol. 2019, 154, 405–412. [Google Scholar] [CrossRef]
- Kaya, C.; Akram, N.A.; Sürücü, A.; Ashraf, M. 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. Sci. Hortic. 2019, 255, 52–60. [Google Scholar] [CrossRef]
- Khan, A.; Khan, S.; Khan, M.A.; Qamar, Z.; Waqas, M. The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: A review. Environ. Sci. Pollut. Res. 2015, 22, 13772–13799. [Google Scholar] [CrossRef]
- Burkhead, J.L.; Gogolin Reynolds, K.A.; Abdel-Ghany, S.E.; Cohu, C.M.; Pilon, M. Copper homeostasis. New Phytol. 2009, 182, 799–816. [Google Scholar] [CrossRef] [PubMed]
- Branco-Neves, S.; Soares, C.; De Sousa, A.; Martins, V.; Azenha, M.; Gerós, H.; Fidalgo, F. An efficient antioxidant system and heavy metal exclusion from leaves make Solanum cheesmaniae more tolerant to Cu than its cultivated counterpart. Food Energy Secur. 2017, 6, 123–133. [Google Scholar] [CrossRef]
- Chamizo-Ampudia, A.; Sanz-Luque, E.; Llamas, A.; Galvan, A.; Fernandez, E.P.-A. Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci. 2017, 22, 163–174. [Google Scholar] [CrossRef]
- Rizwan, M.; Mostofa, M.G.; Ahmad, M.Z.; Imtiaz, M.; Mehmood, S.; Adeel, M.; Dai, Z.; Li, Z.; Aziz, O.; Zhang, Y.; et al. Nitric oxide induces rice tolerance to excessive nickel by regulating nickel uptake, reactive oxygen species detoxification and defense-related gene expression. Chemosphere 2018, 191, 23–35. [Google Scholar] [CrossRef]
- Oz, M.T.; Eyidogan, F.; Yucel, M.; Öktem, H.A. Functional Role of Nitric Oxide Under Abiotic Stress Conditions. In Nitric Oxide Action in Abiotic Stress Responses in Plants; Springer Science and Business Media LLC: Berlin/Heidelberg, Germany, 2015; pp. 21–41. [Google Scholar]
- Yang, H.; Mu, J.; Chen, L.; Feng, J.; Hu, J.; Li, L.; Zhou, J.-M.; Zuo, J. S-Nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol. 2015, 167, 1604–1615. [Google Scholar] [CrossRef] [Green Version]
- Zhang, L.P.; Mehta, S.K.; Liu, Z.P.; Yang, Z.M. Copper-Induced Proline Synthesis is Associated with Nitric Oxide Generation in Chlamydomonas reinhardtii. Plant Cell Physiol. 2008, 49, 411–419. [Google Scholar] [CrossRef]
- Hu, K.-D.; Hu, L.-Y.; Li, Y.-H.; Zhang, F.-Q.; Zhang, H. Protective roles of nitric oxide on germination and antioxidant metabolism in wheat seeds under copper stress. Plant Growth Regul. 2007, 53, 173–183. [Google Scholar] [CrossRef]
- Sharma, A.; Soares, C.; Sousa, B.; Martins, M.; Kumar, V.; Shahzad, B.; Thukral, A.K. Nitric oxide-mediated regulation of oxi-dative stress in plants under metal stress: A review on molecular and biochemical aspects. Physiol. Plant 2020, 168, 318–344. [Google Scholar]
- Da-Silva, C.J.; Canatto, R.A.; Cardoso, A.A.; Ribeiro, C.; Oliveira, J.A. Arsenic-hyperaccumulation and antioxidant system in the aquatic macrophyte Spirodela intermedia W. Koch (Lemnaceae). Theor. Exp. Plant Physiol. 2017, 29, 203–213. [Google Scholar] [CrossRef]
- Nath, S.; Panda, P.; Mishra, S.; Dey, M.; Choudhury, S.; Sahoo, L.; Panda, S.K. Arsenic stress in rice: Redox consequences and regulation by iron. Plant Physiol. Biochem. 2014, 80, 203–210. [Google Scholar] [CrossRef] [PubMed]
- Souri, Z.; Karimi, N.; Farooq, M.A.; Sandalio, L.M. Nitric oxide improves tolerance to arsenic stress in Isatis cappadocica desv. Shoots by enhancing antioxidant defenses. Chemosphere 2020, 239, 124523. [Google Scholar] [CrossRef] [PubMed]
- Souri, Z.; Karimi, N. Enhanced phytoextraction by As hyperaccumulator Isatis cappadocica spiked with sodium nitro-prusside. Soil Sedim. Contam. Int. J. 2017, 26, 457–468. [Google Scholar] [CrossRef]
- Praveen, A.; Gupta, M. 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. Environ. Pollut. 2018, 240, 950–962. [Google Scholar] [CrossRef]
- Singh, P.K.; Indoliya, Y.; Chauhan, A.S.; Singh, S.P.; Singh, A.P.; Dwivedi, S.; Chakrabarty, D. Nitric oxide mediated transcrip-tional modulation enhances plant adaptive responses to arsenic stress. Sci. Rep. 2017, 7, 3592. [Google Scholar] [CrossRef]
- Chakrabarty, D.; Trivedi, P.K.; Misra, P.; Tiwari, M.; Shri, M.; Shukla, D.; Kumar, S.; Rai, A.; Pandey, A.; Nigam, D.; et al. Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 2009, 74, 688–702. [Google Scholar] [CrossRef]
- Chandrakar, V.; Yadu, B.; Meena, R.K.; Dubey, A.; Keshavkant, S. Arsenic-induced genotoxic responses and their amelioration by diphenylene iodonium, 24-epibrassinolide and proline in Glycine max L. Plant Physiol. Biochem. 2017, 112, 74–86. [Google Scholar] [CrossRef]
- Rejeb, K.B.; Abdelly, C.; Savouré, A. How reactive oxygen species and proline face stress together. Plant Physiol. Biochem. 2014, 80, 278–284. [Google Scholar] [CrossRef]
- Chandrakar, V.; Keshavkant, S. Nitric oxide and dimethylthiourea up-regulates pyrroline-5-carboxylate synthetase ex-pression to improve arsenic tolerance in Glycine max L. Environ. Prog. Sustain. Energy 2019, 38, 402–409. [Google Scholar] [CrossRef]
- Tsonev, T.; Lidon, F.J.C. Zinc in plants—An overview. Emir J Food Agric. 2012, 24, 322–333. [Google Scholar]
- Soares, C.; Carvalho, M.; Azevedo, R.A.; Fidalgo, F. Plants facing oxidative challenges—A little help from the antioxidant networks. Environ. Exp. Bot. 2019, 161, 4–25. [Google Scholar] [CrossRef]
- Lin, Y.-F.; Aarts, M.G.M. The molecular mechanism of zinc and cadmium stress response in plants. Cell. Mol. Life Sci. 2012, 69, 3187–3206. [Google Scholar] [CrossRef] [PubMed]
- Kolbert, Z.; Molnár, Á.; Oláh, D.; Feigl, G.; Horváth, E.; Erdei, L.; Lindermayr, C. S-Nitrosothiol signaling is involved in regulating hydrogen peroxide metabolism of zinc-stressed Arabidopsis. Plant Cell. Physiol. 2019, 60, 2449–2463. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Kader, D.Z.E.-A. Role of nitric oxide, glutathione and sulfhydryl groups in zinc homeostasis in plants. Am. J. Plant Physiol. 2007, 2, 59–75. [Google Scholar] [CrossRef]
- Xiong, J.; Fu, G.; Tao, L.; Zhu, C. Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch. Biochem. Biophys. 2010, 497, 13–20. [Google Scholar] [CrossRef]
- Nasiri-Savadkoohi, S.; Saeidi-Sar, S.; Abbaspour, H.; Dehpour, A.A. Protective role of exogenous nitric oxide against zinc toxicity in Plantago major L. Appl. Ecol. Environ. Res. 2017, 15, 511–524. [Google Scholar] [CrossRef]
- Buet, A.; Moriconi, J.I.; Santa-Maria, G.E.; Simontacchi, M. An exogenous source of nitric oxide modulates zinc nutritional status in wheat plants. Plant Physiol. Biochem. 2014, 83, 337–345. [Google Scholar] [CrossRef]
- Sürücü, A.; Mohammad, D.M.; Günal, E.; Budak, M. Concentration of heavy metals in soils along three major roads of Sulaimani, Northeast Iraq. Carpathian J. Earth Environ. Sci. 2018, 13, 523–538. [Google Scholar] [CrossRef]
- Kobylińska, A.; Reiter, R.J.; Posmyk, M.M. Melatonin Protects Cultured Tobacco Cells against Lead-Induced Cell Death via Inhibition of Cytochrome c Translocation. Front. Plant Sci. 2017, 8, 1560. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, J.; Zhang, Z.; Zhang, Y.; Wei, Y.; Jiang, Z. Effects of lead stress on the growth, physiology, and cellular structure of privet seedlings. PLoS ONE 2018, 13, e0191139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Okant, M.; Kaya, C. The role of endogenous nitric oxide in melatonin-improved tolerance to lead toxicity in maize plants. Environ. Sci. Pollut. Res. 2019, 26, 11864–11874. [Google Scholar] [CrossRef]
- Corpas, F.J.; Barroso, J.B. Peroxynitrite (ONOO−) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress. Ann. Bot. 2013, 113, 87–96. [Google Scholar] [CrossRef] [Green Version]
- Bai, X.Y.; Dong, Y.J.; Wang, Q.H.; Xu, L.L.; Kong, J.; Liu, S. Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass. Biol. Plant. 2014, 59, 163–170. [Google Scholar] [CrossRef]
- Oliveira, H. Chromium as an environmental pollutant: Insights on induced plant toxicity, Hindawi Publishing Corporation. J. Bot. 2012, 2012, 375843. [Google Scholar]
- Shanker, A.K.; Cervantes, C.; Loza-Tavera, H.; Avudainayagam, S. Chromium toxicity in plants. Environ Int. 2005, 31, 739–753. [Google Scholar] [CrossRef]
- Huang, M.; Ai, H.; Xu, X.; Chen, K.; Niu, H.; Zhu, H.; Sun, J.; Du, D.; Chen, L. Nitric oxide alleviates toxicity of hexavalent chromium on tall fescue and improves performance of photosystem II. Ecotoxicol. Environ. Saf. 2018, 164, 32–40. [Google Scholar] [CrossRef]
- Kharbech, O.; Sakouhi, L.; Ben Massoud, M.; Mur, L.A.J.; Corpas, F.J.; Djebali, W.; Chaoui, A. Nitric oxide and hydrogen sulfide protect plasma membrane integrity and mitigate chromium-induced methylglyoxal toxicity in maize seedlings. Plant Physiol. Biochem. 2020, 157, 244–255. [Google Scholar] [CrossRef]
- Khan, M.N.; Alamri, S.; Al-Amri, A.A.; Alsubaie, Q.D.; Al-Munqedi, B.; Ali, H.M.; Siddiqui, M.H. Effect of nitric oxide on seed germination and seedling development of tomato under chromium toxicity. J. Plant Growth Regul. 2020, 1–13. [Google Scholar] [CrossRef]
- Han, F.X.; Banin, A.; Su, Y.; Monts, D.L.; Plodinec, J.M.; Kingery, W.L.; Triplett, G.E. Industrial age anthropogenic inputs of heavy metals into the pedosphere. Naturwissenschaften 2002, 89, 497–504. [Google Scholar] [CrossRef]
- Han, F.X.; Su, Y.; Monts, D.L.; Waggoner, C.A.; Plodinec, M.J. Binding, distribution, and plant uptake of mercury in a soil from Oak Ridge, Tennessee, USA. Sci. Total Environ. 2006, 368, 753–768. [Google Scholar] [CrossRef]
- Ahmad, P.; Alyemeni, M.N.; Wijaya, L.; Ahanger, M.A.; Ashraf, M.; Alam, P.; Paray, B.A.; Rinklebe, J. Nitric oxide donor, sodium nitroprusside, mitigates mercury toxicity in different cultivars of soybean. J. Hazard. Mater. 2021, 408, 124852. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Zhang, L.; Zhu, C. Exogenous nitric oxide mediates alleviation of mercury toxicity by promoting auxin transport in roots or preventing oxidative stress in leaves of rice seedlings. Acta Physiol. Plant. 2015, 37, 194. [Google Scholar] [CrossRef]
- Munns, R.; Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 2008, 59, 651–681. [Google Scholar] [CrossRef] [Green Version]
- Munns, R. Genes and salt tolerance: Bringing them together. New Phytol. 2005, 167, 645–663. [Google Scholar] [CrossRef]
- Garthwaite, A.J.; Von Bothmer, R.; Colmer, T.D. Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl− into the shoots. J. Exp. Bot. 2005, 56, 2365–2378. [Google Scholar] [CrossRef] [PubMed]
- Ahmad, P.; Ahanger, M.A.; Alyemeni, M.N.; Wijaya, L.; Alam, P.; Ashraf, M. Mitigation of sodium chloride toxicity in Solanum lycopersicum L. by supplementation of jasmonic acid and nitric oxide. J. Plant Interact. 2018, 13, 64–72. [Google Scholar] [CrossRef] [Green Version]
- Ahmad, P.; Abdel Latef, A.A.; Hashem, A.; Abd_Allah, E.F.; Gucel, S.; Tran, L.S.P. Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front. Plant Sci. 2016, 7, 347. [Google Scholar] [CrossRef] [Green Version]
- Ren, Y.; Wang, W.; He, J.; Zhang, L.; Wei, Y.; Yang, M. Nitric oxide alleviates salt stress in seed germination and early seedling growth of pakchoi (Brassica chinensis L.) by enhancing physiological and biochemical parameters. Ecotoxicol. Environ. Saf. 2020, 187, 109785. [Google Scholar] [CrossRef] [PubMed]
- Shams, M.; Ekinci, M.; Ors, S.; Turan, M.; Agar, G.; Kul, R.; Yildirim, E. Nitric oxide mitigates salt stress effects of pepper seedlings by altering nutrient uptake, enzyme activity and osmolyte accumulation. Physiol. Mol. Biol. Plants 2019, 25, 1149–1161. [Google Scholar] [CrossRef]
- Assaha, D.V.M.; Ueda, A.; Saneoka, H.; Al-Yahyai, R.; Yaish, M.W. The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front. Physiol. 2017, 8, 509. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Wang, L.; Liu, Y.; Zhang, Q.; Wei, Q.; Zhang, W. Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 2006, 224, 545–555. [Google Scholar] [CrossRef]
- Campos, F.V.; Oliveira, J.A.; Pereira, M.G.; Farnese, F.S. Nitric oxide and phytohormone interactions in the response of Lactuca sativa to salinity stress. Planta 2019, 250, 1475–1489. [Google Scholar] [CrossRef]
- Hasanuzzaman, M.; Oku, H.; Nahar, K.; Bhuyan, M.B.; Al Mahmud, J.; Baluska, F.; Fujita, M. Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signaling, and molecular interactions. Plant Biotechnol. Rep. 2018, 12, 77–92. [Google Scholar] [CrossRef]
- Tailor, A.; Tandon, R.; Bhatla, S.C. Nitric oxide modulates polyamine homeostasis in sunflower seedling cotyledons under salt stress. Plant Signal. Behav. 2019, 14, 1667730. [Google Scholar] [CrossRef]
- Akram, N.A.; Hafeez, N.; Farid-Ul-Haq, M.; Ahmad, A.; Sadiq, M.; Ashraf, M. Foliage application and seed priming with nitric oxide causes mitigation of salinity-induced metabolic adversaries in broccoli (Brassica oleracea L.) plants. Acta Physiol. Plant. 2020, 42, 155. [Google Scholar] [CrossRef]
- Gadelha, C.G.; Miranda, R.D.S.; Alencar, N.L.M.; Costa, J.H.; Prisco, J.T.; Gomes-Filho, E. Exogenous nitric oxide improves salt tolerance during establishment of Jatropha curcas seedlings by ameliorating oxidative damage and toxic ion accumulation. J. Plant Physiol. 2017, 212, 69–79. [Google Scholar] [CrossRef]
- Babaei, S.; Niknam, V.; Behmanesh, M. Comparative effects of nitric oxide and salicylic acid on salinity tolerance in saffron (Crocus sativus). Plant Biosyst. Int. J. Deal. All Asp. Plant Biol. 2021, 155, 73–82. [Google Scholar] [CrossRef]
- Chen, Z.; Zhao, X.; Hu, Z.; Leng, P. Nitric oxide modulating ion balance in Hylotelephium erythrostictum roots subjected to NaCl stress based on the analysis of transcriptome, fluorescence, and ion fluxes. Sci. Rep. 2019, 9, 18317. [Google Scholar] [CrossRef]
- Zhao, G.; Zhao, Y.; Yu, X.; Kiprotich, F.; Han, H.; Guan, R.; Wang, R.; Shen, W. Nitric oxide is required for melatonin-enhanced tolerance against salinity stress in rapeseed (Brassica napus L.) seedlings. Int. J. Mol. Sci. 2018, 19, 1912. [Google Scholar] [CrossRef] [Green Version]
- Dong, Y.; Jinc, S.; Liu, S.; Xu, L.; Kong, J. Effects of exogenous nitric oxide on growth of cotton seedlings under NaCl stress. J. Soil Sci. Plant Nutr. 2014, 14, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Begara-Morales, J.C.; Chaki, M.; Valderrama, R.; Mata-Pérez, C.; Padilla, M.N.; Barroso, J.B. The function of S-nitrosothiols during abiotic stress in plants. J. Exp. Bot. 2019, 70, 4429–4439. [Google Scholar] [CrossRef]
- Begara-Morales, J.C.; Sánchez-Calvo, B.; Chaki, M.; Valderrama, R.; Mata-Pérez, C.; López-Jaramillo, J.; Padilla, M.N.; Carreras, A.; Corpas, F.J.; Barroso, J.B. Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J. Exp. Bot. 2014, 65, 527–538. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ahanger, M.A.; Aziz, U.; Alsahli, A.A.; Alyemeni, M.N.; Ahmad, P. Influence of exogenous salicylic acid and nitric oxide on growth, photosynthesis, and ascorbate-glutathione cycle in salt stressed Vigna angularis. Biomolecules 2019, 10, 42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Plant Species | Drought Imposition | Concentration and Source of NO | Plant Response to NO | Reference |
---|---|---|---|---|
Citrullus lanatus (watermelon) | 15% PEG 600 | 100 µM SNP | Reduction in MDA content Increased activity of APX Reduced oxidative damage Increased proline content | [29] |
Glycine max | Withholding water | 100 µM SNP | Reduced water loss and improved biomass due to alteration of stomatal characteristics and hydraulic conductivity | [30] |
Origanum majorana | Withholding water | 30 and 60 µM SNP | Improved water use efficiency Increased anthocyanin, soluble phenol, and flavonoid content Enhanced antioxidant capacity | [31] |
Brassica juncea | 10% PEG 6000 | 100 µM SNP | Antioxidant accumulation Reduction in MDA content Decreased ROS content | [32] |
Triticum aestivum | 15 and 30% PEG | 0.5 mM SNP | Improved antioxidant defence Enhanced glyoxalase system resulting in restoration of leaf relative water content and proline content Enhanced endogenous NO production | [33] |
Zea mays | Withholding water | 50, 100, 150, and 200 µM SNP | 100 µM SNP had a positive impact on chlorophyll content and water status Increased activity of CAT, SOD, and APX Improved activities of GR, GST, GOPX, nitrite and nitrate reductase activity | [34] |
Table | Source and Concentration of Metal | Source and Concentration of Exogenous NO | Plant Species | Impact of NO Treatment | Reference |
---|---|---|---|---|---|
A: Copper | 200, 400 µM CuSO4 | 200, 300 µM SNP | Lactuca sativa | Decreased DNA methylation Decreased genomic template instability Increased POX and SOD activity | [35] |
5, 25, 50 μM CuSO4 | 10 μM SNP | Arabidopsis thaliana | Increased cell viability | [36] | |
200 µM CuCl2 | 100 μM SNP | Lolium perenne | Increased activity of SOD, CAT, APX and POX Increased chlorophyll content and photosynthesis Maintenance of Ion homeostasis | [37] | |
0.2 mM Cu | 0.05 mM SNP | Nicotiana tabacum | Increased chlorophyll content, RUBISCO activity and fresh weight | [38] | |
450 µM CuSO4 | 200 µM SNP | Hordeum vulgare | Enhanced antioxidant enzyme activity and reduced lipid peroxidation Activation of AsA-GSH cycle | [39] | |
B: Cadmium | 150 μM Cd | 150 μM SNP | Hordeum vulgare | Decreased H2O2 and O2− contents Increased AsA, and GSH content Increased expression of HvAOX1a gene | [40] |
200 μM CdSO4 | 200 μM SNP | Catharanthus roseus | Increased melatonin and endogenous NO concentration Increased activities of CAT, SOD, POX Decreased H2O2 and lipid peroxidation in roots | [41] | |
100 μM CdSO4 | 50 μM SNP | Oryza sativa | Decreased Cd uptake by roots Restores RNS/ROS balance | [42] | |
5, 7, or 9 μM CdCl2 | 300 μM SNP | Vigna radiata | Improvement adventitious formation in hypocotyl cuttings Prevents lipid peroxidation Enhanced antioxidant enzyme activity | [43] | |
150 μM | 100 μM SNP | Solanum lycopersicum | Reduced Cd uptake Enhanced AsA-GSH cycle Increased activities of SOD, CAT, GR, MDHAR and APX | [44] | |
C: Arsenic | 75 mg/kg (NaAsO2) | 100 μM SNP | Brassica juncea | Increased activities of antioxidant enzymes Increased thiol and proline biosynthesis Decreased As uptake | [45] |
50 μM (Sodium arsenate) | 100 μM SNP | Brassica seedlings | Recovery of photosynthetic pigments Increased CAT and SOD activity resulting in decreased H2O2 and Recovery of AsA and GSH content | [46] | |
150 μM (Sodium meta arsenite) | 100 μM SNP | Oryza sativa | Enhanced nitrogen and thiol content Improved nitrate reductase and GOGAT activity Improved amino acid content | [47] | |
1.5 mg L−1 As | 0.1 mg L−1 SNP | Pistia stratiotes Leaves | Reduced ROS content Improved photochemical efficiency of PSII Maintained the integrity of cell organelles | [48] | |
D: Zinc | 500 µM ZnSO4.7H2O | 100 μM SNP | Carthamus tinctorius | Reduced Zn translocation from root to shoot Enhanced activity of AsA-GSH cycle and glyoxalase system enzymes | [49] |
100, 200 µM ZnO nanoparticles | 100 μM SNP | Triticum aestivum | Decreased Zn accumulation in xylem and phloem saps Improved activity of AsA-GSH cycle | [50] | |
0.05, 0.5 mM Zn (zinc sulfate) in nutrient solution | 0.1 mM SNP | Zea mays | Increased chlorophyll content Decreased leaf and root Zn content Increased nitrogen and iron content | [51] |
Experimental Plant | NaCl Concentration | Concentration and Source of NO | Impact of NO on Plants | Reference |
---|---|---|---|---|
Jatropa curcas | 100 mM | 75 μM SNP | Reduced oxidative damage Decreased toxic ion and ROS accumulation Increased accumulation of AsA and GSH Increased activity of CAT, SOD and GR | [183] |
Brassica oleracea (Broccoli) | 120 mM | 0.02 mM SNP | Improved CAT, SOD, and POX activity Increased glycine betaine and total phenolic content Reduction in H2O2 and MDA content | [182] |
Crocus sativus (Saffron) | 50 and 100 mM NaCl | 10 µM SNP | Improved growth Accumulation of compatible solutes Increased antioxidant enzyme activity and secondary metabolite biosynthesis | [184] |
Hylotelephium erythrostictum | 200 mM NaCl | 50 μM SNP | Increased Na+ efflux and decreased K+ efflux Increased Ca2+ influx | [185] |
Brassica napus (Rapeseed) | 200 mM NaCl | 10 μM SNP | Redox and ion homeostasis Modulation of antioxidant defence genes SOS2 and NHX1 | [186] |
Cicer arietinum L. (chickpea) | 50 and 100 mM NaCl | 50 μM SNAP (S-nitroso-N-acetylpenicillamine) | Increased osmolyte accumulation Upregulation of CAT, SOD and APX genes Decreased electrolyte leakage, MDA and H2O2 content | [174] |
Gossypium (Cotton) seedlings | 100 mM NaCl | 0.1 and 1.00 mM SNP | Increased K+ Decreased K+/Na+ ratio Increased antioxidant enzyme activity Decreased MDA content | [187] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wani, K.I.; Naeem, M.; Castroverde, C.D.M.; Kalaji, H.M.; Albaqami, M.; Aftab, T. Molecular Mechanisms of Nitric Oxide (NO) Signaling and Reactive Oxygen Species (ROS) Homeostasis during Abiotic Stresses in Plants. Int. J. Mol. Sci. 2021, 22, 9656. https://doi.org/10.3390/ijms22179656
Wani KI, Naeem M, Castroverde CDM, Kalaji HM, Albaqami M, Aftab T. Molecular Mechanisms of Nitric Oxide (NO) Signaling and Reactive Oxygen Species (ROS) Homeostasis during Abiotic Stresses in Plants. International Journal of Molecular Sciences. 2021; 22(17):9656. https://doi.org/10.3390/ijms22179656
Chicago/Turabian StyleWani, Kaiser Iqbal, M. Naeem, Christian Danve M. Castroverde, Hazem M. Kalaji, Mohammed Albaqami, and Tariq Aftab. 2021. "Molecular Mechanisms of Nitric Oxide (NO) Signaling and Reactive Oxygen Species (ROS) Homeostasis during Abiotic Stresses in Plants" International Journal of Molecular Sciences 22, no. 17: 9656. https://doi.org/10.3390/ijms22179656
APA StyleWani, K. I., Naeem, M., Castroverde, C. D. M., Kalaji, H. M., Albaqami, M., & Aftab, T. (2021). Molecular Mechanisms of Nitric Oxide (NO) Signaling and Reactive Oxygen Species (ROS) Homeostasis during Abiotic Stresses in Plants. International Journal of Molecular Sciences, 22(17), 9656. https://doi.org/10.3390/ijms22179656