Crosstalk-interaction of Nitric oxide in plant growth and development under abiotic stress
Nitric oxide (NO) is endogenously produced by short-lived free radicles and dispersed inside plant cells where it takes part in the multi-functional physiological role under optimal as well as biotic and abiotic stress. Under harsh conditions, NO modulates the antioxidant system, maintain osmotic balances, and regulates gene expression by different post-translation modification (PTM). Dose-dependent role of NO to ensure plant survival under adverse condition is well-known but still need précised and scientific research to delineate the underlying mechanisms, which are not clearly known. The endogenous level of NO is also an important parameter to mitigate the negative effect of abiotic stress which is directly or indirectly dependent upon the involvement of other growth regulators. The multidimensional role of NO under salinity, drought, heavy metal toxicity, and extreme temperature has also been discussed with updated research available till date for better understanding. In this review, an effort has been made to talk about the portion subordinate job of NO in plant development and the advancement process under the ordinary and ideal procedure. Moreover, the role of NO in major abiotic stress and its cooperation with significant plant development controllers has additionally been critically discussed.
Abat JK, Mattoo AK, Deswal R (2008). S?nitrosylated proteins of a medicinal CAM plant Kalanchoepinnata–ribulose?1, 5?bisphosphate carboxylase/oxygenase activity targeted for inhibition. The FEBS journal, 275(11):2862-72.
Adimulam SS, Bhatnagar-Mathur P, Santisree P (2017).Interaction of nitric oxide with Phytohormones under drought stress. Journal of Plant Studies, 6(1):58-61.
Ahmad, F., Kamal, A., Singh, A., Ashfaque, F., Alamri, S., & Siddiqui, M. H. (2020) Salicylic acid modulates antioxidant system, defense metabolites, and expression of salt transporter genes in Pisum sativum under salinity stress. Journal of Plant Growth Regulation, 1-14.
Ahmad F, Singh A, Kamal A (2019).Salicylic Acid–Mediated Defense Mechanisms to Abiotic Stress Tolerance.In Plant Signaling Molecules (pp. 355-369).Woodhead Publishing
Ahmad P, Abdel Latef, AA, Hashem A, Abd_Allah EF, Gucel S, Tran LS (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Frontiers in plant science. 31;7:347.
Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Alam P (2018). Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma. 1;255(1):79-93.
Anjum NA, Aref IM, Duarte AC, Pereira E, Ahmad I, Iqbal M (2014). Glutathione and proline can coordinately make plants withstand the joint attack of metal (loid) and salinity stresses. Frontiers in plant science. 21;5:662.
Apel K, Hirt H (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2;55:373-99.
Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gwó?d? EA. (2011). The message of nitric oxide in cadmium challenged plants. Plant science. 1;181(5):612-20.
Asgher M, Per TS, Masood A, Fatma M, Freschi L, Corpas FJ, Khan NA (2017). Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress.Environmental Science and Pollution Research. 1;24(3):2273-85.
Awasthi R, Bhandari K, Nayyar H (2015). Temperature stress and redox homeostasis in agricultural crops.Frontiers in Environmental Science. 17;3:11.
Bai X, Yang L, Yang Y, Ahmad P, Yang Y, Hu X (2011). Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize. J. Proteome. Res. 10, 43494364.
Camejo D, del Carmen Romero-Puertas M, Rodríguez-Serrano M, Sandalio LM, Lázaro JJ, Jiménez A, Sevilla F (2013). Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. Journal of Proteomics. 21;79:87-99.
Cechin I, Cardoso GS, Fumis TD, Corniani N (2015). Nitric oxide reduces oxidative damage induced by water stress in sunflower plants. Bragantia. 74(2):200-6.
Chaki M, Valderrama R, Ferna´ndez-Ocan˜a AM, Carreras A, Go´mez-Rodr?´guez MV, Pedrajas JR (2011). Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J. Exp. Bot. 62, 18031813
Chen, W; J. Yang, C. Qin, C. Jin, J. Mo, T. Ye, S. Zheng, Nitric Oxide Acts Downstream of Auxin to Trigger Root Ferric-Chelate Reductase Activity in Response to Iron Deficiency in Arabidopsis,Plant Physiol. 154 (2010) 810–819
Choudhury S, Panda P, Sahoo L, Panda SK (2013). Reactive oxygen species signaling in plants under abiotic stress.Plant signaling &behavior. 1;8(4):e23681.
Corpas FJ, Palma JM (2018).Nitric oxide on/off in fruit ripening.Plant Biology.;20(5):805-7.
Crawford NM, Galli M, Tischner R, Heimer YM, Okamoto M, Mack A (2006). Response to Plant nitric oxide synthase: back to square one. Trends in Plant Science. 1;11(11):526-7.
Da Silva, C. J., Fontes, E. P. B., & Modolo, L. V. (2017). Salinity-induced accumulation of endogenous H2S and NO is associated with modulation of the antioxidant and redox defense systems in Nicotiana tabacum L. cv. Havana. Plant Science, 256, 148-159.
del R?o LA, Corpas FJ, Barroso JB. (2004). Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry.1;65(7):783-92.
Diao QN, Song YJ, Shi DM, Qi HY (2016). Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersiconesculentum Mill.) seedling. Journal of Zhejiang University-SCIENCE B. 1;17(12):916-30.
Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015). Nitric oxide: a multitasked signaling gas in plants. Molecular plant. 6;8(4):506-20.
Dong YJ, Jinc SS, Liu S, Xu LL, Kong J (2014). Effects of exogenous nitric oxide on growth of cotton seedlings under NaCl stress. Journal of soil science and plant nutrition. 14(1):1-3.
Egbichi I, Keyster M, Ludidi N (2014). Effect of exogenous application of nitric oxide on salt stress responses of soybean.South African Journal of Botany. 1;90:131-6.
El Rasafi, T., Oukarroum, A., Haddioui, A., Song, H., Kwon, E. E., Bolan, N., ... & Rinklebe, J. (2022). Cadmium stress in plants: A critical review of the effects, mechanisms, and tolerance strategies. Critical Reviews in Environmental Science and Technology, 52(5), 675-726.
Esim N, Atici O (2014). Nitric oxide improves chilling tolerance of maize by affecting apoplasticantioxidative enzymes in leaves. Plant growth regulation. 1;72(1):29-38.
Essa TA (2002). Effect of salinity stress on growth and nutrient composition of three soybean (Glycine max L. Merrill) cultivars.Journal of Agronomy and Crop Science. 188(2):86-93.
Fan H, Li T, Guan L, Li Z, Guo N, Cai Y, Lin Y (2012) Effects of exogenous nitric oxide on antioxidation and DNA methylation of Dendrobiumhuoshanense grown under drought stress. Plant Cell, Tissue and Organ Culture (PCTOC). 1;109(2):307-14.
Fan J, Chen K, Amombo E, Hu Z, Chen L, Fu J (2015). Physiological and molecular mechanism of nitric oxide (NO) involved in bermudagrass response to cold stress. PloS one. 15;10(7):e0132991.
Fancy NN, Bahlmann AK, Loake GJ (2017). Nitric oxide function in plant abiotic stress. Plant, cell & environment. 40(4):462-72.
Fares A, Rossignol M, Peltier JB (2011).Proteomics investigation of endogenous S-nitrosylation in Arabidopsis.Biochemical and biophysical research communications. 416(3-4):331-6.
Farouk S, Arafa SA (2018). Mitigation of salinity stress in canola plants by sodium nitroprusside application.Spanish Journal of Agricultural Research. 19;16(3):0802.
Fatima, Abreeq, Tajammul Husain, Mohammad Suhel, Sheo Mohan Prasad, and Vijay Pratap Singh. "Implication of nitric oxide under salinity stress: the possible interaction with other signaling molecules." Journal of Plant Growth Regulation 41, no. 1 (2022): 163-177.
Fatma M, Khan NA (2014). Nitric oxide protects photosynthetic capacity inhibition by salinity in Indian mustard. J Funct Environ Bot. 4(2):106-16.
Fatma M, Masood A, Per TS, Khan NA (2016). Nitric oxide alleviates salt stress inhibited photosynthetic performance by interacting with sulfur assimilation in mustard. Frontiers in plant science. 25;7:521.
Fernández-Marcos M, Sanz L, Lorenzo O (2012). Nitric oxide: an emerging regulator of cell elongation during primary root growth. Plant signaling &behavior. 1;7(2):196-200.
Gayatri G, Agurla S, Raghavendra AS (2103). Nitric oxide in guard cells as an important secondary messenger during stomatal closure.Frontiers in Plant Science. 29;4:425.
Gill SS, Tuteja N (2010).Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.Plant physiology and biochemistry. 1;48(12):909-30.
Groß F, Durner J, Gaupels F (2013). Nitric oxide, antioxidants and prooxidants in plant defence responses. Frontiers in plant science. 29;4:419.
Guo FQ, Crawford NM. Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. The Plant Cell. 2005 Dec 1;17(12):3436-50.
Gupta, S., Devi, L. L., & Singh, A. P. (2022). Nitric Oxide: Interaction with Auxins, Brassinosteroids, and Abscisic Acid. Nitric Oxide in Plants: A Molecule with Dual Roles, 230-247.
Hao GP, Xing,Y, Zhang JH (2008). Role of nitric oxide dependence on nitric oxide synthase-like activity in the water stress signaling of maize seedling. J. Integrat. Plant Biol. 50, 435442.
Hasanuzzaman M, Nahar K, Hossain MS, Anee TI, Parvin K, Fujita M (2017). Nitric oxide pretreatment enhances antioxidant defense and glyoxalase systems to confer PEG-induced oxidative stress in rapeseed. Journal of Plant Interactions. 1;12(1):323-31.
Hayat S, Yadav S, Wani AS, Irfan M, Ahmad A (2011). Nitric oxide effects on photosynthetic rate, growth, and antioxidant activity in tomato. International journal of vegetable science 1;17(4):333-48.
He HY, He LF, Gu MH, Li XF (2012). Nitric oxide improves aluminum tolerance by regulating hormonal equilibrium in the root apices of rye and wheat. Plant Sci. 183, 123130
Hebelstrup KH, Shah JK, Igamberdiev AU. The role of nitric oxide and hemoglobin in plant development and morphogenesis.Physiologiaplantarum. 2013;148(4):457-69.
Hédiji H, Djebali W, Belkadhi A, Cabasson C, Moing A, Rolin D, Brouquisse R, Gallusci P, Chaïbi W (2015). Impact of long-term cadmium exposure on mineral content of Solanumlycopersicum plants: consequences on fruit production. South African Journal of Botany. 1;97:176-81.
Imran QM, Falak N, Hussain A, Mun BG, Sharma A, Lee SU, Kim KM, Yun BW. Nitric oxide responsive heavy metal-associated gene AtHMAD1 contributes to development and disease resistance in Arabidopsis thaliana. Frontiers in plant science. 2016;7:1712.
Ismail GS.Protective role of nitric oxide against arsenic-induced damages in germinating mung bean seeds.Actaphysiologiaeplantarum. 2012;34(4):1303-11.
J. T. Hancock, S. J. Neill, I. D. Wilson, Nitric oxide and ABA in control of plant function, 1217 Plant Sci. 181 (2011) 555-559.
Jeandroz S, Lamotte O, Astier J, Rasul S, Trapet P, Besson-Bard A, Bourque S, Nicolas-Francès V, Ma W, Berkowitz GA, Wendehenne D. There's more to the picture than meets the eye: nitric oxide cross talk with Ca2+ signaling. Plant Physiology. 2013;163(2):459-70.
Jin JW, Xu YF, Huang YF. Protective effect of nitric oxide against arsenic-induced oxidative damage in tall fescue leaves. African Journal of Biotechnology. 2010;9(11):1619-27.
Kausar F, Shahbaz M, Ashraf M. Protective role of foliar-applied nitric oxide in Triticumaestivum under saline stress. Turkish Journal of Botany. 2013,18;37(6):1155-65.
Kong X, Wang T, Li W, Tang W, Zhang D, Dong H. Exogenous nitric oxide delays salt-induced leaf senescence in cotton (Gossypiumhirsutum L.). Actaphysiologiaeplantarum. 2016;1;38(3):61.
Li, Z.G., Yang, S.Z., Long, W.B., Yang, G.X., Shen, Z.Z., 2013b. Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant, Cell Environ. 36, 15641572.
Lopez-Carrion AI, Castellano R, Rosales MA, Ruiz JM, Romero L. Role of nitric oxide under saline stress: implications on proline metabolism. Biologia Plantarum. 2008;1;52(3):587.
Manai J, Kalai T, Gouia H, Corpas FJ (2014). Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum Lycopersicum) plants. Journal of soil science and plant nutrition. 14(2):433-46.
Masindi, V., &Muedi, K. L. (2018).Environmental contamination by heavy metals. Heavy Metals, 19, 2019.
Mishina TE, Lamb C, Zeier J (2007). Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis. Plant, cell & environment. 30(1):39-52.
Monreal JA, Arias-Baldrich C, Pérez-Montaño F, Gandullo J, Echevarría C, García-Mauriño S (2013.) Factors involved in the rise of phosphoenolpyruvate carboxylase-kinase activity caused by salinity in sorghum leaves. Planta. 1;237(5):1401-13.
Mur LA, Prats E, Pierre S, Hall MA, Hebelstrup KH (2013).Integrating nitric oxide into salicylic acid and jasmonic acid/ethylene plant defense pathways. Frontiers in plant science. 27;4:215.
NaserAlavi SM, Arvin MJ, ManoochehriKalantari K (2014). Salicylic acid and nitric oxide alleviate osmotic stress in wheat (Triticumaestivum L.) seedlings. J. Plant Interact. 9 (1), 683688
Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004). Microarray analysis of nitric oxide responsive transcripts in Arabidopsis.Plant Biotechnology Journal. 2(4):359-66.
Parankusam S, Bhatnagar-Mathur P, Sharma KK (2017). Heat-responsive proteome changes reveal molecular mechanisms underlying heat tolerance in chickpeas. Environ. Exp. Bot. 141, 132144.
Parvaneh R, Meysam HS (2012).Effect of different levels of drought stress (PEG 6000 concentrations) on seed germination and Inorganic elements content in purslane (Portulacaoleraceae L.) leaves.Journal of Stress Physiology & Biochemistry. 2012;8(2).
Pasqualini, S., Reale, L., Calderini, O., Pagiotti, R., Ederli, L., 2012.Involvement of protein kinases and calcium in the NO-signalling cascade for defense-gene induction in ozonated tobacco plants.J. Exp. Bot. 63, 44854496.
Patakas AA, Zotos A, Beis AS. Production, localization and possible roles of nitric oxide in drought?stressed grapevines.Australian Journal of Grape and Wine Research. 2010 Feb;16(1):203-9.
Posp?´?sil, P., 2016. Production of reactive oxygen species by photosystem II as a response to light and temperature stress. Front. Plant Sci. 7, 1950
Prado AM, Colaço R, Moreno N, Silva AC, Feijó JA. The targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Molecular plant. 2008 Jul 1;1(4):703-14.
Prakash, V., Vishwakarma, K., Singh, V. P., Rai, P., Ramawat, N., Tripathi, D. K., & Sharma, S. (2020). NO and ROS implications in the organization of root system architecture. Physiologia plantarum, 168(2), 473-489.
Procházková D, Wilhelmová NA. Nitric oxide, reactive nitrogen species and associated enzymes during plant senescence.Nitric Oxide. 2011 Mar 15;24(2):61-5.
Ruan H, Shen W, Ye M, Xu L. Protective effects of nitric oxide on salt stress-induced oxidative damage to wheat (Triticumaestivum L.) leaves. Chinese Science Bulletin. 2002 Apr 1;47(8):677.
Sadeghipour O. Pretreatment with nitric oxide reduces lead toxicity in cowpea (Vignaunguiculata [L.] walp.). Archives of Biological Sciences. 2016 Jun 24;68(1):165-75.
Sami F, Faizan M, Faraz A, Siddiqui H, Yusuf M, Hayat S. Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post-translational modifications in modulating diverse plant stress. Nitric Oxide. 2018 Feb 28;73:22-38.
Samsampour D, Sadeghi F, Asadi M, Ebrahimzadeh A. Effect of nitric oxide (NO) on the induction of callus and antioxidant capacity of Hyoscyamusniger under in vitro salt stress. J Appl
Santisree P, Bhatnagar-Mathur P, Sharma KK. NO to drought-multifunctional role of nitric oxide in plant drought: do we have all the answers?.Plant Science. 2015 Oct 1;239:44-55.
Shi H, Ye T, Zhu JK, Chan Z. Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. Journal of Experimental Botany. 2014 May 27;65(15):4119-31.
Shrivastava P, Kumar R. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi journal of biological sciences. 2015 Mar 1;22(2):123-31.
Simontacchi M, Garcia-Mata C, Bartoli CG, Santa-Maria GE, Lamattina L. Nitric oxide as a key component in hormone-regulated processes. Plant cell reports. 2013 Jun 1;32(6):853-66.
Singh AP, Dixit G, Kumar A, Mishra S, Kumar N, Dixit S, Singh PK, Dwivedi S, Trivedi PK, Pandey V, Dhankher OP. A protective role for nitric oxide and salicylic acid for arsenite phytotoxicity in rice (Oryza Sativa L.).Plant physiology and biochemistry. 2017 Jun 1;115:163-73.
Sokolovski, S M. R. Blatt, Nitric oxide block of outward-rectifying K+ channels indicates direct control by protein nitrosylation in guard cells, Plant Physiol. 136 (2004) 4275-4284.
Sun B, Jing Y, Chen K, Song L, Chen F, Zhang L. Protective effect of nitric oxide on iron deficiency-induced oxidative stress in maize (Zea mays).Journal of plant physiology. 2007 May 3;164(5):536-43.
Sun, L.R., Hao, F.S., Lu, B.S., Ma, L.Y., 2010. AtNOA1 modulates nitric oxide accumulation and stomatal closure induced by salicylic acid in Arabidopsis. Plant Signal.Behav. 5 (8), 10221024
Suzuki N, Mittler R. Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiologiaplantarum. 2006 Jan;126(1):45-51.
Tan, J., Zhuo, C., Guo, Z., 2013. Nitric oxide mediates cold- and dehydration-induced expression of a novel MfHyPRP that confers tolerance to abiotic stress. Physiol. Plant 149, 310320.
Tian X, Lei Y. Nitric oxide treatment alleviates drought stress in wheat seedlings. Biologiaplantarum. 2006 Dec 1;50(4):775-8.
Uchida, A., Jagendorf, A.T., Hibino, T., Takabe, T., Takabe, T., 2002. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 163, 515-523
Wang Y, Loake GJ, Chu C (2013). Cross-talk of nitric oxide and reactive oxygen species in plant programmed cell death. Frontiers in Plant Science.4:314.
Wen D, Gong B, Sun S, Liu S, Wang X, Wei M, Yang F, Li Y, Shi Q (2016) Promoting roles of melatonin in adventitious root development of Solanumlycopersicum L. by regulating auxin and nitric oxide signaling. Frontiers in plant science. 25;7:718.
Wu XX, Zhu XH, Chen JL, Yang SJ, Ding HD, Zha DS (2013). Nitric oxide alleviates adverse salt-induced effects by improving the photosynthetic performance and increasing the anti-oxidant capacity of eggplant (Solanummelongena L.). The Journal of Horticultural Science and Biotechnology. 88(3):352-60.
Xu LL, Fan ZY, Dong YJ, Kong J, Bai XY (2015). Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of two peanut cultivars under cadmium stress. Biol. Plant. 59 (1), 171182.
Yang L, Han R, Sun Y (2013). Effects of exogenous nitric oxide on wheat exposed to enhanced ultraviolet-B radiation. American Journal of Plant Sciences. 4(06):1285.
Ye YU, Li ZH, Xing DA (2013). Nitric oxide promotes MPK6?mediated caspase?3?like activation in cadmium?induced Arabidopsis thaliana programmed cell death. Plant, cell & environment. 36(1):1-5.
Yu M, Lamattina L, Spoel SH, Loake GJ (2014). Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytologist. 202(4):1142-56.
Yu Q, Sun L, Jin H, Chen Q, Chen Z, Xu M (2012). Lead-induced nitric oxide generation plays a critical role in lead uptake by Pogonatherumcrinitum root cells. Plant and Cell Physiology. 53(10):1728-36.
Zafra A., Rodríguez-García MI, de Dios Alché J (2010). Cellular localization of ROS and NO in olive reproductive tissues during flower development.BMC Plant Biology. 10(1):36.
Zandalinas SI, Balfago´n D, Arbona V, Go´mez-Cadenas A, Inupakutika MA, Mittler R (2016). ABA is required for the accumulation of APX1 and MBF1c during a combination of water deficit and heat stress. J. Exp. Bot. 67 (18), 5381-5390.
Zhang A, Zhang J, Zhang J, Ye N, Zhang H, Tan M, Jiang M (2010). Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant and Cell Physiology. 6;52(1):181-92.
Zhang, H., Zhu, J., Gong, Z., & Zhu, J. K. (2022). Abiotic stress responses in plants. Nature Reviews Genetics, 23(2), 104-119.
Zhao Z, Chen G, Zhang C (2001). Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings. Functional Plant Biology. 28(10):1055-61.
Ziogas V, Tanou G, Filippou P, Diamantidis G, Vasilakakis M, Fotopoulos V, (2013). Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant. Physiol. Biochem. 68, 118-26
Department of Biotechnology, Ashoka Institute of Technology and Management, Varanasi (Affiliated to Dr. APJ. Abdul Kalam Technical University, Lucknow), UP, India- 221007
Department of Bioengineering, Integral University, Lucknow, UP, India-2