How nitric oxide donors can protect plants in a changing environment: what we know so far and perspectives

Amedea B. Seabra; Halley C. Oliveira; Amedea B. Seabra; Halley C. Oliveira

doi:10.3934/molsci.2016.4.692

AIMS Molecular Science

2016, Volume 3, Issue 4: 692-718. doi: 10.3934/molsci.2016.4.692

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How nitric oxide donors can protect plants in a changing environment: what we know so far and perspectives

Amedea B. Seabra ^{1
,
,},
Halley C. Oliveira ²

1.
Center of Natural and Human Sciences, Universidade Federal do ABC (UFABC), Santo André, SP, Brazil
2.
Department of Animal and Plant Biology, Universidade Estadual de Londrina (UEL), Londrina, PR, Brazil

Received: 09 October 2016 Accepted: 12 December 2016 Published: 13 December 2016

The free radical nitric oxide (NO) plays important roles in plant growth and defense. Owing to its small size and lipophilicity, NO acts as a crucial signaling molecule in plants, crossing cell membranes and enhancing cell communication. Indeed, NO donors have been shown to modulate a variety of physiological processes, such as plant greening, seed germination, iron homeostasis and mitochondrial respiration. Recently, several papers have reported the protective actions upon application of low molecular weight NO donors in plants under abiotic stress. Exogenous NO is able to improve plant tolerance to several abiotic stresses, such as drought, salinity, metal toxicity, and extreme temperatures. This protection is assigned to the NO-mediated redox signaling in plants, which involves interplay with reactive oxygen species and modulation of gene expression and protein function. This review reports and discusses the recent advantages, pitfalls, challenges, and perspectives in the applications of low molecular weight NO donors in plants under abiotic stress. The combination of nanotechnology and NO donors as an efficient approach to protect plants under challenging environments is also discussed.
- nitric oxide,
- plant defense,
- abiotic stress,
- nitric oxide donors,
- redox signaling
Citation: Amedea B. Seabra, Halley C. Oliveira. How nitric oxide donors can protect plants in a changing environment: what we know so far and perspectives[J]. AIMS Molecular Science, 2016, 3(4): 692-718. doi: 10.3934/molsci.2016.4.692

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Abstract

The free radical nitric oxide (NO) plays important roles in plant growth and defense. Owing to its small size and lipophilicity, NO acts as a crucial signaling molecule in plants, crossing cell membranes and enhancing cell communication. Indeed, NO donors have been shown to modulate a variety of physiological processes, such as plant greening, seed germination, iron homeostasis and mitochondrial respiration. Recently, several papers have reported the protective actions upon application of low molecular weight NO donors in plants under abiotic stress. Exogenous NO is able to improve plant tolerance to several abiotic stresses, such as drought, salinity, metal toxicity, and extreme temperatures. This protection is assigned to the NO-mediated redox signaling in plants, which involves interplay with reactive oxygen species and modulation of gene expression and protein function. This review reports and discusses the recent advantages, pitfalls, challenges, and perspectives in the applications of low molecular weight NO donors in plants under abiotic stress. The combination of nanotechnology and NO donors as an efficient approach to protect plants under challenging environments is also discussed.

References

[1]	Santisree P, Bhatnagar-Mathur P, Sharma KK (2015) NO to drought-multifunctional role of nitric oxide in plant drought: Do we have all the answers? Plant Sci 239: 44-55. doi: 10.1016/j.plantsci.2015.07.012
[2]	Simontacchi M, Galatro A, Ramos-Artuso F, et al. (2015) Plant survival in a changing environment: The role of nitric oxide in plant responses to abiotic stress. Front Plant Sci 6: 977.
[3]	Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4: 398.
[4]	Boyarshinov AV, Asafova EV (2011) Stress responses of wheat leaves to dehydration: participation of endogenous NO and effect of sodium nitroprusside. Russ J Plant Physl 58: 1034-1039. doi: 10.1134/S1021443711060033
[5]	Hatamzadeh A, Nalousi AM, Ghasemnezhad A, et al. (2014) The potential of nitric oxide for reducing oxidative damage induced by drought stress in two turfgrass species, creeping bentgrass and tall fescue. Grass Forage Sci 70: 538-548.
[6]	Farooq M, Basra SMA, Wahid A, et al. (2009) Exogenously applied nitric oxide Enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.) J Agron Crop Sci 195: 254-261.
[7]	Boogar AR, Salehi H, Jowkar A (2014) Exogenous nitric oxide alleviates oxidative damage in turfgrasses under drought stress. ‎South Afr J Bot 92: 78-82. doi: 10.1016/j.sajb.2014.02.005
[8]	Cechin I, Cardoso GS, Fumis TF, et al. (2015) Nitric oxide reduces oxidative damage induced by water stress in sunflower plants. Bragantia 74: 200-206. doi: 10.1590/1678-4499.353
[9]	Fan Q-J, Liu J-H (2012) Nitric oxide is involved in dehydration/drought tolerance in Poncirus trifoliata seedlings through regulation of antioxidant systems and stomatal response. Plant Cell Rep 31: 145-154. doi: 10.1007/s00299-011-1148-1
[10]	Cai W, Liu W, Wang W-S, et al. (2015) Overexpression of rat neurons nitric oxide synthase in rice enhances drought and salt tolerance. PLoS One 10: e0131599. doi: 10.1371/journal.pone.0131599
[11]	Fan H, Li T, Guan L, et al. (2012) Effects of exogenous nitric oxide on antioxidation and DNA methylation of Dendrobium huoshanense grown under drought stress. Plant Cell Tiss Organ Cult 109: 307-314. doi: 10.1007/s11240-011-0096-3
[12]	Sandalio LM, Romero-Puertas MC (2015) Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. Ann Bot 116: 475-485. doi: 10.1093/aob/mcv074
[13]	Wang X, Li S, Liu Y, Ma C (2015) Redox regulated peroxisome homeostasis. Redox Biol 4: 104-108.
[14]	Wang P, Du Y, Hou YJ, et al. (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci U S A 112: 613-618. doi: 10.1073/pnas.1423481112
[15]	Chen J, Xiao Q, Wang C, et al. (2014) Nitric oxide alleviates oxidative stress caused by salt in leaves of amangrove species, Aegiceras corniculatum. Aquat Bot 117: 41-47. doi: 10.1016/j.aquabot.2014.04.004
[16]	Grun S, Lindermayr C, Sell S, et al. (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57: 507-516 doi: 10.1093/jxb/erj053
[17]	Palmieri MC, Sell S, Huang X, et al. (2008) Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59: 177-186 doi: 10.1093/jxb/erm345
[18]	Besson-Bard A, Astier J, Rasul S, et al. (2009) Current view of nitric oxide-responsive genes in plants. Plant Sci 177: 302-309.
[19]	Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubis J (2009) Involvement of nitric oxide in water stress-induced responses of cucumber roots. Plant Sci 177: 682-690. doi: 10.1016/j.plantsci.2009.09.007
[20]	Silveira NM, Frungillo L, Marcos FCC, et al. (2016) Exogenous nitric oxide improves sugarcane growth and photosynthesis under water deficit. Planta 244: 181-190. doi: 10.1007/s00425-016-2501-y
[21]	Seabra AB, Rai M, Durán N (2014) Nano carriers for nitric oxide delivery and its potential applications in plant physiological process: A mini review. J Plant Biochem Biotechnol 23: 1-10. doi: 10.1007/s13562-013-0204-z
[22]	Seabra AB, Justo GZ, Haddad PS (2015) State of the art, challenges and perspectives in the design of nitric oxide-releasing polymeric nanomaterials for biomedical applications. Biotechnol Adv 33: 1370-1379. doi: 10.1016/j.biotechadv.2015.01.005
[23]	Seabra AB, Durán N (2010) Nitric oxide-releasing vehicles for biomedical applications. J Mater Chem 20: 1624-1637. doi: 10.1039/B912493B
[24]	Ullah S, Kolo Z, Egbichi I, et al. (2016) Nitric oxide influences glycine betaine content and ascorbate peroxidase activity in maize. ‎South Afr J Bot 105: 218-225. doi: 10.1016/j.sajb.2016.04.003
[25]	Zhang L, Li X, Li X, et al. (2016) Exogenous nitric oxide protects against drought-induced oxidative stress in Malus rootstocks. Turk J Bot 40: 17-27. doi: 10.3906/bot-1407-31
[26]	Ziogas V, Tanou G, Belghazi M, et al. (2015) Roles of sodium hydrosulfide and sodium nitroprusside as priming molecules during drought acclimation in citrus plants. Plant Mol Biol 89: 433-450. doi: 10.1007/s11103-015-0379-x
[27]	Bai X, Yang L, Tian M, et al. (2011) Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS One 6: e20714
[28]	Egbichi I, Keyster M, Ludidi N (2014) Effect of exogenous application of nitric oxide on salt stress responses of soybean. South Afr J Bot 90: 131-136. doi: 10.1016/j.sajb.2013.11.002
[29]	Qiao W, Li C, Fan L-M (2014) Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses. Environ Exp Bot 100: 84-93. doi: 10.1016/j.envexpbot.2013.12.014
[30]	Li X, Pan Y, Chang B (2016) NO promotes seed germination and seedling growth under high salt may depend on EIN3 protein in Arabidopsis. Front Plant Sci 6: 1203.
[31]	Molassiotis A, Job D, Ziogas V, et al. (2016) Citrus plants: A model system for unlocking the secrets of NO and ROS-inspired priming against salinity and drought. Front Plant Sci 7: 229.
[32]	Ahmad P, Latef AAA, Hashem A, et al. (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7: 347.
[33]	Du S-T, Liu Y, Zhang P, et al. (2015) Atmospheric application of trace amounts of nitric oxide enhances tolerance to salt stress and improves nutritional quality in spinach (Spinacia oleracea L.). Food Chem 173: 905-911. doi: 10.1016/j.foodchem.2014.10.115
[34]	Fan H-F, Du C-X, Guo S-R (2013) Nitric oxide enhances salt tolerance in cucumber seedlings by regulating free polyamine content. Environ Exper Bot 86: 52- 59. doi: 10.1016/j.envexpbot.2010.09.007
[35]	Fatma M, Masood A, Per TS, et al. (2016) Interplay between nitric oxide and sulfur assimilation in salt tolerance in plants. Crop J 4: 153-161. doi: 10.1016/j.cj.2016.01.009
[36]	Krasylenko YA, Yemets AI, Blume YB (2010) Functional role of nitric oxide in plants. Russ J Plant Physl 57: 451-461. doi: 10.1134/S1021443710040011
[37]	Moller IM, Sweetlove LJ (2010) ROS signaling-specificity is required. Trends Plant Sci 7: 370-374.
[38]	Kaya C, Ashraf M, Sonmez O, et al. (2015) Exogenously applied nitric oxide confers tolerance to salinity-induced oxidative stress in two maize (Zea mays L.) cultivars differing in salinity tolerance. Turk J Agric For 39: 909-919.
[39]	Zhao L, Zhang F, Guo J, et al. (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134: 849-857. doi: 10.1104/pp.103.030023
[40]	Poor, P. Laskay G, Tari I (2015) Role of nitric oxide in salt stress-induced programmed cell death and defence mechanisms. In: Khan MN, Mobin M, Mohammad F, Corpas FJ (eds) Nitric oxide action in abiotic stress responses in plants. Charm: Springer International Publishing Switzerlans, 2015. pp. 193-219.
[41]	Chen J, Xiong D-Y, Wang W-H, et al. (2013) Nitric oxide mediates root K⁺/Na⁺ balance in a mangrove plant, Kandelia obovata, by enhancing the expression of AKT1-Type K⁺ channel and Na⁺/H⁺ antiporter under high salinity. PLoS One 8: e71543. doi: 10.1371/journal.pone.0071543
[42]	Jamali B, Eshghi S, Tafazoli E (2015) Mineral composition of ‘selva’ strawberry as affected by time of application of nitric oxide under saline conditions. Hort Environ Biotechnol 56: 273-279. doi: 10.1007/s13580-015-0116-z
[43]	Liu S, Dong Y, Xu L, et al. (2014) Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings. Plant Growth Regul 73: 67-78. doi: 10.1007/s10725-013-9868-6
[44]	Fan H-F, Du C-X, Ding L, et al. (2013) Effects of nitric oxide on the germination of cucumber seeds and antioxidant enzymes under salinity stress. Acta Physiol Plant 35: 2707-2719. doi: 10.1007/s11738-013-1303-0
[45]	Mostofa MG, Fujita M, Tran L-S P (2015) Nitric oxide mediates hydrogen peroxide- and salicylic acid induced salt tolerance in rice (Oryza sativa L.) seedlings. Plant Growth Regul 77: 265-277. doi: 10.1007/s10725-015-0061-y
[46]	Kaur C, Ghosh A, Pareek A, et al. (2014) Glyoxalases and stress tolerance in plants. Biochem Soc Trans 42: 485-490. doi: 10.1042/BST20130242
[47]	Hossain MA, Hossain MZ, Fujita M (2009) Stress induced changes of methylglyoxal level and Glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust J Crop Sci 3: 53-64.
[48]	Gomes K, Poor P, Horvath E, et al. (2011) Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiol Plant 142: 179-192.
[49]	Dinler BS, Antoniou C, Fotopoulos V (2014) Interplay between GST and nitric oxide in the early response of soybean (Glycine max L.) plants to salinity stress. J Plant Physiol 171: 1740-1747.
[50]	Oliveira HC, Gomes BC, Pelegrino MT, et al. (2016) Nitric oxide-releasing chitosan nanoparticles alleviate the effects of salt stress in maize plants. Nitric Oxide 61: 10-19. doi: 10.1016/j.niox.2016.09.010
[51]	Emamverdian A, Ding Y, Mokhberdoran F, et al. (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015: 756120.
[52]	Singh S, Parihar P, Singh R, et al. (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6: 1143.
[53]	Sade H, Meriga B, Surapu V, et al. (2016) Toxicity and tolerance of aluminum in plants: tailoring plants to suit to acid soils. Biometals 29: 187-210.
[54]	Yadav SK (2010) Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South Afr J Bot 76: 167-179. doi: 10.1016/j.sajb.2009.10.007
[55]	Anjum NA, Hasanuzzaman M, Hossain MA, et al. (2015) Jacks of metal/metalloid chelation trade in plants—an overview. Front Plant Sci 6: 192.
[56]	Anjum NA, Gill SS, Gill R, et al. (2014) Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple, and associated enzymes. Protoplasma 251: 1265-1283. doi: 10.1007/s00709-014-0636-x
[57]	Paradiso A, Berardino R, de Pinto MC, et al. (2008) Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49: 362-374. doi: 10.1093/pcp/pcn013
[58]	Inostroza-Blancheteau C, Rengel Z, Alberdi M, et al. (2012) Molecular and physiological strategies to increase aluminum resistance in plants. Mol Biol Rep 39: 2069-2079. doi: 10.1007/s11033-011-0954-4
[59]	Ovecka M, Takac T (2014) Managing heavy metal toxicity stress in plants: Biological and biotechnological tools. Biotechnol Adv 32: 73-86. doi: 10.1016/j.biotechadv.2013.11.011
[60]	He H, He L, Gu M (2014) The diversity of nitric oxide function in plant responses to metal stress. Biometals 27: 219.228. doi: 10.1007/s10534-014-9711-1
[61]	He J, Y Ren Y, Xiulan C, et al. (2014) Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicol Environ Saf 108: 114-119.
[62]	Besson-Bard A, Gravot A, Richaud P, et al. (2009) 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 149: 1302-1315. doi: 10.1104/pp.108.133348
[63]	Valentovicova K, Haluskova, Huttova J, et al. (2010) Effect of cadmium on diaphorase activity and nitric oxide production in barley root tips. J Plant Physiol 167: 10-14. doi: 10.1016/j.jplph.2009.06.018
[64]	Xiong J, Lu H, Lu KX, et al. (2009) Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta 230: 599-610.
[65]	Xu J, Wang W, Yin H, et al. (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326: 321-330. doi: 10.1007/s11104-009-0011-4
[66]	Rodriguez-Serrano M, Romero-Puertas MC, Zabalza A, et al. (2006) Cadmium effect on oxidative metabolismo of peã (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29: 1532-1544.
[67]	Rodriguez-Serrano M, Romero-Puertas MC, Pazmino DM, et al. (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150: 229-243. doi: 10.1104/pp.108.131524
[68]	Duan X, Li X, Ding F (2015) Interaction of nitric oxide and reactive oxygen species and associated regulation of root growth in wheat seedlings under zinc stress. Ecotoxicol Environ Saf 113: 95-102. doi: 10.1016/j.ecoenv.2014.11.030
[69]	Chmielowska-Bak J, Deckert J (2013) Nitric oxide mediates Cd dependent induction of signaling-associated genes. Plant Signal Behav 8: 12.
[70]	Peto A, Lehotai N, Lozano-Juste J, et al. (2011) Involvement of nitric oxide and auxin in signal transduction of copper-induced morphological responses in Arabidopsis seedlings. Ann Bot 108: 449-457. doi: 10.1093/aob/mcr176
[71]	Hu Y, You J, Liang X (2015) Nitrate reductase-mediated nitric oxide production is involved in copper tolerance in shoots of hulless barley. Plant Cell Rep 34: 367-379. doi: 10.1007/s00299-014-1715-3
[72]	Sun C, Lu L, Liu L, et al. (2014) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage by aluminum though enhacement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol 201: 1240-1250. doi: 10.1111/nph.12597
[73]	Peto A, Lehotai N, Feigl G, et al. (2013) Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis. Plant Cell Rep 32: 1913-1923.
[74]	Singh AP, Dixit G, Kumar A, et al. (2016) Nitric oxide alleviated arsenic toxicity by modulation of antioxidants and thiol metabolism in rice (Oryza sativa L.). Front Plant Sci 6: 1272.
[75]	Singh VP, Srivastava PK, Prasad SM (2013) Nitric oxide alleviates arsenic-induced toxic effects in ridged Luffa seedlings. Plant Physiol Biochem 71: 155-163. doi: 10.1016/j.plaphy.2013.07.003
[76]	Chen F, Wang F, Sun H, et al. (2013) Genotype-dependent effect of exogenous nitric oxide on cd-induced changes in antioxidative metabolism, ultrastructure, and photosynthetic performance in barley seedlings (Hordeum vulgare). J Plant Growth Regul 29: 394-408.
[77]	Liu S, Yang R, Pan Y, et al. (2015) Nitric oxide contributes to minerals absorption, proton pumps and hormone equilibrium under cadmium excess in Trifolium repens L. plants. Ecotoxicol Environ Saf 119: 35-46. doi: 10.1016/j.ecoenv.2015.04.053
[78]	Wang D, Liu Y, Tan X, et al. (2015) Effect of exogenous nitric oxide on antioxidative system and S-nitrosylation in leaves of Boehmeria nivea (L.) Gaud under cadmium stress. Environ Sci Pollut Res 22: 3489-3497.
[79]	Yang L, Ji J, Harris-Shultz KR, et al. (2016) The dynamic changes of the plasma membrane proteins and the protective roles of nitric oxide in rice subjected to heavy metal cadmium stress. Front Plant Sci 7: 190.
[80]	Abdel-Kader DZE (2007) Role of nitric oxide, glutathione and sulfhydryl groups in zinc homeostasis in plants. Am J Plant Physiol 2: 59-75. doi: 10.3923/ajpp.2007.59.75
[81]	Chen J, Liu X, Wang C, et al. (2015) Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings. J Haz Mat 297: 173-182. doi: 10.1016/j.jhazmat.2015.04.077
[82]	Liu S, Yang E, Pan Y, et al. (2016) Beneficial behavior of nitric oxide in copper-treated medicinal plants. J Haz Mat 314: 140-154. doi: 10.1016/j.jhazmat.2016.04.042
[83]	Kaur G, Singh HP, Batish DR, et al. (2015) Exogenous nitric oxide (NO) interferes with lead (Pb)-induced toxicity by detoxifying reactive oxygen species in hydroponically grown wheat (Triticum aestivum) roots. PLoS One 10: e0138713.
[84]	Kovacik J, Babula P, Hedbavny J, et al. (2014) Manganese-induced oxidative stress in two ontogenetic stages ofchamomile and amelioration by nitric oxide. Plant Sci 215-216: 1-10. doi: 10.1016/j.plantsci.2013.10.015
[85]	Kazemi N, Khavari-Nejad RA, Fahimi H, et al. (2010) Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Sci Hortic 126: 402-407.
[86]	Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4: 273.
[87]	Rapacz M, Ergon A, Hoglind M, et al. (2014) Overwintering of herbaceous plants in a changing climate. Still more questions than answers. Plant Sci 225: 34-44.
[88]	Theocharis A, Clement C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235: 1091-1105. doi: 10.1007/s00425-012-1641-y
[89]	Hasanuzzaman M, Nahar K, Alam MM, et al. (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14: 9643-9684. doi: 10.3390/ijms14059643
[90]	Strimbeck GR, Schaberg PG, Fossdal CG, et al. (2015) Extreme low temperature tolerance in woody plants. Front Plant Sci 6: 884.
[91]	Mathur S, Agrawal D, Jajoo A (2014) Photosynthesis: response to high temperature stress. J Photochem Photobiol B 137: 116-126. doi: 10.1016/j.jphotobiol.2014.01.010
[92]	Teskey R, Wertin T, Bauweraerts I, et al. (2015) Responses of tree species to heat waves and extreme heat events. Plant Cell Environ 38: 1699-1712. doi: 10.1111/pce.12417
[93]	Janmohammadi M, Zolla L, Rinalducci S (2015) Low temperature tolerance in plants: Changes at the protein level. Phytochemistry 117: 76-89. doi: 10.1016/j.phytochem.2015.06.003
[94]	Puyaubert J, Baudoin E (2014) New clues for a cold case: nitric oxide response to low temperature. Plant Cell Environ 37: 2623-2630. doi: 10.1111/pce.12329
[95]	Zhao MG, Chen L, Zhang LL, et al. (2009). Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151: 755-767.
[96]	Cantrel C, Vazquez T, Puyaubert J, et al. (2011) Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytol 189: 415-427. doi: 10.1111/j.1469-8137.2010.03500.x
[97]	Liu Y, Jiang H, Zhao Z, et al. (2010) Nitric oxide synthase like activity dependent nitric oxide production protects against chilling-induced oxidative damage in Chorispora bungeana suspension cultured cells. Plant Physiol Biochem 48: 936-944.
[98]	Xu M, Dong J, Zhang M, et al. (2012) Cold-induced endogenous nitric oxide generation plays a role in chilling tolerance of loquat fruit during postharvest storage. Postharvest Biol Technol 65: 5-12. doi: 10.1016/j.postharvbio.2011.10.008
[99]	Sehrawat A, Gupta R, Deswal R (2013) Nitric oxide-cold stress signalling cross-talk, evolution of a novel regulatory mechanism. Proteomics 13: 1816-1835
[100]	Song L, Ding W, Shen J, et al. (2008) Nitric oxide mediates abscisic acid induced thermotolerance in the calluses from two ecotypes of reed under heat stress. Plant Sci 175: 826-832. doi: 10.1016/j.plantsci.2008.08.005
[101]	Xuan Y, Zhou S, Wang L, et al. (2010) Nitric oxide functions as a signal and acts upstream of AtCaM3 in the thermotolerance in Arabidopsis seedlings. Plant Physiol 153: 1895-1906. doi: 10.1104/pp.110.160424
[102]	Bavita A, Shashi B, Navtej SB (2012) Nitric oxide alleviates oxidative damage induced by high temperature stress in wheat. Indian J Exp Biol 50: 372-378.
[103]	Lee U, Wie C, Fernandez BO, et al. (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20: 786-802. doi: 10.1105/tpc.107.052647
[104]	Chaki M, Valderrama R, Fernández-Ocaña AM, et al. (2009) Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J Exp Bot 60: 4221-4234. doi: 10.1093/jxb/erp263
[105]	Fan J, Chen K, Amombo E, et al. (2015) Physiological and molecular mechanism of nitric oxide (NO) involved in bermudagrass response to cold stress. PLoS One 10: e0132991. doi: 10.1371/journal.pone.0132991
[106]	Esim N, Atici O, Mutlu S (2014) Effects of exogenous nitric oxide in wheat seedlings under chilling stress. Toxicol Ind Health 30: 268-274. doi: 10.1177/0748233712457444
[107]	Esim N, Atici O (2014) Nitric oxide improves chilling tolerance of maize by affecting apoplastic antioxidative enzymes in leaves. Plant Growth Regul 72: 29-38. doi: 10.1007/s10725-013-9833-4
[108]	Li X, Jiang H, Liu F (2013) Induction of chilling tolerance in wheat during germination by pre-soaking seed with nitric oxide and gibberellin. Plant Growth Regul 71: 31-40. doi: 10.1007/s10725-013-9805-8
[109]	Pakkish Z, Tabatabaienia MS (2016) The use and mechanism of NO to prevent frost damage to flower of apricot. Sci Hort 198: 318-325. doi: 10.1016/j.scienta.2015.12.004
[110]	Zhu LQ, Zhou J, Zhu SH (2010) Effect of a combination of nitric oxide treatment and intermittent warming on prevention of chilling injury of ‘Feicheng’ peach fruit during storage. Food Chem 121: 165-170. doi: 10.1016/j.foodchem.2009.12.025
[111]	Yang H, Wu F, Cheng J (2011) Reduced chilling injury in cucumber by nitric oxide and the antioxidant response. Food Chem 127: 1237-1242.
[112]	Zaharah SS, Singh Z (2011) Postharvest nitric oxide fumigation alleviates chilling injury, delays fruit ripening and maintains quality in cold-stored ‘KensingtonPride’ mango. Postharvest Biol Technol 60: 202-210. doi: 10.1016/j.postharvbio.2011.01.011
[113]	Wu B, Guo Q, Li Q, et al. (2014) Impact of postharvest nitric oxide treatment on antioxidant enzymes and related genes in banana fruit in response to chilling tolerance. Postharvest Biol Technol 92: 157-163. doi: 10.1016/j.postharvbio.2014.01.017
[114]	Li Z, Yang S, Long W, et al. (2013) 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: 1564-1572. doi: 10.1111/pce.12092
[115]	Yang W, Sun Y, Chen S, et al. (2011) The effect of exogenously applied nitric oxide on photosynthesis and antioxidant activity in heat stressed chrysanthemum. Biol Plant 55: 737-740. doi: 10.1007/s10535-011-0178-4
[116]	Chen K, Chen L, Fan J, et al. (2013) Alleviation of heat damage to photosystem II by nitric oxide in tall fescue. Photosynth Res 116: 21-31. doi: 10.1007/s11120-013-9883-5
[117]	Tan J, Wang C, Xiang B, et al. (2013) Hydrogen peroxide and nitric oxide mediated cold- and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant Cell Environ 36: 288-299. doi: 10.1111/j.1365-3040.2012.02573.x
[118]	Li C, Li T, Zhang D, et al. (2013) Exogenous nitric oxide effect on fructan accumulation and FBEs expression in chilling-sensitive and chilling-resistant wheat. Environ Exp Bot 86: 2-8. doi: 10.1016/j.envexpbot.2011.12.032
[119]	Uchida A, Jagendorf AT, Hibino T, et al. (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163: 515-523. doi: 10.1016/S0168-9452(02)00159-0
[120]	Camejo D, Romero-Puertas MC, Rodríguez-Serrano M, et al. (2013) Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J Proteomics 79: 87-99.
[121]	Yun BW, Feechan A, Yin M, et al. (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478: 264-268.
[122]	Ortega-Galisteo AP, Rodriguez-Serrano M, Pazmino DM, et al. (2012) S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63: 2089-2103.
[123]	Correa-Aragunde N, Foresi N, Lamattina L (2013) Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulations of ascorbate peroxidase as a case study. J Exp Bot 66: 2913-2921.
[124]	Begara-Morales JC, Sanchez-Calvo B, Chaki M, et al. (2013) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65: 527-538.
[125]	de Pinto MC, Locato V, Sgobba A, et al. (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol 163: 1766-1775. doi: 10.1104/pp.113.222703
[126]	Yu M, Lamattina L, Spoel SH, et al. (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202: 1142-1156. doi: 10.1111/nph.12739
[127]	Enkhardt U, Pommer U (2000) Influence of nitric oxide and nitrite on the activity of cinnamic acid 4-hydroxylase of Zea mays in vitro. J Appl Bot 74: 151-154.
[128]	Navarre DA, Wendehenne D, Durner J, et al. (2000) Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol 122: 573-582. doi: 10.1104/pp.122.2.573
[129]	Oliveira HC, Salgado I (2014). Role of plant mitochondria in nitric oxide homeostasis during oxygen deficiency. In: Khan MN, Mobin M,Mohammad F,Corpas FJ, editors. Nitric oxide in plants: metabolism and role in stress physiology. Switzerland: Springer International Publishing. p. 57-74.
[130]	Corpas FJ, Chaki M, Leterrier M, et al. (2009) Protein tyrosine nitration: a new challenge in plants. Plant Signal Behav 4: 920-923. doi: 10.4161/psb.4.10.9466
[131]	Corpas FJ, del Río LA, Barroso JB (2013) Protein tyrosine nitration in higher plants under natural and stress conditions. Front Plant Sci 4: 29.
[132]	Del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66: 2827-2837. doi: 10.1093/jxb/erv099
[133]	Pedroso MC, Magalhaes JR, Durzan D (2000) Nitric oxide induces cell death in Taxus cells. Plant Sci 157: 173-180. doi: 10.1016/S0168-9452(00)00278-8
[134]	Savvides A, Ali S, Tester M, et al. (2016) Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci 21: 4. doi: 10.1016/j.tplants.2015.11.014
[135]	Wodala B, Ördög A, Horváth F (2010) The cost and risk of using sodium nitroprusside as a NO donor in chlorophyll fluorescence experiments. J Plant Physiol 167: 1109-1111. doi: 10.1016/j.jplph.2010.03.013

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