The effects of foliar application of melatonin on some physiological and biochemical characteristics and expression of fatty acid desaturase gene in pistachio seedlings (Pistacia vera L.) under freezing stress

References

• Afshari H, Hokmabadi H, Ebadi A, Laee G. 2010. Measurement of chemical and non-chemical parameters of three native pistachio cultivars of Damghan region (Iran) for studying spring frost. Asian J Chem. 22:2356–2366.
   Google Scholar
• Aghdam MS, Fard JR. 2017. Melatonin treatment attenuates postharvest decay and maintains nutritional quality of strawberry fruits (Fragaria× anannasa cv. Selva) by enhancing GABA shunt activity. Food Chem. 221:1650–1657.
   PubMed Web of Science ®Google Scholar
• Akçay N, Bor M, Karabudak T, Özdemir F, Türkan I. 2012. Contribution of Gamma amino butyric acid (GABA) to salt stress responses of Nicotiana sylvestris CMSII mutant and wild type plants. J Plant Physiol. 169:452–458.
   PubMed Web of Science ®Google Scholar
• Akula R, Ravishankar GA. 2011. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav. 6:1720–1731.
   PubMedGoogle Scholar
• Alexieva V, Sergiev I, Mapelli S, Karanov E. 2001. The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ. 24:1337–1344.
   Web of Science ®Google Scholar
• Ariizumi T, Kishitani S, Inatsugi R, Nishida I, Murata N, Toriyama K. 2002. An increase in unsaturation of fatty acids in phosphatidylglycerol from leaves improves the rates of photosynthesis and growth at low temperatures in transgenic rice seedlings. Plant Cell Physiol. 43:751–758.
   PubMed Web of Science ®Google Scholar
• Arnao MB, Hernández-Ruiz J. 2014. Melatonin: plant growth regulator and/or biostimulator during stress? Trends Plant Sci. 19:789–797.
   PubMed Web of Science ®Google Scholar
• Arnao MB, Hernández-Ruiz J. 2015. Chapter 11 – Phytomelatonin: searching for plants with high levels for use as a natural nutraceutical. In: Atta-ur-Rahman FRS, editor. Studies in natural products chemistry. Netherlands: Elsevier Science Publishers; p. 519–545.
   Google Scholar
• Bałabusta M, Szafrańska K, Posmyk MM. 2016. Exogenous melatonin improves antioxidant defense in cucumber seeds (Cucumis sativus L.) germinated under chilling stress. Front Plant Sci. 7:1–12.
   PubMed Web of Science ®Google Scholar
• Bano-Otalora B, Madrid JA, Rol MA. 2020. Melatonin alleviates circadian system disruption induced by chronic shifts of the light-dark cycle in Octodon degus. J Pineal Res. 68:1–13.
   Web of Science ®Google Scholar
• Bates LS. 1973. Rapid determination of free proline for water stress studies. Plant Soil. 39:205–207.
   Web of Science ®Google Scholar
• Bizzarri M, Proietti S, Cucina A, Reiter RJ. 2013. Molecular mechanisms of the pro-apoptotic actions of melatonin in cancer: a review. Expert Opin Ther Tar. 17:1483–1496.
   PubMed Web of Science ®Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem. 72:248–254.
   PubMed Web of Science ®Google Scholar
• Cen H, Wang T, Liu H, Tian D, Zhang Y. 2020. Melatonin application improves salt tolerance of alfalfa (Medicago sativa L.) by enhancing antioxidant capacity. Plants. 9:1–17.
   Google Scholar
• Ceraulo L, Ferrugia M, Tesoriere L, Segreto S, Livrea MA, Liveri VT. 1999. Interactions of melatonin with membrane models: portioning of melatonin in AOT and lecithin reversed micelles. J Pineal Res. 26:108–112.
   PubMed Web of Science ®Google Scholar
• Chen J, Xu C, Liang L. 1999. Effect of low temperature on protein and proline in banana (Musa spp.) leaves. J South China Agric Univ. 20:54–58.
   Google Scholar
• Chinnusamy V, Zhu JK, Sunkar R. 2010. Gene regulation during cold stress acclimation in plants. In: Sunkar R, editor. Plant stress tolerance: methods and protocols. Totowa: Humana Press; p. 39–55.
   Google Scholar
• D´cunha GB, Satyanarayan V, Nair PM. 1996. Purification of phenylalanine ammonialyase from Rhodotorula glutinis. Phytochem. 42:17–20.
   Web of Science ®Google Scholar
• Dhindsa RS, Dhindsa P, Thorpe AT. 1981. Leaf senescence correlated with increased levels of membrane permeability and lipid peroxidation and decrease levels of superoxide dismutase and catalase. J Exp Bot. 32:93–101.
   Web of Science ®Google Scholar
• Ellman GL. 1959. Tissue sulfhydryl groups. Arch Biochem Bioph. 82:70–77.
   PubMed Web of Science ®Google Scholar
• Erdal S. 2012. Androsterone-induced molecular and physiological changes in maize seedlings in response to chilling stress. Plant Physiol Biochem. 57:1–7.
   PubMed Web of Science ®Google Scholar
• Fan J, Hu Z, Xie Y, Chan Z, Chen K, Amombo E, Chen L, Fu J. 2015. Alleviation of cold damage to photosystem II and metabolisms by melatonin in Bermudagrass. Front Plant Sci. 6:1–14.
   PubMed Web of Science ®Google Scholar
• Foyer CH, Lopez-Delgado H, Dat JF, Scott IM. 1997. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant. 100:241–254.
   Web of Science ®Google Scholar
• Franco R, Cidlowski J. 2009. Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ. 16:1303–1314.
   PubMed Web of Science ®Google Scholar
• García JJ, López-Pingarrón L, Almeida-Souza P, Tres A, Escudero P, García-Gil FA, Tan DX, Reiter RJ, Ramírez JM, Bernal-Pérez M. 2014. Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: a review. J Pineal Res. 56:225–237.
   PubMed Web of Science ®Google Scholar
• Griffith M, Antikainen M. 1996. Extracellular ice formation in freezing-tolerant plants. Adv Low Temp Biol. 3:107–139.
   Google Scholar
• Heath RL, Packer L. 1968. Photoperoxidation in isolated chloroplast, kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 125:189–198.
   PubMed Web of Science ®Google Scholar
• Hossain Z, Nouri MZ, Komatsu S. 2012. Plant cell organelle proteomics in response to abiotic stress. J Proteome Res. 11:37–48.
   PubMed Web of Science ®Google Scholar
• Janas KM, Posmyk MM. 2013. Melatonin, an underestimated natural substance with great potential for agricultural application. Acta Physiol Plant. 35:3285–3292.
   Web of Science ®Google Scholar
• Jannatizadeh A, Aghdam MS, Luo Z, Razavi F. 2019. Impact of exogenous melatonin application on chilling injury in tomato fruits during cold storage. Food Bioproc Tech. 12:741–750.
   Web of Science ®Google Scholar
• Kampfenkel K, Vanmontagu M, Inze D. 1995. Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem. 225:165–167.
   PubMed Web of Science ®Google Scholar
• Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL. 2007. Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J. 50:967–981.
   PubMed Web of Science ®Google Scholar
• Karimi R, Ershadi A. 2015. Role of exogenous abscisic acid in adapting of ‘Sultana’ grapevine to low temperature stress. Acta Physiol Plant. 37:1–11.
   Web of Science ®Google Scholar
• Kim HS, Lee EJ, Lim S-T, Han J-A. 2015. Self-enhancement of GABA in rice bran using various stress treatments. Food Chem. 172:657–662.
   PubMed Web of Science ®Google Scholar
• Kolodziejczyk I, Dzitko K, Szewczyk R, Posmyk MM. 2016. Exogenous melatonin improves corn (Zea mays L.) embryo proteome in seeds subjected to chilling stress. J Plant Physiol. 193:47–56.
   PubMed Web of Science ®Google Scholar
• Kostopoulou Z, Therios I, Roumeliotis E, Kanellis AK, Molassiotis A. 2015. Melatonin combined with ascorbic acid provides salt adaptation in Citrus aurantium L. seedlings. Plant Physiol Biochem. 86:155–165.
   PubMed Web of Science ®Google Scholar
• Kratsch H, Wise R. 2000. The ultrastructure of chilling stress. Plant Cell Environ. 23:337–350.
   Web of Science ®Google Scholar
• Lado J, Rodrigo MJ, López-Climent M, Gómez-Cadenas A, Zacarías L. 2016. Implication of the antioxidant system in chilling injury tolerance in the red peel of grapefruit. Postharvest Biol Tec. 111:214–223.
   Web of Science ®Google Scholar
• Lee HY, Byeon Y, Back K. 2014. Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco. J Pineal Res. 57:262–268.
   PubMed Web of Science ®Google Scholar
• Lee DH, Lee CB. 2000. Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci. 159:75–85.
   PubMed Web of Science ®Google Scholar
• Li T, Jiang S, Lu C, Yang W, Yang Z, Hu W, Xin Z, Yang Y. 2019. Melatonin: another avenue for treating osteoporosis? J Pineal Res. 66:1–12.
   Web of Science ®Google Scholar
• Li C, Wang P, Wei ZW, Liang D, Liu CH, Yin LJ DF, Fu MY, Ma FW. 2012. The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. J Pineal Res. 53:298–306.
   PubMed Web of Science ®Google Scholar
• Lichtenthaler HK. 1987. Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 148:350–383.
   Web of Science ®Google Scholar
• Liu N, Gong B, Jin Z, Wang X, Wei M, Yang F, Li Y, Shi Q. 2015. Sodic alkaline stress mitigation by exogenous melatonin in tomato needs nitric oxide as a downstream signal. J Plant Physiol. 186-187:68–77.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 25:402–408.
   PubMed Web of Science ®Google Scholar
• Mannino G, Caradonna F, Cruciata I, Lauria A, Perrone A, Gentile C. 2019. Melatonin reduces inflammatory response in human intestinal epithelial cells stimulated by interleukin-1β. J Pineal Res. 67:1–11.
   Web of Science ®Google Scholar
• Mannino G, Gentile C, Maffei ME. 2019. Chemical partitioning and DNA fingerprinting of some pistachio (Pistacia vera L.) varieties of different geographical origin. Phytochem. 160:40–47.
   PubMed Web of Science ®Google Scholar
• Meir S, Philosoph-Hadas S, Aharoni N. 1992. Ethylene-increased accumulation of fluorescent lipid-peroxidation products detected during senescence of parsley by a newly developed method. J Am Soc Hortic Sci. 117:128–132.
   Web of Science ®Google Scholar
• Mittler R, Vanderauwer S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Breusegem FV. 2011. ROS signaling: the new wave? Trends Plant Sci. 16:300–309.
   PubMed Web of Science ®Google Scholar
• Moustafa-Farag M, Almoneafy A, Mahmoud A, Elkelish A, Arnao MB, Li L, Ai S. 2020. Melatonin and its protective role against biotic stress impacts on plants. Biomolecules. 10:1–12.
   Web of Science ®Google Scholar
• Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22:867–880.
   Web of Science ®Google Scholar
• Palma F, Carvajal F, Ramos JM, Jamilena M, Garrido D. 2015. Effect of putrescine application on maintenance of zucchini fruit quality during cold storage: Contribution of GABA shunt and other related nitrogen metabolites. Postharvest Biol Technol. 99:131–140.
   Web of Science ®Google Scholar
• Plewa MJ, Smith SR, Wanger ED. 1991. Dieth yldithiocarbamate suppresses the plant activation of aromatic amines into mutagens by inhibiting tobacco cell peroxidase. Mutat Res. 247:57–64.
   PubMed Web of Science ®Google Scholar
• Posmyk MM, Kuran H, Marciniak K, Janas KM. 2008. Presowing seed treatment with melatonin protects red cabbage seedlings against toxic copper ion concentrations. J Pineal Res. 45:24–31.
   PubMed Web of Science ®Google Scholar
• Potters G, De Gara L, Asard H, Horemans N. 2002. Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem. 40:537–548.
   Web of Science ®Google Scholar
• Pourhanifeh M, Sharifi M, Reiter R, Abdolhossein D, Asemi Z. 2019. Melatonin and non-small cell lung cancer: New insights into signaling pathways. Cancer Cell Int. 19:1–7.
   PubMed Web of Science ®Google Scholar
• Qian Y, Tan D-X, Reiter RJ, Shi H. 2015. Comparative metabolomic analysis highlights the involvement of sugars and glycerol in melatonin-mediated innate immunity against bacterial pathogen in Arabidopsis. Sci Rep. 5:1–11.
   Web of Science ®Google Scholar
• Roe JH. 1955. The determination of sugar in blood and spinal fluid with anthrone reagent. J Biol Chem. 212:335–343.
   PubMed Web of Science ®Google Scholar
• Sarropoulou VN, Therios IN, Dimassi-Theriou KN. 2012. Melatonin promotes adventitious root regeneration in in vitro shoot tip explants of the commercial sweet cherry rootstocks CAB-6P (Prunus cerasus L.), Gisela 6 (P. cerasus× P. canescens), and MxM 60 (P. avium× P. mahaleb). J Pineal Res. 52:38–46.
   PubMed Web of Science ®Google Scholar
• Severcan F, Sahin I, Kazancı N. 2005. Melatonin strongly interacts with zwitterionic model membranes—evidence from Fourier transform infrared spectroscopy and differential scanning calorimetry. Biochim Biophys Acta. 1668:215–222.
   PubMed Web of Science ®Google Scholar
• Shao HB, Chu LY, Shao MA, Jaleel CA, Mi HM. 2008. Higher plant antioxidants and redox signaling under environmental stresses. C R Biol. 331:433–441.
   PubMed Web of Science ®Google Scholar
• Shelp BJ, Bozzo GG, Trobacher CP, Zarei A, Deyman KL, Brikis CJ. 2012. Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Sci. 193-194:130–135.
   PubMed Web of Science ®Google Scholar
• Shi H, Jiang C, Ye T, Tan D-x, Reiter RJ, Zhang H, Liu R, Chan Z. 2015. Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. J Exp Bot. 66:681–694.
   PubMed Web of Science ®Google Scholar
• Singh RP, Chidambara Murthy KN, Jayaprakasha GK. 2002. Studies on the antioxidant activity of pomegranate (Punica granatum) peel and seed extracts using in vitro models. J Agric Food Chem. 50:81–86.
   PubMed Web of Science ®Google Scholar
• Singleton VL, Orthofer R, Lamuela-Raventós RM. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol. 299:152–178.
   Web of Science ®Google Scholar
• Tan DX, Hardeland R, Manchester LC, Korkmaz A, Ma S, Rosales-Corral S, Reiter RJ. 2012. Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science. J Exp Bot. 63:577–597.
   PubMed Web of Science ®Google Scholar
• Tan DX, Manchester LC, Liu X, Rosales-Corral SA, Acuna-Castroviejo D, Reiter RJ. 2013. Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin's primary function and evolution in eukaryotes. J Pineal Res. 54:127–138.
   PubMed Web of Science ®Google Scholar
• Triantaphylides C, Havaux M. 2009. Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci. 14:219–228.
   PubMed Web of Science ®Google Scholar
• Turi CE, Axwik KE, Murch SJ. 2014. In vitro conservation, phytochemistry, and medicinal activity of Artemisia tridentata Nutt.: metabolomics as a hypothesis-generating tool for plant tissue culture. Plant Growth Regul. 74:239–250.
   Web of Science ®Google Scholar
• Turk H, Erdal S, Genisel M, Atici O, Demir Y, Yanmis D. 2014. The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul. 74:139–152.
   Web of Science ®Google Scholar
• Upadhyaya A, Davis T, Walser R, Galbraith A, Sankhla N. 1989. Uniconazole-induced alleviation of low-temperature damage in relation to antioxidant activity. HortScience. 24:955–957.
   Web of Science ®Google Scholar
• Wan YY, Zhang Y, Zhang L, Zhou ZQ, Li X, Wang XJ, Bai JG. 2015. Caffeic acid protects cucumber against chilling stress by regulating antioxidant enzyme activity and proline and soluble sugar contents. Acta Physiol Plant. 37:1–10.
   Web of Science ®Google Scholar
• Wang GJ, Miao W, Wang JY, Ma DR, Li JQ, Chen WF. 2013. Effects of exogenous abscisic acid on antioxidant system in weedy and cultivated rice with different chilling sensitivity under chilling stress. J Agro Crop Sci. 199:200–208.
   Web of Science ®Google Scholar
• Wang P, Sun X, Chang C, Feng F, Liang D, Cheng L, Ma F. 2013. Delay in leaf senescence of Malus hupehensis by long-term melatonin application is associated with its regulation of metabolic status and protein degradation. J Pineal Res. 55:267–274.
   PubMed Web of Science ®Google Scholar
• Wang P, Sun X, Li C, Wei Z, Liang D, Ma F. 2013. Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. J Pineal Res. 54:292–302.
   PubMed Web of Science ®Google Scholar
• Wang P, Yin L, Liang D, Li C, Ma F, Yue Z. 2012. Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate–glutathione cycle. J Pineal res. 53:11–20.
   PubMed Web of Science ®Google Scholar
• Wei S, Smits MG, Tang X, Kuang L, Meng H, Ni S, Xiao M, Zhou X. 2020. Efficacy and safety of melatonin for sleep onset insomnia in children and adolescents: a meta-analysis of randomized controlled trials. Sleep Med. 68:1–8.
   PubMed Web of Science ®Google Scholar
• Xing SG, Jun YB, Hau ZW, Liang LY. 2007. Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem. 45:560–566.
   PubMed Web of Science ®Google Scholar
• Xu XD, Sun Y, Guo XQ, Sun B, Zhang J. 2010. Effects of exogenous melatonin on ascorbate metabolism system in cucumber seedlings under high temperature stress. Yingyong Shengtai Xuebao. 21:2580–2586.
   Google Scholar
• Yu X, Peng Y, Zhang M, Shao YJ, Su W, Tang Z. 2006. Water relations and expression analysis of plasma membrane in trinsic proteins in sensitive and tolerant rice during chiling and recovery. Cell Res. 16:599–608.
   PubMed Web of Science ®Google Scholar
• Zamani Bahramabadi E, Rezanejad F, Sasan H. 2011. Sequensing and expression study of dehydrin gene under cold and short day treatments in seedlings and reganerated shoots of pistachio (Pistacia vera L.). Kerman: Shahid Bahonar University of Kerman.
   Google Scholar
• Zhang L, Jia J, Xu Y, Wang Y, Hao J, Li T. 2012. Production of transgenic Nicotiana sylvestris plants expressing melatonin synthetase genes and their effect on UV-B-induced DNA damage. In Vitro Cell Dev Biol Plant. 48:275–282.
   Web of Science ®Google Scholar
• Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S, Guo YD. 2015. Roles of melatonin in abiotic stress resistance in plants. J Exp Bot. 66:647–656.
   PubMed Web of Science ®Google Scholar
• Zhang J, Wu X, Niu R, Liu Y, Liu N, Xu W, Wang Y. 2012. Cold-resistance evaluation in 25 wild grape species. Vitis. 51:153–160.
   Web of Science ®Google Scholar
• Zhang HJ, Zhang N, Yang RC, Wang L, Sun QQLDB, Cao YY, Weeda S, Zhao B, Ren S, Guo YD. 2014. Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J Pineal Res. 57:269–279.
   PubMed Web of Science ®Google Scholar
• Zhang N, Zhao B, Zhang HJ, Weeda S, Yang C, Yang ZC, Ren S, Guo YD. 2013. Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res. 54:15–23.
   PubMed Web of Science ®Google Scholar