CLC number: S641.2
On-line Access: 2024-08-27
Received: 2023-10-17
Revision Accepted: 2024-05-08
Crosschecked: 2016-11-07
Cited: 3
Clicked: 4952
Qian-nan Diao, Yong-jun Song, Dong-mei Shi, Hong-yan Qi. Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersicon esculentum Mill.) seedling[J]. Journal of Zhejiang University Science B, 2016, 17(12): 916-930.
@article{title="Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersicon esculentum Mill.) seedling",
author="Qian-nan Diao, Yong-jun Song, Dong-mei Shi, Hong-yan Qi",
journal="Journal of Zhejiang University Science B",
volume="17",
number="12",
pages="916-930",
year="2016",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1600102"
}
%0 Journal Article
%T Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersicon esculentum Mill.) seedling
%A Qian-nan Diao
%A Yong-jun Song
%A Dong-mei Shi
%A Hong-yan Qi
%J Journal of Zhejiang University SCIENCE B
%V 17
%N 12
%P 916-930
%@ 1673-1581
%D 2016
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1600102
TY - JOUR
T1 - Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersicon esculentum Mill.) seedling
A1 - Qian-nan Diao
A1 - Yong-jun Song
A1 - Dong-mei Shi
A1 - Hong-yan Qi
J0 - Journal of Zhejiang University Science B
VL - 17
IS - 12
SP - 916
EP - 930
%@ 1673-1581
Y1 - 2016
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1600102
Abstract: Polyamines (PAs) and nitric oxide (NO) are vital signals in modulating plant response to abiotic stress. However, to our knowledge, studies on the relationship between NO and PAs in response to cold stress in tomato are limited. Accordingly, in this study, we investigated the effects of putrescine (Put) and spermidine (Spd) on NO generation and the function of Spd-induced NO in the tolerance of tomato seedling under chilling stress. Spd increased NO release via the nitric oxide synthase (NOS)-like and nitrate reductase (NR) enzymatic pathways in the seedlings, whereas Put had no such effect. Moreover, H2O2 might act as an upstream signal to stimulate NO production. Both exogenous NO donor (sodium nitroprusside (SNP)) and Spd enhanced chilling tolerance in tomato, thereby protecting the photosynthetic system from damage. Compared to chilling treatment alone, Spd enhanced the gene expressions of superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and ascorbate peroxidase (APX), and their enzyme activities in tomato leaves. However, a scavenger or inhibitor of NO abolished Spd-induced chilling tolerance and blocked the increased expression and activity due to Spd of these antioxidant enzymes in tomato leaves under chilling stress. The results showed that NO induced by Spd plays a crucial role in tomato’s response to chilling stress.
[1]Alcázar, R., Altabella, T., Marco, F., et al., 2010. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta, 231(6):1237-1249.
[2]Alemayehu, A., Zelinová, V., Bočová, B., et al., 2015. Enhanced nitric oxide generation in root transition zone during the early stage of cadmium stress is required for maintaining root growth in barley. Plant Soil, 390(1):213-222.
[3]Angelini, R., Tisi, A., Rea, G., et al., 2008. Involvement of polyamine oxidase in wound healing. Plant Physiol., 146(1):162-177.
[4]Arasimowicz-Jelonek, M., Floryszak-Wieczorek, J., Kubiś, J., 2009. Interaction between polyamine and nitric oxide signaling in adaptive responses to drought in cucumber. J. Plant Growth Regul., 28(2):177-186.
[5]Bais, H.P., Ravishankar, G.A., 2002. Role of polyamines in the ontogeny of plants and their biotechnological applications. Plant Cell Tissue Org. Cult., 69(1):1-34.
[6]Baker, N.R., 2008. Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu. Rev. Plant Biol., 59:89-113.
[7]Besson-Bard, A., Pugin, A., Wendehenne, D., 2008. New insights into nitric oxide signaling in plants. Annu. Rev. Plant Biol., 59:21-39.
[8]Besson-Bard, A., Astier, J., Rasul, S., et al., 2009. Current view of nitric oxide-responsive genes in plants. Plant Sci., 177(4):302-309.
[9]Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72(1):248-254.
[10]Bright, J., Desikan, R., Hancock, J.T., et al., 2006. ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J., 45(1):113-122.
[11]Cakmak, I., Marschner, H., 1992. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol., 98(4):1222-1227.
[12]Cheng, L., Sun, R.R., Wang, F.Y., et al., 2012. Spermidine affects the transcriptome responses to high temperature stress in ripening tomato fruit. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 13(4):283-297.
[13]Corpas, F.J., Barroso, J.B., Carreras, A., et al., 2006. Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta, 224(2):246-254.
[14]Courtois, C., Besson, A., Dahan, J., et al., 2008. Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. J. Exp. Bot., 59(2):155-163.
[15]Cuevas, J.C., López-Cobollo, R., Alcázar, R., et al., 2008. Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol., 148(2):1094-1105.
[16]Delledonne, M., Xia, Y., Dixon, R.A., et al., 1998. Nitric oxide functions as a signal in plant disease resistance. Nature, 394(6693):585-588.
[17]del Rı́o, L.A., Javier Corpas, F., Barroso, J.B., 2004. Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry, 65(7):783-792.
[18]Desikan, R., Griffiths, R., Hancock, J., et al., 2002. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. PNAS, 99(25):16314-16318.
[19]Dickinson, B.C., Chang, C.J., 2011. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat. Chem. Biol., 7(8):504-511.
[20]Dordas, C., Hasinoff, B.B., Igamberdiev, A.U., et al., 2003. Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J., 35(6):763-770.
[21]Esim, N., Atici, O., 2014. Nitric oxide improves chilling tolerance of maize by affecting apoplastic antioxidative enzymes in leaves. Plant Growth Regul., 72(1):29-38.
[22]Fan, H.F., Du, C.X., Guo, S.R., 2013. Nitric oxide enhances salt tolerance in cucumber seedlings by regulating free polyamine content. Environ. Exp. Bot., 86:52-59.
[23]Filippou, P., Antoniou, C., Fotopoulos, V., 2013. The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radic. Biol. Med., 56:172-183.
[24]Finkel, T., Holbrook, J.N., 2000. Oxidants, oxidative stress and the biology of ageing. Nature, 408(6809):239-247.
[25]Giannopolitis, C.N., Ries, S.K., 1977. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol., 59(2):309-314.
[26]Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem., 48(12):909-930.
[27]Gong, B., Li, X., Bloszies, S., et al., 2014. Sodic alkaline stress mitigation by interaction of nitric oxide and polyamines involves antioxidants and physiological strategies in Solanum lycopersicum. Free Radical Biol. Med., 71:36-48.
[28]Groppa, M.D., Benavides, M.P., 2008. Polyamines and abiotic stress: recent advances. Amino Acids, 34(1):35-45.
[29]Groppa, M.D., Rosales, E.P., Iannone, M.F., et al., 2008. Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry, 69(14):2609-2615.
[30]Guan, Y., Hu, J., Wang, X., et al., 2009. Seed priming with chitosan improves maize germination and seedling growth in relation to physiological changes under low temperature stress. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 10(6):427-433.
[31]Guan, Y., Lin, H., Ma, L., et al., 2014. Nitric oxide and hydrogen peroxide are important signals mediating the allelopathic response of Arabidopsis to p-hydroxybenzoic acid. Physiol. Plant., 152(2):275-285.
[32]Guo, F.Q., Okamoto, M., Crawford, N.M., 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science, 302(5642):100-103.
[33]Gupta, K.J., Fernie, A.R., Kaiser, W.M., et al., 2011. On the origins of nitric oxide. Trends Plant Sci., 16(3):160-168.
[34]Gupta, K., Dey, A., Gupta, B., 2013. Plant polyamines in abiotic stress responses. Acta Physiol. Plant., 35(7):2015-2036.
[35]He, L., Nada, K., Kasukabe, Y., et al., 2002. Enhanced susceptibility of photosynthesis to low-temperature photoinhibition due to interruption of chill-induced increase of S-adenosylmethionine decarboxylase activity in leaves of spinach (Spinacia oleracea L.). Plant Cell Physiol., 43(2):196-206.
[36]Hussain, S.S., Ali, M., Ahmad, M., et al., 2011. Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol. Adv., 29(3):300-311.
[37]Iannone, M.F., Rosales, E.P., Groppa, M.D., et al., 2013. H2O2 involvement in polyamine-induced cell death in tobacco leaf discs. J. Plant Growth Regul., 32(4):745-757.
[38]Igarashi, K., Kashiwagi, K., 2000. Polyamines: mysterious modulators of cellular functions. Biochem. Biophys. Res. Commun., 271(3):559-564.
[39]Jiang, Y.P., Cheng, F., Zhou, Y.H., et al., 2012. Hydrogen peroxide functions as a secondary messenger for brassinosteroids-induced CO2 assimilation and carbohydrate metabolism in Cucumis sativus. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 13(10):811-823.
[40]Kusano, T., Yamaguchi, K., Berberich, T., et al., 2007. Advances in polyamine research in 2007. J. Plant Res., 120(3):345-350.
[41]Kwak, J.M., Mori, I.C., Pei, Z.M., et al., 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J., 22(11):2623-2633.
[42]Li, X., Gong, B., Xu, K., 2014. Interaction of nitric oxide and polyamines involves antioxidants and physiological strategies against chilling-induced oxidative damage in Zingiber officinale Roscoe. Sci. Hort., 170:237-248.
[43]Li, Z., Zhou, H., Peng, Y., et al., 2015. Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. Plant Growth Regul., 76(1):71-82.
[44]Liu, D.F., Zhang, D., Liu, G.Q., et al., 2013. Influence of heat stress on leaf ultrastructure, photosynthetic performance, and ascorbate peroxidase gene expression of two pear cultivars (Pyrus pyrifolia). J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 14(12):1070-1083.
[45]Lizárraga-Paulín, E.G., Miranda-Castro, S.P., Moreno-Martínez, E., et al., 2013. Maize seed coatings and seedling sprayings with chitosan and hydrogen peroxide: their influence on some phenological and biochemical behaviors. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 14(2):87-96.
[46]Lu, C., Qiu, N., Wang, B., 2003. Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J. Exp. Bot., 54(383):851-860.
[47]Martin-Tanguy, J., 2001. Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul., 34(1):135-148.
[48]Moschou, P.N., Paschalidis, K.A., Delis, I.D., et al., 2008. Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell., 20(6):1708-1724.
[49]Moschou, P.N., Wu, J., Cona, A., et al., 2012. The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J. Exp. Bot., 63(14):5003-5015.
[50]Mostofa, M.G., Yoshida, N., Fujita, M., 2014. Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regul., 73(1):31-44.
[51]Murphy, M.E., Noack, E., 1994. Nitric oxide assay using hemoglobin method. Methods Enzymol., 233:240-250.
[52]Nakano, Y., Asada, K., 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol., 22(5):867-880.
[53]Nayyar, H., 2005. Putrescine increases floral retention, pod set and seed yield in cold stressed chickpea. J. Agron. Crop Sci., 191(5):340-345.
[54]Neill, S.J., Desikan, R., Hancock, J.T., 2003. Nitric oxide signalling in plants. New Phytol., 159(1):11-35.
[55]Neill, S.J., Bright, J., Desikan, R., et al., 2008. Nitric oxide evolution and perception. J. Exp. Bot., 59(1):25-35.
[56]Ninnemann, H., Maier, J., 1996. Indications for the occurrence of nitric oxide synthases in fungi and plants and the involvement in photoconidiation of Neurospora crassa. Photochem. Photobiol., 64(2):393-398.
[57]Pál, M., Szalai, G., Janda, T., 2015. Speculation: polyamines are important in abiotic stress signaling. Plant Sci., 237:16-23.
[58]Parvin, S., Lee, O.R., Sathiyaraj, G., et al., 2014. Spermidine alleviates the growth of saline-stressed ginseng seedlings through antioxidative defense system. Gene, 537(1):70-78.
[59]Pasqualini, S., Meier, S., Gehring, C., et al., 2009. Ozone and nitric oxide induce cGMP-dependent and -independent transcription of defence genes in tobacco. New Phytol., 181(4):860-870.
[60]Patterson, B.D., MacRae, E.A., Ferguson, I.B., 1984. Estimation of hydrogen peroxide in plant extracts using titanium(IV). Anal. Biochem., 139(2):487-492.
[61]Pei, Z.M., Murata, Y., Benning, G., et al., 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature, 406(6797):731-734.
[62]Planchet, E., Gupta, K.J., Sonoda, M., et al., 2005. Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J., 41(5):732-743.
[63]Puyang, X.H., An, M.Y., Han, L., et al., 2015. Protective effect of spermidine on salt stress induced oxidative damage in two Kentucky bluegrass (Poa pratensis L.) cultivars. Ecotoxicol. Environ. Saf., 117:96-106.
[64]Quan, L.J., Zhang, B., Shi, W.W., et al., 2008. Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J. Integr. Plant Biol., 50(1):2-18.
[65]Rider, J.E., Hacker, A., Mackintosh, C.A., et al., 2007. Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids, 33(2):231-240.
[66]Rizza, F., Pagani, D., Stanca, A.M., et al., 2001. Use of chlorophyll fluorescence to evaluate the cold acclimation and freezing tolerance of winter and spring oats. Plant Breed., 120(5):389-396.
[67]Rockel, P., Strube, F., Rockel, A., et al., 2002. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot., 53(366):103-110.
[68]Rosales, E.P., Iannone, M.F., Groppa, M.D., et al., 2012. Polyamines modulate nitrate reductase activity in wheat leaves: involvement of nitric oxide. Amino Acids, 42(2):857-865.
[69]Sairam, R.K., Srivastava, G.C., 2002. Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci., 162(6):897-904.
[70]Scheible, W.R., Gonzalez-Fontes, A., Lauerer, M., et al., 1997. Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell, 9(5):783-798.
[71]Shu, S., Yuan, L.Y., Guo, S.R., et al., 2012. Effects of exogenous spermidine on photosynthesis, xanthophyll cycle and endogenous polyamines in cucumber seedlings exposed to salinity. Afr. J. Biotechnol., 11(22):6064-6074.
[72]Siddiqui, M.H., Al-Whaibi, M.H., Basalah, M.O., 2011. Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma, 248(3):447-455.
[73]Silveira, V., Santa-Catarina, C., Tun, N.N., et al., 2006. Polyamine effects on the endogenous polyamine contents, nitric oxide release, growth and differentiation of embryogenic suspension cultures of Araucaria angustifolia (Bert.) O. Ktze. Plant Sci., 171(1):91-98.
[74]Song, Y., Diao, Q., Qi, H., 2015. Polyamine metabolism and biosynthetic genes expression in tomato (Lycopersicon esculentum Mill.) seedlings during cold acclimation. Plant Growth Regul., 75(1):21-32.
[75]Su, G.X., Zhang, W.H., Liu, Y.L., 2006. Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean. J. Integr. Plant Biol., 48(4):426-432.
[76]Sun, H., Li, J., Song, W., et al., 2015. Nitric oxide generated by nitrate reductase increases nitrogen uptake capacity by inducing lateral root formation and inorganic nitrogen uptake under partial nitrate nutrition in rice. J. Exp. Bot., 66(9):2449-2459.
[77]Tambussi, E.A., Bartoli, C.G., Guiamet, J.J., et al., 2004. Oxidative stress and photodamage at low temperatures in soybean (Glycine max L. Merr.) leaves. Plant Sci., 167(1):19-26.
[78]Tanou, G., Job, C., Rajjou, L., et al., 2009. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J., 60(5):795-804.
[79]Tanou, G., Ziogas, V., Belghazi, M., et al., 2014. Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ., 37(4):864-885.
[80]Tewari, R.K., Prommer, J., Watanabe, M., 2013. Endogenous nitric oxide generation in protoplast chloroplasts. Plant Cell Rep., 32(1):31-44.
[81]Thomas, R.L., Jen, J.J., Morr, C.V., 1982. Changes in soluble and bound peroxidase—IAA oxidase during tomato fruit development. J. Food Sci., 47(1):158-161.
[82]Tian, X., Lei, Y., 2006. Nitric oxide treatment alleviates drought stress in wheat seedlings. Biol. Plant., 50(4):775-778.
[83]Tun, N.N., Santa-Catarina, C., Begum, T., et al., 2006. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol., 47(3):346-354.
[84]Velikova, V., Yordanov, I., Edreva, A., 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci., 151(1):59-66.
[85]Verma, S., Mishra, S.N., 2005. Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J. Plant Physiol., 162(6):669-677.
[86]Wi, S.J., Kim, W.T., Park, K.Y., 2006. Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants. Plant Cell Rep., 25(10):1111-1121.
[87]Wimalasekera, R., Tebartz, F., Scherer, G.F., 2011. Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci., 181(5):593-603.
[88]Xiong, J., Fu, G., Yang, Y., et al., 2012. Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research? J. Exp. Bot., 63(1):33-41.
[89]Yamamoto, A., Shim, I.S., Fujihara, S., 2012. Chilling-stress responses by rice seedlings grown with different ammonium concentrations and its relationship to leaf spermidine content. J. Plant Biol., 55(3):191-197.
[90]Yamasaki, H., Cohen, M.F., 2006. NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci., 11(11):522-524.
[91]Yang, J.C., Zhang, J.H., Liu, K., et al., 2007. Involvement of polyamines in the drought resistance of rice. J. Exp. Bot., 58(6):1545-1555.
[92]Yoda, H., Yamaguchi, Y., Sano, H., 2003. Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol., 132(4):1973-1981.
[93]Yoda, H., Hiroi, Y., Sano, H., 2006. Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol., 142(1):193-206.
[94]Zapata, P.J., Serrano, M., Pretel, M.T., et al., 2004. Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci., 167(4):781-788.
[95]Zemojtel, T., Fröhlich, A., Palmieri, M.C., et al., 2006. Plant nitric oxide synthase: a never-ending story? Trends Plant Sci., 11(11):524-525.
[96]Zhang, A., Jiang, M., Zhang, J., et al., 2007. 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., 175(1):36-50.
[97]Zhou, B., Guo, Z., Xing, J., et al., 2005. Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J. Exp. Bot., 56(422):3223-3228.
[98]Zhou, R., Yu, X., Kjær, K.H., et al., 2015. Screening and validation of tomato genotypes under heat stress using Fv/Fm to reveal the physiological mechanism of heat tolerance. Environ. Exp. Bot., 118:1-11.
[99]List of electronic supplementary materials
[100]Fig. S1 Effects of exogenous Put and Spd on leNR and leNOS1 relative expression in the leaves of tomato under chilling stress
[101]Table S1 Gene accession numbers and primer sequences of tomato NR and NOS1 in this study
Open peer comments: Debate/Discuss/Question/Opinion
<1>