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Effects of nitric oxide and Fe supply on recovery of Fe deficiency induced chlorosis in peanut plants

  • Original Paper
  • Published:
Biologia Plantarum

Abstract

The effects of nitric oxide (NO) and/or iron (Fe) supplied to Fe deficient plants have been investigated in peanut (Arachis hypogaea L.) grown in Hoagland nutrient solution with or without Fe. Two weeks after Fe deprivation, recovery was induced by addition of 250 μM sodium nitroprusside (SNP, a NO donor) and/or 50 μM Fe (Fe-EDTA) to the Fe deprived (-Fe) nutrient solution. Activities of antioxidant enzymes, leaf chlorophyll (Chl), and active Fe content decreased, whereas activities of H+-ATPase, ferric-chelate reductase (FCR), nitrate reductase, and nitric oxide synthase and NO production increased in Fe deficient plants, consequently an Fe chlorosis symptom appeared obviously. In contrast, these symptoms disappeared gradually after two weeks with NO and/or Fe supply, which caused an increases in leaf Chl and active Fe content, especially following by co-treatment with NO and Fe to values found in Fe sufficient plants. Increased activities of antioxidant enzymes (superoxide dismutase, peroxidase, and catalase) and decreased accumulation of reactive oxygen species (H2O2, O •−2 ) and malondialdehyde enhanced the ability of resistance to oxidative stress. Supplied NO alone had the obvious effect on increased NO production and on activity of H+-ATPase and FCR, whereas root length and root/shoot ratio were most effectively increased by Fe supplied alone. Co-treatment with NO and Fe did the best effects on recovery peanut chlorosis symptoms by significantly increased Chl and available Fe content and adjusted distribution of Fe and other mineral elements (Ca, Mg, and Zn) in both leaves and roots.

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Abbreviations

Car:

carotenoid

CAT:

catalase

Chl:

chlorophyll

FCR:

ferric-chelate reductase

LSD:

least significant diffrence

MDA:

malondialdehyde

NR:

nitrate reductase

NOS:

nitric oxide synthase

O •−2 :

superoxide anion

PM:

plasma membrane

POD:

peroxidase

ROS:

reactive oxygen species

SNP:

sodium nitroprusside

SOD:

superoxide dismutase

References

  • Airaki, M., Leterrier, M., Mateos, R.M., Valderrama, R., Chaki, M., Barroso, J.B., Del Río, L.A., Palma, J.M., Corpas, F.J.: Metabolism of reactive oxygen species and reactive nitrogen species in pepper (1 L.) plants under low temperature stress. - Plant Cell Environ. 35: 281–295, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Arnaud, N., Murgia, I., Boucherez, J., Briat, J.F., Cellier, F., Gaymard, F.: An iron induced nitric oxide burst precedes ubiquitin-dependent protein degradation for Arabidopsis AtFer1 ferritin gene expression. - J. biol. Chem. 281: 23579–88, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Asai, S., Ohta, K., Yoshioka, H.: MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. - Plant Cell. 20: 1390–1406, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Attree, R., Dua, B., Xu, B.J.: Distribution of phenolic compounds in seed coat and cotyledon, and their contribution to antioxidant capacities of red and black seed coat peanuts (1 L.). - Ind. Crops Prod. 67: 448–456, 2015.

    Article  CAS  Google Scholar 

  • Bacaicoa, E., Mora, V., Zamarreño, Á. M., Fuentes, M., Casanova, E., García-Mina, J.M.: Auxin: a major player in the shoot-to-root regulation of root Fe-stress physiological responses to Fe deficiency in cucumber plants. - Plant Physiol. Biochem. 49: 545–556, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Besson-Bard, A., Pugin, A., Wendehenne, D.: New insights into nitric oxide signaling in plants. - Annu. Rev. Plant Biol. 59: 21–39, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248–254, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Briat, J.F., Dubos, C., Gaymard, F.: Iron nutrition, biomass production, and plant product quality. - Trends Plant Sci. 20: 33–40, 2014.

    Article  PubMed  Google Scholar 

  • Briat, J.F., Duc, C., Ravet, K., Gaymard, F.: Ferritin and iron storage in plants. - Biochim. biophys. Acta. 1800: 806–814, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Briskin, D.P., Leonard, R.T., Hodges, T.K.: Isolation of the plasma membrane: markers and general principles. - Method. Enzymol. 148: 542–558 1987.

    Article  CAS  Google Scholar 

  • Chen, W.W., Yang, J.L., Qin, C., Jin, C.W., Mo, J.H., Ye, T., Zheng, S.J.: Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis. - Plant Physiol. 154: 810–819, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colangelo, E.P., Guerinot, M.L.: The essential basic helix-loophelix protein FIT1 is required for the iron deficiency response. - Plant Cell. 16: 3400–3412, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connolly, E.L., Campbell, N.H., Grotz, N., Prichard, C.L., Guerinot, M.L.: Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. - Plant Physiol. 133: 1102–1110, 2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conte, S.S., Walker, E.L.: Transporters contribute to iron trafficking in plants. - Mol. Plant. 4: 464–76, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Ding, F., Wang, X.F., Shi, Q.H., Wang, L., Yang, F.J., Gao, Q.H.: Exogenous nitric oxide alleviated the inhibition of photosynthesis and antioxidant enzyme activities in irondeficient Chinese cabbage (Brassica chinensis L.) - Agr. Sci. China 7: 168–179, 2008.

    Article  CAS  Google Scholar 

  • Du, S.T., Liu, Y., Zhang, P., Liu, H.J., Zhang, X.Q., Zhang, R.R.: 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, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Marcos, M., Sanz, L., Lewis, D.R., Lorenzo, O.: Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1(PIN1)- dependent acropetal auxin transport. - Proc. nat. Acad. Sci. USA 108: 18506–18511, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao, L., Shi, Y.X.: Genetic differences in resistance to iron deficiency chlorosis in peanut. - J. Plant Nutr. 30: 37–52, 2007.

    Article  CAS  Google Scholar 

  • García, M.J., Suárez, V., Romera, F.J., Alcántara, E., Pérez-Vicente, R.: A new model involving ethylene, nitric oxide and Fe to explain the regulation of Fe-acquisition genes in Strategy I plants. - Plant Physiol. Biochem. 49: 537–544, 2011.

    Article  PubMed  Google Scholar 

  • García-Mina, J.M., Bacaicoa, E., Fuentes, M., Casanova, E.: Fine regulation of leaf iron use efficiency and iron root uptake under limited iron bioavailability. - Plant Sci. 198: 39–45, 2013.

    Article  PubMed  Google Scholar 

  • Graziano, M., Beligni, M.V., Lamattina, L.: Nitric oxide improves internal iron availability in plants. - Plant Physiol. 130: 1852–1859, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graziano, M., Lamattina, L.: Nitric oxide and iron in plants: an emerging and converging story. - Trends Plant Sci. 10: 4–8, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Graziano, M., Lamattina, L.: Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. - Plant J. 52: 949–960, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Guo, F.Q., Okamoto, M., Crawford, N.M.: Identification of a plant nitric oxide synthase gene involved in hormonal signaling. - Science 302: 100–103, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Halliwell, B.: Reactive species and antioxidants redox biology is a fundamental theme of aerobic life. - Plant Physiol. 141: 312–322, 2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hakan, C. A., Vahap, K.: Some parameters in relation to iron nutrition status of peach orchads. - J. Biol. environ. Sci. 1: 111–115, 2007.

    Google Scholar 

  • Heath, R.L., Packer, L.: Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. - Arch. Biochem. Biophys. 125: 189–198, 1968.

    Article  CAS  PubMed  Google Scholar 

  • Hell, R., Stephan, U.W.: Iron uptake, trafficking and homeostasis in plants. - Planta 216: 541–551, 2003.

    CAS  PubMed  Google Scholar 

  • Hindt, M.N., Guerinot, M.L.: Getting a sense for signals: regulation of the plant iron deficiency response. - Biochim. biophys. Acta 1823: 1521–1530, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoagland, D.R., Arnon, D.I.: The water-culture method for growing plants without soil. - Calif. Agr. Exp. Sta. Circular 347: 1–32, 1950.

    Google Scholar 

  • Ishimaru, Y., Kim, S.A., Tsukamoto, T., Oki, H., Kobayashi, T., Watanabe, S., Matsuhashi, S., Takahashi, M., Nakanishi, H., Mori, S., Nishizawa, N.K.: Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. - Proc. nat. Acad. Sci. USA. 104: 7373–7378, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jasid, S., Simontacchi, M., Puntarulo, S.: Exposure to nitric oxide protects against oxidative damage but increases the labile iron pool in sorghum embryonic axes. - J. exp. Bot. 59: 3953–3962, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaworski, E.G.: Nitrate reductase assay in intact plant tissues. - Biochem. biophys. Res. Commun. 43: 1274–1279, 1971.

    Article  CAS  PubMed  Google Scholar 

  • Jelali, N., Donnini, S., Dell’Orto, M., Abdelly, C., Gharsalli, M., Zocchi, G.: Root antioxidant responses of two Pisum sativum cultivars to direct and induced Fe deficiency. - Plant Biol. 16: 607–614, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Kabir, A.H., Rahman, M.M., Haider, S.A., Paul, N.K.: Mechanisms associated with differential tolerance to Fe deficiency in okra (Abelmoschus esculentus Moench). - Environ. exp. Bot. 112: 16–26, 2015.

    Article  CAS  Google Scholar 

  • Knudson, L.L., Tibbitts, T.W., Edwards, G.E.: Measurement of ozone injury by determination of leaf chlorophyll concentration. - Plant Physiol. 60: 606–608, 1977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi, T., Nishizawa, N.K.: Iron uptake, translocation and regulation in higher plants. - Annu Rev. Plant Biol. 63: 131–152, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Kong, J., Dong, Y.J., Song, Y.L., Bai, X.Y., Tian, X.Y., Xu, L.L., Liu, S., He, Z.L.: Role of exogenous nitric oxide in alleviating iron deficiency stress of peanut seedlings (Arachis hypogaea L.). - J. Plant Growth Regul. 35: 31–43, 2016.

    Article  CAS  Google Scholar 

  • Kong, J., Dong, Y.J., Xu, L.L., Liu, S., Bai, X.Y.: Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of Arachis hypogaea L. - Bot. Stud. 55: 1–9, 2014.

    Article  Google Scholar 

  • Kumar, P., Tewari, R.K., Sharma, P.N.: Sodium nitroprussidemediated alleviation of iron deficiency and modulation of antioxidant responses in maize plants. - AoB Plants 2010, plq002. doi: 10.1093/aobpla/plq002

    Google Scholar 

  • Larbi, A., Abadía, A., Abadía, J., Morales, F.: Down coregulation of light absorption, photochemistry, and carboxylation in Fe-deficient plants growing in different environments. - Photosynth. Res. 89: 113–126, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Larbi, A., Abadía, A., Morales, F., Abadía, J.: Fe resupply to Fe-deficient sugar beet plants leads to rapid changes in the violaxanthin cycle and other photosynthetic characteristics without de novo chlorophyll synthesis. - Photosynth. Res. 79: 59–69, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Larbi, A., Morales, F., Abadía, A., Abadía, J.: Changes in iron and organic acid concentrations in xylem sap and apoplastic fluid of iron-deficient Beta vulgaris plants in response to iron resupply. - J. Plant Physiol. 167: 255–260, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S., Chiecko, J.C., Kim, S.A., Walker, E.L., Lee, Y., Guerinot, M.L., An, G.: Disruption of OsYSL15 leads to iron inefficiency in rice plants. - Plant Physiol. 150: 786–800, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H.: Principles and Techniques of Plant Physiological Experiment. - Higher Education Press, Beijing 2000.

    Google Scholar 

  • Liu, B., Rennenberg, H., Kreuzwieser, J.: Hypoxia induces stem and leaf nitric oxide (NO) emission from poplar seedlings. - Planta 241: 579–589, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Liu, S.L., Yang, R.T., Pan, Y.Z., Ma, M.D., Pan, J., Zhao, Y., Cheng, Q.S., Wu, M.X., Wang, M.H., Zhang, L.: Nitric oxide contributes to minerals absorption, proton pumps and hormone equilibrium under cadmium excess in Trifolium repens L. plants. - Ecotox. Environ. Safety 119: 35–46, 2015.

    Article  CAS  Google Scholar 

  • López-Millán, A.F., Morales, F., Abadía, A., Abadía, J.: Changes induced by Fe deficiency and Fe resupply in the organic acid metabolism of sugar beet (Beta vulgaris L.) leaves. - Physiol Plant. 112: 3–38, 2001.

    Article  Google Scholar 

  • Manai, J., Gouia, H., Corpas, F.J.: Redox and nitric oxide homeostasis are affected in tomato (Solanum lycopersicum) roots under salinity-induced oxidative stress. - J Plant Physiol. 171: 1028–1035, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Mahmoudi, H., Labidi, N., Ksouri, R., Gharsalli, M., Abdelly, C.: Differential tolerance to iron deficiency of chickpea varieties and Fe resupply effects. - Compt. Rend. Biol. 330: 237–246, 2007.

    Article  CAS  Google Scholar 

  • Martin, M., Colman, M.J.R., Gomez-Casati, D.F., Lamattina, L., Zabaleta, E.J.: Nitric oxide accumulation is required to protect against iron-mediated oxidative stress in frataxindeficient Arabidopsis plants. - FEBS Lett. 583: 542–548, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Mengel, K., Kirkby, E.A.: Principles of Plant Nutrition. - Kluwer Academic Publishers, Dordrecht 2001.

    Book  Google Scholar 

  • Morrissey, J., Guerinot, M.L.: Iron uptake and transport in plants: the good, the bad, and the ionome. - Chem. Rev. 109: 4553–67, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nickel, K.S., Cunningham, B.A.: Improved peroxidase assay method using leuco 2,3,6-trichloro indophenol and application to comparative measurements of peroxidase catalysis. - Anal. Biochem. 27: 292–299, 1969.

    Article  CAS  PubMed  Google Scholar 

  • Ohinishi, T., Gall, R.S., Mayer, M.L.: An improved assay of inorganic phosphate in the presence of extralabile phosphate compounds: application to the ATPase assay in the presence of phosphocreatine. - Anal. Biochem. 69: 261–267, 1975.

    Article  Google Scholar 

  • Osorio, J., Osorio, M.L., Correia, P.J., De Varennes, A., Pestana, M.: Chlorophyll fluorescence imaging as a tool to understand the impact of iron deficiency and resupply on photosynthetic performance of strawberry plants. - Sci. Hort. 165: 148–155, 2014.

    Article  CAS  Google Scholar 

  • Palmgren, M.G.: Plant plasma membrane H+-ATPase: powerhouses for nutrient uptake. - Annu. Rev. Plant Biol. 52: 817–845, 2001.

    Article  CAS  Google Scholar 

  • Patra, H.L., Kar, M., Mishre, D.: Catalase activity in leaves and cotyledons during plant development and senescence. - Biochem. Pharmacol. 172: 385–390, 1978.

    CAS  Google Scholar 

  • Pätsìkkä, E., Kairavuo, M., Šeršen, F., Aro, E.M., Tyystjärvi, E.: Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. - Plant Physiol. 129: 1359–1367, 2002.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira, M.P., Santos, C., Gomes, A., Vasconcelos, M.W.: Cultivar variability of iron uptake mechanisms in rice (Oryza sativa L.) - Plant Physiol. Biochem. 85: 21–30, 2014.

  • Pestana, M., Correia, P.J., Saavedra, T., Gama, F., Abadía, A., De Varennes, A.: Development and recovery of iron deficiency by iron resupply to roots or leaves of strawberry plants. - Plant Physiol. Biochem. 53: 1–5, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Pii, Y., Penn, A., Terzano, R., Crecchio, C., Mimmo, T., Cesco, S.: Plant-microorganism-soil interactions influence the Fe availability in the rhizosphere of cucumber plants. - Plant Physiol. Biochem. 87: 45–52, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Ramirez, L., Simontacchi, M., Murgia, I., Zabaleta, E., Lamattina, L.: Nitric oxide, nitrosyl iron complexes, ferritin and frataxin: a well equipped team to preserve plant iron homeostasis. - Plant Sci. 181: 582–592, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Ramirez, L., Zabaleta, E.J., Lamattina, L.: Nitric oxide and frataxin: Two players contributing to maintain cellular iron homeostasis. - Ann. Bot. 105: 801–810, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Ranieri, A., Castagna, A., Baldan, B., Soldatini, G.F.: Iron deficiency differently affects peroxidase isoforms in sunflower. - J. exp. Bot. 52: 25–35, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Rockel, P., Strube, F., Rockel, A., Wildt, J., Kaiser, W.M.: Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. - J. exp. Bot. 53: 103–110, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt, W.: Iron solutions: acquisition strategies and signaling pathways in plants. - Trends Plant Sci. 8: 188–193, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Shi, G.R., Su, G.Q., Lu, Z.W., Liu, C.F., Wang, X.M.: Relationship between biomass, seed components and seed Cd concentration in various peanut (Arachis hypogaea L.) cultivars grown on Cd-contaminated soils. - Ecotox. Environ. Safety 110: 174–181, 2014.

    Article  CAS  Google Scholar 

  • Shi, Q. H., Ding, F., Wang, X. F., Wei, M.: Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. - Plant Physiol. Biochem. 45: 542–550, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Shi, Q.H., Zhu, Z.J.: Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. - Environ. exp. Bot. 63: 317–326, 2008.

    Article  CAS  Google Scholar 

  • Simontacchi, M., Buet, A., Lamattina, L., Puntarulo, S.: Exposure to nitric oxide increases the nitrosyl-iron complexes content in Sorghum embryonic axes. - Plant Sci. 183: 159–166, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Sokolovski, S.G., Blatt, M.R.: Nitric oxide and plant ion channel control. - In: Lamattina, L., Polacco, J.C. (ed.): Nitric Oxide in Plant Growth, Development and Stress Physiology. Pp. 153–171. Springer, Berlin - Heidelberg 2007.

    Chapter  Google Scholar 

  • Stewart, R.C., Bewley, J.D.: Lipid peroxidation associated with accelerated aging of soybean axes. - Plant Physiol. 65: 245–248, 1980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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). - J. Plant Physiol. 164: 536–543, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Su, Y., Liu, J.L., Lu, Z.W., Wang, X.M., Zhang, Z., Shi, G.G.: Effects of iron deficiency on subcellular distribution and chemical forms of cadmium in peanut roots in relation to its translocation. - Environ. exp. Bot. 97: 40–48, 2014.

    Article  CAS  Google Scholar 

  • Takker, P.N., Kaur. N.P.: HCl method for Fe2+ estimation to resolve iron chlorosis in plants. - J. Plant Nutr. 7: 81–90, 1984.

    Article  Google Scholar 

  • Tomasi, N., Rizzardo, C., Monte, R., Gottardi, S., Jelali, N., Terzano, R., Vekemans, B., De Nobili, M., Varanini, Z., Pinton, R., Cesco, S.: Micro-analytical, physiological and molecular aspects of Fe acquisition in leaves of Fe-deficient tomato plants resupplied with natural Fe-complexes in nutrient solution. - Plant Soil 325: 25–38, 2009.

    Article  CAS  Google Scholar 

  • Ueno, T., Yoshimura, T.: The physiological activity and in vivo distribution of dinitrosyl dithiolate iron complex. - Jap. J. Pharmacol 82: 95–101, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Velikova, V., Yordanov, I., Edreva, A.: Oxidative stress and some antioxidant systems in acid rain-treated bean plants. - Plant Sci. 151: 59–66, 2000.

    Article  CAS  Google Scholar 

  • Vert, G.A., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, M.L., Briat, J.F., Curie, C.: IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. - Plant Cell 14: 1223–1233, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wendehenne, D., Pugin, A., Klessig, D.F., Durner, J.: Nitric oxide: comparative synthesis and signaling in animal and plant cells. - Trends Plant Sci. 6: 177–83, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Xiong, H.C., Guo, X.T., Kobayashi, T., Kakei, Y., Nakanishi, H., Nozoye, T., Zhang, L.X., Shen, H.Y., Qiu, W., Nishizawa, N.K., Zuo, Y.M.: Expression of peanut iron regulated transporter 1 in tobacco and rice plants confers improved iron nutrition. - Plant Physiol. Biochem. 80: 83–89, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Xiong, Y., Yuan, L.W., Deng, H.W., Li, Y.J., Chen, B.M.: Elevated serum endogenous inhibitor of nitric oxide synthase and endothelial dysfunction in aged rats. - Clin. exp. Pharmacol. 28: 842–847, 2001.

    Article  CAS  Google Scholar 

  • Xu, J., Yin, H.X., Liu, X.J., Yuan, T., Mi, Q., Yang, L.L., Xie, Z.X., Wang, W.Y.: Nitric oxide alleviates Fe deficiencyinduced stress in Solanum nigrum. - Biol. Plant. 53: 784–788, 2009.

    Article  CAS  Google Scholar 

  • Xu, Y.F., Sun, X.L., Jin, J.W., Zhou. H.: Protective effect of nitric oxide on light-induced oxidative damage in leaves of tall fescue. - J. Plant Physiol. 167: 512–518, 2010.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. College of Resources and Environment, Shandong Agricultural University, Tai’An, 271018, P.R. China

    Y. L. Song, Y. J. Dong, X. Y. Tian & W. W. Wang

  2. Institute of Food and Agricultural Sciences, University of Florida, Fort Pierce, FL, 34945, USA

    Z. L. He

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Correspondence to Y. J. Dong.

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Acknowledgments: The authors thank Dr. Pingping Yang (the College of Animal Science and Technology, the Shandong Agricultural University, China) for supplying instruments and patient guidance. This research was financially supported by the Taishan Scholars at Seed Industry Talent Project, the Shandong Province Seed Industry Project, and the Shandong Provincial Natural Science Foundation of China (ZR2013CM003).

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Song, Y.L., Dong, Y.J., Tian, X.Y. et al. Effects of nitric oxide and Fe supply on recovery of Fe deficiency induced chlorosis in peanut plants. Biol Plant 61, 155–168 (2017). https://doi.org/10.1007/s10535-016-0642-2

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