Effects of root addition and foliar application of nitric oxide and salicylic acid in alleviating iron deficiency induced chlorosis of peanut seedlings

References

• Ahmàd, P., G. Nabi, and M. Ashraf. 2006. Cadmium-induced oxidative damage in mustard (Brassica juncea (L.) Czern.& Coss.) plants can be alleviated by salicylic acid. South African. Journal of Botany 7: 36–44.
   Google Scholar
• Arnaud, N., I. Murgia, J. Boucherez, J. F. Briat, F. Cellier, and F. Gaymard. 2006. An iron-induced nitric oxide burst precedes ubiquitin-dependent protein degradation for Arabidopsis AtFer1 ferritin gene expression. Journal of Biological Chemistry 33: 23579–23588.
   Web of Science ®Google Scholar
• Bacaicoa, E., M. Z. Ángel, L. Diane, and B. Roberto. 2009. relationship between the hormonal balance and the regulation of iron deficiency stress responses in cucumber. Journal of the American Society for Horticultural Science 134: 589–601.
   Web of Science ®Google Scholar
• Briat, J. F., C. Duc, K. Ravet, and F. Gaymard. 2010. Ferritins and iron storage in plants. Biochimica et Biophysica Acta 1800: 806–814.
   PubMed Web of Science ®Google Scholar
• Briskin, D. P., R. T. Leonard, and T. K. Hodges. 1987. Isolation of the plasma membrane: markers and general principles. Methods in Enzymology 148: 542–558.
   Web of Science ®Google Scholar
• Chen, W. W., J. L. Yang, C. Qin, C. W. Jin, J. H. Mo, T. Ye, and S. J. Zheng. 2010. Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in responses to iron deficiency in Arabidopsis. Plant Physiology 154: 810–819.
   PubMed Web of Science ®Google Scholar
• Connolly, E. L., N. Campbell, N. Grotz, C. L. Prichard, and M. L. Guerinot. 2003. Overexpression of the FRO2 Ferric Chelate reductase confers tolerance to growth on low iron and uncovers post-transcriptional control. Plant Physiololgy 133: 1102–1110.
   PubMed Web of Science ®Google Scholar
• Ding, H., L. H. Duan, J. Li, H. Yan, M. Zhao, F. S. Zhang, and W. X. Li. 2010. Cloning and functional analysis of the peanut iron transporter AhIRT1 during iron deficiency stress and intercropping with maize. Journal of Plant Physiology 167: 996–1002.
   PubMed Web of Science ®Google Scholar
• Ding, F., X. F. Wang, Q. H. Shi, M. L. Wang, F. J. Yang, and Q. H. Gao. 2008. Exogenous nitric oxide alleviated the inhibition of photosynthesis and antioxidant enzyme activities in iron-deficient Chinese cabbage (Brassica chinensis L.). Agricultural Sciences in China 7: 168–179.
   Google Scholar
• Eichert, T., J. J. Peguero-Pina, E. Gil-Pelegrín, A. Heredia, and V. Fernández. 2010. Effects of iron chlorosis and iron resupply on leaf xylem architecture, water relations, gas exchange and stomatal performance of field-grown peach (Prunus persica). Plant Physiologly 138: 48–59.
   Web of Science ®Google Scholar
• Eide, D., M. Broderius, J. Fett, and M. L. Guerinot. 1996. A novel iron–regulated metal transporter from plants identified by functional expression in yeast. Proceedings of the National Academy of Sciences of the United States of America 93: 5624–5628.
   PubMed Web of Science ®Google Scholar
• Fernández, V., R. V. Del, L. Pumariño, E. Igartua, J. Abadía, and A. Abadía. 2008. Foliar fertilization of peach (Prunus persica (L) Batsch) with different iron formulations: Effects on re-greening, iron concentration and mineral composition in treated and untreated leaf surfaces. Scientia Horticulturae 117: 241–248.
   Web of Science ®Google Scholar
• Gao, L., and Y. X. Shi. 2007. Genetic differences in resistance to iron deficiency chlorosis in peanut. Journal of Plant Nutrition 30: 37–52.
   Web of Science ®Google Scholar
• Gévaudant, F., D. Geoffrey, E. V. Stedingk, R. M. Zhao, P. Morsomme, and M. Boutry. 2007. Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance. Plant Physiology 144: 1763–1776.
   PubMed Web of Science ®Google Scholar
• González-Vallejo, E. B., F. Morales, L. Cistué, A. Abadía, and J. Abadía. 2000. Iron deficiency decreases the Fe (III)-chelate reducing activity of leaf protoplasts. Plant Physiology 122: 337–344.
   PubMed Web of Science ®Google Scholar
• Graziano, M., M. V. Beligni, and L. Lamattina. 2002. Nitric oxide improves internal iron availability in plants. Plant Physiology 130: 1852–1859.
   PubMed Web of Science ®Google Scholar
• Graziano, M., and L. Lamattina. 2005. Nitric oxide and iron in plants: an emerging and converging story. Trends in Plant Science 10: 4–8.
   PubMed Web of Science ®Google Scholar
• Graziano, M., and L. Lamattina. 2007. Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. The Plant Journal 52: 949–960.
   PubMed Web of Science ®Google Scholar
• Gunes, A., A. Inal, M. Alpaslan, F. Eraslan, E. G. Bagci, and N. Cicek. 2007. Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Journal of Plant Physiology 164: 728–736.
   PubMed Web of Science ®Google Scholar
• Guo, X. T., H. Y., Xiong, W. Shen, C. Q. Qiu, Z. Ji, J. Zhang, and Y. M. Zuo. 2014. Dynamics in the rhizosphere and iron–uptake gene expression in peanut induced by intercropping with maize: Role in improving iron nutrition in peanut. Plant Physiology and Biochemistry 76C: 36–43.
   Web of Science ®Google Scholar
• Hakan, C. A., and K. Vahap. 2007. Some parameters in relation to iron nutrition status of peach orchards. Journal of Environmental Biology 1: 111–115.
   Google Scholar
• Han, Z. H., C. Q. Han, X. F. Xu, and Q. Wang. 2005. Relationship between iron deficiency stress and endogenous hormones in iron efficient versus inefficient apple genotypes. Journal of Plant Nutrition 28: 1887–1895.
   Web of Science ®Google Scholar
• Heath, R. L., and L. Packer. 1968. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysic 125: 189–198.
   PubMed Web of Science ®Google Scholar
• Hell, R., and U. W. Stephan. 2003. Iron uptake, trafficking and homeostasis in plants. Planta 216: 541–51.
   PubMed Web of Science ®Google Scholar
• Hoagland, D. R., and D. I. Arnon. 1950. The water culture method for growing plants without soil. Circular. California Agricultural Experiment Station Circular 347: 29–32.
   Google Scholar
• Horvath, E., S. Szalai, and T. Janda. 2007. Induction of abiotic stress tolerance by salicylic acid signaling. Journal of Plant Growth Regulation 26: 290–300.
   Web of Science ®Google Scholar
• Ishimaru, Y., S. A. Kim, T. Tsukamoto, H. Oki, T. Kobayashi, S. Watanabe, S. Matsuhashi, M. Takahashi, H. Nakanishi, S. Mori, and N. K. Nishizawa. 2007. Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. Proceedings of the National Academy of Sciences of the USA 104: 7373–7378.
   PubMed Web of Science ®Google Scholar
• Janda, T., G. Szalai, I. Tari, and E. Paldi. 1999. Hydroponic treatment with salicylic acid decreases the effect of chilling injury in maize (Zea mays L.) plants. Planta 208: 175–180.
   Web of Science ®Google Scholar
• Jin, C. W., G. Y. You, Y. F. He, C. X. Tang, P. Wu, and S. J. Zheng. 2007. Iron deficiency–induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiology 144: 278–285.
   PubMed Web of Science ®Google Scholar
• Kanai, M., M. Hirai, M. Yoshiba, T. Tadano, and K. Higuchi. 2009. Iron deficiency causes zinc excess in Zea mays. Soil Science and Plant Nutrition 55: 271–276.
   Web of Science ®Google Scholar
• Kang, H. M., and M. E. Saltveit. 2002. Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Plant Physiology 115: 571–576.
   Web of Science ®Google Scholar
• Kazemi, N., R. A. Khavari-Nejad, H. Fahimi, S. Saadatmand, T. Nejad-Sattari. 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. Scientia Horticulturae 126: 402–407.
   Web of Science ®Google Scholar
• Khodary, S. E. A. 2004. Effect of salicylic acid on the growth, photosynthesis and carbohydrate metabolism in salt stressed maize plants. International Journal of Agriculture and Biology 6: 1–4.
   Google Scholar
• Knudson, L. L., T. W. Tibbitts, and G. E. Edwards. 1977. Measurement of ozone injury by determination of leaf chlorophyll concentration. Plant Physiology 60: 606–608.
   PubMed Web of Science ®Google Scholar
• Kong, J., Y. J. Dong, L. L. Xu, S. Liu, and X. Y. Bai. 2013. Role of exogenous nitric oxide in alleviating iron deficiency-induced peanut chlorosis on calcareous soil. Journal of Plant Interactions 9: 450–459.
   Web of Science ®Google Scholar
• Kong, J., Y. J. Dong, L. L. Xu, S. Liu, and X. Y. Bai. 2014a. Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of Arachis hypogaea L. Botanical Studies 55: 9–20.
   PubMed Web of Science ®Google Scholar
• Kong, J., Y. J. Dong, L. L. Xu, S. Liu, and X. Y. Bai. 2014b. Effects of exogenous salicylic acid on alleviating chlorosis induced by iron deficiency in peanut seedlings (Arachis hypogaea L). Journal of Plant Growth Regulation 33: 715–729.
   Web of Science ®Google Scholar
• Lamattina, L., C. Garcia-Mata, M. Graziano, and G. Pagnussat. 2003. Nitric oxide: the versatility of an extensive signal molecule. Annual Review of Plant Physiology and Plant Molecular Biology 54: 109–136.
   PubMed Web of Science ®Google Scholar
• Larkindale, J., and M. R. Knight. 2002. Protection against heat stress induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiology 128: 682–695.
   PubMed Web of Science ®Google Scholar
• Li, S. P., Y. B. Yuan, G. S. Liu, C. L. Liu, Y. Z. Wang, and P. H. Li. 2010. Relationship between salicylic acid and iron in their regulations of the growth of strawberry tissue culture plants. Scientia Agricultura Sinica 43: 2751–2758.
   Google Scholar
• Li, C. J., X. P. Zhu, and F. S. Zhang. 2000. Role of shoot in regulation of iron deficiency responses in cucumber and bean plants. Journal of Plant Nutrition 23: 1809–1818.
   Web of Science ®Google Scholar
• Ma, Y. H., F. W. Ma, J. K. Zhang, M. Y. Li, Y. H. Wang, and D. Liang. 2008. Effects of high temperature on activities and gene expression of enzymes involved in ascorbate-glutathione cycle in apple leaves. Plant Science 175: 761–766.
   Web of Science ®Google Scholar
• Marschner, H. 1995. Mineral Nutrition of Higher Plants, 2nd edn. London: Academic Press, London.
   Google Scholar
• Marschner, H., V. Róheld, and M. Kissel. 1987. Localization of phytosiderophore release and of iron uptake along intact barley roots. Physiologia Plantarum 71: 157–162.
   Web of Science ®Google Scholar
• Mittler, R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7: 405–410.
   PubMed Web of Science ®Google Scholar
• Morales, F., R. Belkhodjia, A. Abadia, and J. Abadfa. 2006. Photosystem IIefficiency and mechanisms of energy dissipation in iron deficient, field-grown pear trees (Pyrus communis L.). Photosynthesis Research 63: 9–21.
   Web of Science ®Google Scholar
• Munne-Bosch, S., and J. Peñuelas. 2003. Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta 217: 758–766.
   PubMed Web of Science ®Google Scholar
• Nickel, K. S., and B. A. Cunningham. 1969. Improved peroxidase assay method using leuco 2,3,6–trichloro indophenol and application to comparative measurements of peroxidase catalysis. Analytical Biochemistry 27: 292–299.
   PubMed Web of Science ®Google Scholar
• Ohinishi, T., R. S. Gall, and M. L. Mayer. 1975. An improved assay of inorganic phosphate in the presence of extralabile phosphate compounds: application to the ATPase assay in the presence of phosphocreatine. Analytical Biochemistry 69: 261–267.
   PubMed Web of Science ®Google Scholar
• Oki, H., S. Kim, H. Nakanishi, M. Takahashi, H. Yamaguchi, S. Mori, and N. K. Nishizawa. 2004. Directed evolution of yeast ferric reductase to produce plants with tolerance to iron deficiency in alkaline soils. Soil Science and Plant Nutrition 50: 1159–1165.
   Web of Science ®Google Scholar
• Palmgren, M. G., and J. F. Harper. 1999. Pumping with plant P-type ATPases. Journal of Experimental Botany 50: 883–893.
   Web of Science ®Google Scholar
• Patra, H. L., M. Kar, and D. Mishre. 1978. Catalase activity in leaves and cotyledons during plant development and senescence. Biochemical Pharmacology 172: 385–390.
   Google Scholar
• Ranieri, A., A. Castagna, B. Baldan, and G. F. Soldatini. 2001. Iron deficiency differently affects peroxidase isoforms in sunflower. Journal of Experimental Botany 52: 25–35.
   PubMed Web of Science ®Google Scholar
• Robinson, N.J., C. M. Procter, E. L. Connolly, and M. L. Guerinot. 1999. A ferric-chelate reductase for iron uptake from soils. Nature 397: 694–697.
   PubMed Web of Science ®Google Scholar
• Santi, S., and W. Schmidt. 2009. Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytologist 183: 1072–1084.
   PubMed Web of Science ®Google Scholar
• Shakirova, F. M., A. R. Sakhbutdinova, M. V. Bezrukova, R. A. Fatkhutdinova, and D. R. Fatkhutdinova. 2003. Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Science 164: 317–322.
   Web of Science ®Google Scholar
• Shen, H. Y., H. C. Xiong, X. T. Guo, and Y. M. Zuo. 2011. Progress of molecular mechanism of iron uptake and translocation in plants. Plant Nutrition and Fertilizer Science 17: 1522–1530.
   Google Scholar
• Shenker, M., and Y. Chen. 2005. Increasing iron availability to crops: fertilizers, organo-fertilizers, and biological approaches. Soil Science and Plant Nutrition 51: 1–17.
   Web of Science ®Google Scholar
• Shi, G. R., Q. S. Cai, Q. Q. Liu, and L.Wu. 2009. Salicylic acid–mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake, photosynthesis, and antioxidant enzymes. Acta Physiologiae Plantarum. 31: 969–977.
   Web of Science ®Google Scholar
• Shi, Q. H., and Z. J. Zhu. 2008. Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environmental and Experimental Botany 63: 317–326.
   Web of Science ®Google Scholar
• Slaymaker, D. H., D. A. Navarre, D. Clark, O. del Pozo, G. B. Martin, and D. F. Klessig. 2002. The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proceedings of the National Academy of Sciences of the United States of America 99: 11640–11645.
   PubMed Web of Science ®Google Scholar
• Stamler, J. S., D. J. Singel, and J. Loscalzo. 1992. Biochemistry of nitric oxide and its Redox-Activated forms. Science 258: 1898–1902.
   PubMed Web of Science ®Google Scholar
• Stewart, R. R., and J. D. Bewley. 1980. Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiology 65: 245–248.
   PubMed Web of Science ®Google Scholar
• Sun, B., Y. Jing, K. Chen, L. Song, F. Chen, and L. Zhang. 2007. Protective effect of nitric oxide on iron deficiency-induced oxidative stress in maize (Zea mays L). Journal of Plant Physiology 164: 536–543.
   PubMed Web of Science ®Google Scholar
• Thoiron, S., N. Pascal, and J. F. Briat. 1997. Impact of iron deficiency and iron re–supply during the early stages of vegetative development in maize (Zea mays L.). Plant Cell and Environment 20: 1051–1060.
   Web of Science ®Google Scholar
• Thomine, S., F. Lelièvre, E. Debarbieux, J. I. Schroeder, and H. Barbier-Brygoo. 2003. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. The Plant Journal 34: 685–695.
   PubMed Web of Science ®Google Scholar
• Vasconcelos, M., H. Eckert, V. Arahana, G. Graef, M. A. Grusak, and T. Clemente. 2006. Molecular and phenotypic characterization of transgenic soybean expressing the Arabidopsis ferric chelate reductase gene, FRO2. Planta 224: 1116–1128.
   PubMed Web of Science ®Google Scholar
• Vicence, M. R. S., and J. Plasencia. 2011. Salicylic acid beyond defence: its role in plant growth and development. Journal of Experimental Botany 62: 3321–3338.
   PubMed Web of Science ®Google Scholar
• Wang, Q, H. X. Liang, Y. J. Dong, L. L. Xu, X. W. Zhang, J. Hou, and Z. Y. Fan. 2013. Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regulation 69: 11–20.
   Web of Science ®Google Scholar
• Watts, R. N., and D. R. Richardson. 2002. The mechanism of nitrogen monoxide (NO)-mediated iron mobilization from cells. NO intercepts iron before incorporation into ferritin and indirectly mobilizes iron from ferritin in a glutathione–dependent manner. European Journal of Biochemistry 269: 3383–3392.
   PubMedGoogle Scholar
• Webb, A. A. R., M. R. McAinsh, J. E. Taylor, and A. M. Hetherington. 1996. Calcium ions as intracellular second messengers in higher plants. Advances in Botanical Research 22: 45–96.
   Web of Science ®Google Scholar
• Wild, J., D. Kley, A. Rockel, P. Rockel, and H. J. Segschneider. 1997. Emission of NO from several higher plant species. Journal of Geophysical Research Atmospheres 102: 5919–5928.
   Web of Science ®Google Scholar
• Winder, T. L., and J. N. Nishio. 1997. Early iron deficiency stress response in leaves of sugar beet. Plant Physiology 108: 1487–1494.
   Web of Science ®Google Scholar
• Wink, D. A., and J. B. Mitchell. 1998. Chemical biology of nitric oxide: Insights into regulatory, cytotoxic and cytoprotective mechanisms of nitric oxide. Free Radical Biology and Medicine 28: 434–456.
   Web of Science ®Google Scholar
• Xu, L. L., Y. J.Dong, J. Kong, S. Liu, Z. Y. Fan, J. Hou, and X. Y. Bai. 2013. Effects of exogenous NO supplied with different approaches on cadmium toxicity in lettuce seedlings. Plant Biosystems 149: 270–279.
   Web of Science ®Google Scholar
• Zhang, X. W., Y. J. Dong, X. K. Qiu, G. Q. Hu, Y. H. Wang, and Q. H. Wang. 2012. Exogenous nitric oxide alleviates iron-deficiency chlorosis in peanut growing on calcareous soil. Plant Soil and Environment 58: 111–120.
   Web of Science ®Google Scholar
• Zhang, X. W., M. Zhang, Q. H. Wang, X. K. Qiu, G. Q. Hu, and Y. J. Dong. 2013. Effect of exogenous nitric oxide on physiological characteristic of peanut under iron-deficient stress. Plant Nutrition and Fertilizer Science 17: 665–673.
   Google Scholar
• Zuo, Y., L. Ren, F. Zhang, and R. F. Jiang. 2007. Bicarbonate concentration as affected by soil water content controls iron nutrition of peanut plants in a calcareous soil. Plant Physiology and Biochemistry 45: 23–36.
   Web of Science ®Google Scholar