Abstract
Iron (Fe), an important micronutrient and a critical determinant of plant growth and human nutrition, is deficient in cultivable soils and limits crop productivity and nutritional quality of food grains. Plants tolerant to Fe deficiency reveal either or all of these i.e., a higher uptake of Fe, better root to shoot partitioning of Fe or a higher remobilization of relatively immobile Fe. The physiological and biochemical regulators of in-plant Fe-remobilization are not clearly understood. The present study was conducted to elucidate the effect of Fe and nitrogen (N) deficiency, either alone or in combination, on plant growth attributes, shoot, root Fe and N uptake and Fe remobilization from a fully developed 2nd older leaf (OL) to a younger developing 3rd leaf (YL) in bread and durum wheat. Dual nutrient deficiency of N and Fe induced senescence, measured in terms of reduced chlorophyll and higher expression of NAM-B1activity. High nitrogen availability reduced Fe translocation as evident from a higher Fe retention in OL under N sufficient treatments (N+Fe+ and N+Fe−) than the N deficient treatments (N−Fe+ and N−Fe−) and could be correlated with transcript level expression of the DMAS gene. The present study provides evidence for the N and Fe deficiency induced senescence as the key determinant of Fe-remobilization in wheat, facilitated by a hyped biosynthesis of phytosiderophore. The results indicate that any favourable manipulation or selection for higher Fe remobilization process could improve nutrient deficiency tolerance of wheat and aid in grain biofortification.
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References
Abdallah M, Dubousset L, Meuriot F, Etienne P, Avice JC, Ourry A (2010) Effect of mineral sulphur availability on nitrogen and sulphur uptake and remobilization during the vegetative growth of Brassica napus L. J Exp Bot 61(10):2635–2646
Aciksoz SB, Yazici A, Ozturk L, Cakmak I (2011) Biofortification of wheat with iron through soil and foliar application of nitrogen and iron fertilizers. Plant Soil 349(1–2):215–225
Agüera E, Cabello P, De La Haba P (2010) Induction of leaf senescence by low nitrogen nutrition in sunflower (Helianthus annuus) plants. Physiol Plant 138(3):256–267
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24(1):1
Asplund L, Bergkvist G, Leino MW, Westerbergh A, Weih M (2013) Swedish spring wheat varieties with the rare high grain protein allele of NAM-B1 differ in leaf senescence and grain mineral content. PLOS One 8(3):59704
Avice JC, Etienne P (2014) Leaf senescence and nitrogen remobilization efficiency in oilseed rape (Brassica napus L.). J Exp Bot 65(14):3813–3824
Barunawati N, HettwerGiehl RF, Bauer B, Von Wirén N (2013) The influence of inorganic nitrogen fertilizer forms on micronutrient retranslocation and accumulation in grains of winter wheat. Front Plant Sci 4:320
Bashir K, Inoue H, Nagasaka S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. J Biol Chem 281(43):32395–32402
Beasley JT, Bonneau JP, Johnson AA (2017) Characterisation of the nicotianamine aminotransferase and deoxymugineic acid synthase genes essential to Strategy II iron uptake in bread wheat (Triticum aestivum L.). PLOS One 12(5)
Briat JF, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends Plant Sci 20(1):33–40
Cakmak I, Pfeiffer WH, McClafferty B (2010) Review: biofortification of durum wheat with zinc and iron. Cereal Chem 87(1):10–20
Christiansen MW, Gregersen PL (2014) Members of the barley NAC transcription factor gene family show differential co-regulation with senescence-associated genes during senescence of flag leaves. J Exp Bot 65:4009–4022
Davies PJ, Gan S (2012) Towards an integrated view of monocarpic plant senescence. Russ J Plant Physiol 59(4):467–478
De Benoist B, McLean E, Egli I, Cogswell M, Cogswell M (2008) WHO global database on anaemia. WHO, Geneva, pp 1993–2005
Distelfeld A, Avni R, Fischer AM (2014) Senescence, nutrient remobilization, and yield in wheat and barley. J Exp Bot 65(14):3783–3798
Gan S, Amasino RM (1997) Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). Plant Physiol 113(2):313
Giehl RF, von Wirén N (2014) Root nutrient foraging. Plant Physiol 166(2):509–517
Grillet L, Mari S, Schmidt W (2014) Iron in seeds—loading pathways and subcellular localization. Front Plant Sci 4:535
Hiscox JT, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57(12):1332–1334
Khobra R, Singh B (2017) Phytosiderophore release in relation to multiple micro nutrient metal deficiency in wheat. J Plant Nutr 41(6):679–688
Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS lett 581(12):2273–2280
Kjeldahl J (1883) A new method for the determination of nitrogen in organic matter. Am J Analyt Chem 22(1):366–382
Köster J, Shi R, Von Wiren N, Weber G (2011) Evaluation of different column types for the hydrophilic interaction chromatographic separation of iron-citrate and copper-histidine species from plants. J Chromatogr A 1218(30):4934–4943
Kutman UB, Kutman BY, Ceylan Y, Ova EA, Cakmak I (2012) Contributions of root uptake and remobilization to grain zinc accumulation in wheat depending on post-anthesis zinc availability and nitrogen nutrition. Plant Soil 361(1–2):177–187
Pearce S, Tabbita F, Cantu D, Buffalo V, Avni R, Vazquez-Gross H, Dubcovksy J (2014) Regulation of Zn and Fe transporters by the GPC1 gene during early wheat monocarpic senescence. BMC Plant Biol 14(1):1
Pfaffl MW (2004) Quantification strategies in real-time PCR. AZ Quant PCR 1:89–113
Rengel Z, Graham RD (1996) Uptake of zinc from chelate-buffered nutrient solutions by wheat genotypes differing in zinc efficiency. J Exp Bot 47(2):217–226
Shi R, Weber G, Köster J, Reza-Hajirezaei M, Zou C, Zhang F, von Wirén N (2012) Senescence-induced iron mobilization in source leaves of barley (Hordeumvulgare) plants. New Phytol 195(2):372–383
Shiferaw B, Smale M, Braun HJ, Duveiller E, Reynolds M, Muricho G (2013) Crops that feed the world 10. Past successes and future challenges to the role played by wheat in global food security. Food Secur 5(3):291–317
Shojima S, Nishizawa NK, Fushiya S, Nozoe S, Irifune T, Mori S (1990) Biosynthesis of phytosiderophores in vitro biosynthesis of 2′-deoxymugineic acid from L-methionine and nicotianamine. Plant Physiol 93(4):1497–1503
Shukla AK, Tiwari PK, Prakash C (2014) Micronutrients deficiencies vis-a-vis food and nutritional security of India. Indian J Fertil 10(12):94–112
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314(5803):1298–1301
Waters BM, Uauy C, Dubcovsky J, Grusak MA (2009) Wheat (Triticum aestivum) NAM proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain. J Exp Bot 60(15):4263–4274
White PJ, Broadley MR (2011) Physiological limits to zinc biofortification of edible crops. Front Plant Sci 2:80
Zhang FS, Römheld V, Marschner H (1991) Diurnal rhythm of release of phytosiderophores and uptake rate of zinc in iron-deficient wheat. J Soil Sci Plant Nutr 37(4):671–678
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SP acknowledges funding support in terms of ICAR scholarship for the Masters program.
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Parveen, S., Ranjan, R.K., Anand, A. et al. Combined deficiency of nitrogen and iron increases senescence induced remobilization of plant immobile iron in wheat. Acta Physiol Plant 40, 211 (2018). https://doi.org/10.1007/s11738-018-2782-9
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DOI: https://doi.org/10.1007/s11738-018-2782-9