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NaCl alleviates iron deficiency through facilitating root cell wall iron reutilization and its translocation to the shoot in Arabidopsis thaliana

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Abstract

Aims

The present study was undertaken to investigate the mechanism underlying NaCl-alleviated Fe (iron) deficiency in Arabidopsis thaliana Col-0 (Columbia ecotype).

Methods

Six-week-old Col-0 with rosettes of similar diameters was grown in full-strength nutrient solution lacking Fe (Fe-deficient) or full-strength nutrient solution (Fe-sufficient) with or without 10 mM NaCl for 7 days. Roots were then harvested for analysis of total Fe content, soluble Fe concentration, and abscisic acid (ABA) content as well as for cell wall and RNA extraction, while shoots were harvested for total Fe content and soluble Fe concentration measurements.

Results

The total Fe content and the soluble Fe concentration were higher in roots and shoots of −Fe + NaCl-treated plants than −Fe-treated plants, whereas Fe retention in the cell wall was reduced, suggesting the presence of a cell wall Fe-reutilization mechanism. This conclusion was confirmed by the observation that less hemicelluloses Fe was found in plants under −Fe + NaCl treatment. In addition, associated to the upregulation of genes related to the long-distance transport of Fe, such as FRD3 (FERRIC REDUCTASE DEFECTIVE3), YSL2 (YELLOW STRIPE-LIKE), and NAS1 (NICOTIANAMINE SYNTHASE1) under −Fe + NaCl treatment, more Fe was available in shoots. Furthermore, endogenous ABA is involved in NaCl-alleviated Fe deficiency, as the addition of Flu (fluridone), an inhibitor of ABA biosynthesis, abolished the positive effect of NaCl on Fe deficiency.

Conclusions

Under −Fe condition, NaCl not only is involved in the reutilization of cell wall Fe but also participates in the translocation of Fe from root to shoot in Arabidopsis, partially through its effect on ABA contents.

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References

  • Ali L, Rahmatullah, Ranjha AM, Aziz T, Maqsood MA, Ashraf M (2006) Differential potassium requirement and its substitution by sodium in cotton genotypes. Pak J Agric Sci 43:3–4

    Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    Article  CAS  PubMed  Google Scholar 

  • Anderegg G, Ripperger H (1989) Correlation between metal complex formation and biological activity of nicotianamine analogues. J Chem Soc Chem Commun 10:647–650

    Article  Google Scholar 

  • Battie-Laclau P, Laclau J-P, Piccolo MC, Arenque BC, Beri C, Mietton L, Muniz MRA, Jordan-Meille L, Buckeridge MS, Nouvellon Y, Ranger J, Bouillet JP (2013) Influence of potassium and sodium nutrition on leaf area components in Eucalyptus grandis trees. Plant Soil 371:19–35

    Article  CAS  Google Scholar 

  • Bernstein N, Shoresh M, Xu Y, Huang B (2010) Involvement of the plant antioxidative response in the differential growth sensitivity to salinity of leaves vs roots during cell development. Free Radical Bio Med 49:1161–1171

    Article  CAS  Google Scholar 

  • Box S, Schachtman DP (2000) The effect of low concentrations of sodium on potassium uptake and growth of wheat. Funct Plant Biol 27:175–182

    Article  CAS  Google Scholar 

  • Brown JC, Ambler JE (1973) “Reductants” released by roots of Fe-deficient soybeans. Agron J 65:311–314

    Article  CAS  Google Scholar 

  • Brownell PF, Crossland CJ (1972) The requirement for sodium as a micronutrient by species having the C4 dicarboxylic photosynthetic pathway. Plant Physiol 49:794–797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conde A, Silva P, Agasse A, Conde C, Geros H (2011) Mannitol transport and mannitol dehydrogenase activities are coordinated in Olea europaea under salt and osmotic stresses. Plant Cell Physiol 52:1766–1775

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Bio 6:850–861

    Article  CAS  Google Scholar 

  • Curie C, Briat JF (2003) Iron transport and signaling in plants. Annu Rev Plant Biol 54:183–206

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349

    Article  CAS  PubMed  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegen F (2000) Dual action of the active oxygen species during plant stress responses. CMLS 57:779–995

    Article  CAS  PubMed  Google Scholar 

  • DeCosta W, Zörb C, Hartung W, Schubert S (2007) Salt resistance is determined by osmotic adjustment and abscisic acid in newly developed maize hybrids in the first phase of salt stress. Physiol Plant 131:311–321

    CAS  Google Scholar 

  • DiDonato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414

    Article  CAS  PubMed  Google Scholar 

  • Ding Z, Li S, An X, Liu X, Qin H, Wang D (2009) Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Genet Genomics 36:17–29

    Article  CAS  PubMed  Google Scholar 

  • Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci U S A 93:5624–5628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gattward JN, Almeida AAF, Souza JO, Gomes FP, Kronzucker HJ (2012) Sodium-potassium synergism in Theobroma cacao: stimulation of photosynthesis, water-use efficiency and mineral nutrition. Physiol Plant 146:350–362

    Article  CAS  PubMed  Google Scholar 

  • Green LS, Rogers EE (2004) FRD3 controls iron localization in Arabidopsis thaliana. Plant Physiol 136:2523–2531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerinot ML, Yi Y (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104:815–820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51:463–499

    Article  CAS  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    Article  CAS  PubMed  Google Scholar 

  • He JY, Zhu C, Ren YF, Yan YP, Cheng C, Jiang DA, Sun ZX (2008) Uptake, subcellular distribution, and chemical forms of cadmium in wild-type and mutant rice. Pedosphere 18:371–377

    Article  CAS  Google Scholar 

  • Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa NK, Mori S (1999) Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol 119:471–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin CW, You GY, He YF, Tang CX, Wu P, Zheng SJ (2007) Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiol 144:278–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SA, Punshon T, Lanzirotti A, Li LT, Alonso JM, Ecker JR, Guerinot L (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314:1295–1298

    Article  CAS  PubMed  Google Scholar 

  • Klatte M, Schuler M, Wirtz M, Straube CF, Hell R, Bauer P (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150:257–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kravchik M, Bernstein N (2013) Effects of salinity on the transcriptome of growing maize leaf cells point at cell-age specificity in the involvement of the antioxidative response in cell growth restriction. BMC Genomics 14:1

    Article  Google Scholar 

  • Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C, Neumann D, Thomine S (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei GJ, Zhu XF, Wang ZW, Dong F, Dong NY, Zheng SJ (2014) Abscisic acid alleviates iron deficiency by promoting root iron reutilization and transport from root to shoot in Arabidopsis. Plant Cell Environ 37:852–863

    Article  CAS  PubMed  Google Scholar 

  • Li BH, Li Q, Xiong LM, Kronzucker HJ, Kramer U, Shi WM (2012) Arabidopsis plastid AMOS1/EGY1 integrates abscisic acid signaling to regulate global gene expression response to ammonium stress. Plant Physiol 160:2040–2051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma JF, Zheng SJ, Hiradate S, Matsumoto H (1997) Detoxifying aluminum with buckwheat. Nature 390:569–570

    Article  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Munns R, Tester M (2008) Mechanism of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Murgia I, Vazzola V, Tarantino D, Cellier F, Ravet K, Briat JF, Sovae C (2007) Knock-out of ferritin AtFer1 causes earlier onset of age-dependent leaf senescence in Arabidopsis. Plant Physiol Biochem 45:898–907

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  CAS  PubMed  Google Scholar 

  • Neves-Piestun BG, Bernstein N (2005) Salinity-induced changes in the nutritional status of expanding cells may impact leaf growth inhibition in maize. Funct Plant Biol 32:141–152

    Article  CAS  Google Scholar 

  • Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57:1017–1023

    Article  CAS  PubMed  Google Scholar 

  • Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric chelate reductase for iron uptake from soils. Nature 397:694–697

    Article  CAS  PubMed  Google Scholar 

  • Rogers EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14:1787–1799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roschzttardtz H, Séguéla-Arnaud M, Briat JF, Vert G, Curie C (2011) The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell 23:2725–2737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Römheld V, Marschner H (1981) Iron deficiency stress induced morphological and physiological changes in root tips of sunflower. Plant Physiol 53:354–360

    Article  Google Scholar 

  • Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084

    Article  CAS  PubMed  Google Scholar 

  • Schmohl N, Horst WJ (2000) Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cells grown in suspension culture. Plant Cell Environ 23:735–742

    Article  CAS  Google Scholar 

  • Seo M, Peeters AJ, Koiwai H, Oritani T, Marion-Poll A, Zeevaart JA, Koornneef M, Kamiya Y, Koshiba T (2000) The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proc Natl Academy Sci USA 97:12908–12913

    Article  CAS  Google Scholar 

  • Singh NK, Larosa PC, Handa AK, Hasegawa PM, Bressan RA (1987) Hormonal regulation of protein synthesis associated with salt tolerance in plant cells. Proc Natl Acad Sci U S A 84:739–743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singleton VL, Rossi JAJ (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Viticult 16:144–158

    CAS  Google Scholar 

  • Sivakumar P, Sharmila P, Saradhi PP (2000) Proline alleviates salt-stress-induced enhancement in ribulose-1, 5-bisphosphate oxygenase activity. Biochem Biophys Res Commun 279:512–515

    Article  CAS  PubMed  Google Scholar 

  • Taiz L, Zeiger E (2010) Plant physiol. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Thomine S, Lelièvre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695

    Article  CAS  PubMed  Google Scholar 

  • Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters BM, Chu HH, DiDonato RJ, Roberts LA, Eisley RB, Lahner B, Walker EL (2006) Mutations in Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141:1446–1458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woolley JT (1957) Sodium and silicon as nutrients for the tomato plant. Plant Physiol 32:317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong L, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13:2063–2083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong L, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang JL, Chen WW, Chen LQ, Qin C, Jin CW, Shi YZ, Zheng SJ (2013) The 14-3-3 protein GENERAL REGULATORY FACTOR11 (GRF11) acts downstream of nitric oxide to regulate iron acquisition in Arabidopsis thaliana. New Phytol 197:815–824

    Article  CAS  PubMed  Google Scholar 

  • Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF (2009) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol 149:297–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshino M, Murakami K (1998) Interaction of iron with polyphenolic compounds: application to antioxidant characterization. Anal Biochem 257:40–44

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka T, Endo T, Satoh S (1998) Restoration of seed germination at supraoptimal temperatures by fluridone, an inhibitor of abscisic acid biosynthesis. Plant Cell Physiol 39:307–312

    Article  CAS  Google Scholar 

  • Zhu C, Schraut D, Hartung W, Schäffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56:2971–2981

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  CAS  PubMed  Google Scholar 

  • Zhu XF, Shi YZ, Lei GJ, Fry SC, Zhang BC, Zhou YH, Zheng SJ (2012a) XTH31, encoding an in vitro XEH/XET-active enzyme, regulates aluminum sensitivity by modulating in vivo XET action, cell wall xyloglucan content, and aluminum binding capacity in Arabidopsis. Plant Cell 24:4731–4747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu XF, Lei GJ, Jiang T, Liu Y, Li GX, Zheng SJ (2012b) Cell wall polysaccharides are involved in P-deficiency-induced Cd exclusion in Arabidopsis thaliana. Planta 236:989–997

    Article  CAS  PubMed  Google Scholar 

  • Zhu XF, Wang ZW, Wan JX, Sun Y, Wu YR, Li GX, Shen RF, Zheng SJ (2015) Pectin enhances rice (Oryza sativa) root phosphorus remobilization. J Exp Bot 66:1017–1024

    Article  CAS  PubMed  Google Scholar 

  • Zhu XF, Wang B, Song WF, Zheng SJ, Shen RF (2016) Putrescine alleviates iron deficiency via NO-dependent reutilization of root cell-wall Fe in Arabidopsis. Plant Physiol 170:558–567

    Article  CAS  PubMed  Google Scholar 

  • Zörb C, Geilfus CM, Mühling KH, Ludwig-Müller J (2013) The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J Plant Physiol 170:220–224

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was funded by the National Key Basic Research Program of China (No. 2014CB441000) and “Strategic Priority Research Program” of the Chinese Academy of Sciences (Nos. XDB15030302 and XDB15030202). We thank three anonymous reviewers for their valuable comments to improve the quality of our work.

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  1. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Xiao Fang Zhu, Qi Wu, Lu Zheng & Ren Fang Shen

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Qi Wu

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  1. Xiao Fang Zhu
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Correspondence to Ren Fang Shen.

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Zhu, X.F., Wu, Q., Zheng, L. et al. NaCl alleviates iron deficiency through facilitating root cell wall iron reutilization and its translocation to the shoot in Arabidopsis thaliana . Plant Soil 417, 155–167 (2017). https://doi.org/10.1007/s11104-017-3248-3

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