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Glutathione supplementation prevents iron deficiency in Medicago scutellata grown in rock sand under different levels of bicarbonate

  • Zahra Gheshlaghi
  • Reza KhorassaniEmail author
  • Javier Abadía
  • Ana Alvarez-Fernández
  • Adrián Luis-Villarroya
  • Amir Fotovat
  • Mohammad Kafi
Regular Article

Abstract

Background and aims

The effects of root glutathione (GSH) supplementation on leaf chlorophyll, Fe concentrations and contents in leaves, stems and roots, and traits associated to Fe deficiency were studied in Medicago scutellata plants grown in rock sand under conditions of Fe deficiency, in the presence of different concentrations of bicarbonate.

Methods

Plants were grown in acid-washed rock sand irrigated with a zero Fe solution (pH 7.8 with 0.5 g L−1 CaCO3) or a 45 μM Fe(III)-EDDHA solution (5 mM MES, pH 5.5), with 0, 5 or 15 mM NaHCO3, and 250 mL of 1 mM GSH was added daily to half of the pots.

Results

Iron deficiency caused characteristic symptoms in plants, with GSH supplementation relieving them. Glutathione supplementation led to increases in total Fe, chlorophyll and leaf total and extractable Fe, whereas root Fe concentrations decreased. Traits associated to Fe deficiency, including changes in biomass, root morphology, carboxylate contents and antioxidant parameters became less intense with GSH supplementation.

Conclusions

Glutathione supplementation allowed plants to take up Fe from the rock sand via a reductive solubilization mechanism. Also, the distribution of Fe within the plant changed, with more Fe being allocated to the shoot tissues and less to the roots.

Keywords

Iron Iron chlorosis Iron oxides Root fertilisation Legumes 

Abbreviations

Chl

Chlorophyll

GSH

Glutathione

SPAD

Soil-Plant Analyses Development

Notes

Acknowledgements

Authors acknowledge the support of the Department of Soil Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran. This work was part of the research project on M. scutellata 3/41380. Support was obtained by the Spanish State Research Agency (project AGL2016-75226-R, AEI/FEDER, EU). Authors thank Cristina Ortega Palmeiro for help with the Fe(III)-oxide solubilization experiments with the Olis spectrophotometer.

Supplementary material

11104_2019_4314_MOESM1_ESM.docx (1.8 mb)
ESM 1 (DOCX 1812 kb)

References

  1. Abadía J, Monge E, Montañés L, Heras L (1984) Extraction of iron from plant leaves by Fe (II) chelators. J Plant Nutr 7:777–784CrossRefGoogle Scholar
  2. Abadía J, López-Millán A-F, Rombolà A, Abadía A (2002) Organic acids and Fe deficiency: a review. Plant Soil 241:75–86CrossRefGoogle Scholar
  3. Abadía J, Vázquez S, Rellán-Álvarez R, El-Jendoubi H, Abadía A, Álvarez-Fernández A, López-Millán A-F (2011) Towards a knowledge-based correction of iron chlorosis. Plant Physiol Biochem 49:471–482PubMedCrossRefPubMedCentralGoogle Scholar
  4. Akram S, Siddiqui MN, Hussain BMN, Bari MAA, Mostofa MG, Hossain MA, Tran LSP (2017) Exogenous glutathione modulates salinity tolerance of soybean [Glycine max (L.) Merrill] at reproductive stage. J Plant Growth Regul 36:877–888CrossRefGoogle Scholar
  5. Alhendawi RA (2011) Comparisons between effects of bicarbonate and high pH on iron uptake, FeIII reducing capacity of the roots, PEP carboxylase activity, organic acid composition and cation-anion balance of the xylem sap of maize seedlings. Am J Plant Nutr Fertiliz Technol 1:36–47CrossRefGoogle Scholar
  6. Álvarez-Fernández A, Paniagua P, Abadía J, Abadía A (2003) Effects of Fe deficiency chlorosis on yield and fruit quality in peach (Prunus persica L. Batsch). J Agric Food Chem 51:5738–5744PubMedCrossRefPubMedCentralGoogle Scholar
  7. Álvarez-Fernández A, Melgar JC, Abadía J, Abadía A (2011) Effects of moderate and severe iron deficiency chlorosis on fruit yield, appearance and composition in pear (Pyrus communis L.) and peach (Prunus persica L. Batsch). Environ Exp Bot 71:280–286CrossRefGoogle Scholar
  8. Álvarez-Parrilla E, de la Rosa LA, Amarowicz R, Shahidi F (2011) Antioxidant activity of fresh and processed Jalapeño and Serrano peppers. J Agric Food Chem 59:163–173PubMedCrossRefPubMedCentralGoogle Scholar
  9. Amirbahman A, Sigg L, von Gunten U (1997) Reductive dissolution of Fe(III) (hydr)oxides by cysteine: kinetics and mechanism. J. Colloid Interf Sci 194:194–206CrossRefGoogle Scholar
  10. Andaluz S, Rodríguez-Celma J, Abadía A, Abadía J, López-Millán A-F (2009) Time course induction of several key enzymes in Medicago truncatula roots in response to Fe deficiency. Plant Physiol Biochem 47:1082–1088PubMedCrossRefPubMedCentralGoogle Scholar
  11. AOAC (2000) Official methods of analysis. Association of Analytical Chemists, Washington, p 334Google Scholar
  12. Arias-Baldrich C, Bosch N, Begines D, Feria AB, Monreal JA, García-Mauriño S (2015) Proline synthesis in barley under iron deficiency and salinity. J Plant Physiol 183:121–129PubMedCrossRefPubMedCentralGoogle Scholar
  13. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15PubMedPubMedCentralCrossRefGoogle Scholar
  14. Astolfi S, Pii Y, Terzano R, Mimmo T, Celletti S, Allegretta I, Lafiandra D, Cesco S (2018) Does Fe accumulation in durum wheat seeds benefit from improved whole-plant sulfur nutrition? J Cereal Sci 83:74–82CrossRefGoogle Scholar
  15. Bardsley CE, Lancaster JD (1962) Determination of reserve Sulphur and soluble sulphate in soils. Soil Sci Soc Am Proc 24:265–268CrossRefGoogle Scholar
  16. Barreira JCM, Visnevschi-Necrasov T, Nunes E, Cunha SC, Pereira G, Oliveira MBPP (2015) Medicago spp. as potential sources of bioactive isoflavones: characterization according to phylogenetic and phenologic factors. Phytochemistry 116:230–238PubMedCrossRefPubMedCentralGoogle Scholar
  17. Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  18. Batth R, Jain M, Kumari S, Mustafiz A (2017) Glyoxalase system: a glutathione-dependent pathway for abiotic stress tolerance in plants. In: Glutathione in plant growth, development, and stress tolerance. Springer International Publishing, Cham, pp 235–263CrossRefGoogle Scholar
  19. Bauhus J, Messier C (1999) Evaluation of fine root length and diameter measurements obtained using RHIZO image analysis. Agron J 91:142–147CrossRefGoogle Scholar
  20. Ben Abdallah H, Mai HJ, Álvarez-Fernández A, Abadía J, Bauer P (2017) Natural variation reveals contrasting abilities to cope with alkaline and saline soil among different Medicago truncatula genotypes. Plant Soil 418:45–60CrossRefGoogle Scholar
  21. Benton-Jones J, Wolf B, Mills HA (1991) Plant analysis handbook: a practical sampling, preparation, analysis, and interpretation guide. Micro-Macro-Publishing, AthensGoogle Scholar
  22. Bonneville S, Van Cappellen P, Behrends T (2004) Microbial reduction of iron(III) oxyhydroxides: effects of mineral solubility and availability. Chem Geol 212:255–268CrossRefGoogle Scholar
  23. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedPubMedCentralCrossRefGoogle Scholar
  24. Briat JF, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends Plant Sci 20:33–40PubMedCrossRefPubMedCentralGoogle Scholar
  25. Carlberg I, Mannervik B (1985) Glutathione reductase. Meth Enzymol 113:484–490PubMedCrossRefPubMedCentralGoogle Scholar
  26. Celletti S, Paolacci AR, Mimmo T, Pii Y, Cesco S, Ciaffi M, Astolfi S (2016) The effect of excess sulfate supply on iron accumulation in three graminaceous plants at the early vegetative phase. Environ Exp Bot 128:31–38CrossRefGoogle Scholar
  27. Cheng MC, Ko K, Chang WL, Kuo WC, Chen GH, Lin TP (2015) Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant J 83:926–939PubMedCrossRefPubMedCentralGoogle Scholar
  28. Connorton JM, Balk J, Rodríguez-Celma J (2017) Iron homeostasis in plants. A brief overview Metallomics 9:813–823PubMedPubMedCentralGoogle Scholar
  29. El Jendoubi H, Melgar JC, Álvarez-Fernández A, Sanz M, Abadía A, Abadía J (2011) Setting good practices to assess the efficiency of iron fertilizers. Plant Physiol Biochem 49:483–488PubMedCrossRefPubMedCentralGoogle Scholar
  30. Farag MA, Hufman D, Lei Z, Summer LW (2007) Metabolic profiling and systematic identification of flavonoids and isoflavonoids in roots and cell cultures of Medicago truncatula using HPLC–UV–ESI-MS and GC–MS. Phytochemistry 68:342–354PubMedCrossRefPubMedCentralGoogle Scholar
  31. Filippou P, Antoniou C, Yelamanchili S, Fotopoulos V (2012) NO loading: efficiency assessment of five commonly used application methods of sodium nitroprusside in Medicago truncatula plants. Plant Physiol Biochem 60:115–118PubMedCrossRefPubMedCentralGoogle Scholar
  32. Frendo P, Gallesi D, Turnbull R, Van de Sype G, Hérouart D, Puppo A (1999) Localization of glutathione and homoglutathione in Medicago truncatula is correlated to a differential expression of genes involved in their synthesis. Plant J 17:215–219CrossRefGoogle Scholar
  33. Gao Y, Tian Q, Zhang WH (2014) Systemic regulation of sulfur homeostasis in Medicago truncatula. Planta 239:79–96PubMedCrossRefPubMedCentralGoogle Scholar
  34. Gheshlaghi Z, Khorassani R, Abadía J, Kafi M, Fotovat A (2019) Glutathione foliar fertilisation prevents lime-induced iron chlorosis in soil grown Medicago scutellata. J Plant Nutr Soil Sci, in press (doi:  https://doi.org/10.1002/jpln.2018006692)
  35. Ghorbani M (2013) The economic geology of Iran. Springer, Mineral deposits and natural resourcesCrossRefGoogle Scholar
  36. Goławska S, Łukasik I, Kapusta T, Janda B (2010) Analysis of flavonoids content in alfalfa Ecol Chem En A 17:261–267Google Scholar
  37. Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plant 23:249–268CrossRefGoogle Scholar
  38. Heidari M, Sarani S (2012) Growth, biochemical components and ion content of chamomile (Matricaria chamomilla L.) under salinity stress and iron deficiency. J Saudi Soc Agric Sci 11:37–42Google Scholar
  39. Herrmann KM (1995) The shikimate pathway as an entry to aromatic secondary metabolism. Plant Physiol 107:2–7CrossRefGoogle Scholar
  40. Hindt MN, Guerinot ML (2012) Getting a sense for signals: regulation of the plant iron deficiency response. Biochim Biophys Acta 1823:1521–1530PubMedPubMedCentralCrossRefGoogle Scholar
  41. Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, de Stefano M, Delledonne M, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602PubMedCrossRefPubMedCentralGoogle Scholar
  42. Jelali N, Wissal M, Dell’Orto M, Abdelly C, Gharsalli M, Zocchi G (2010) Changes of metabolic responses to direct and induced Fe deficiency of two Pisum sativum cultivars. Environ Exp Bot 68:238–246CrossRefGoogle Scholar
  43. Jiménez S, Morales F, Abadía A, Abadía J, Moreno MA, Gogorcena Y (2009) Elemental 2-D mapping and changes in leaf iron and chlorophyll in response to iron re-supply in iron-deficient GF 677 peach-almond hybrid. Plant Soil 315:93–106CrossRefGoogle Scholar
  44. Karimi E, Oskoueian E, Oskoueian A, Omidvar V, Hendra R, Nazeran H (2013) Insight into the functional and medicinal properties of Medicago sativa (alfalfa) leaves extract. J Med Plants Res 7:290–297Google Scholar
  45. Katyal JC, Sharma BD (1984) Some modification in the assay of Fe2+ in 1-10, o-phenanthroline extracts of fresh plant tissues. Plant Soil 79:449–450CrossRefGoogle Scholar
  46. Koen E, Szymańska K, Klinguer A, Dobrowolska G, Besson-Bard A, Wendehenne D (2012) Nitric oxide and glutathione impact the expression of iron uptake- and iron transport-related genes as well as the content of metals in A. thaliana plants grown under iron deficiency. Plant Signal Behav 7:1246–1250PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kovacs I, Durner J, Lindermayr C (2015) Crosstalk between nitric oxide and glutathione is required for NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol 208:860–872PubMedCrossRefPubMedCentralGoogle Scholar
  48. Kovacs I, Holzmeister C, Wirtz M, Geerlof A, Fröhlich T, Römling G, Kuruthukulangarakoola GT, Linster E, Hell R, Arnold GJ, Durner J, Lindermayr C (2016) ROS-mediated inhibition of S-nitrosoglutathione reductase contributes to the activation of antioxidative mechanisms. Front Plant Sci 10:1669Google Scholar
  49. Ksouri R, M’rah S, Gharsalli M, Lachaâl M (2006) Biochemical responses to true and bicarbonate-induced iron deficiency in grapevine genotypes. J. Plant Nutr 29:305–315CrossRefGoogle Scholar
  50. Lindsay WL, Schwab AP (1982) The chemistry of iron in soils and its availability to plants. J Plant Nutr 5:821–840CrossRefGoogle Scholar
  51. Liu C, Zachara JM, Foster NS, Strickland J (2007) Kinetics of reductive dissolution of hematite by bioreduced anthraquinone-2,6-disulfonate. Environ Sci Technol 41:7730–7735PubMedCrossRefPubMedCentralGoogle Scholar
  52. López-Millán AF, Morales F, Gogorcena Y, Abadía A, Abadía J (2001a) Iron resupply-mediated deactivation of root responses to iron deficiency in sugar beet. Aust J Plant Physiol 28:171–180Google Scholar
  53. López-Millán A-F, Morales F, Abadía A, Abadía J (2001b) Changes induced by Fe deficiency and Fe resupply in the organic acid metabolism of sugar beet (Beta vulgaris) leaves. Physiol Plant 112:31–38PubMedCrossRefPubMedCentralGoogle Scholar
  54. Lucena JJ (2003) Fe chelates for remediation of Fe chlorosis in strategy I plants. J Plant Nutr 26:1969–1984CrossRefGoogle Scholar
  55. Luwe M, Takahama U, Heber U (1993) Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacia oleracea L.) leaves. Plant Physiol 101:969–976PubMedPubMedCentralCrossRefGoogle Scholar
  56. M’sehli W, Youssfi S, Donnini S, Dell'Orto M, De Nisi P, Zocchi G, Abdelly C, Gharsalli M (2008) Root exudation and rhizosphere acidification by two lines of Medicago ciliaris in response to lime-induced iron deficiency. Plant Soil 312:151–162CrossRefGoogle Scholar
  57. M’sehli W, Dell’Orto M, De Nisi P, Donnini S, Abdelly C, Zocchi G, Gharsalli M (2009a) Responses of two ecotypes of Medicago ciliaris to direct and bicarbonate-induced iron deficiency conditions. Acta Physiol Plant 31:667–673CrossRefGoogle Scholar
  58. M’sehli W, Dell’Orto M, Donnini S, De Nisi P, Zocchi G, Abdelly C, Gharsalli M (2009b) Variability of metabolic responses and antioxidant defence in two lines of Medicago ciliaris to Fe deficiency. Plant Soil 320:219–230CrossRefGoogle Scholar
  59. M’sehli W, Houmani H, Donnini S, Zocchi G, Abdelly C, Gharsalli M (2014) Iron deficiency tolerance at leaf level in Medicago ciliaris plants. Am J Plant Sci 05:2541–2553CrossRefGoogle Scholar
  60. Marschner P (2012) Marschner’s Mineral Nutrition of Higher Plants, Ed. 3. Academic Press, San DiegoCrossRefGoogle Scholar
  61. Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M (1999) Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol 121:879–888PubMedPubMedCentralCrossRefGoogle Scholar
  62. May M, Vernoux T, Leaver C, Van Montagu M, Inze’D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49: 649–667Google Scholar
  63. Medina-Juarez LA, Molina-Quijada DMA, Del-Toro-Sánchez CL, González-Aguilar GA, Gámez-Meza N (2012) Antioxidant activity of peppers (Capsicum annuum L.) extracts and characterization of their phenolic constituents. Interciencia 37:588–593Google Scholar
  64. Mollering H (1985) L-malate. In: Methods of Enzymatic Analysis (Bergmeyer HU, ed.), 3rd ed., Vol. VII, pp. 39–47, VCH Publishers (UK) Ltd., Cambridge, UKGoogle Scholar
  65. Msilini N, Attia H, Rabhi M, Karray N, Lachaâl M, Ouerghi Z (2012) Responses of two lettuce cultivars to iron deficiency. Exp Agric 48:523–535CrossRefGoogle Scholar
  66. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015a) Glutathione-induced drought stress tolerance in mung bean: coordinated roles of the antioxidant defence and methylglyoxal detoxification systems. AoB Plants 7:plv069PubMedPubMedCentralCrossRefGoogle Scholar
  67. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015b) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54CrossRefGoogle Scholar
  68. Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  69. Nikolic M, Römheld V (2002) Does high bicarbonate supply to roots change availability of iron in the leaf apoplast? Plant Soil 241:67–74CrossRefGoogle Scholar
  70. Pérez-Sanz A, Lucena JJ (1995) Synthetic iron oxides as sources of Fe in a hydroponic culture of sunflower. In: Iron Nutrition in Soils and Plants 241–246 (Abadía J ed.), Kluwer Academic Publishers, The NetherlandsGoogle Scholar
  71. Rabhi M, Barhoumi Z, Ksouri R, Abdelly C, Gharsalli M (2007) Interactive effects of salinity and iron deficiency in Medicago ciliaris. C R Biol 330:779–788PubMedCrossRefPubMedCentralGoogle Scholar
  72. Ramírez L, Bartoli CG, Lamattina L (2013) Glutathione and ascorbic acid protect Arabidopsis plants against detrimental effects of iron deficiency. J Exp Bot 64:3169–3178PubMedCrossRefPubMedCentralGoogle Scholar
  73. Rellán-Álvarez R, Hernández LE, Abadía J, Álvarez-Fernández A (2006) Direct and simultaneous determination of reduced and oxidized glutathione and homoglutathione by liquid chromatography-electrospray/mass spectrometry in plant tissue extracts. Anal Biochem 356:254–264PubMedCrossRefPubMedCentralGoogle Scholar
  74. Rios JJ, Carrasco-Gil S, Abadía A, Abadía J (2016) Using Perl’s staining to trace the iron uptake pathway in leaves of a prunus rootstock treated with iron foliar fertilizers. Front Plant Sci 7:893PubMedPubMedCentralCrossRefGoogle Scholar
  75. Rodrigues F, Almeida I, Sarmento B, Amaral MH, Oliveira MBPP (2014) Study of the isoflavone content of different extracts of Medicago spp. as potential active ingredient. Industrial Crop Prod 57:110–115CrossRefGoogle Scholar
  76. Rodríguez-Celma J, Lattanzio G, Grusak MA, Abadía A, Abadía J, López-Millán A-F (2011a) Root responses of Medicago truncatula plants grown in two different iron deficiency conditions: changes in root protein profile and riboflavin biosynthesis. J Proteome Res 10:2590–2601PubMedCrossRefPubMedCentralGoogle Scholar
  77. Rodríguez-Celma J, Vázquez-Reina S, Orduna J, Abadía A, Abadía J, Álvarez-Fernández A, López-Millán A-F (2011b) Characterization of flavins in roots of Fe-deficient strategy in plants, with a focus on Medicago truncatula. Plant Cell Physiol 52:2173–2189PubMedCrossRefPubMedCentralGoogle Scholar
  78. Sabir A, Ekbic H (2010) Response of four grapevine (Vitis spp.) genotypes to direct or bicarbonate-induced iron deficiency. Spanish J Agric Res 8:823–829CrossRefGoogle Scholar
  79. Santos CS, Serrão I, Vasconcelos MW (2016) Comparative analysis of iron deficiency chlorosis responses in soybean (Glycine max) and barrel medic (Medicago truncatula). Rev Ciências Agrárias 39:538–549CrossRefGoogle Scholar
  80. Schwertmann U (1991) Solubility and dissolution of iron oxides. Plant Soil 130:1–25CrossRefGoogle Scholar
  81. Sieh D, Krajinski F, Hoefgen R, Devers EA, Watanabe M, Brueckner F (2012) The arbuscular mycorrhizal symbiosis influences sulfur starvation responses of Medicago truncatula. New Phytol 197:606–616PubMedCrossRefPubMedCentralGoogle Scholar
  82. Silva L, Carvalho H (2013) Possible role of glutamine synthetase in the NO signaling response in root nodules by contributing to the antioxidant defenses. Front Plant Sci 4:1–8CrossRefGoogle Scholar
  83. Sisó-Terraza P, Luis-Villarroya A, Fourcroy P, Briat JF, Abadía A, Gaymard F, Abadía J, Álvarez-Fernández A (2016a) Accumulation and secretion of coumarinolignans and other coumarins in Arabidopsis thaliana roots in response to iron deficiency at high pH. Front Plant Sci 7:1–22CrossRefGoogle Scholar
  84. Sisó-Terraza P, Rios JJ, Abadía J, Abadía A, Álvarez-Fernández A (2016b) Flavins secreted by roots of iron-deficient Beta vulgaris enable mining of ferric oxide via reductive mechanisms. New Phytol 209:733–745PubMedCrossRefPubMedCentralGoogle Scholar
  85. Stochmal A, Kowalska I, Janda B, Perrone A, Piacente S, Oleszek W (2009) Gentisic acid conjugates of Medicago truncatula roots. Phytochemistry 70:1272–1276PubMedCrossRefPubMedCentralGoogle Scholar
  86. Vadas TM, Ahner BA (2009) Extraction of lead and cadmium from soils by cysteine and glutathione. J Environ Qual 38:2245–2252PubMedCrossRefPubMedCentralGoogle Scholar
  87. Vergauwen B, Verstraete K, Senadheera DB, Dansercoer A, Cvitkovitch DG, Guédon E, Savvides SN (2013) Molecular and structural basis of glutathione import in gram-positive bacteria via GshT and the cystine ABC importer TcyBC of Streptococcus mutans. Mol Microbiol 89:288–303PubMedCrossRefPubMedCentralGoogle Scholar
  88. Visnevschi-Necrasov T, Barreira JCM, Cunha SC, Pereira G, Nunes E, Oliveira MBPP (2014) Advances in isoflavone profile characterisation using matrix solid-phase dispersion coupled to HPLC/DAD in Medicago species. Phytochem Anal 26:40–46PubMedCrossRefPubMedCentralGoogle Scholar
  89. Wang JW, Zheng LP, Wu JY, Tan RX (2006) Involvement of nitric oxide in oxidative burst phenylalanine ammonia-lyase activation and taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide Biol Chem 15:351–358CrossRefGoogle Scholar
  90. Wang X, Chen W, Zhou Y, Han J, Zhao J, Shi D, Yang C (2012) Comparison of adaptive strategies of alfalfa (Medicago sativa L.) to salt and alkali stresses. Aust J Crop Sci 6:309–315Google Scholar
  91. Waters BM, Amundsen K, Graef G (2018) Gene expression profiling of iron deficiency chlorosis sensitive and tolerant soybean indicates key roles for phenylpropanoids under alkalinity stress. Front Plant Sci 9:10PubMedPubMedCentralCrossRefGoogle Scholar
  92. Wingate VPM, Lawton MA, Lamb CJ, Dalton D, Minchin F, Iturbe-Ormaetxe I, Rubio M, Moran J, Gordon A, Becana M (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–210PubMedPubMedCentralCrossRefGoogle Scholar
  93. Zaharieva TB, Abadía J (2003) Iron deficiency enhances the levels of ascorbate, glutathione, and related enzymes in sugar beet roots. Protoplasma 221:269–275PubMedPubMedCentralGoogle Scholar
  94. Zaharieva T, Yamashita K, Matsumoto H (1999) Iron deficiency induced changes in ascorbate content and enzyme activities related to ascorbate metabolism in cucumber roots. Plant Cell Physiol 40:273–280CrossRefGoogle Scholar
  95. Zaharieva TB, Gogorcena Y, Abadía J (2004) Dynamics of metabolic responses to iron deficiency in sugar beet roots. Plant Sci 166:1045–1050CrossRefGoogle Scholar
  96. Zamboni A, Celletti S, Zenoni S, Astolfi S, Varanini Z (2017) Root physiological and transcriptional response to single and combined S and Fe deficiency in durum wheat. Environ Exp Bot 143:172–184CrossRefGoogle Scholar
  97. Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 56:3223–3228PubMedCrossRefPubMedCentralGoogle Scholar
  98. Zuchi S, Watanabe M, Hubberten H-M, Bromke M, Osorio S, Fernie AR, Celletti C, Paolacci AR, Catarcione G, Ciaffi M, Hoefgen R, Astolfi S (2015) The interplay between sulfur and iron nutrition in tomato. Plant Physiol 169:2624–2639PubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Soil Science, Faculty of AgricultureFerdowsi University of MashhadMashhadIran
  2. 2.Department of Plant Nutrition, Aula Dei Experimental StationConsejo Superior de Investigaciones Científicas (CSIC)ZaragozaSpain
  3. 3.Department of Agronomy, Faculty of AgricultureFerdowsi University of MashhadMashhadIran

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