Abstract
Purpose
The aim of this work was to test the hypothesis that Fe mining sub-products and thiols can alleviate a moderate Fe-deficiency in the Strategy I species soybean (Glycine max) grown in a calcareous soil in greenhouse conditions.
Methods
Combinations of three Fe sources [Fe(III)-EDDHA and two Fe mining sub-products, one containing Fe oxides and FeS2 and the other Fe oxides], and three thiols (glutathione, dithiothreitol and thiophenol) were applied in solution to the soil, three times in a 55 day period, and different parameters related to Fe deficiency were measured. The thiol-mediated solubilization of Fe from the Fe mining sub-products was assessed by measuring in the solution total Fe and the reducible Fe pool using an Fe(II) chelator.
Results
Application of Fe-EDDHA, the two Fe mining sub-products and the three thiols relieved the Fe deficiency symptoms to different extents, increased the Fe concentrations and contents throughout the plant and changed the redox state of leaves and roots, as judged from the changes in reduced and oxidized glutathione, ascorbate and antioxidant enzymes. When using Fe(III)-EDDHA, the addition of thiols led to a better leaf regreening. However, the addition of thiols did not cause further regreening in the case of the Fe mining sub-products, in spite of being able to solubilize Fe from them.
Conclusion
Application of Fe-mining sub-products, thiols and the combination of Fe(III)-EDDHA and thiols could be used to alleviate moderate Fe deficiency in G. max grown in a calcareous soil.
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References
Abadía J, Monge E, Montañés L, Heras L (1984) Extraction of iron from plant leaves by Fe (II) chelators. J Plant Nutr 7:777–784. https://doi.org/10.1080/01904168409363241
Abadía J, López-Millán A-F, Rombolà A, Abadía A (2002) Organic acids and Fe deficiency: A review. Plant Soil 241:75–86. https://doi.org/10.1023/A:1016093317898
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 49:471–482. https://doi.org/10.1016/j.plaphy.2011.01.026
Álvarez-Fernández A, García-Laviña P, Fidalgo C, Abadía J, Abadía A (2004) Foliar fertilization to control iron chlorosis in pear (Pyrus communis L.) trees. Plant Soil 263:5–15. https://doi.org/10.1023/B:PLSO.0000047717.97167.d4
Ambikadevi VR, Lalithambika M (2000) Effect of organic acids on ferric iron removal from iron-stained kaolinite. Appl Clay Sci 16:133–145. https://doi.org/10.1016/S0169-1317(99)00038-1
Amirbahman A, Sigg L, Von Gunten U (1997) Reductive dissolution of Fe(III) (hydr)oxides by cysteine: Kinetics and mechanism. J Colloid Interface Sci 194:194–206. https://doi.org/10.1006/jcis.1997.5116
AOAC (2000) Official methods of analysis association of analytical chemists, Washington DC, p 334
Ariga T, Hazama K, Yanagisawa S, Yoneyama T (2014) Chemical forms of iron in xylem sap from graminaceous and non-graminaceous plants. Soil Sci Plant Nutr 60:460–469. https://doi.org/10.1080/00380768.2014.922406
Astolfi S, Celletti S, Vigani G, Mimmo T, Cesco S (2021) Interaction between sulfur and iron in plants. Front Plant Sci 12:670308. https://doi.org/10.3389/fpls.2021.670308
Atencio L, Salazar J, Moran Lauter AN, Gonzales MD, O’Rourke JA, Graham MA (2021) Characterizing short and long term iron stress responses in iron deficiency tolerant and susceptible soybean (Glycine max L. Merr.). Plant Stress 2:100012. https://doi.org/10.1016/j.stress.2021.100012
Bardsley CE, Lancaster JD (1960) Determination of reserve sulfur and soluble sulfates in soils. Soil Sci Soc Am J 24:265–268. https://doi.org/10.2136/sssaj1960.03615995002400040015x
Benton-Jones J, Wolf B, Mills HA (1991) Plant analysis handbook: A practical sampling, preparation, analysis, and interpretation guide. Micro-Macro-Publishing, Athens
Berríos J, Illanes A, Aroca G (2004) Spectrophotometric method for determining gibberellic acid in fermentation broths. Biotechnol Lett 26:67–70. https://doi.org/10.1023/B:BILE.0000009463.98203.8b
Blesa MA, Marinovich HA, Baumgartner EC, Maroto AJG (1987) mechanism of dissolution of magnetite by oxalic acid-ferrous ion solutions. Inorg Chem 26:3713–3717. https://doi.org/10.1021/ic00269a019
Bremner JM, Mulvaney CS(1982) Nitrogen-total. In: Page AL, Miller RH, Keeney DR (Eds), Methods of soil analysis, Part 2, 2nd edn., Agron. Monogr. 9, ASA-CSSA-SSSA, Madison, pp 595–624
Briat JF, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends Plant Sci 20:33–40. https://doi.org/10.1016/j.tplants.2014.07.005
Brown JC, Ambler JE (1973) “Reductants” released by roots of Fe-deficient soybeans. Agron J 65:311–314
Carlberg I, Mannervik B (1985) Glutathione reductase. Meth Enzymol 113:484–490
Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493. https://doi.org/10.1093/jxb/err145
Chen J, Wu FH, Shang YT, Wang WH, Hu WJ, Simon M, Liu X, Shangguan ZP, Zheng HL (2015) Hydrogen sulphide improves adaptation of Zea mays seedlings to iron deficiency. J Exp Bot 66:6605–6622. https://doi.org/10.1093/jxb/erv368
Chen J, Zhang NN, Pan Q, Lin X-Y, Shangguan Z, Zhang J-H, Wei G-H (2020a) Hydrogen sulphide alleviates iron deficiency by promoting iron availability and plant hormone levels in Glycine max seedlings. BMC Plant Biol 20:383. https://doi.org/10.1186/s12870-020-02601-2
Chen S, Jia H, Wang X, Shi C, Wang X, Ma P, Wang J, Ren M, Li J (2020b) Hydrogen sulfide positively regulates abscisic acid signaling through persulfidation of SnRK2.6 in guard cells. Mol Plant 13:732–744. https://doi.org/10.1016/j.molp.2020.01.004
Cieschi MT, Polyakov AY, Lebedev VA, Volkov DS, Pankratov DA, Veligzhanin AA, Perminova IV, Lucena JJ (2019) Eco-friendly iron-humic nanofertilizers synthesis for the prevention of iron chlorosis in soybean (Glycine max) grown in calcareous soil. Front Plant Sci 10:413. https://doi.org/10.3389/fpls.2019.00413
Connorton JM, Balk J, Rodríguez-Celma J (2017) Iron homeostasis in plants-a brief overview. Metallomics 9:813–823. https://doi.org/10.1039/c7mt00136c
Cornell RM, Schindler PW (1987) Photochemical dissolution of goethite in acid/oxalate solution. Clays Clay Miner 35:347–352. https://doi.org/10.1346/CCMN.1987.0350504
Cornell RM, Schwertmann U (2004) The iron oxides: structure, properties, reactions, occurrences and uses, 2nd edn. Wiley-VCH, Verlag GmbH & Co. KGaA, Weinheim. ISBN: 3-527-30274-3. https://www.wiley.com/en-us/9783527606443
Corwin DL, Rhoades JD (1982) An improved technique for determining soil electrical conductivity-depth relations from above-ground electromagnetic measurements. Soil Sci Soc Am J 46:517–520. https://doi.org/10.2136/sssaj1982.03615995004600030014x
d’Arcy-Lameta A (1986) Study of soybean and lentil root exudates. Plant Soil 92:113–123. https://doi.org/10.1007/BF02372272
Eitel EM, Taillefert M (2017) Mechanistic investigation of Fe(III) oxide reduction by low molecular weight organic sulfur species. Geochim Cosmochim Acta 215:173–188. https://doi.org/10.1016/j.gca.2017.07.016
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 49:483–488. https://doi.org/10.1016/j.plaphy.2011.02.013
Gamble AV, Howe JA, Delaney D, van Santen E, Yates R (2014) Iron chelates alleviate iron chlorosis in soybean on high pH soils. Agron J 106:1251–1257. https://doi.org/10.2134/agronj13.0474
García-Marco S, Martínez N, Yunta F, Hernández-Apaolaza L, Lucena JJ (2006) Effectiveness of ethylenediamine-N(o-hydroxyphenylacetic)-N′(p-hydroxyphenylacetic) acid (o,p-EDDHA) to supply iron to plants. Plant Soil 279:31–40. https://doi.org/10.1007/s11104-005-8218-5
García-Mina JM, Bacaicoa E, Fuentes M, Casanova E (2013) Fine regulation of leaf iron use efficiency and iron root uptake under limited iron bioavailability. Plant Sci 198:39–45. https://doi.org/10.1016/j.plantsci.2012.10.001
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 182:607–624. https://doi.org/10.1002/jpln.201800692
Gheshlaghi Z, Khorassani R, Abadía J, Álvarez-Fernández A, Luis-Villarroya A, Fotovat A, Kafi M (2020) Glutathione supplementation prevents iron deficiency in Medicago scutellata grown in rock sand under different levels of bicarbonate. Plant Soil 446:43–63. https://doi.org/10.1007/s11104-019-04314-4
Gheshlaghi Z, Luis-Villarroya A, Álvarez-Fernández A, Khorassani R, Abadía J (2021) Iron deficient Medicago scutellata grown in nutrient solution at high pH accumulates and secretes large amounts of flavins. Plant Sci 303:110664. https://doi.org/10.1016/j.plantsci.2020.110664
Goos RJ, Johnson BE (2000) A comparison of three methods for reducing iron-deficiency chlorosis in soybean. Agron J 92:1135–1139. https://doi.org/10.2134/agronj2000.9261135x
Graham TL (1991) Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiol 95:594–603. https://doi.org/10.1104/pp.95.2.594
Hansen NC, Jolley VD, Naeve SL, Goos RJ (2004) Iron deficiency of soybean in the North Central U.S. and associated soil properties. Soil Sci Plant Nutr 50:983–987. https://doi.org/10.1080/00380768.2004.10408564
Hlavay J, Prohaska T, Weisz M, Wenzel WW, Stingeder GJ (2004) Determination of trace elements bound to soil and sediment fractions (IUPAC Technical Report). Pure Appl Chem 76:415–442. https://doi.org/10.1351/pac200476020415
Jolley VD, Brown JC (1987) Soybean response to iron-deficiency stress as related to iron supply in the growth medium. J Plant Nutr 10:637–651. https://doi.org/10.1080/01904168709363597
Jolley VD, Stevens WB, Terry RE, Orf JH (1992) Root iron-reduction capacity for genotypic evaluation of iron efficiency in soybean. J Plant Nutr 15:1679–1690. https://doi.org/10.1080/01904169209364430
Katyal JC, Sharma BD (1984) Some modification in the assay of Fe2+ in 1–10, o-phenanthroline extracts of fresh plant tissues. Plant Soil 79:449–450. https://doi.org/10.1007/BF02184337
Kaya C, Ashraf M (2019) The mechanism of hydrogen sulfide mitigation of iron deficiency-induced chlorosis in strawberry (Fragaria × ananassa) plants. Protoplasma 256:371–382. https://doi.org/10.1007/s00709-018-1298-x
Kaya C, Higgs D, Ashraf M, Alyemeni MN, Ahmad P (2020) Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) plants to iron deficiency and salt stress alone or in combination. Physiol Plant 168:256–277. https://doi.org/10.1111/ppl.12976
Kelen M, Çubuk Demiralay E, Şen S, Özkan G (2004) Separation of abscisic acid, indole-3-acetic acid, gibberellic acid in 99 R (Vitis berlandieri x Vitis rupestris) and rose oil (Rosa damascena Mill.) by reversed phase liquid chromatography. Turkish J Chem 28:603–610
Khan MN, Siddiqui MH, Al-Solami MA, Basahi RA, Siddiqui ZH, Alamri S (2021) Cysteine and hydrogen sulfide: A complementary association for plant acclimation to abiotic stress. In: Khan MN, Siddiqui MH, Alamri S, Corpas FJ (eds) Hydrogen sulfide and plant acclimation to abiotic stresses, plant in challenging environments, vol 1. Springer, Cham, pp 187–214. https://doi.org/10.1007/978-3-030-73678-1_11
Kiene RP, Malloy KD, Taylor BF (1990) Sulfur-containing amino acids as precursors of thiols in anoxic coastal sediments. Appl Environ Microbiol 56:156–161. https://doi.org/10.1128/aem.56.1.156-161.1990
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 7:1246–1250. https://doi.org/10.4161/psb.21548
Li M, Zhang P, Adeel M, Guo Z, Chetwynd AJ, Ma C, Bai T, Hao Y, Rui Y (2021) Physiological impacts of zero valent iron, Fe3O4 and Fe2O3 nanoparticles in rice plants and their potential as Fe fertilizers. Environ Pollut 269:116134. https://doi.org/10.1016/j.envpol.2020.116134
Lima MRM, Diaz SO, Lamego I, Grusak MA, Vasconcelos MW, Gil AM (2014) Nuclear magnetic resonance metabolomics of iron deficiency in soybean leaves. J Proteome Res 13:3075–3087. https://doi.org/10.1021/pr500279f
Lin S, Cianzio S, Shoemaker R (1997) Mapping genetic loci for iron deficiency chlorosis in soybean. Mol Breed 3:219–229. https://doi.org/10.1023/A:1009637320805
Loeppert RH, Suarez DL (1996) Carbonate and gypsum. Methods of soil analysis Part III, Chemical methods. Soil Science Society of America, Madison, pp 437–474
López-Millán A-F, Grusak MA, Abadía A, Abadía J (2013) Iron deficiency in plants: an insight from proteomic approaches. Front Plant Sci 4:254. https://doi.org/10.3389/fpls.2013.00254
Luwe M, Takahama U, Heber U (1993) Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacia oleracea L.) leaves. Plant Physiol 101:969–976. https://doi.org/10.1104/pp.101.3.969
M’sehli W, Dell’Orto M, Donnini M, De Nisi S, Zocchi G, Abdelly C, Gharsalli M (2009) Variability of metabolic responses and antioxidant defence in two lines of Medicago ciliaris to Fe deficiency. Plant Soil 320:219–230. https://doi.org/10.1007/s11104-008-9887-7
Masaoka Y, Kojima M, Sugihara S, Yoshihara T, Koshino M, Ichihara A (1993) Dissolution of ferric phosphate by alfalfa (Medicago sativa L.) root exudates. Plant Soil 155–156:75–78. https://doi.org/10.1007/BF00024987
Masato O (1980) An improved method for determination of l-ascorbic acid and l-dehydroascorbic acid in blood plasma. Clin Chim Acta 103:259–268. https://doi.org/10.1016/0009-8981(80)90144-8
Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M (1999) Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol 121:879–888. https://doi.org/10.1104/pp.121.3.879
Merry R, Dobbels AA, Sadok W, Naeva S, Stupar RM, Lorenz AJ (2022) Iron deficiency in soybean. Crop Sci 62:36–52. https://doi.org/10.1002/csc2.20661
Mira MM, Asmundson B, Renault S, Hill RD, Stasolla C (2021) Suppression of the soybean (Glycine max) Phytoglobin GmPgb1 improves tolerance to iron stress. Acta Physiol Plant 43:147. https://doi.org/10.1007/s11738-021-03315-0
Mollering H (1985) L-malate. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol VII, 3rd edn. VCH Publishers (UK) Ltd., Cambridge, pp 39–47
Mollering H (1989) Citrate. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol VII, 3rd edn. VCH Publishers (UK) Ltd., Cambridge, pp 2–12
Moran Lauter AN, Peiffer GA, Yin T, Whitham SA, Cook D, Shoemaker RC, Graham MA (2014) Identification of candidate genes involved in early iron deficiency chlorosis signaling in soybean (Glycine max) roots and leaves. BMC Genomics 15:702. https://doi.org/10.1186/1471-2164-15-702
Morrison KD, Bristow TF, Kennedy MJ (2013) The reduction of structural iron in ferruginous smectite via the amino acid cysteine: Implications for an electron shuttling compound. Geochim Cosmochim Acta 106:152–163. https://doi.org/10.1016/j.gca.2012.12.006
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Sparks DL (ed) Methods of soil analysis, Chemical methods, Vol. 5, part 3. Soil Science Society of America Inc., Madison, pp 961–1010
Nozoye T (2018) The nicotianamine synthase gene is a useful candidate for improving the nutritional qualities and Fe-deficiency tolerance of various crops. Front Plant Sci 9:340. https://doi.org/10.3389/fpls.2018.00340
Nozoye T, Kim S, Kakei Y, Takahashi M, Nakanishi H, Nishizawa NK (2014) Enhanced levels of nicotianamine promote iron accumulation and tolerance to calcareous soil in soybean. Biosci Biotechnol Biochem 78:1677–1684. https://doi.org/10.1080/09168451.2014.936350
Panias D, Taxiarchou M, Paspaliaris I, Kontopoulos A (1996) Mechanisms of dissolution of iron oxides in aqueous oxalic acid solutions. Hydrometallurgy 42:257–265. https://doi.org/10.1016/0304-386X(95)00104-O
Qiu W, Dai J, Wang N, Guo X, Zhang X, Zuo Y (2017) Effects of Fe-deficient conditions on Fe uptake and utilization in P-efficient soybean. Plant Physiol Biochem 112:1–8. https://doi.org/10.1016/j.plaphy.2016.12.010
Rahman MA, Kabir AH, Song Y, Guo X, Zhang X, Zuo Y (2021) Nitric oxide prevents Fe deficiency-induced photosynthetic disturbance, and oxidative stress in alfalfa by regulating Fe acquisition and antioxidant defense. Antioxidants 10:1556. https://doi.org/10.3390/antiox10101556
Rahman MA, Bagchi R, El-Shehawi AM, Elseehy MM, Anee SA, Lee K-W, Kabir AH (2022) Physiological and molecular characterization of strategy-I responses and expression of Fe-transporters in Fe-deficient soybean. South Afr J Bot 147:942–950. https://doi.org/10.1016/j.sajb.2022.03.052
Raj KK, Pandey RN, Singh B, Meena MC, Talukdar A, Chakraborty D (2021) Response of soybean genotypes to iron limiting stress in calcareous vertisol under ambient and elevated CO2 and temperature conditions. J Environ Biol 42:295–301. https://doi.org/10.22438/JEB/42/2/MRN-1226
Ramírez L, Graziano M, Lamattina L (2008) Decoding plant responses to iron deficiency. Plant Signal Behav 3:795–797. https://doi.org/10.4161/psb.3.10.5874
Ramírez L, Bartoli CG, Lamattina L (2013) Glutathione and ascorbic acid protect Arabidopsis plants against detrimental effects of iron deficiency. J Exp Bot 64:3169–3178. https://doi.org/10.1093/jxb/ert153
Rellán-Álvarez R, El-Jendoubi H, Wohlgemut G, Abadía A, Fiehn O, Abadía J, Álvarez-Fernández A (2011) Metabolite profile changes in xylem sap and leaf extracts of strategy I plants in response to iron deficiency and resupply. Front Plant Sci 2:66. https://doi.org/10.3389/fpls.2011.00066
Rios JJ, Carrasco-Gil S, Abadía A, Abadía J (2016) Using Perls staining to trace the iron uptake pathway in leaves of a Prunus rootstock treated with iron foliar fertilizers. Front Plant Sci 7:893. https://doi.org/10.3389/fpls.2016.00893
Robe K, Izquierdo E, Vignols F, Rouached H, Dubos C (2021) The coumarins: secondary metabolites playing a primary role in plant nutrition and health. Trends Plant Sci 26:248–259. https://doi.org/10.1016/j.tplants.2020.10.008
Rodríguez-Lucena P, Ropero E, Hernández-Apaolaza L, Lucena JJ (2010a) Iron supply to soybean plants through the foliar application of IDHA/Fe3+: effect of plant nutritional status and adjuvants. J Sci Food Agric 90:2633–2640. https://doi.org/10.1002/jsfa.4132
Rodríguez-Lucena P, Hernández-Apaolaza L, Lucena JJ (2010b) Comparison of iron chelates and complexes supplied as foliar sprays and in nutrient solution to correct iron chlorosis of soybean. J Plant Nutr Soil Sci 173:120–126. https://doi.org/10.1002/jpln.200800256
Rogers EE, Wu X, Stacey G, Nguyen HT (2009) Two MATE proteins play a role in iron efficiency in soybean. J Plant Physiol 166:1453–1459. https://doi.org/10.1016/j.jplph.2009.02.009
Santos CS, Silva AI, Serrão I, Carvalho AL, Vasconcelos MW (2013) Transcriptomic analysis of iron deficiency related genes in the legumes. Food Res Int 54:1162–1171. https://doi.org/10.1016/j.foodres.2013.06.024
Santos CS, Roriz M, Carvalho SMP, Vasconcelos MW (2015) Iron partitioning at an early growth stage impacts iron deficiency responses in soybean plants (Glycine max L.). Front Plant Sci 6:325. https://doi.org/10.3389/fpls.2015.00325
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 39:538–549. https://doi.org/10.19084/rca16090
Santos CS, Ozgur R, Uzilday B, Turkan I, Roriz M, Rangel AOSS, Calvalho SMP, Vasconcelos MW (2019) Understanding the role of the antioxidant system and the tetrapyrrole cycle in iron deficiency chlorosis. Plants 8:348. https://doi.org/10.3390/plants8090348
Shanmugam V, Tsednee M, Yeh K-C (2012) Zinc tolerance induced by iron 1 reveals the importance of glutathione in the cross-homeostasis between zinc and iron in Arabidopsis thaliana Plant J 69:1006–1017. https://doi.org/10.1111/j.1365-313X.2011.04850.x
Singh S, Kumar V (2020) Mercury detoxification by absorption, mercuric ion reductase, and exopolysaccharides: a comprehensive study. Environ Sci Pollut Res Int 27:27181–27201. https://doi.org/10.1007/s11356-019-04974-w
Sisó-Terraza P, Rios JJ, Abadía J, Abadía A, Álvarez-Fernández A (2016) Flavins secreted by roots of iron-deficient Beta vulgaris enable mining of ferric oxide via reductive mechanisms. New Phytol 209:733–745. https://doi.org/10.1111/nph.13633
Sorensen J (1988) Dimethylsulfide and methane thiol in sediment porewater of a Danish estuary. Biogeochemistry 6:201–210. https://doi.org/10.1007/BF02182996
Stander HM, Harrison STL, Broadhurst JL (2022) Using south african sulfide-enriched coal processing waste for amelioration of calcareous soil: A pre-feasibility study. Min Eng 180:107457. https://doi.org/10.1016/j.mineng.2022.107457
Tiffin LO (1970) Translocation of iron citrate and phosphorus in xylem exudate of soybean. Plant Physiol 45:280–283. https://doi.org/10.1104/pp.45.3.280
Tighe M, Lockwood P, Wilson S, Lisle L (2004) Comparison of digestion methods for ICP-OES analysis of a wide range of analytes in heavy metal contaminated soil samples with specific reference to arsenic and antimony. Commun Soil Sci Plant Anal 35:1369–1385. https://doi.org/10.1081/CSS-120037552
Vairavamurthy A, Mopper K (1987) Geochemical formation of organosulphur compounds (thiols) by addition of H2S to sedimentary organic matter. Nature 329:623–625. https://doi.org/10.1038/329623a0
Vasconcelos MW, Grusak MA (2014) Morpho-physiological parameters affecting iron deficiency chlorosis in soybean (Glycine max L.). Plant Soil 374:161–172. https://doi.org/10.1007/s11104-013-1842-6
Vasconcelos MW, Clemente TE, Grusak MA (2014) Evaluation of constitutive iron reductase (AtFRO2) expression on mineral accumulation and distribution in soybean (Glycine max L). Front Plant Sci 5:112. https://doi.org/10.3389/fpls.2014.00112
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 89:288–303. https://doi.org/10.1111/mmi.12274
Wallace A, Mueller RT, Patel PM, Soufi SM (1976) Use of waste pyrites from mine operations on highly calcareous soil. Commun Soil Sci Plant Anal 7:57–60. https://doi.org/10.1080/00103627609366613
Wallace A, Romney EM, Wallace GA, Mueller RT, Cha JW (1980) Pyrite as a source of iron for plants. J Plant Nutr 2:193–195. https://doi.org/10.1080/01904168009362762
Wang B, Wei H, Xue Z, Zhang WH (2017) Gibberellins regulate iron deficiency-response by influencing iron transport and translocation in rice seedlings (Oryza sativa). Ann Bot 119:945–956. https://doi.org/10.1093/aob/mcw250
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 9:10. https://doi.org/10.3389/fpls.2018.00010
Wiersma JV (2005) High rates of Fe-EDDHA and seed iron concentration suggest partial solutions to iron deficiency in soybean. Agron J 97:924–934. https://doi.org/10.2134/agronj2004.0309
Yang Y, Chen L, Yu J et al (2020) Promoting mechanism of electronic shuttle for bioavailability of Fe(III) oxide and its environmental significance. Water Supply 20:1157–1166
Zaharieva TB, Abadía J (2003) Iron deficiency enhances the levels of ascorbate, glutathione, and related enzymes in sugar beet roots. Protoplasma 221:269–275. https://doi.org/10.1007/s00709-002-0051-6
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 40:273–280. https://doi.org/10.1093/oxfordjournals.pcp.a029538
Zaharieva TB, Gogorcena Y, Abadía J (2004) Dynamics of metabolic responses to iron deficiency in sugar beet roots. Plant Sci 166:1045–1050. https://doi.org/10.1016/j.plantsci.2003.12.017
Zocchi G (2006) Metabolic changes in iron-stressed dicotyledonous plants. In: Barton LL, Abadía J (eds) Iron nutrition in plants and Rhizospheric microorganisms. Springer, Dordrecht, pp 359–370. https://doi.org/10.1007/1-4020-4743-6_18
Zocchi G, Cocucci S (1990) Fe uptake mechanism in Fe-efficient cucumber roots. Plant Physiol 92:908–911. https://doi.org/10.1104/pp.92.4.908
Zocchi G, De Nisi P, Dell’Orto M, Espen L, Gallina PM (2007) Iron deficiency differently affects metabolic responses in soybean roots. J Exp Bot 58:993–1000. https://doi.org/10.1093/jxb/erl259
Acknowledgements
Work supported by the Department of Soil Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran (research project on G. max 2/51555), the Spanish Ministry of Science and Innovation (Grant PID2020-115856RB-100 funded by MCIN/AEI/https://doi.org/10.13039/501100011033) and the Aragón Government (group A09-20R). Authors thank J. Rodríguez-Celma for reading the manuscript and provide useful comments.
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Gheshlaghi, Z., Khorassani, R. & Abadia, J. Two Fe mining sub-products and three thiol compounds alleviate Fe deficiency in soybean (Glycine max L.) grown in a calcareous soil in greenhouse conditions. Plant Soil 482, 469–490 (2023). https://doi.org/10.1007/s11104-022-05702-z
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DOI: https://doi.org/10.1007/s11104-022-05702-z