Glutathione supplementation prevents iron deficiency in Medicago scutellata grown in rock sand under different levels of bicarbonate
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.
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.
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.
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.
KeywordsIron Iron chlorosis Iron oxides Root fertilisation Legumes
Soil-Plant Analyses Development
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.
- 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
- AOAC (2000) Official methods of analysis. Association of Analytical Chemists, Washington, p 334Google Scholar
- Benton-Jones J, Wolf B, Mills HA (1991) Plant analysis handbook: a practical sampling, preparation, analysis, and interpretation guide. Micro-Macro-Publishing, AthensGoogle Scholar
- 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)
- Goławska S, Łukasik I, Kapusta T, Janda B (2010) Analysis of flavonoids content in alfalfa Ecol Chem En A 17:261–267Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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