Abstract
Many chemicals, including herbicides, are routinely applied to crops for weed management and food production improvement. However, the intensive use of herbicides could lead eventually to a great environmental threat due to their persistence and accumulation in the ecosystems and contamination of soils. Furthermore, the possible effect of these chemicals on nutrient uptake and assimilation in crops has only recently been discussed. The present study aimed at understanding the effect of the herbicide terbuthylazine (TBA), a herbicide commonly applied to control weeds in leguminous species and triazine tolerant crops, on the capability of maize plants to cope with iron (Fe) shortage. The application of 2 and 5 mg L−1 TBA caused a significant reduction of root Fe concentration. This reduction might be attributed to a decreased release of phytosiderophores, which in turn could be ascribed to a reduced sulfur assimilation. Results provide evidence that TBA impairs Fe uptake and accumulation in non-target plants most likely interacting with sulfur-assimilating enzymes [ATP sulfurylase and O-acetylserine(thiol)lyase].
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Astolfi S, Zuchi S, Cesco S, Varanini Z, Pinton R (2004) Influence of iron nutrition on sulphur uptake and metabolism in maize (Zea mays L.) roots. Soil Sci Plant Nutr 50:1079–1083
Astolfi S, Cesco S, Zuchi S, Neumann G, Roemheld V (2006) Sulphur starvation reduces phytosiderophores release by Fe-deficient barley plants. Soil Sci Plant Nutr 52:80–85
Bellaloui N, Reddy KN, Zablotowicz RM, Abbas HK, Abel CA (2009) Effects of glyphosate application on seed iron and root ferric (III) reductase in soybean cultivars. J Agric Food Chem 57:9569–9574
Bocchini M, Bartucca ML, Ciancaleoni S, Mimmo T, Cesco S, Pii Y, Albertini E, Del Buono D (2015) Iron deficiency in barley plants: phytosiderophore release, iron translocation, and DNA methylation. Front Plant Sci. doi:10.3389/fpls.2015.00514 (article 514)
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Ciaffi M, Paolacci AR, Celletti S, Catarcione G, Kopriva S, Astolfi S (2013) Transcriptional and physiological changes in the S assimilation pathway due to single or combined S and Fe deprivation in durum wheat (Triticum durum L.) seedlings. J Exp Bot 64:1663–1675
Dean JR, Wade G, Barnabas IJ (1996) Determination of triazine herbicides in environmental samples. J Chromatogr A 733:295–335
Del Buono D, Ioli G (2011) Glutathione S-transferases of Italian ryegrass (Lolium multiflorum): activity toward some chemicals, safener modulation and persistence of atrazine and fluorodifen in the shoots. J Agric Food Chem 59:1324–1329
Del Buono D, Micheli M, Scarponi L, Standardi A (2006) Activity of glutathione S-transferase toward some herbicides and its regulation by benoxacor in non-embryogenic callus and in vitro regenerated tissues of Zea mays. Pest Biochem Physiol 85:61–67
Del Buono D, Ioli G, Nasini L, Proietti P (2011) A comparative study on the interference of two herbicides in wheat and Italian ryegrass and on their antioxidant activities and detoxification rates. J Agric Food Chem 59:12109–12115
Del Buono D, Astolfi S, Mimmo T, Bartucca ML, Celletti S, Ciaffi M, Cesco S (2015) Effects of terbuthylazine on phytosiderophores release in iron deficient barley. Environ Exp Bot 116:32–38
Dinelli G, Vicari A, Catizone P (1996) Monitoring of herbicide pollution in water by capillary electrophoresis. J Chromatogr A 733:337–344
Eker S, Ozturk L, Yazici A, Erenoglu B, Römheld V, Cakmak I (2006) Foliar applied glyphosate substantially reduced uptake and transport of iron and manganese in sunflower. J Agric Food Chem 54:10019–10025
Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 81:2273–2280
Konstantinou IK, Hela DG, Albanis TA (2006) The status of pesticide pollution in surface waters (rivers and lakes) of Greece. Part I. Review on occurrence and levels. Environ Pollut 141:555–570
Liang T, Ding H, Wang G, Kang J, Pang H, Lv J (2016) Sulfur decreases cadmium translocation and enhances cadmium tolerance by promoting sulfur assimilation and glutathione metabolism in Brassica chinensis L. Ecotoxicol Environ Saf 124:129–137
Marschner H, Römheld V, Kissel M (1986) Different strategies in higher plants mobilization and uptake of iron. J Plant Nutr 6:695–713
Matocha JE, Hopper FL (2001) Influence of terbufos and nicosulfuron on iron chlorosis and growth of corn. J Plant Nutr 24:1445–1455
Mimmo T, Del Buono D, Terzano R, Tomasi N, Vigani G, Crecchio C, Pinton R, Zocchi G, Cesco S (2014) Rhizospheric organic compounds in the soil–microorganism–plant system: their role in iron availability. Eur J Soil Sci 65:629–642
Mori S, Nishizawa N (1987) Methionine as a dominant precursor of phytosiderophores in Graminaceae plants. Plant Cell Physiol 28:1081–1092
Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286:5446–5454
Ozturk L, Yazici A, Eker S, Gokmen O, Römheld V, Cakmak I (2008) Glyphosate inhibition of ferric reductase activity in iron deficient sunflower roots. New Phytol 177:899–906
Pajuelo E, Carrasco JA, Romero LC, Chamber MA, Gotor C (2007) Evaluation of the metal phytoextraction potential of crop legumes. Regulation of the expression of O-acetylserine (thiol)lyase under metal stress. Plant Biol 9:672–681
Scarponi L, Quagliarini E, Del Buono D (2006) Induction of wheat and maize glutathione S-transferase by some herbicide safeners and their effect on enzyme activity against butachlor and terbuthylazine. Pest Manag Sci 62:927–932
Sebastian A, Nangia A, Prasad MNV (2017) Carbon-bound iron oxide nanoparticles prevent calcium-induced iron deficiency in Oryza sativa L. J Agric Food Chem 65(3):557–564
Shenker M, Hadar Y, Chen Y (1995) Rapid method for accurate determination of colorless siderophores and synthetic chelates. Soil Sci Soc Am J 59:1612–1618
Stipičević S, Galzina N, Udiković-Kolić N, Jurina T, Mendaš G, Dvoršćak M, Petrić I, Barić K, Drevenka V (2015) Distribution of terbuthylazine and atrazine residues in crop-cultivated soil: the effect of herbicide application rate on herbicide persistence. Geoderma 259:300–309
Vega JM, Rubiales MA, Vilchez C, Vigara J (2005) Effect of abiotic stress on photosynthesis, respiration and antioxidant system in Chlamydomonas reinhardtii. Phyton Ann Rei Bot 45:97–106
Yatusevich R, Mugford SG, Matthewman C, Gigolashvili T, Frerigmann H, Delaney S, Koprivova A, Flugge UI, Kopriva S (2010) Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J 62:1–11
Zuchi S, Cesco S, Astolfi S (2012) High S supply improves Fe accumulation in durum wheat plants grown under Fe limitation. Environ Exp Bot 77:25–32
Acknowledgements
This work has been financially supported by the Italian MIUR (FIRB-Programma“Futuro in Ricerca” 2012-RBFR127WJ9).
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Communicated by MG dos Santos.
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Bartucca, M.L., Celletti, S., Mimmo, T. et al. Terbuthylazine interferes with iron nutrition in maize (Zea mays) plants. Acta Physiol Plant 39, 235 (2017). https://doi.org/10.1007/s11738-017-2537-z
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DOI: https://doi.org/10.1007/s11738-017-2537-z