Abstract
Proton-selective microelectrodes were used to determine sulfate uptake by roots of intact plant seedlings. The response of H+ fluxes to sulfate addition showed to be a good proxy for sulfate uptake by the sulfate/H+ co-transport system. H+ influx and increase in root surface pH was much higher in sulfate-deprived seedlings than in seedlings grown with sufficient sulfate. The opposite was true for the response of H+ fluxes to nitrate addition. By using this method sulfate uptake could be mapped along the root axis, which revealed higher uptake rates in mature regions. Sulfate deprived roots showed a lower root surface pH, which correlated strongly with the response to sulfate addition. A possible contribution of this component to a higher sulfate uptake capacity under sulfur deficiency was further tested by using the fungal toxin fusicoccin, which permanently activates the plasma membrane H+-pumping ATPase. Application of fusicoccin lowered the pH of sufficient roots to the level of deficient roots, indicating a more activated state of the ATPase under sulfur deficiency rather than a higher abundance.
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References
Bloom AJ, Caldwell RM (1988) Root excision decreases nutrient absorption and gas fluxes. Plant Physiol 87:794–796
Buchner P, Stuiver CEE, Westerman S, Wirtz M, Hell R, Hawkesford MJ, De Kok LJ (2004) Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiol 136:3396–3408
Bunney TD, van den Wijngaard PW, De Boer AH (2002) 14-3-3 protein regulation of proton pumps and ion channels. Plant Mol Biol 50:1041–1051
Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28:1230–1246
Clarkson DT, Saker LR (1989) Sulphate influx in wheat and barley roots becomes more sensitive to specific protein-binding reagents when plants are sulphate-deficient. Planta 178:249–257
Clarkson DT, Saker LR, Purves JV (1989) Depression of nitrate and ammonium transport in barley plants with diminished sulphate status. Evidence of co-regulation of nitrogen and sulphate intake. J Exp Bot 40:953–963
De Boer AH, van Kleeff PJ, Gao J (2013) Plant 14-3-3 proteins as spiders in a web of phosphorylation. Protoplasma 250:425–440
De Vos CR, Lubberding HJ, Bienfait HF (1986) Rhizosphere acidification as a response to iron deficiency in bean plants. Plant Physiol 81:842–846
Garnett TP, Shabala SN, Smethurst PJ, Newman IA (2001) Simultaneous measurement of ammonium, nitrate and H+ fluxes along the length of eucalypt roots. Plant Soil 236:55–62
Hawkesford MJ, Davidian J-C, Grignon C (1993) Sulphate/H+ cotransport in plasma-membrane vesicles isolated from roots of Brassica napus L: increased transport in membranes isolated from sulphur-starved plants. Planta 190:297–304
Hawkesford MJ, Buchner P, Hopkins L, Howarth JR (2003) Sulphate uptake and transport. In: Abrol YP, Ahmad A (eds) Sulphur in plants. Kluwer, Dordrecht, pp 71–86
Haynes RJ (1990) Active ion uptake and maintenance of cation-anion balance: a critical examination of their role in regulating rhizosphere pH. Plant Soil 126:247–264
Henriksen GH, Bloom AJ, Spanswick RM (1990) Measurement of net fluxes of ammonium and nitrate at the surface of barley roots using ion-selective microelectrodes. Plant Physiol 93:271–280
Herschbach C, Rennenberg H (1994) Influence of glutathione (GSH) on net uptake of sulphate and sulphate transport in tobacco plants. J Exp Bot 45:1069–1076
Hopkins L, Parmar S, Błaszczyk A, Hesse H, Hoefgen R, Hawkesford MJ (2005) O-Acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol 138:433–440
Jahn T, Fuglsang AT, Olsson A, Brüntrup IM, Collinge DB, Volkmann D, Larsson C (1997) The 14-3-3 protein interacts directly with the C-terminal region of the plant plasma membrane H (+)-ATPase. Plant Cell 9:1805–1814
Johansson F, Sommarin M, Larsson C (1993) Fusicoccin activates the plasma membrane H+-ATPase by a mechanism involving the C-terminal inhibitory domain. Plant Cell 5:321–327
Koralewska A, Stuiver CEE, Posthumus FS, Kopriva S, Hawkesford MJ, De Kok LJ (2008) Regulation of sulfate uptake, expression of the sulfate transporters Sultr1;1 and Sultr1;2, and APS reductase in Chinese cabbage (Brassica pekinensis) as affected by atmospheric H2S nutrition and sulfate deprivation. Funct Plant Biol 35:318–327
Koralewska A, Buchner P, Stuiver CEE, Posthumus FS, Kopriva S, Hawkesford MJ, De Kok LJ (2009) Expression and activity of sulfate transporters and APS reductase in curly kale in response to sulfate deprivation and re-supply. J Plant Physiol 166:168–179
Lanfermeijer FC, Staal M, Malinowski R, Stratmann JW, Elzenga JTM (2008) Micro-electrode flux estimation confirms that the Solanum pimpinellifolium cu3 mutant still responds to systemin. Plant Physiol 146:129–139
Moore DM, Overstreet R, Jacobson L (1961) Uptake of magnesium and its interaction with calcium in excised barley roots. Plant Physiol 36:290–295
Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211:121–130
Newman IA (2001) Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant Cell Environ 24:1–14
Plassard C, Meslem M, Souche G (1999) Localization and quantification of net fluxes of H+ along maize roots by combined use of pH-indicator dye videodensitometry and H+-selective microelectrodes. Plant Soil 211:29–39
Prosser IM, Purves JV, Saker LR, Clarkson DT (2001) Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. J Exp Bot 52:113–121
Reich M, Aghajanzadeh T, Stuiver CEE, Koralewska A, De Kok LJ (2015) Impact of sulfate salinity on the uptake and metabolism of sulfur in Chinese cabbage. In: De Kok LJ, Hawkesford MJ, Rennenberg H, Saito K, Schnug E (eds) Molecular physiology and ecophysiology of sulfur. Springer, Cham, pp 227–238
Reich M, Shahbaz M, Prajapati DH, Parmar S, Hawkesford MJ, De Kok LJ (2016) Interactions of sulfate with other nutrients as revealed by H2S fumigation of Chinese cabbage. Front Plant Sci 7:541
Rouached H, Wirtz M, Alary R, Hell R, Arpat AB, Davidian J-C, Fourcroy P, Berthomieu P (2008) Differential regulation of the expression of two high-affinity sulfate transporters, SULTR1;1 and SULTR1;2, in Arabidopsis. Plant Physiol 147:897–911
Rubinigg M, Stulen I, Elzenga JTM, Colmer TD (2002) Spatial patterns of radial oxygen loss and nitrate net flux along adventitious roots of rice raised in aerated or stagnant solution. Funct Plant Biol 29:1475–1481
Saito K (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr Opin Plant Biol 3:188–195
Schimansky C (1981) The influence of certain experimental parameters on the flux characteristics of Mg-28 in the case of barley seedlings in hydroculture experiments. Landwirtsch Forsch 34:154–163
Shabala SN, Newman IA, Morris J (1997) Oscillations in H+ and Ca2+ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiol 113:111–118
Shabala SN, Pang J, Zhou M, Shabala L, Cuin TA, Nick P, Wegner LH (2009) Electrical signalling and cytokinins mediate effects of light and root cutting on ion uptake in intact plants. Plant Cell Environ 32:194–207
Shin R, Jez JM, Basra A, Zhang B, Schachtman DP (2011) 14-3-3 Proteins fine-tune plant nutrient metabolism. FEBS Lett 585:143–147
Smith FW, Ealing PM, Hawkesford MJ, Clarkson DT (1995) Plant members of a family of sulfate transporters reveal functional subtypes. Proc Natl Acad Sci U S A 92:9373–9377
Staal M, De Cnodder T, Simon D, Vandenbussche F, Van Der Straeten D, Verbelen JP, Elzenga JTM, Vissenberg K (2011) Apoplastic alkalinization is instrumental for the inhibition of cell elongation in the Arabidopsis root by the ethylene precursor 1-aminocyclopropane-1-carboxylic acid. Plant Physiol 155:2049–2055
Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, de Almeida EJ, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci U S A 94:11102–11107
Taylor AR, Bloom AJ (1998) Ammonium, nitrate, and H+ fluxes along the maize root. Plant Cell Environ 21:1255–1263
Vreeburg RA, Benschop JJ, Peeters AJ, Colmer TD, Ammerlaan AH, Staal M, Elzenga JTM, Staals RHJ, Darley CP, McQueen-Mason SJ, Voesenek LA (2005) Ethylene regulates fast apoplastic acidification and expansin. A transcription during submergence-induced petiole elongation in Rumex palustris. Plant J 43:597–610
Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29:465–473
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Reich, M., Staal, M., De Kok, L.J., Elzenga, J.T.M. (2017). Localization of Sulfate Uptake and pH Changes at Sulfur-Deprived Roots of Intact Brassica pekinensis Seedlings by Using H+-Selective Microelectrodes. In: De Kok, L., Hawkesford, M., Haneklaus, S., Schnug, E. (eds) Sulfur Metabolism in Higher Plants - Fundamental, Environmental and Agricultural Aspects. Proceedings of the International Plant Sulfur Workshop. Springer, Cham. https://doi.org/10.1007/978-3-319-56526-2_16
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DOI: https://doi.org/10.1007/978-3-319-56526-2_16
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