Biologia plantarum 58:507-514, 2014 | DOI: 10.1007/s10535-014-0438-1

Plasma membrane H+-ATPase in sorghum roots as affected by potassium deficiency and nitrogen sources

J. C. Alvarez-Pizarro1, E. Gomes-Filho1,*, J. T. Prisco1, M. F. Grossi-De-Sá2, O. B. De Oliveira-Neto2,3, R. Da Rocha Fragoso2
1 Departamento de Bioquímica e Biologia Molecular, Instituto Nacional de Ciência e Tecnologia em Salinidade, Universidade Federal do Ceará, Fortaleza, Ceará-Brazil
2 Embrapa Recursos Genéticos e Biotecnologia, Parque Estação Biológica, Brasília, DF, Brazil
3 Centro Universitário Unieuro, Brasília, DF, Brazil

We studied the influence of inorganic nitrogen sources (NO3 - or NH4 +) and potassium deficiency on expression and activity of plasma membrane (PM) H+-ATPase in sorghum roots. After 15 d of cultivation at 0.2 mM K+, the plants were transferred to solutions lacking K+ for 2 d. Then, K+ depletion assays were performed in the presence or absence of vanadate. Further, PMs from K+-starved roots were extracted and used for the kinetic characterization of ATP hydrolytic activity and the immunodetection of PM H+-ATPase. Two major genes coding PM H+-ATPase (SBA1 and SBA2) were analyzed by real-time PCR. PM H+-ATPase exhibited a higher Vmax and Km in NH4 +-fed roots compared with NO3 - -fed roots. The optimum pH of the enzyme was slightly lower in NO3 - -fed roots than in NH4 +-fed roots. The vanadate sensitivity was similar. The expressions of SBA1 and SBA2 increased in roots grown under NH4 +. Concomitantly, an increased content of the enzyme in PM was observed. The initial rate of K+ uptake did not differ between plants grown with NO3 - or NH4 +, but it was significantly reduced by vanadate in NH4 +-grown plants.

Keywords: ammonium; immunodetection; K+ uptake; nitrate; Sorghum bicolor; vanadate
Subjects: plasma membrane; ATPase; potassium; nitrogen; ammonium; nitrate; vanadate; phylogenetic analysis; sorghum

Received: October 17, 2013; Revised: November 29, 2013; Accepted: January 10, 2014; Published: September 1, 2014Show citation

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Alvarez-Pizarro, J.C., Gomes-Filho, E., Prisco, J.T., Grossi-De-Sá, M.F., Oliveira-Neto, O.B., & Da Rocha Fragoso, R. (2014). Plasma membrane H+-ATPase in sorghum roots as affected by potassium deficiency and nitrogen sources. Biologia plantarum, 58(3), 507-514. doi: 10.1007/s10535-014-0438-1.
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    References

    1. Alvarez-Pizarro, J.C., Gomes-Filho, E., Prisco, J.T., Grossi-de-Sá, M.F., Oliveira-Neto, O.B.: NH4 +-stimulated low-K+ uptake is associated with the induction of H+ extrusion by the plasma membrane H+-ATPase in sorghum roots under K+ deficiency. - J. Plant Physiol. 168: 1617-1626, 2011. Go to original source...
    2. Arango, M., Gévaudant, F., Oufattole, M., Boutry, M.: The plasma membrane proton pump ATPase: the significance of gene subfamilies. - Planta 216: 355-365, 2003.
    3. Bradford, M.M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    4. Britto, D.T., Kronzucker, H.J.: NH4 + toxicity in higher plants: a critical review. - J. Plant Physiol. 159: 567-584, 2002. Go to original source...
    5. Campos, F., Perez-Castiñeira, J.R., Villalba, J.M., Culiañez-Marciá, F.A., Sánchez, F., Serrano, R.: Localization of plasma membrane H+-ATPase in nodules of Phaseolus vulgaris L. - Plant mol. Biol. 32: 1043-1053, 1996. Go to original source...
    6. Claassen, N., Barber, S.A.: A method for characterizing the relation between nutrient concentration and flux into roots of intact plants. - Plant Physiol. 54: 564-568, 1974. Go to original source...
    7. Dell'Orto, M., Santi, S., De Nisi, P., Cesco, S., Varanini, Z., Zocchi, G., Pinton, R.: Development of Fe-deficiency responses in cucumber (Cucumis sativus L.) roots: involvement of plasma membrane H+-ATPase activity. - J. exp. Bot. 51: 695-701, 2000.
    8. De Souza, A.M., Carvalho, T.L.G., Sabino, P.M., Vives, D., Fontes, C.F.L., Lopes, A.G., Caruso-Neves, C.: Characterization and partial isolation of ouabain-insensitive Na+- ATPase in MDCK I cells. - Biochimie 89: 1425-1432, 2007. Go to original source...
    9. Frias, I., Caldeira, M.T., Pérez-Castiñeira, J.R., Navarro-Aviñó, J.P., Culiañez-Maciá, F.A., Kuppinger, O., Stransky, H., Pagés, M., Hager, A., Serrano, R.: A major isoform of the maize plasma membrane H+-ATPase: characterization and induction by auxin in coleoptiles. - Plant Cell 8: 1533-1544, 1996.
    10. Gaxiola, R.A., Palmgren, M.G., Schumacher, K.: Plant proton pumps. - FEBS Lett. 581: 2204-2214, 2007. Go to original source...
    11. Gerendás, J., Ratcliffe, R.G., Sattelmacher, B.: Relationship between intracellular pH and N metabolism in maize (Zea mays L.) roots. - Plant Soil 155/156: 167-170, 1993. Go to original source...
    12. Hadži-Tašković Šukalović, V., Vuletić, M.: Heterogeneity of maize root mitochondria from plants grown in the presence of ammonium. - Biol. Plant. 44: 101-104, 2001.
    13. Hirsch, R., Lewis, B.D., Spalding, E.P., Sussman, M.R.: A role for the AKT1 potassium channel in plant nutrition. - Science 280: 918-921, 1998. Go to original source...
    14. Lang, B., Kaiser, W.: Solute content and energy status of roots of barley plants cultivated at different pH on nitrate- or ammonium-nitrogen. - New Phytol. 128: 451-459, 1994. Go to original source...
    15. Lefebvre, B., Arango, M., Oufattole, M., Crouzet, J., Purnelle, B., Boutry, M.: Identification of a Nicotiana plumbaginifolia plasma membrane H+-ATPase gene expressed in the pollen tube. - Plant mol. Biol. 58: 775-787, 2005. Go to original source...
    16. Marschner, H. (ed): Mineral Nutrition of Higher Plants. - Academic Press, London 1995.
    17. Martínez-Cordero, M., Martínez, V., Rubio, F.: High-affinity K+ uptake in pepper plants. - J. exp. Bot. 56: 1553-1562, 2005. Go to original source...
    18. Monreal, J.A., Feria, A.B., Vinardell, J.M., Vidal, J., Echevarría, C., Garcia-Mauriño, S.: ABA modulates the degradation of phosphoenolpyruvate carboxylase kinase in sorghum leaves. - FEBS Lett. 581: 3468-3472, 2007. Go to original source...
    19. Palmgren, M.G.: Plant plasma membrane H+-ATPase: power house for nutrient uptake. - Annu. Rev. Plant Physiol. Plant mol. Biol. 52: 817-845, 2001. Go to original source...
    20. Palmgren, M.G., Christensen, G.: Functional comparisons between plant plasma membrane H+-ATPase isoforms expressed in yeast. - J. biol. Chem. 269: 3027-3033, 1994.
    21. Palmgren, M.G., Harper, J.F.: Pumping with plant P-type ATPases. - J. exp. Bot. 50: 883-893, 1999. Go to original source...
    22. Palmgren, M.G., Sommarin, M., Serrano, R., Larsson, C.: Identification of an autoinhibitory domain in the C-terminal region of the plant plasma membrane H+-ATPase. - J. biol. Chem. 266: 20470-20475, 1991.
    23. Paterson, A.H., Bowers, J.E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., Haberer, G., Hellsten, U., Mitros, T., Poliakov, A., Schmutz, J., Spannagl, M., Tang, H., Wang, X., Wicker, T., Bharti, A.K., Chapman, J., Feltus, F.A., Gowik, U., Grigoriev, I.V., Lyons, E., Maher, C.A., Martis, M., Narechania, A., Otillar, R.P., Penning, B.W., Salamov, A.A., Wang, Y., Zhang, L., Carpita, N.C., Freeling, M., Gingle, A.R., Hash, C.T., Keller, B., Klein, P., Kresovich, S., McCann, M.C., Ming, R., Peterson, D.G., Mehboob-ur-Rahman, Ware, D., Westhoff, P., Mayer, K.F., Messing, J., Rokhsar, D.S.: The Sorghum bicolor genome and the diversification of grasses. - Nature 457: 551-556, 2009. Go to original source...
    24. Roldán, M., Donaire, J.P., Pardo, J.M., Serrano, R.: Regulation of root plasma membrane H+-ATPase in sunflower seedlings. - Plant Sci. 79: 163-172, 1991. Go to original source...
    25. Ruan, J., Gerendás, J., Härdter, R., Sattelmacher, B.: Effect of nitrogen form and root-zone pH on growth and nitrogen uptake of tea (Camellia sinensis) plants. - Ann. Bot. 99: 301-310, 2007. Go to original source...
    26. Rubio, F., Nieves-Cordones, M., Alemán, F., Martínez, V.: Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the high-affinity range of concentration. - Physiol. Plant. 134: 598-608, 2008. Go to original source...
    27. Samuels, A.L., Fernando, M., Glass, A.D.M.: Immunofluorescent localization of plasma membrane H+-ATPase in barley roots and effects of K+ nutrition. - Plant Physiol. 99: 1509-1514, 1992. Go to original source...
    28. Santa-María, G.E., Danna, C.H., Czibener, C.: High-affinity potassium transport in barley roots. Ammonium-sensitive and -insensitive pathways. - Plant Physiol. 123: 297-306, 2000. Go to original source...
    29. Santi, S., Schmidt, W.: Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. - New Phytol. 183: 1072-1084, 2009. Go to original source...
    30. Shen, H., Chen, J., Wang, Z., Yang, C., Sasaki, T., Yamamoto, Y., Matsumoto, H., Yan, X.: Root plasma membrane H+-ATPase is involved in the adaptation of soybean phosphorus adaptation. - J. exp. Bot. 57: 1353-1362, 2006. Go to original source...
    31. Shih, C., Chu, I.K., Yip, W.K., Lo, C.: Differential expression of two flavonoid 3'-hydrolase cDNAs involved in biosynthesis of anthocyanin pigments and 3-deoxyanthocyanidin phytoalexins in sorghum. - Plant Cell Physiol. 47: 1412-1419, 2006. Go to original source...
    32. Spalding, E.P., Hirsch, R.E., Lewis, D.R., Qi, Z., Sussman, M.R., Lewis, B.D.: Potassium uptake supporting plant growth in the absence of AKT1 channel activity. - J. gen. Physiol. 113: 909-918, 1999. Go to original source...
    33. Sperandio, M.V.L., Santos, L.A., Bucher, C.A., Fernandes, M.S., Souza, S.R.: Isoforms of plasma membrane H+-ATPase in rice roots and shoot are differentially induced by starvation and resupply of NO3 - or NH4 +. - Plant Sci. 180: 251-258, 2011. Go to original source...
    34. Van Beusichem, M.L., Kirkby, E.A., Baas, R.: Influence of nitrate and ammonium nutrition on the uptake, assimilation, and distribution of nutrients in Ricinus communis. - Plant Physiol. 86: 914-921, 1988. Go to original source...
    35. Widell, S., Lundborg, T., Larsson, C.: Plasma membrane from oat prepared by partition in an aqueous polymer two-phase system. - Plant Physiol. 70: 1429-1435, 1982. Go to original source...
    36. Yamashita, K., Kasai, M., Ezaki, B., Shibasaka, M., Yamamoto, Y., Matsumoto, H., Sasakawa, M.: Stimulation of H+ extrusion and plasma membrane H+-ATPase activity of barley roots by ammonium treatment. - Soil Sci. Plant Nutr. 41: 133-140, 1995. Go to original source...
    37. Yan, F., Feuerle, R., Schäffer, S., Fortmeier, H., Schubert, S.: Adaptation of active proton pumping and plasmalemma ATPase activity of corn roots to low root medium pH. - Plant Physiol. 117: 311-319, 1998. Go to original source...
    38. Yan, F., Zhu, Y., Müller, C., Zörb, C., Schubert, S.: Adaptation of H+-pumping and plasma membrane H+-ATPase activity in proteoid roots of white lupin under phosphate deficiency. - Plant Physiol. 129: 50-63, 2002. Go to original source...
    39. Zhu, Y., Di, T., Xu, G., Chen, X., Zeng, H., Yan, F., Shen, Q.: Adaptation of plasma membrane H+-ATPase of rice roots to low pH as related to ammonium nutrition. - Plant Cell Environ. 32: 1428-1440, 2009. Go to original source...

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