Navegar

Colección

Datos Estadísticas

Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Plant cell vacuoles occupy up to 90% of the cell volume and, beyond their physiological function, are constantly subjected to water and solute exchange. The osmotic flow and vacuole volume dynamics relies on the vacuole membrane -the tonoplast- and its capacity to regulate its permeability to both water and solutes. The osmotic permeability coefficient (Pf) is the parameter that better characterizes the water transport when submitted to an osmotic gradient. Usually, Pf determinations are made in vitro from the initial rate of volume change, when a fast (almost instantaneous) osmolality change occurs. When aquaporins are present, it is accepted that initial volume changes are only due to water movements. However, in living cells osmotic changes are not necessarily abrupt but gradually imposed. Under these conditions, water flux might not be the only relevant driving force shaping the vacuole volume response. In this study, we quantitatively investigated volume dynamics of isolated Beta vulgaris root vacuoles under progressively applied osmotic gradients at different pH, a condition that modifies the tonoplast Pf. We followed the vacuole volume changes while simultaneously determining the external osmolality time-courses and analyzing these data with mathematical modeling. Our findings indicate that vacuole volume changes, under progressively applied osmotic gradients, would not depend on the membrane elastic properties, nor on the non-osmotic volume of the vacuole, but on water and solute fluxes across the tonoplast. We found that the volume of the vacuole at the steady state is determined by the ratio of water to solute permeabilites (Pf /Ps), which in turn is ruled by pH. The dependence of the permeability ratio on pH can be interpreted in terms of the degree of aquaporin inhibition and the consequently solute transport modulation. This is relevant in many plant organs such as root, leaves, cotyledons, or stems that perform extensive rhythmic growth movements, which very likely involve considerable cell volume changes within seconds to hours. © 2016 Vitali, Sutka, Amodeo, Chara and Ozu.

Registro:

Documento: Artículo
Título:The water to solute permeability ratio governs the osmotic volume dynamics in beetroot vacuoles
Autor:Vitali, V.; Sutka, M.; Amodeo, G.; Chara, O.; Ozu, M.
Filiación:Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Instituto de Biodiversidad y Biología Experimental y Aplicada, Universidad de Buenos Aires and Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
System Biology Group (SysBio), Institute of Physics of Liquids and Biological Systems (IFLYSIB) CONICET, University of La Plata, La Plata, Argentina
Center for Information Services and High Performance Computing, Technische Universität Dresden, Dresden, Germany
Departamento de Fisiología y Biofísica, Facultad de Medicina, Instituto de Fisiología y Biofísica (IFIBIO-Houssay), Universidad de Buenos Aires y Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Palabras clave:Beta vulgaris; Gradual gradients; Mathematical modeling; Red beet; Simulation; Solute flux; Vacuole; Water flux
Año:2016
Volumen:7
Número:September
DOI: http://dx.doi.org/10.3389/fpls.2016.01388
Título revista:Frontiers in Plant Science
Título revista abreviado:Front. Plant Sci.
ISSN:1664462X
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_1664462X_v7_nSeptember_p_Vitali

Referencias:

  • Alexander, J.T., Factors affecting quality (1971) Advances in Sugar Beet Production: Principles and Practices, pp. 371-382. , R. T. Johnson, J. T. Alexander, G. E. Rush, and G. R. Hawkes (Ames, IA: Iowa State University Press
  • Alexandre, J., Lassalles, J.-P., Thellier, M., Electrical noise measurements on red beet vacuoles (1986) Plant Physiol, 81, pp. 1147-1150
  • Amodeo, G., Sutka, M., Dorr, R., Parisi, M., Protoplasmic pH modifies water and solute transfers in Beta vulgaris root vacuoles (2002) J. Membr. Biol, 187, pp. 175-184
  • Beauzamy, L., Nakayama, N., Boudaoud, A., Flowers under pressure: Ins and outs of turgor regulation in development (2014) Ann. Bot, 114, pp. 1517-1533
  • Blatt, M.R., Wang, Y., Leonhardt, N., Hills, A., Exploring emergent properties in cellular homeostasis using On Guard to model K+ and other ion transport in guard cells (2014) J. Plant Physiol, 171, pp. 770-778
  • Chara, O., Espelt, M.V., Krumschnabel, G., Schwarzbaum, P.J., Regulatory volume decrease and P receptor signaling in fish cells: Mechanisms, physiology, and modeling approaches (2011) J. Exp. Zool. a Ecol. Genet. Physiol, 315, pp. 175-202
  • Chen, T.H., Murata, N., Glycinebetaine protects plants against abiotic stress: Mechanisms and biotechnological applications (2011) Plant Cell Environ, 34, pp. 1-20
  • Chrispeels, M.J., Maurel, C., Aquaporins: The molecular basis of hydraulic water movement between cells? (1994) Plant Physiol, 105, pp. 9-13
  • Cosgrove, D., Steudle, E., Water relations of growing pea epicotyl segments (1981) Planta, 153, pp. 343-350
  • Davies, J.M., Hunt, I., Sanders, D., Vacuolar H+-pumping ATPase variable transport coupling ratio controlled by pH (1994) Proc. Nat. Acad. Sci. U.S.A., 91, pp. 8547-8551
  • De, D.N., (Ed.) (2000). “Functions of vacuoles,” Plant Cell Vacuoles, an Introduction, pp. 163-248. , Collingwood: CSIRO Publishing
  • Felle, H.H., PH: Signal and messenger in plant cells (2001) Plant Biol, 3, pp. 577-591
  • Felle, H.H., PH regulation in anoxic plants (2005) Ann. Bot, 96, pp. 519-532
  • Finkelstein, A., (1987) Water Movement through Lipid Bilayers, Pores, and Plasma Membranes, , New York, NY: Wiley & Sons
  • Fleurat-Lessard, P., Frangne, N., Maeshima, M., Ratajczak, R., Bonnemain, J.L., Martinoia, E., Increased expression of vacuolar aquaporin and H+-ATPase related to motor cell function in Mimosa pudica L (1997) Plant Physiol, 114, pp. 827-834
  • Franks, P.J., Buckley, T.N., Shope, J.C., Mott, K.A., Guard cell volume and pressure measured concurrently by confocal microscopy and the cell pressure probe (2001) Plant Physiol, 125, pp. 1577-1584
  • Frick, A., Järvå, M., Törnroth-Horsefield, S., Structural basis for pH gating of plant aquaporins (2013) FEBS Lett, 587, pp. 989-993
  • Giaquinta, R.T., Sucrose hydrolysis in relation to phloem translocation in Beta vulgaris (1977) Plant Physiol, 60, pp. 339-343
  • Giaquinta, R.T., Sucrose translocation and storage in the sugar beet (1979) Plant Physiol, 63, pp. 828-832
  • Hafke, J.B., Hafke, Y., Smith, J.A., Lüttge, U., Thiel, G., Vacuolar malate uptake is mediated by an anion-selective inward rectifier (2003) Plant J, 35, pp. 116-128
  • Hernandez, J.A., Cristina, E., Modeling cell volume regulation in non- excitable cells: The roles of the Na+ pump and of cotransport systems (1998) Am. J. Physiol, 275, pp. C1067-C1080
  • Jarillo, J.A., Capel, J., Tang, R.H., Yang, H.Q., Alonso, J.M., Ecker, J.R., An Arabidopsis circadian clock component interacts with both CRY1 and phyB (2001) Nature, 410, pp. 487-490
  • Kedem, O., Katchalsky, A., Thermodynamic analysis of the permeability of biological membranes to non-electrolytes (1958) Biochim. Biophys. Acta, 27, pp. 229-246
  • Kholodova, V.P., Bolyakina, Y.P., Meshcheryakov, A.B., Ritcher, E., Ehwald, R., Mashkova, A.K., Transport and distribution of solutes in sugar beet roots (1989) Structural and Functional Aspects of Transport in Roots, pp. 79-84. , B. C. Loughman, O. Gasparikova, and J. Kolek (Dordrecht: Kluwer Academic Publishers
  • Kronzucker, H.J., Britto, D.T., Sodium transport in plants: A critical review (2011) New Phytol, 189, pp. 54-81
  • Kulichikhin, K.Y., Greenway, H., Byrne, L., Colmer, T.D., Regulation of intracellular pH during anoxia in rice coleoptiles in acidic and near neutral conditions (2009) J. Exp. Bot, 60, pp. 2119-2128
  • Kuwagata, T., Murai-Hatano, M., Osmotic water permeability of plasma and vacuolar membranes in protoplasts II: Theoretical basis (2007) J. Plant Res, 120, pp. 193-208
  • Leigh, R.A., Branton, D., Isolation of vacuoles from root storage tissue of Beta vulgaris L (1976) Plant Physiol, 58, pp. 656-662
  • Leigh, R.A., Rees, T., Fuller, W.A., Banfield, J., The location of acid invertase activity and sucrose in vacuoles of storage roots of beetroot (Beta vulgaris L.) (1979) Biochem. J, 178, pp. 539-547
  • Leitaõ, L., Prista, C., Moura, T.F., Loureiro-Dias, M.C., Soveral, G., Grapevine aquaporins: Gating of a tonoplast intrinsic protein (TIP2;1) by cytosolic pH (2012) Plos ONE, 7, pp. e33219
  • Lucio, A.D., Santos, R.A., Mesquita, O.N., Measurements and modeling of water transport and osmoregulation in a single kidney cell using (2003) Phys. Rev. E Stat. Nonlin. Soft. Matter. Phys, 68, pp. 41906-41915
  • Ludewig, F., Flügge, U.-I., Role of metabolite transporters in source- sink carbon allocation (2013) Front. Plant Sci, 4, p. 231
  • Macrobbie, E.A.C., Osmotic effects on vacuolar ion release in guard cells (2006) Proc. Natl. Acad. Sci. U.S.A., 103, pp. 135-1140
  • Martinière, A., Bassil, E., Jublanc, E., Alcon, C., Reguera, M., Sentenac, H., In vivo intracellular pH measurements in Tobacco and Arabidopsis reveal an unexpected pH gradient in the endomembrane system (2013) Plant Cell, 25, pp. 4028-4043
  • Martinoia, E., Meyer, S., De Angeli, A., Nagy, R., Vacuolar transporters in their physiological context (2012) Annu. Rev. Plant Biol, 63, pp. 183-213
  • Matile, P., Biochemistry and function of vacuoles (1978) Ann. Rev. Plant Physiol. Plant Mol. Biol, 29, pp. 193-213
  • Mauch, F., Staehelin, L.A., Functional implications of the subcellular localization of ethylene-induced chitinase and β-1,3-Glucanase in bean leaves (1989) Plant Cell, 1, pp. 447-457
  • Milford, G.F.J., Plant Structure and Crop Physiology (2006) A. P. Draycott, , Sugar Beet, Oxford, UK: Blackwell Publishing Ltd
  • Mills, D., Robinson, K., Hodges, T.K., Sodium and potassium fluxes and compartmentation in roots of a triplex and oat (1985) Plant Physiol, 78, pp. 500-509
  • Morillon, R., Lassalles, J.P., Osmotic water permeability of isolated vacuoles (1999) Planta, 210, pp. 80-84
  • Moshelion, M., Moran, N., Chaumont, F., Dynamic changes in the osmotic water permeability of protoplast plasma membrane (2004) Plant Physiol, 135, pp. 2301-2317
  • Murai-Hatano, M., Kuwagata, T., Osmotic water permeability of plasma and vacuolar membranes in protoplasts I. High osmotic water permeability in radish (Raphanus sativus) root cells as measured by a new method (2007) J. Plant Res, 120, pp. 175-189
  • Németh-Cahalan, K.L., Hall, J.E., Ph and Calcium regulate the water permeability of aquaporin 0 (2000) J. Biol. Chem, 275, pp. 6777-6782
  • Neuhaus, H.E., Transport of primary metabolites across the plant vacuolar membrane (2007) FEBS Lett, 581, pp. 2223-2226
  • Nobel, P.S., (2009) Water, in Physicochemical and Environmental Plant Physiology, pp. 45-99. , 4th Edn. (San Diego, CA: Academic Press; Elsevier
  • Ozu, M., Dorr, R.A., Gutiérrez, F., Politi, M.T., Toriano, R., Human AQP1 is a constitutively open channel that closes by a membrane-tension- mediated mechanism (2013) Biophys. J., 104, pp. 85-95
  • Peyronnet, R., Tran, D., Girault, T., Frachisse, J.-M., Mechanosensitive channels: Feeling tension in a world under pressure (2014) Front. Plant Sci, 5, p. 558
  • Pickard, W.F., Modelling the swelling assay for aquaporin expression (2008) J. Math. Biol, 57, pp. 883-903
  • Pourcel, L., Irani, N.G., Lu, Y., Riedl, K., Schwartz, S., The formation of anthocyanic vacuolar inclusions in Arabidopsis thaliana and implications for the sequestrations of anthocyanin pigments (2010) Mol. Plant, 3, pp. 78-90
  • Preston, G.M., Piazza Carroll, T., Guggino, W.B., Agre, P., Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein (1992) Science, 256, pp. 385-387
  • Richer, E., Ehwald, R., Apoplastic mobility of sucrose in storage parenchyma of sugar beet (1983) Physiol. Plant, 58, pp. 263-268
  • Siefritz, F., Otto, B., Bienert, G.P., Van Der Krol, A., Kaldenhoff, R., The plasma membrane aquaporin NtAQP1 is a key component of the leaf unfolding mechanism in tobacco (2004) Plant J, 37, pp. 147-155
  • Sommer, A., Mahlknecht, G., Obermeyer, G., Measuring the osmotic water permeability of the plant protoplast plasma membrane: Implication of the non-osmotic volume (2007) J. Membr. Biol, 215, pp. 111-123
  • Soto, G., Fox, R., Ayub, N., Alleva, K., Guaimas, F., Erijman, E.J., TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana (2010) Plant J, 64, pp. 1038-1047
  • Steudle, E., Boyer, J.S., Hydraulic resistance to radial water flow in growing hypocotyl of soybean measured by a new pressure-perfusion technique (1985) Planta, 164, pp. 189-200
  • Sutka, M., Alleva, K., Parisi, M., Amodeo, G., Tonoplast vesicles of Beta vulgaris storage root show funtional aquaporins regulated by protons (2005) Biol. Cell, 97, pp. 837-846
  • Swanson, S.J., Choi, W.-G., Chanoca, A., Gilroy, S., In vivo imaging of Ca2+, pH, and reactive oxygen species using fluorescent probes in plants (2011) Annu. Rev. Plant Biol, 62, pp. 273-297
  • Tomos, A.D., Leigh, R.A., Palta, J.A., Williams, J.H.H., Sucrose and cell water relations (1992) C. J. Pollock and J. F. Farrar, pp. 71-89. , Carbon Partitioning within and between Organisms, Oxford: Biosis Scientific Publishers
  • Törnroth-Horsefield, S., Wang, Y., Hedfalk, K., Johanson, U., Karlsson, M., Tajkhorshid, E., Structural mechanism of plant aquaporin gating (2006) Nature, 439, pp. 688-694
  • Tournaire-Roux, C., Sutka, M., Javot, H., Gout, E., Gerbeau, P., Luu, D.T., Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins (2003) Nature, 425, pp. 393-397
  • Volkov, V., Salinity tolerance in plants. Quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes (2015) Front. Plant Sci, 6, p. 873
  • Ward, J.M., Schroeder, J.I., Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure (1994) Plant Cell, 6, pp. 669-683
  • Wendler, S., Zimmermann, U., Compartment analysis of plant cells by means of turgor pressure relation: I. Theoretical considerations (1985) J. Membr. Biol, 85, pp. 121-132
  • Wink, M., Compartmentation of secondary metabolites and xenobiotics in plant vacuoles (1997) The Plant Vacuole, Advances in Botanical Research, pp. 141-169. , R. A. Leigh and D. Sanders (London: Academic Press
  • Wyse, R.E., Sucrose uptake by sugar beet tap root tissue (1979) Pant Physiol, 64, pp. 837-841
  • Zhang, W.H., Tyerman, S.D., Inhibition of water channels by HgCl2 in intact wheat root cells (1999) Plant Physiol, 120, pp. 849-858

Citas:

---------- APA ----------
Vitali, V., Sutka, M., Amodeo, G., Chara, O. & Ozu, M. (2016) . The water to solute permeability ratio governs the osmotic volume dynamics in beetroot vacuoles. Frontiers in Plant Science, 7(September).
http://dx.doi.org/10.3389/fpls.2016.01388
---------- CHICAGO ----------
Vitali, V., Sutka, M., Amodeo, G., Chara, O., Ozu, M. "The water to solute permeability ratio governs the osmotic volume dynamics in beetroot vacuoles" . Frontiers in Plant Science 7, no. September (2016).
http://dx.doi.org/10.3389/fpls.2016.01388
---------- MLA ----------
Vitali, V., Sutka, M., Amodeo, G., Chara, O., Ozu, M. "The water to solute permeability ratio governs the osmotic volume dynamics in beetroot vacuoles" . Frontiers in Plant Science, vol. 7, no. September, 2016.
http://dx.doi.org/10.3389/fpls.2016.01388
---------- VANCOUVER ----------
Vitali, V., Sutka, M., Amodeo, G., Chara, O., Ozu, M. The water to solute permeability ratio governs the osmotic volume dynamics in beetroot vacuoles. Front. Plant Sci. 2016;7(September).
http://dx.doi.org/10.3389/fpls.2016.01388