Artículo

Este artículo es de Acceso Abierto y puede ser descargado en su versión final desde nuestro repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

In plant sexual reproduction, water and solute movement are tightly regulated, suggesting the involvement of aquaporins. We previously identified TIP5;1 and TIP1;3 as the only Arabidopsis aquaporin genes that are selectively and highly expressed in mature pollen, and showed that they can transport both water and urea when expressed in Xenopus oocytes. Here, we show that TIP5;1 has unusual characteristics, as its water transport activity is regulated by pH. Analysis of the water transport activity of a mutant version of TIP5;1 (TIP5;1-H131A) and amino acid alignment with other plant aquaporins regulated by pH suggested that a conserved motif is involved in pH sensing. GFP-TIP5;1 is located in the mitochondria of pollen tubes. The single mutants tip1;3 and tip5;1, as well as the tip1;3 tip5;1 double mutant, are fertile, but all mutants had shorter than normal pollen tubes when germinated in vitro in the absence of exogenous nitrogen. Thus, we propose that TIP5;1 and TIP1;3 are involved in nitrogen recycling in pollen tubes of Arabidopsis thaliana. © 2010 The Authors. The Plant Journal © 2010 Blackwell Publishing Ltd.

Registro:

Documento: Artículo
Título:TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana
Autor:Soto, G.; Fox, R.; Ayub, N.; Alleva, K.; Guaimas, F.; Erijman, E.J.; Mazzella, A.; Amodeo, G.; Muschietti, J.
Filiación:Instituto de Ingeniería Genética y Biología Molecular (INGEBI-CONICET), Vuelta de Obligado 2490 Piso 2, 1428 Buenos Aires, Argentina
Instituto de Genética 'Ewald A. Favret', Centro de Investigaciõn en Ciencias Veterinarias y Agronõmicas (CICVyA), Instituto Nacional de Tecnología Agropecuaria (INTA), Castelar, Argentina
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Departamento de Química Orgánica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:aquaporins; mitochondria; nitrogen metabolism; pH sensing; urea; Aquaporins; Arabidopsis; Arabidopsis thaliana; Double mutants; In-vitro; nitrogen metabolism; pH sensing; Plant sexual reproduction; Pollen tube; Remobilization; Single mutant; Solute movement; Water transport; Xenopus oocyte; Amino acids; Glycoproteins; Metabolism; Mitochondria; pH sensors; Urea; Nitrogen; aquaporin; Arabidopsis protein; nitrogen; plant RNA; TIP5;1 protein, Arabidopsis; water; Arabidopsis; article; gene expression regulation; genetics; metabolism; mitochondrion; pH; phylogeny; pollen tube; Aquaporins; Arabidopsis; Arabidopsis Proteins; Hydrogen-Ion Concentration; Mitochondria; Mutagenesis, Insertional; Nitrogen; Phylogeny; Pollen Tube; RNA, Plant; Water; Arabidopsis; Arabidopsis thaliana
Año:2010
Volumen:64
Número:6
Página de inicio:1038
Página de fin:1047
DOI: http://dx.doi.org/10.1111/j.1365-313X.2010.04395.x
Título revista:Plant Journal
Título revista abreviado:Plant J.
ISSN:09607412
CODEN:PLJUE
CAS:aquaporin, 215587-75-0; nitrogen, 7727-37-9; water, 7732-18-5; Aquaporins; Arabidopsis Proteins; Nitrogen, 7727-37-9; RNA, Plant; TIP5;1 protein, Arabidopsis; Water, 7732-18-5
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_09607412_v64_n6_p1038_Soto.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09607412_v64_n6_p1038_Soto

Referencias:

  • Abramoff, M.D., Magalhaes, P.J., Ram, S.J., Image processing with imageJ (2004) Biophotonics International, 11 (7), pp. 36-41
  • Amiry-Moghaddam, M., Lindland, H., Zelenin, S., Roberg, B.A., Gundersen, B.B., Petersen, P., Rinvik, E., Ottersen, O.P., Brain mitochondria contain aquaporin water channels: Evidence for the expression of a short AQP9 isoform in the inner mitochondrial membrane (2005) FASEB Journal, 19 (11), pp. 1459-1467. , DOI 10.1096/fj.04-3515com
  • Beebo, A., Thomas, D., Der, C., Sanchez, L., Leborgne-Castel, N., Marty, F., Schoefs, B., Bouhidel, K., Life with and without AtTIP1;1, an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles (2009) Plant Mol. Biol., 70, pp. 193-209
  • Bienert, G.P., Moller, A.L.B., Kristiansen, K.A., Schulz, A., Moller, I.M., Schjoerring, J.K., Jahn, T.P., Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes (2007) Journal of Biological Chemistry, 282 (2), pp. 1183-1192. , http://www.jbc.org/cgi/reprint/282/2/1183, DOI 10.1074/jbc.M603761200
  • Boavida, L.C., McCormick, S., Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana (2007) Plant Journal, 52 (3), pp. 570-582. , DOI 10.1111/j.1365-313X.2007.03248.x
  • Brownfield, D.L., Todd, C.D., Deyholos, M.K., Analysis of Arabidopsis arginase gene transcription patterns indicates specific biological functions for recently diverged paralogs (2008) Plant Mol. Biol., 67, pp. 429-440
  • Calamita, G., Ferri, D., Gena, P., Liquori, G.E., Cavalier, A., Thomas, D., Svelto, M., The inner mitochondrial membrane has aquaporin-8 water channels and is highly permeable to water (2005) Journal of Biological Chemistry, 280 (17), pp. 17149-17153. , DOI 10.1074/jbc.C400595200
  • Calamita, G., Gena, P., Meleleo, D., Ferri, D., Svelto, M., Water permeability of rat liver mitochondria: A biophysical study (2006) Biochimica et Biophysica Acta - Biomembranes, 1758 (8), pp. 1018-1024. , DOI 10.1016/j.bbamem.2006.07.008, PII S0005273606002707, Auquporins
  • Clough, S.J., Bent, A.F., Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana (1998) Plant Journal, 16 (6), pp. 735-743
  • Faye, L., Greenwood, J.S., Chrispeels, M.J., Urease in jack bean (Canavalia ensiformis [L.] DC) seeds is a cytosolic protein (1986) Planta, 168, pp. 579-585
  • Ferri, D., Mazzone, A., Liquori, G.E., Cassano, G., Svelto, M., Calamita, G., Ontogeny, distribution, and possible functional implications of an unusual aquaporin, AQP8, in mouse liver (2003) Hepatology, 38 (4), pp. 947-957. , DOI 10.1053/jhep.2003.50397
  • Fischer, M., Kaldenhoff, R., On the pH regulation of plant aquaporins (2008) J. Biol. Chem., 283, pp. 33889-33892
  • Flores, T., Todd, C.D., Tovar-Mendez, A., Dhanoa, P.K., Correa-Aragunde, N., Hoyos, M.E., Brownfield, D.M., Polacco, J.C., Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development (2008) Plant Physiology, 147 (4), pp. 1936-1946. , http://www.plantphysiol.org/cgi/reprint/147/4/1936, DOI 10.1104/pp.108.121459
  • Gena, P., Fanelli, E., Brenner, C., Svelto, M., Calamita, G., News and views on mitochondrial water transport (2009) Front. Biosci., 14, pp. 4189-4198
  • Glaser, E., Sjoling, S., Tanudji, M., Whelan, J., Mitochondrial protein import in plants: Signals, sorting, targeting, processing and regulation (1998) Plant Molecular Biology, 38 (1-2), pp. 311-338
  • Goldraij, A., Polacco, J.C., Arginase is inoperative in developing soybean embryos (1999) Plant Physiology, 119 (1), pp. 297-303
  • Goldraij, A., Polacco, J.C., Arginine degradation by arginase in mitochondria of soybean seedling cotyledons (2000) Planta, 210 (4), pp. 652-658
  • Gomes, D., Agasse, A., Thiebaud, P., Delrot, S., Geros, H., Chaumont, F., Aquaporins are multifunctional water and solute transporters highly divergent in living organisms (2009) Biochim. Biophys. Acta, 1788, pp. 1213-1228
  • Harrison, S.J., Mott, E.K., Parsley, K., Aspinall, S., Gray, J.C., Cottage, A., A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation (2006) Plant Methods, 2, p. 19
  • Heazlewood, J.L., Verboom, R.E., Tonti-Filippini, J., Small, I., Millar, A.H., SUBA: The Arabidopsis subcellular database (2007) Nucleic Acids Research, 35 (SUPPL. 1), pp. D213-D218. , DOI 10.1093/nar/gkl863
  • Johnson-Brousseau, S.A., McCormick, S., A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes (2004) Plant Journal, 39 (5), pp. 761-775. , DOI 10.1111/j.1365-313X.2004.02147.x, Techniques for Molecular Analysis
  • Kaasik, A., Safiulina, D., Zharkovsky, A., Veksler, V., Regulation of mitochondrial matrix volume (2007) American Journal of Physiology - Cell Physiology, 292 (1), pp. C157-C163. , http://ajpcell.physiology.org/cgi/reprint/292/1/C157.pdf, DOI 10.1152/ajpcell.00272.2006
  • Klebl, F., Wolf, M., Sauer, N., A defect in the yeast plasma membrane urea transporter Dur3p is complemented by CpNIP1, a Nod26-like protein from zucchini (Cucurbita pepo L.), and by Arabidopsis thaliana δ-TIP or γ-TIP (2003) FEBS Letters, 547 (1-3), pp. 69-74. , DOI 10.1016/S0014-5793(03)00671-9
  • Kojima, S., Bohner, A., Von Wiren, N., Molecular mechanisms of urea transport in plants (2006) Journal of Membrane Biology, 212 (2), pp. 83-91. , DOI 10.1007/s00232-006-0868-6
  • Koncz, C., Schell, J., The promoter of the TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector (1986) Mol. Gen. Genet., 204, pp. 383-396
  • Kumar, S., Tamura, K., Nei, M., MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment (2004) Brief. Bioinform., 5, pp. 150-163
  • Lee, Y.-H., Tegeder, M., Selective expression of a novel high-affinity transport system for acidic and neutral amino acids in the tapetum cells of Arabidopsis flowers (2004) Plant Journal, 40 (1), pp. 60-74. , DOI 10.1111/j.1365-313X.2004.02186.x
  • Li, Y., Rosso, M.G., Viehoever, P., Weisshaar, B., GABI-kat simplesearch: An Arabidopsis thaliana T-DNA mutant database with detailed information for confirmed insertions (2007) Nucleic Acids Research, 35 (SUPPL. 1), pp. D874-D878. , DOI 10.1093/nar/gkl753
  • Li, L.G., Sokolov, L.N., Yang, Y.H., Li, D.P., Ting, J., Pandy, G.K., Luan, S., A mitochondrial magnesium transporter functions in Arabidopsis pollen development (2008) Mol. Plant, 1, pp. 675-685
  • Liu, L.-H., Ludewig, U., Gassert, B., Frommer, W.B., Von Wiren, N., Urea Transport by Nitrogen-Regulated Tonoplast Intrinsic Proteins in Arabidopsis (2003) Plant Physiology, 133 (3), pp. 1220-1228. , DOI 10.1104/pp.103.027409
  • Loque, D., Ludewig, U., Yuan, L., Von Wiren, N., Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH 3 transport into the vacuole (2005) Plant Physiology, 137 (2), pp. 671-680. , DOI 10.1104/pp.104.051268
  • Ma, T., Yang, B., Verkman, A.S., Cloning of a novel water and urea-permeable aquaporin from mouse expressed strongly in colon, placenta, liver, and heart (1997) Biochemical and Biophysical Research Communications, 240 (2), pp. 324-328. , DOI 10.1006/bbrc.1997.7664
  • Masclaux, C., Valadier, M.H., Brugiere, N., Morot-Gaudry, J.F., Hirel, B., Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence (2000) Planta, 211, pp. 510-518
  • Maurel, C., Plant aquaporins: Novel functions and regulation properties (2007) FEBS Letters, 581 (12), pp. 2227-2236. , DOI 10.1016/j.febslet.2007.03.021, PII S001457930700275X, Plant Transporters and Channels
  • Mazzella, M.A., Arana, M.V., Staneloni, R.J., Phytochrome control of the Arabidopsis transcriptome anticipates seedling exposure to light (2005) Plant Cell, 17, pp. 2507-2516. , et al
  • Nemeth-Cahalan, K.L., Hall, J.E., PH and calcium regulate the water permeability of aquaporin 0 (2000) J. Biol. Chem., 275, pp. 6777-6782
  • Parton, R.M., Fischer-Parton, S., Trewavas, A.J., Watahiki, M.K., Pollen tubes exhibit regular periodic membrane trafficking events in the absence of apical extension (2003) Journal of Cell Science, 116 (13), pp. 2707-2719. , DOI 10.1242/jcs.00468
  • Polacco, J.C., Krueger, R.W., Winkler, R.G., Structure and possible ureide degrading function of the ubiquitous urease of soybean (1985) Plant Physiol., 79, pp. 794-800
  • Rimon, A., Gerchman, Y., Olami, Y., Schuldiner, S., Padan, E., Replacements of histidine 226 of NhaA-Na+/H+ antiporter of Escherichia coli. Cysteine (H226C) or serine (H226S) retain both normal activity and pH sensitivity, aspartate (H226D) shifts the pH profile toward basic pH, and alanine (H226A) inactivates the carrier at all pH values (1995) J. Biol. Chem., 270, pp. 26813-26817
  • Rontein, D., Wu, W.-I., Voelker, D.R., Hanson, A.D., Mitochondrial phosphatidylserine decarboxylase from higher plants. Functional complementation in yeast, localization in plants, and overexpression in Arabidopsis (2003) Plant Physiology, 132 (3), pp. 1678-1687. , DOI 10.1104/pp.103.023242
  • Safiulina, D., Veksler, V., Zharkovsky, A., Kaasik, A., Loss of mitochondrial membrane potential is associated with increase in mitochondrial volume: Physiological role in neurones (2006) Journal of Cellular Physiology, 206 (2), pp. 347-353. , DOI 10.1002/jcp.20476
  • Saito, C., Ueda, T., Abe, H., Wada, Y., Kuroiwa, T., Hisada, A., Furuya, M., Nakano, A., A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis (2002) Plant Journal, 29 (3), pp. 245-255. , DOI 10.1046/j.0960-7412.2001.01189.x
  • Sakamoto, W., Spielewoy, N., Bonnard, G., Murata, M., Wintz, H., Mitochondrial localization of AtOXA1, an Arabidopsis homologue of yeast Oxa1p involved in the insertion and assembly of protein complexes in mitochondrial inner membrane (2000) Plant Cell Physiol., 41, pp. 1157-1163
  • Schneidereit, A., Scholz-Starke, J., Buttner, M., Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis (2003) Plant Physiology, 133 (1), pp. 182-190. , DOI 10.1104/pp.103.026674
  • Schussler, M.D., Alexandersson, E., Bienert, G.P., Kichey, T., Laursen, K.H., Johanson, U., Kjellbom, P., Jahn, T.P., The effects of the loss of TIP1;1 and TIP1;2 aquaporins in Arabidopsis thaliana (2008) Plant J., 56, pp. 756-767
  • Scott, R., Hodge, R., Paul, W., Draper, J., The molecular biology of anther differentiation (1991) Plant Sci., 80, pp. 167-191
  • Soria, L.R., Fanelli, E., Altamura, N., Svelto, M., Marinelli, R.A., Calamita, G., Aquaporin-8-facilitated mitochondrial ammonia transport (2010) Biochem. Biophys. Res. Commun., 393, pp. 217-221
  • Soto, G., Alleva, K., Mazzella, M.A., Amodeo, G., Muschietti, J.P., AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea (2008) FEBS Lett., 582, pp. 4077-4082
  • Tournaire-Roux, C., Sutka, M., Javot, H., Gout, E., Gerbeau, P., Luu, D.-T., Bligny, R., Maurel, C., Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins (2003) Nature, 425 (6956), pp. 393-397. , DOI 10.1038/nature01853
  • Tsukaguchi, H., Shayakul, C., Berger, U.V., Mackenzie, B., Devidas, S., Guggino, W.B., Van Hoek, A.N., Hediger, M.A., Molecular characterization of a broad selectivity neutral solute channel (1998) Journal of Biological Chemistry, 273 (38), pp. 24737-24743. , DOI 10.1074/jbc.273.38.24737
  • Twell, D., Yamaguchi, J., McCormick, S., Pollen-specific gene expression in transgenic plants: Coordinate regulation of two different tomato gene promotors during microsporogenesis (1990) Development, 109 (3), pp. 705-713
  • Vander Willigen, C., Postaire, O., Tournaire-Roux, C., Boursiac, Y., Maurel, C., Expression and inhibition of aquaporins in germinating Arabidopsis seeds (2006) Handbook of Environmental Chemistry, Volume 5: Water Pollution, 47 (9), pp. 1241-1250. , DOI 10.1093/pcp/pcj094
  • Vera-Estrella, R., Barkla, B.J., Bohnert, H.J., Pantoja, O., Novel regulation of aquaporins during osmotic stress (2004) Plant Physiology, 135 (4), pp. 2318-2329. , DOI 10.1104/pp.104.044891
  • Wang, Y., Zhang, W.-Z., Song, L.-F., Zou, J.-J., Su, Z., Wu, W.-H., Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in arabidopsis (2008) Plant Physiology, 148 (3), pp. 1201-1211. , http://www.plantphysiol.org/cgi/reprint/148/3/1201, DOI 10.1104/pp.108.126375
  • Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., Provart, N.J., An "electronic fluorescent pictograph" Browser for exploring and analyzing large-scale biological data sets (2007) PLoS ONE, 2 (8), pp. e718. , http://www.plosone.org/article/fetchObjectAttachment.action?uri= info%3Adoi%2F10.1371%2Fjournal.pone.0000718&representation=PDF, DOI 10.1371/journal.pone.0000718
  • Witte, C.-P., Rosso, M.G., Romeis, T., Identification of three urease accessory proteins that are required for urease activation in arabidopsis (2005) Plant Physiology, 139 (3), pp. 1155-1162. , DOI 10.1104/pp.105.070292
  • Wudick, M.M., Luu, D.T., Maurel, C., A look inside: Localization patterns and functions of intracellular plant aquaporins (2009) New Phytol., 184, pp. 289-302
  • Yang, B., Zhao, D., Verkman, A.S., Evidence against functionally significant aquaporin expression in mitochondria (2006) Journal of Biological Chemistry, 281 (24), pp. 16202-16206. , http://www.jbc.org/cgi/reprint/281/24/16202, DOI 10.1074/jbc.M601864200
  • Yasui, M., Hazama, A., Kwon, T.H., Nielsen, S., Guggino, W.B., Agre, P., Rapid gating and anion permeability of an intracellular aquaporin (1999) Nature, 402, pp. 184-187
  • Yoon, G.M., Dowd, P.E., Gilroy, S., McCubbin, A.G., Calcium-dependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity (2006) Plant Cell, 18 (4), pp. 867-878. , DOI 10.1105/tpc.105.037135
  • Yuan, L., Graff, L., Loque, D., Kojima, S., Tsuchiya, Y.N., Takahashi, H., Von Wiren, N., AtAMT1;4, a pollen-specific high-affinity ammonium transporter of the plasma membrane in Arabidopsis (2009) Plant Cell Physiol., 50, pp. 13-25
  • Zeuthen, T., Klaerke, D.A., Transport of water and glycerol in aquaporin 3 is gated by H+ (1999) Journal of Biological Chemistry, 274 (31), pp. 21631-21636
  • Zhang, X., Henriques, R., Lin, S.S., Niu, Q.W., Chua, N.H., Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method (2006) Nat. Protoc., 1, pp. 641-646
  • Zonia, L.E., Stebbins, N.E., Polacco, J.C., Essential role of urease in germination of nitrogen-limited Arabidopsis thaliana seeds (1995) Plant Physiol., 107, pp. 1097-1103

Citas:

---------- APA ----------
Soto, G., Fox, R., Ayub, N., Alleva, K., Guaimas, F., Erijman, E.J., Mazzella, A.,..., Muschietti, J. (2010) . TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana. Plant Journal, 64(6), 1038-1047.
http://dx.doi.org/10.1111/j.1365-313X.2010.04395.x
---------- CHICAGO ----------
Soto, G., Fox, R., Ayub, N., Alleva, K., Guaimas, F., Erijman, E.J., et al. "TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana" . Plant Journal 64, no. 6 (2010) : 1038-1047.
http://dx.doi.org/10.1111/j.1365-313X.2010.04395.x
---------- MLA ----------
Soto, G., Fox, R., Ayub, N., Alleva, K., Guaimas, F., Erijman, E.J., et al. "TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana" . Plant Journal, vol. 64, no. 6, 2010, pp. 1038-1047.
http://dx.doi.org/10.1111/j.1365-313X.2010.04395.x
---------- VANCOUVER ----------
Soto, G., Fox, R., Ayub, N., Alleva, K., Guaimas, F., Erijman, E.J., et al. TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana. Plant J. 2010;64(6):1038-1047.
http://dx.doi.org/10.1111/j.1365-313X.2010.04395.x