Artículo

Pérez Di Giorgio, J.A.; Soto, G.C.; Muschietti, J.P.; Amodeo, G. "Pollen aquaporins: The solute factor" (2016) Frontiers in Plant Science. 7(November 2016)
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Abstract:

In the recent years, the biophysical properties and presumed physiological role of aquaporins (AQPs) have been expanded to specialized cells where water and solute exchange are crucial traits. Complex but unique processes such as stomatal movement or pollen hydration and germination have been addressed not only by identifying the specific AQP involved but also by studying how these proteins integrate and coordinate cellular activities and functions. In this review, we referred specifically to pollen-specific AQPs and analyzed what has been assumed in terms of transport properties and what has been found in terms of their physiological role. Unlike that in many other cells, the AQP machinery in mature pollen lacks plasma membrane intrinsic proteins, which are extensively studied for their high water capacity exchange. Instead, a variety of TIPs and NIPs are expressed in pollen. These findings have altered the initial understanding of AQPs and water exchange to consider specific and diverse solutes that might be critical to sustaining pollen’s success. The spatial and temporal distribution of the pollen AQPs also reflects a regulatory mechanism that allowing a properly adjusting water and solute exchange. © 2016 Pérez Di Giorgio, Soto, Muschietti and Amodeo.

Registro:

Documento: Artículo
Título:Pollen aquaporins: The solute factor
Autor:Pérez Di Giorgio, J.A.; Soto, G.C.; Muschietti, J.P.; Amodeo, G.
Filiación:Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Instituto de Genética Ewald A. Favret, Centro de Investigación en Ciencias Veterinarias y Agronómicas, Instituto Nacional de Tecnología Agropecuaria - Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Biodiversidad y Biología Experimental y Aplicada, Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Department of Biochemistry and Molecular Medicine, Université de Montréal, Montréal, QC, Canada
Palabras clave:Aquaporin; Fertilization; Membrane intrinsic protein; Plant fitness; Pollen germination; Solute permeability; Water and solute transport; Water channel
Año:2016
Volumen:7
Número:November 2016
DOI: http://dx.doi.org/10.3389/fpls.2016.01659
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_nNovember2016_p_PerezDiGiorgio

Referencias:

  • Abascal, F., Irisarri, I., Zardoya, R., Diversity and evolution of membrane intrinsic proteins (2014) Biochim. Biophys. Acta, 1840, pp. 1468-1481
  • Abercrombie, J.M., O’Meara, B.C., Moffatt, A.R., Williams, J.H., Developmental evolution of flowering plant pollen tube cell walls: Callose synthase (CalS) gene expression patterns (2011) Evodevo, 2, p. 14
  • Allen, A.M., Lexer, C., Hiscock, S.J., Comparative analysis of pistil transcriptomes reveals conserved and novel genes expressed in dry, wet, and semidry stigmas (2010) Plant Physiol., 154, pp. 1347-1360
  • Alleva, K., Chara, O., Amodeo, G., Aquaporins: Another piece in the osmotic puzzle (2012) FEBS Lett., 586, pp. 2991-2999
  • Almasalmeh, A., Krenc, D., Wu, B., Beitz, E., Structural determinants of the hydrogen peroxide permeability of aquaporins (2014) FEBS J., 281, pp. 647-656
  • Anderberg, H.I., Kjellbom, P., Johanson, U., Annotation of Selaginella moellendorffii major intrinsic proteins and the evolution of the protein family in terrestrial plants (2012) Front. Plant Sci., 20, p. 33
  • Beitz, E., Wu, B., Holm, L.M., Schultz, J.E., Zeuthen, T., Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons (2006) Proc. Natl. Acad. Sci. U.S.A., 103, pp. 269-274
  • Benkert, R., Obermeyer, G., Bentrup, F.W., The turgor pressure of growing lily pollen tubes (1997) Protoplasma., 198, pp. 1-8
  • Bienert, G.P., Chaumont, F., Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide (2014) Biochim. Biophys. Acta, 1840, pp. 1596-1604
  • Bienert, G.P., Jahn, T.P., Major intrinsic proteins and arsenic transport in plants: New players and their potential role (2010) Adv. Exp. Med. Biol., 679, pp. 111-125
  • Blevins, D.G., Lukaszewski, K.M., Boron in plant structure and function (1998) Annu. Rev. Plant Physiol. Plant Mol. Biol., 49, pp. 481-500
  • Bock, K.W., Honys, D., Ward, J.M., Padmanaban, S., Nawrocki, E.P., Hirschi, K.D., Integrating membrane transport with male gametophyte development and function through transcriptomics (2006) Plant Physiol., 140, pp. 1151-1168
  • Borges, F., Gomes, G., Gardner, R., Moreno, N., McCormick, S., Feijó, J.A., Comparative transcriptomics of Arabidopsis sperm cells (2008) Plant Physiol., 148, pp. 1168-1181
  • Bots, M., Feron, R., Uehlein, N., Weterings, K., Kaldenhoff, R., Mariani, T., PIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development (2005) J. Exp. Bot., 56, pp. 113-121
  • Bots, M., Vergeldt, F., Wolters-Arts, M., Weterings, K., van As, H., Mariani, C., Aquaporins of the PIP2 class are required for efficient anther dehiscence in tobacco (2005) Plant Physiol., 137, pp. 1049-1056
  • Choi, W.G., Roberts, D.M., Arabidopsis NIP2; 1, a major intrinsic protein transporter of lactic acid induced by anoxic stress (2007) J. Biol. Chem., 282, pp. 24209-24218
  • Danielson, J.H., Johanson, U., Phylogeny of major intrinsic proteins (2010) MIPs and Their Role in the Exchange of Metalloids, 679, pp. 19-31. , eds T. Jahn and G. Bienert (New York, NY: Springer)
  • Dixit, R., Rizzo, C., Nasrallah, M., Nasrallah, J., The Brassica MIPMOD gene encodes a functional water channel that is expressed in the stigma epidermis (2001) Plant Mol. Biol., 45, pp. 51-62
  • Dutta, R., Robinson, K.R., Identification and characterization of stretch-activated ion channels in pollen protoplasts (2004) Plant Physiol., 135, pp. 1398-1406
  • Fetter, K., Van Wilder, V., Moshelion, M., Chaumont, F., Interactions between plasma membrane aquaporins modulate their water channel activity (2004) Plant Cell, 16, pp. 215-228
  • Firon, N., Nepi, M., Pacini, E., Water status and associated processes mark critical stages in pollen development and functioning (2012) Ann. Bot., 109, pp. 1201-1214
  • Fu, D., Libson, A., Miercke, L.J., Weitzman, C., Nollert, P., Krucinski, J., Structure of a glycerol-conducting channel and the basis for its selectivity (2000) Science, 290, pp. 481-486
  • Fu, D., Lu, M., The structural basis of water permeation and proton exclusion in aquaporins (review) (2007) Mol. Membr. Biol., 24, pp. 366-374
  • Guan, Y., Guo, J., Li, H., Yang, Z., Signaling in pollen tube growth: Crosstalk, feedback, and missing links (2013) Mol. Plant, 6, pp. 1053-1064
  • Gupta, A.B., Verma, R.K., Agarwal, V., Vajpai, M., Bansal, V., Sankararamakrishnan, R., MIPModDB: A central resource for the superfamily of major intrinsic proteins (2011) Nucleic Acids Res., 40, pp. D362-D369
  • Hamilton, E.S., Jensen, G.S., Maksaev, G., Katims, A., Sherp, A.M., Haswell, E.S., Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination (2015) Science, 350, pp. 438-441
  • Helling, D., Possart, A., Cottier, S., Klahre, U., Kost, B., Pollen tube tip growth depends on plasma membrane polarization mediated by Tobacco PLC3 activity and endocytic membrane recycling (2006) Plant Cell, 18, pp. 3519-3534
  • Hepler, P.K., Vidali, L., Cheung, A.Y., Polarized cell growth in higher plants (2001) Annu. Rev. Cell Dev. Biol., 17, pp. 159-187
  • Herrera, M., Garvin, J.L., Aquaporins as gas channels (2011) Pflugers. Arch., 462, pp. 623-630
  • Hill, A.E., Shachar-Hill, B., Shachar-Hill, Y., What are aquaporins for? J (2004) Membr. Biol., 197, pp. 1-32
  • Hill, A.E., Shachar-Hill, Y., Are aquaporins the missing transmembrane osmosensors? J (2015) Membr. Biol., 248, pp. 753-765
  • Ho, J.D., Yeh, R., Sandstrom, A., Chorny, I., Harries, W.E., Robbins, R.A., Crystal structure of human aquaporin 4 at 1.8 Å and its mechanism of conductance (2009) Proc. Natl. Acad. Sci. U.S.A., 106, pp. 7437-7442
  • Honys, D., Twell, D., Transcriptome analysis of haploid male gametophyte development in Arabidopsis (2004) Genome Biol., 5, p. R85
  • Ishikawa, F., Suga, S., Uemura, T., Sato, M.H., Maeshima, M., Novel type aquaporin SIPs are mainly localized to the ER membrane and show cellspecific expression in Arabidopsis thaliana (2005) FEBS Lett., 579, pp. 5814-5820
  • Johnson, S., McCormick, S., Pollen germinates precociously in the anthers of raring-to-go, an Arabidopsis gametophytic mutant (2001) Plant Physiol., 126, pp. 685-695
  • Kaldenhoff, R., Kai, L., Uehlein, N., Aquaporins and membrane diffusion of CO2 in living organisms (2014) Biochim. Biophys. Acta, 1840, pp. 1592-1595
  • Kitchen, P., Day, R.E., Salman, M.M., Conner, M.T., Bill, R.M., Conner, A.C., Beyond water homeostasis: Diverse functional roles of mammalian aquaporins (2015) Biochim. Biophys. Acta, 1850, pp. 2410-2421
  • Kreida, S., Törnroth-Horsefield, S., Structural insights into aquaporin selectivity and regulation (2015) Curr. Opin. Struct. Biol., 33, pp. 126-134
  • Kurusu, T., Kuchitsu, K., Nakano, M., Nakayama, Y., Iida, H., Plant mechanosensing and Ca2+ transport (2013) Trends Plant Sci., 18, pp. 227-233
  • Li, T., Choi, W., Wallace, I.S., Baudry, J., Roberts, D.M., AtNIP7; 1: An anther-specific boric acid transporter of the AQP superfamily regulated by an unusual Tyrosine in Helix 2 of the transport pore (2011) Biochemistry, 50, pp. 6633-6641
  • Lolle, S.J., Hsu, W., Pruitt, R.E., Genetic analysis of organ fusion in Arabidopsis thaliana (1998) Genetics, 149, pp. 607-619
  • Loraine, A.E., McCormick, S., Estrada, A., Patel, K., Qin, P., PRNASeq of Arabidopsis pollen uncovers novel transcription and alternative splicing. (2013) Plant Physiol., 162, pp. 1092-1109
  • Maeshima, M., Ishikawa, F., ER membrane aquaporins in plants (2008) Pflugers Arch. Eur. J. Physiol., 456, pp. 709-716
  • Marin-Olivier, M., Chevalier, T., Fobis-Loisy, I., Dumas, C., Gaude, T., Aquaporin PIP genes are not expressed in the stigma papillae in Brassica oleracea (2000) Plant J., 2, pp. 231-240
  • Matsuda, T., Matsushima, M., Nabemoto, M., Osaka, M., Sakazono, S., Masuko-Suzuki, H., Transcriptional characteristics and differences in Arabidopsis stigmatic papilla cells pre- And post-pollination (2015) Plant Cell Physiol., 56, pp. 663-673
  • Maurel, C., Boursiac, Y., Luu, D.T., Santoni, V., Shahzad, Z., Verdoucq, L., Aquaporins in plants (2015) Physiol. Rev., 95, pp. 1321-1358
  • Maurel, C., Verdoucq, L., Rodrigues, O., Aquaporins and plant transpiration (2016) Plant Cell Environ., 39, pp. 2580-2587
  • Mitani-Ueno, N., Yamaji, N., Zhao, F.J., Ma, J.F., The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic (2011) J. Exp. Bot., 62, pp. 4391-4398
  • Murata, K., Mitsuoka, K., Hirai, T., Walz, T., Structural determinants of water permeation through aquaporin-1 (2000) Nature, 407, pp. 599-605
  • Neely, J.D., Christensen, B.M., Nielsen, S., Agre, P., Heterotetrameric composition of aquaporin-4 water channels (1999) Biochemistry, 38, pp. 11156-11163
  • Ozu, M., Dorr, R.A., Gutiérrez, F., Politi, M.T., Toriano, R., Human AQP1 is a constitutively open channel that closes by a membrane-tensionmediated mechanism (2013) Biophys. J., 104, pp. 85-95
  • Pérez Di Giorgio, J., Bienert, G.P., Ayub, N., Yaneff, A., Barberini, M.L., Mecchia, M.A., Pollen-specific aquaporins NIP4; 1 and NIP4; 2 are required for pollen development and pollination in Arabidopsis thaliana (2016) Plant Cell, 28, pp. 1053-1077
  • Pérez Di Giorgio, J., Soto, G., Alleva, K., Jozefkowicz, C., Amodeo, G., Muschietti, J.P., Prediction of aquaporin function by integrating evolutionary and functional analyses (2014) J. Membr. Biol., 247, pp. 107-125
  • Pierson, E.S., Miller, D.D., Callaham, D.A., Shipley, A.M., Rivers, B.A., Cresti, M., Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: Effect of BAPTA-type buffers and hypertonic media (1994) Plant Cell, 6, pp. 1815-1828
  • Pina, C., Pinto, F., Feijo, J.A., Becker, J.D., Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation (2005) Plant Physiol., 138, pp. 744-756
  • Pommerrenig, B., Diehn, T.A., Bienert, G.P., Metalloido-porins: Essentiality of Nodulin 26-like intrinsic proteins in metalloid transport (2015). (2015) Plant Sci., 238, pp. 212-227
  • Preston, G.M., Carroll, T.P., Guggino, W.B., Agre, P., Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein (1992) Science, 256, pp. 385-387
  • Qin, Y., Leydon, A.R., Manziello, A., Pandey, R., Mount, D., Denic, S., Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil (2009) PLoS Genet., 5
  • Safiarian, M.J., Pertl-Obermeyer, H., Lughofer, P., Hude, R., Bertl, A., Obermeyer, G., Lost in traffic? The K+ channel of lily pollen, LilKT1, is detected at the endomembranes inside yeast cells, tobacco leaves, and lily pollen. (2015) Plant Traffic Transp., 10, p. 47
  • Sharma, B., Bhatla, S.C., Accumulation and scavenging of reactive oxygen species and nitric oxide correlate with stigma maturation and pollen-stigma interaction in sunflower (2013) Acta Physiol. Plant., 35, pp. 2777-2787
  • Sommer, A., Geist, B., Da Ines, O., Gehwolf, R., Schäffner, A.R., Obermeyer, G., Ectopic expression of Arabidopsis thaliana plasma membrane intrinsic protein 2 aquaporins in lily pollen increases the plasma membrane water permeability of grain but not of tube protoplasts (2008) New Phytol., 180, pp. 787-797
  • Soto, G., Alleva, K., Amodeo, G., Muschietti, J., Ayub, N.D., New insight into the evolution of aquaporins from flowering plants and vertebrates: Orthologous identification and functional transfer is possible (2012) Gene, 503, pp. 165-176
  • Soto, G., Alleva, K., Mazzella, M.A., Amodeo, G., Muschietti, J.P., AtTIP1; 3 and AtTIP5; 1, the only highly expressed Arabidopsis pollenspecific aquaporins, transport water and urea (2008) FEBS Lett., 582, pp. 4077-4082
  • 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
  • Sui, H., Han, B.G., Lee, J.K., Walian, P., Jap, B.K., Structural basis of water-specific transport through the AQP1 water channel (2001) Nature, 414, pp. 872-878
  • Tani, K., Mitsuma, T., Hiraoki, Y., Kamegawa, A., Nishikawa, K., Tanimura, Y., Mechanism of aquaporin-4‘s fast and highly selective water conduction and proton exclusion (2009) J. Mol. Biol., 389, pp. 694-706
  • Tian, S., Wang, X., Li, P., Wang, H., Ji, H., Xie, J., Plant aquaporin AtPIP1; 4 links apoplastic H2O2 induction to disease immunity pathways (2016) Plant Physiol., 17, pp. 1635-1650
  • Verbavatz, J.M., Brown, D., Sabolič, I., Valenti, G., Ausiello, D.A., Van Hoek, A.N., Tetrameric assembly of CHIP28 water channels in liposomes and cell membranes: A freeze fracture study (1993) J. Cell Biol., 123, pp. 605-618
  • Wallace, I.S., Wills, D.M., Guenther, J.F., Roberts, D.M., Functional selectivity for glycerol of the nodulin 26 subfamily of plant membrane intrinsic proteins (2002) FEBS Lett., 523, pp. 109-112
  • 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 Physiol., 148, pp. 1201-1211
  • Williams, J.H., Novelties of the flowering plant pollen tube underlie diversification of a key life history stage (2008) Proc. Natl. Acad. Sci. U.S.A., 105, pp. 11259-11263
  • Williams, J.H., The evolution of pollen germination timing in flowering plants: Austrobailey ascandens (Austrobaileyaceae) (2012) AoB Plants, 2012
  • Wree, D., Wu, B., Zeuthen, T., Beitz, E., Requirement for asparagine in the aquaporin NPA sequence signature motifs for cation exclusion (2011) FEBS J., 278, pp. 740-748
  • Wudick, M.M., Luu, D.-T., Tournaire-Roux, C., Sakamoto, W., Maurel, C., Vegetative and sperm cell-specific aquaporins of Arabidopsis thaliana highlight the vacuolar equipment of pollen and contribute to plant reproduction (2014) Plant Physiol., 164, pp. 1697-1706
  • Yaaran, A., Moshelion, M., Role of aquaporins in a composite model of water transport in the leaf (2016) Int. J. Mol. Sci., 17
  • Yaneff, A., Sigaut, L., Marquez, M., Alleva, K., Pietrasanta, L.I., Amodeo, G., Heteromerization of PIP aquaporins affects their intrinsic permeability (2014) Proc. Natl. Acad. Sci. U.S.A., 111, pp. 231-236
  • Zerzour, R., Kroeger, J., Geitmann, A., Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties (2009) Dev. Biol., 334, pp. 437-446
  • Zinta, G., Khan, A., AbdElgawad, H., Verma, V., Srivastava, A.K., Unveiling the redox control of plant reproductive development during abiotic stress (2016) Front. Plant. Sci., 7, p. 700

Citas:

---------- APA ----------
Pérez Di Giorgio, J.A., Soto, G.C., Muschietti, J.P. & Amodeo, G. (2016) . Pollen aquaporins: The solute factor. Frontiers in Plant Science, 7(November 2016).
http://dx.doi.org/10.3389/fpls.2016.01659
---------- CHICAGO ----------
Pérez Di Giorgio, J.A., Soto, G.C., Muschietti, J.P., Amodeo, G. "Pollen aquaporins: The solute factor" . Frontiers in Plant Science 7, no. November 2016 (2016).
http://dx.doi.org/10.3389/fpls.2016.01659
---------- MLA ----------
Pérez Di Giorgio, J.A., Soto, G.C., Muschietti, J.P., Amodeo, G. "Pollen aquaporins: The solute factor" . Frontiers in Plant Science, vol. 7, no. November 2016, 2016.
http://dx.doi.org/10.3389/fpls.2016.01659
---------- VANCOUVER ----------
Pérez Di Giorgio, J.A., Soto, G.C., Muschietti, J.P., Amodeo, G. Pollen aquaporins: The solute factor. Front. Plant Sci. 2016;7(November 2016).
http://dx.doi.org/10.3389/fpls.2016.01659