Aquaporins are multifunctional membrane channels that facilitate the transmembrane transport of water and solutes. When transmembrane mineral nutrient transporters exhibit the same expression patterns as aquaporins under diverse temporal and physiological conditions, there is a greater probability that they interact. In this study, genome-wide temporal profiling of transcripts analysis and coexpression network-based approaches are used to examine the significant specificity correlation of aquaporins and transmembrane solute transporters in developing maize leaf. The results indicate that specific maize aquaporins are related to specific transmembrane solute transporters. The analysis demonstrates a systems-level correlation between aquaporins, nutrient transporters, and the homeostasis of mineral nutrients in developing maize leaf. Our results provide a resource for further studies into the physiological function of these aquaporins. 1. Introduction Water can take different paths on its way through the leaf, in addition to radial water flux, water movement across leaf cell membranes is important for water homeostasis, increasing cell volume, maintaining turgor during expansion, regulating the opening and closure of stomata, and controlling leaf movement [1]. Water movement through cell membranes is facilitated by water channels called aquaporins. Plant aquaporins exhibit multiplicity and diversity, and fall into seven subfamilies loosely based on intracellular locations and sequence similarities: the plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), NOD26-like intrinsic proteins (NIPs), small, basic intrinsic proteins (SIPs), the GlpF-like intrinsic proteins (GIPs), hybrid intrinsic proteins (HIP), and the uncategorized X intrinsic proteins (XIP) [2]. Plant aquaporins are significant not only in plant-water relations, but also in physiological aspects such as nutrient transport and metal/metalloid toxicity [3, 4]. Flexas et al. provided evidence for the in vivo involvement of NtAQP1 in mesophyll CO2 conductance, suggesting a significant role for PIPs in CO2 diffusivity [5]. Ludewig and Dynowski have shown that AtTIP1;1 and AtTIP1;2 conduct H2O2 when heterologously expressed in yeast [6]. Azad et al. described TgTIP1;1- and TgTIP1;2-mediated H2O2 conductance by fluorescence assay in Tulipa gesneriana. Recent studies have investigated the selectivity mechanisms of aquaporins, nutrient transporters and homeostasis of mineral nutrients in most plant groups [7]. Hove and Bhave performed a comprehensive analysis of all plant
References
[1]
W. Majeran, B. Zybailov, A. J. Ytterberg, J. Dunsmore, Q. Sun, and K. J. van Wijk, “Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheat cells,” Molecular and Cellular Proteomics, vol. 7, no. 9, pp. 1609–1638, 2008.
[2]
J. H. Danielson and U. Johanson, “Unexpected complexity of the Aquaporin gene family in the moss Physcomitrella patens,” BMC Plant Biology, vol. 8, article 45, 2008.
[3]
C. Maurel, “Plant aquaporins: novel functions and regulation properties,” FEBS Letters, vol. 581, no. 12, pp. 2227–2236, 2007.
[4]
J. M. Ward, P. Maser, and J. I. Schroeder, “Plant ion channels: gene families, physiology, and functional genomics analyses,” Annual Review of Physiology, vol. 71, pp. 59–82, 2009.
[5]
J. Flexas, M. Ribas-Carbó, D. T. Hanson et al., “Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo,” Plant Journal, vol. 48, no. 3, pp. 427–439, 2006.
[6]
U. Ludewig and M. Dynowski, “Plant aquaporin selectivity: where transport assays, computer simulations and physiology meet,” Cellular and Molecular Life Sciences, vol. 66, no. 19, pp. 3161–3175, 2009.
[7]
A. K. Azad, N. Yoshikawa, T. Ishikawa, Y. Sawa, and H. Shibata, “Substitution of a single amino acid residue in the aromatic/arginine selectivity filter alters the transport profiles of tonoplast aquaporin homologs,” Biochim Biophys Acta, vol. 1818, no. 1, pp. 1–11, 2011.
[8]
R. M. Hove and M. Bhave, “Plant aquaporins with non-aqua functions: deciphering the signature sequences,” Plant Molecular Biology, vol. 75, no. 4-5, pp. 413–430, 2011.
[9]
N. V. Obroucheva and I. A. Sin'kevich, “Aquaporins and cell growth,” Russian Journal of Plant Physiology, vol. 57, no. 2, pp. 153–165, 2010.
[10]
A. Br？utigam, S. Hoffmann-Benning, and A. P. M. Weber, “Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes,” Plant Physiology, vol. 148, no. 3, pp. 568–579, 2008.
[11]
S. Covshoff, W. Majeran, P. Liu, J. M. Kolkman, K. J. Van Wijk, and T. P. Brutnell, “Deregulation of maize C4 photosynthetic development in a mesophyll cell-defective mutant,” Plant Physiology, vol. 146, no. 4, pp. 1469–1481, 2008.
[12]
G. Friso, W. Majeran, M. Huang, Q. Sun, and K. J. van Wijk, “Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly,” Plant Physiology, vol. 152, no. 3, pp. 1219–1250, 2010.
[13]
E. Breeze, E. Harrison, S. McHattie et al., “High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation,” Plant Cell, vol. 23, no. 3, pp. 873–894, 2011.
[14]
S. Liu, L. Lin, P. Jiang, D. Wang, and Y. Xing, “A comparison of RNA-Seq and high-density exon array for detecting differential gene expression between closely related species,” Nucleic Acids Research, vol. 39, no. 2, pp. 578–588, 2011.
[15]
Z. Wang, M. Gerstein, and M. Snyder, “RNA-Seq: a revolutionary tool for transcriptomics,” Nature Reviews Genetics, vol. 10, no. 1, pp. 57–63, 2009.
[16]
B. Matthieu, K. Thorsten, J. M. Anthony, V. Jean-Luc, P. Thomas, and F. Wieland, “Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves,” Journal of Experimental Botany, vol. 62, no. 12, pp. 4127–4142, 2011.
[17]
L. Pinghua, P. Lalit, and G. Neeru, “The developmental dynamics of the maize leaf transcriptome,” Nature Genetics, vol. 42, no. 12, pp. 1060–1067, 2010.
[18]
B. Usadel, T. Obayashi, M. Mutwil et al., “Co-expression tools for plant biology: opportunities for hypothesis generation and caveats,” Plant, Cell and Environment, vol. 32, no. 12, pp. 1633–1651, 2009.
[19]
I. Lee, B. Ambaru, P. Thakkar, E. M. Marcotte, and S. Y. Rhee, “Rational association of genes with traits using a genome-scale gene network for Arabidopsis thaliana,” Nature Biotechnology, vol. 28, no. 2, pp. 149–156, 2010.
[20]
G. W. Bassel, H. Lan, E. Glaab et al., “Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 23, pp. 9709–9714, 2011.
[21]
M. Mutwil, S. Klie, T. Tohge et al., “PlaNet: combined sequence and expression comparisons across plant networks derived from seven species,” Plant Cell, vol. 23, no. 3, pp. 895–910, 2011.
[22]
W. B. George, G. Enrico, and M. Julietta, “Functional network construction in arabidopsis using rule-based machine learning on large-scale data sets,” The Plant Cell, vol. 23, pp. 3101–3116, 2011.
[23]
S. M. Brady and N. J. Provart, “Web-queryable large-scale data sets for hypothesis generation in plant biology,” Plant Cell, vol. 21, no. 4, pp. 1034–1051, 2009.
[24]
J. Ruan, A. K. Dean, and W. Zhang, “A general co-expression network-based approach to gene expression analysis: comparison and applications,” BMC Systems Biology, vol. 4, article 8, 2010.
[25]
M. E. Smoot, K. Ono, J. Ruscheinski, P. L. Wang, and T. Ideker, “Cytoscape 2.8: new features for data integration and network visualization,” Bioinformatics, vol. 27, no. 3, Article ID btq675, pp. 431–432, 2011.
[26]
M. Katsuhara, Y. T. Hanba, K. Shiratake, and M. Maeshima, “Expanding roles of plant aquaporins in plasma membranes and cell organelles,” Functional Plant Biology, vol. 35, no. 1, pp. 1–14, 2008.
[27]
D. Gomes, A. Agasse, P. Thiébaud, S. Delrot, H. Gerós, and F. Chaumont, “Aquaporins are multifunctional water and solute transporters highly divergent in living organisms,” Biochimica et Biophysica Acta, vol. 1788, no. 6, pp. 1213–1228, 2009.
[28]
F. Chopin, M. Orsel, M. F. Dorbe et al., “The Arabidopsis ATNRT2.7 nitrate transporter controls nitrate content in seeds,” Plant Cell, vol. 19, no. 5, pp. 1590–1602, 2007.
[29]
M. Dynowski, G. Schaaf, D. Loque, O. Moran, and U. Ludewig, “Plant plasma membrane water channels conduct the signalling molecule H2O2,” Biochemical Journal, vol. 414, no. 1, pp. 53–61, 2008.
[30]
T. Kataoka, N. Hayashi, T. Yamaya, and H. Takahashi, “Root-to-shoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature.,” Plant physiology, vol. 136, no. 4, pp. 4198–4204, 2004.
[31]
N. Yoshimoto, E. Inoue, K. Saito, T. Yamaya, and H. Takahashi, “Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in arabidopsis,” Plant Physiology, vol. 131, no. 4, pp. 1511–1517, 2003.
[32]
D. R. Lewis, G. Wu, K. Ljung, and E. P. Spalding, “Auxin transport into cotyledons and cotyledon growth depend similarly on the ABCB19 Multidrug Resistance-like transporter,” Plant Journal, vol. 60, no. 1, pp. 91–101, 2009.
[33]
C. Maurel, H. Javot, V. Lauvergeat et al., “Molecular physiology of aquaporins in plants,” International Review of Cytology, vol. 215, pp. 105–148, 2002.
[34]
T. Higuchi, S. Suga, T. Tsuchiya et al., “Molecular cloning, water channel activity and tissue specific expression of two isoforms of radish vacuolar aquaporin,” Plant and Cell Physiology, vol. 39, no. 9, pp. 905–913, 1998.
[35]
J. Jeong, C. Cohu, L. Kerkeb, M. Pilon, E. L. Connolly, and M. L. Guerinot, “Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 30, pp. 10619–10624, 2008.
[36]
H. Wu, L. Li, J. Du, Y. Yuan, X. Cheng, and H. Q. Ling, “Molecular and biochemical characterization of the Fe(III) chelate reductase gene family in Arabidopsis thaliana,” Plant and Cell Physiology, vol. 46, no. 9, pp. 1505–1514, 2005.
[37]
K. L. Fitzpatrick and R. J. Reid, “The involvement of aquaglyceroporins in transport of boron in barley roots,” Plant, Cell and Environment, vol. 32, no. 10, pp. 1357–1365, 2009.
[38]
M. Gaspar, A. Bousser, I. Sisso？ff, O. Roche, J. Hoarau, and A. Mahé, “Cloning and characterization of ZmPIP1-5b, an aquaporin transporting water and urea,” Plant Science, vol. 165, no. 1, pp. 21–31, 2003.
[39]
R. Stadler, M. Büttner, P. Ache et al., “Diurnal and light-regulated expression of AtSTP1 in guard cells of Arabidopsis,” Plant Physiology, vol. 133, no. 2, pp. 528–537, 2003.
[40]
S. M. Sherson, G. Hemmann, G. Wallace et al., “Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars,” Plant Journal, vol. 24, no. 6, pp. 849–857, 2000.
[41]
A. Wormit, O. Trentmann, I. Feifer et al., “Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport,” Plant Cell, vol. 18, no. 12, pp. 3476–3490, 2006.
[42]
G. Schaaf, A. Schikora, J. H？berle et al., “A putative function for the Arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis,” Plant and Cell Physiology, vol. 46, no. 5, pp. 762–774, 2005.
[43]
S. Yokoi, F. J. Quintero, B. Cubero et al., “Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response,” Plant Journal, vol. 30, no. 5, pp. 529–539, 2002.
[44]
H. Shin, H. S. Shin, G. R. Dewbre, and M. J. Harrison, “Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments,” Plant Journal, vol. 39, no. 4, pp. 629–642, 2004.
[45]
J. Misson, M. C. Thibaud, N. Bechtold, K. Raghothama, and L. Nussaume, “Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants,” Plant Molecular Biology, vol. 55, no. 5, pp. 727–741, 2004.
[46]
A. Marmagne, M. Vinauger-Douard, D. Monachello et al., “Two members of the Arabidopsis CLC (chloride channel) family, AtCLCe and AtCLCf, are associated with thylakoid and Golgi membranes, respectively,” Journal of Experimental Botany, vol. 58, no. 12, pp. 3385–3393, 2007.
[47]
J. Von Der Fecht-Bartenbach, M. Bogner, M. Dynowski, and U. Ludewig, “CLC-b-mediated no3-/H+ exchange across the tonoplast of arabidopsis vacuoles,” Plant and Cell Physiology, vol. 51, no. 6, pp. 960–968, 2010.
[48]
J. V. D. Fecht-Bartenbach, M. Bogner, M. Krebs, Y. D. Stierhof, K. Schumacher, and U. Ludewig, “Function of the anion transporter AtCLC-d in the trans-Golgi network,” Plant Journal, vol. 50, no. 3, pp. 466–474, 2007.
[49]
C. S. Chiang, G. Stacey, and Y. F. Tsay, “Mechanisms and functional properties of two peptide transporters, AtPTR2 and fPTR2,” Journal of Biological Chemistry, vol. 279, no. 29, pp. 30150–30157, 2004.
[50]
W. Song, S. Koh, M. Czako et al., “Antisense expression of the peptide transport gene AtPTR2-B delays flowering and arrests seed development in transgenic Arabidopsis plants,” Plant Physiology, vol. 114, no. 3, pp. 927–935, 1997.
[51]
O. Cagnac, A. Bourbouloux, D. Chakrabarty, M. Y. Zhang, and S. Delrot, “AtOPT6 transports glutathione derivatives and is induced by primisulfuron,” Plant Physiology, vol. 135, no. 3, pp. 1378–1387, 2004.
[52]
A. Reinders, J. A. Panshyshyn, and J. M. Ward, “Analysis of transport activity of Arabidopsis sugar alcohol permease homolog AtPLT5,” Journal of Biological Chemistry, vol. 280, no. 2, pp. 1594–1602, 2005.
[53]
M. Nieves-Cordones, F. Alemán, V. Martínez, and F. Rubio, “The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions,” Molecular Plant, vol. 3, no. 2, pp. 326–333, 2010.
[54]
F. Rubio, F. Alemán, M. Nieves-Cordones, and V. Martínez, “Studies on Arabidopsis athak5, atakt1 double mutants disclose the range of concentrations at which AtHAK5, AtAKT1 and unknown systems mediate K+ uptake,” Physiologia Plantarum, vol. 139, no. 2, pp. 220–228, 2010.
[55]
I. Hwang, H. Sze, and J. F. Harper, “A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 11, pp. 6224–6229, 2000.
