The roles of selectivity filters in determining aluminum transport by AtNIP1;2

References

• Maurel C, Verdoucq L, Luu D-T, Santoni V. D-T Luu and V Santoni. Plant aquaporins: membrane channels with multiple integrated functions. Annual Review of Plant Biology. 2008;59(1):1–7. doi:https://doi.org/10.1146/annurev.arplant.59.032607.092734.
   PubMedGoogle Scholar
• Tyerman SD, McGaughey SA, Qiu J. AJ Yool and CS Byrt. Adaptable and multifunctional ion-conducting aquaporins. Annual Review of Plant Biology. 2021;72:703-736. doi:https://doi.org/10.1146/annurev-arplant-081720-013608.
   Google Scholar
• Hove RM, Bhave M. Plant aquaporins with non-aqua functions: deciphering the signature sequences. Plant Molecular Biology. 2011;75(4–5):413–430. doi:https://doi.org/10.1007/s11103-011-9737-5.
   PubMed Web of Science ®Google Scholar
• Verbavatz J-M, Brown D, Sabolić I, Valenti G, Ausiello D, Van Hoek AN, Ma T, Verkman AS. Tetrameric assembly of CHIP28 water channels in liposomes and cell membranes: a freeze-fracture study. Journal of Cell Biology. 1993;123(3):605–618. doi:https://doi.org/10.1083/jcb.123.3.605.
   PubMed Web of Science ®Google Scholar
• Jung JS, Preston GM, Smith BL, Guggino WB, Agre P. WB Guggino and P Agre. Molecular structure of the water channel through aquaporin CHIP. The Hourglass Model. Journal of Biological Chemistry. 1994;269(20):14648–14654. doi:https://doi.org/10.1016/S0021-9258(17)36674-7.
   PubMed Web of Science ®Google Scholar
• Forrest KL, Bhave M. Major intrinsic proteins (MIPs) in plants: a complex gene family with major impacts on plant phenotype. Functional & Integrative Genomics. 2007;7(4):263–289. doi:https://doi.org/10.1007/s10142-007-0049-4.
   PubMed Web of Science ®Google Scholar
• de Groot BL, Grubmüller H. Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science. 2001;294(5550):2353–2357. doi:https://doi.org/10.1126/science.1066115.
   PubMed Web of Science ®Google Scholar
• Wallace IS, Roberts DM. Homology modeling of representative subfamilies of arabidopsis major intrinsic proteins. Classification Based on the Aromatic/arginine Selectivity Filter. Plant Physiology. 2004;135:1059–1068.
   Google Scholar
• Wallace IS, Choi W-G, Roberts DM. The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochimica Et Biophysica Acta (BBA) - Biomembranes. 2006;1758(8):1165–1175. doi:https://doi.org/10.1016/j.bbamem.2006.03.024.
   PubMed Web of Science ®Google Scholar
• Fu D, Libson A, Miercke LJW, Weitzman C, Nollert P, Krucinski J, Stroud RM. Structure of a glycerol-conducting channel and the basis for its selectivity. Science. 2000;290(5491):481–486. doi:https://doi.org/10.1126/science.290.5491.481.
   Google Scholar
• Sui H, Han B-G, Lee JK, Walian P, Jap. BK. Structural basis of water-specific transport through the AQP1 water channel. Nature. 2001;414(6866):872–878. doi:https://doi.org/10.1038/414872a.
   PubMed Web of Science ®Google Scholar
• Ilan B, Tajkhorshid E, Schulten K, Voth GA. The mechanism of proton exclusion in aquaporin channels. Proteins: Structure, Function, and Bioinformatics. 2004;55(2):223–228. doi:https://doi.org/10.1002/prot.20038.
   PubMed Web of Science ®Google Scholar
• Tajkhorshid E, Nollert P, Jensen MØ, Miercke LJ, O’Connell J, Stroud RM, Schulten K. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science. 2002;296(5567):525–530. doi:https://doi.org/10.1126/science.1067778.
   PubMed Web of Science ®Google Scholar
• Kong Y, Ma J. Dynamic mechanisms of the membrane water channel aquaporin-1 (AQP1). Proceedings of the National Academy of Sciences. 2001;98:14345–14349. doi:https://doi.org/10.1073/pnas.251507998.
   Google Scholar
• Thomas D, Bron P, Ranchy G, Duchesne L, Cavalier A, Rolland J-P, Raguénès-Nicol C, Hubert J-F, Haase W, Delamarche C, et al. Aquaglyceroporins, one channel for two molecules. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2002;1555(1–3):181–186. doi:https://doi.org/10.1016/S0005-2728(02)00275-X.
   PubMed Web of Science ®Google Scholar
• Stroud RM, Savage D, Miercke LJ, Lee JK, Khademi S, Harries W. Selectivity and conductance among the glycerol and water conducting aquaporin family of channels. FEBS Letters. 2003;555(1):79–84. doi:https://doi.org/10.1016/S0014-5793(03)01195-5.
   PubMed Web of Science ®Google Scholar
• Park J, Saier M Jr. Phylogenetic characterization of the MIP family of transmembrane channel proteins. The Journal of Membrane Biology. 1996;153(3):171–180. doi:https://doi.org/10.1007/s002329900120.
   PubMed Web of Science ®Google Scholar
• Froger A, Thomas D, Delamarche C, Tallur B. Prediction of functional residues in water channels and related proteins. Protein Science. 1998;7(6):1458–1468. doi:https://doi.org/10.1002/pro.5560070623.
   PubMed Web of Science ®Google Scholar
• Azad AK, Yoshikawa N, Ishikawa T, Sawa Y, Shibata H. Substitution of a single amino acid residue in the aromatic/arginine selectivity filter alters the transport profiles of tonoplast aquaporin homologs. Biochimica Et Biophysica Acta (Bba)-biomembranes. 2012;1818(5491):1–11. doi:https://doi.org/10.1016/j.bbamem.2011.09.014.
   PubMedGoogle Scholar
• Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall S, Fraysse L, Weig AR, Kjellbom P. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiology. 2001;126(4):1358–1369. doi:https://doi.org/10.1104/pp.126.4.1358.
   PubMed Web of Science ®Google Scholar
• Dean RM, Rivers RL, Zeidel ML, Roberts DM. Purification and functional reconstitution of soybean nodulin 26. An Aquaporin with Water and Glycerol Transport Properties. Biochemistry. 1999;38:347–353.
   Google Scholar
• Weig AR, Jakob C. Functional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae. FEBS Letters. 2000;481(3):293–298. doi:https://doi.org/10.1016/S0014-5793(00)02027-5.
   PubMed Web of Science ®Google Scholar
• Choi W-G, Roberts DM. Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. Journal of Biological Chemistry. 2007;282(33):24209–24218. doi:https://doi.org/10.1074/jbc.M700982200.
   PubMed Web of Science ®Google Scholar
• Wallace IS, Roberts DM. Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry. 2005;44(51):16826–16834. doi:https://doi.org/10.1021/bi0511888.
   PubMed Web of Science ®Google Scholar
• Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M. A silicon transporter in rice. Nature. 2006;440(7084):688–691. doi:https://doi.org/10.1038/nature04590.
   PubMed Web of Science ®Google Scholar
• Zhao XQ, Mitani N, Yamaji N, Shen RF, Ma. JF. Involvement of silicon influx transporter OsNIP2;1 in selenite uptake in rice. Plant Physiology. 2010;153(4):1871–1877. doi:https://doi.org/10.1104/pp.110.157867.
   PubMed Web of Science ®Google Scholar
• Wang Y, Li R, Li D, Jia X, Zhou D, Li J, Lyi SM, Hou S, Huang Y, Kochian LV, Liu J. NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis. Proceedings of the National Academy of Sciences. 2017; 114:5047–5052. doi:https://doi.org/10.1073/pnas.1618557114.
   Google Scholar
• Bienert GP, Thorsen M, Schüssler MD, Nilsson HR, Wagner A, Tamás MJ, Jahn TP. A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biology. 2008;6(1):1–15. doi:https://doi.org/10.1186/1741-7007-6-26.
   PubMedGoogle Scholar
• Isayenkov SV, Maathuis FJ. The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Letters. 2008;582(11):1625–1628. doi:https://doi.org/10.1016/j.febslet.2008.04.022.
   PubMed Web of Science ®Google Scholar
• Kamiya T, Fujiwara T. Arabidopsis NIP1;1 transports antimonite and determines antimonite sensitivity. Plant and Cell Physiology. 2009;50(11):1977–1981. doi:https://doi.org/10.1093/pcp/pcp130.
   PubMed Web of Science ®Google Scholar
• Kamiya T, Tanaka M, Mitani N, Ma JF, Maeshima M, Fujiwara T. NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. Journal of Biological Chemistry. 2009;284(4):2114–2120. doi:https://doi.org/10.1074/jbc.M806881200.
   PubMed Web of Science ®Google Scholar
• Kato Y, Miwa K, Takano J, Wada M, Fujiwara T. Highly boron deficiency-tolerant plants generated by enhanced expression of NIP5;1, a boric acid channel. Plant and Cell Physiology. 2009;50(1):58–66. doi:https://doi.org/10.1093/pcp/pcn168.
   PubMed Web of Science ®Google Scholar
• Takano J, Wada M, Ludewig U, Schaaf G, Wirén NV, Fujiwara. T. Arabidopsis major intrinsic protein NIP5;1 Is essential for efficient boron uptake and plant development under boron limitation. Plant Cell. 2006;18(6):1498–1509. doi:https://doi.org/10.1105/tpc.106.041640.
   PubMed Web of Science ®Google Scholar
• Mitani N, Yamaji N, Ma. JF. Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflügers Archiv-European Journal of Physiology. 2008;456(4):679–686. doi:https://doi.org/10.1007/s00424-007-0408-y.
   PubMed Web of Science ®Google Scholar
• Wallace IS, Wills DM, Guenther JF, Roberts DM. Functional selectivity for glycerol of the nodulin 26 subfamily of plant membrane intrinsic proteins. FEBS Letters. 2002;523(1–3):109–112. doi:https://doi.org/10.1016/S0014-5793(02)02955-1.
   PubMed Web of Science ®Google Scholar
• Kochian LV, Piñeros MA, Liu J, Magalhaes JV. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annual Review of Plant Biology. 2015;66(1):571–598. doi:https://doi.org/10.1146/annurev-arplant-043014-114822.
   PubMedGoogle Scholar
• Wang Y, Cai Y, Cao Y, Liu. J. Aluminum-activated root malate and citrate exudation is independent of NIP1;2-facilitated root-cell-wall aluminum removal in Arabidopsis. Plant Signaling & Behavior. 2018;13(1):e1422469. doi:https://doi.org/10.1080/15592324.2017.1422469.
   PubMed Web of Science ®Google Scholar
• Liu J, Magalhaes JV, Shaff J, Kochian LV. Aluminum‐activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant Journal. 2009;57(3):389–399. doi:https://doi.org/10.1111/j.1365-313X.2008.03696.x.
   PubMed Web of Science ®Google Scholar
• Liu J, Luo X, Shaff J, Liang C, Jia X, Li Z, Magalhaes J, Kochian LV. A promoter‐swap strategy between the AtALMT and AtMATE genes increased Arabidopsis aluminum resistance and improved carbon‐use efficiency for aluminum resistance. Plant Journal. 2012;71(2):327–337. doi:https://doi.org/10.1111/j.1365-313X.2012.04994.x.
   PubMed Web of Science ®Google Scholar
• Hoekenga OA, Maron LG, Piñeros MA, Cançado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto, H, Yamamoto Y, Koyama, H, Kochian LV. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proceedings of the National Academy of Sciences 2006;103(25):9738–9743. doi:https://doi.org/10.1073/pnas.0602868103.
   Google Scholar
• Wang Y, Yu W, Cao Y, Cai Y, Lyi SM, Wu W, Kang Y, Liang C, Liu J. An exclusion mechanism is epistatic to an internal detoxification mechanism in aluminum resistance in Arabidopsis. BMC Plant Biology. 2020;20:122. doi:https://doi.org/10.1186/s12870-020-02338-y.
   Google Scholar
• Miwa K, Tanaka M, Kamiya T, Fujiwara T. Molecular Mechanisms of Boron Transport in Plants: Involvement of Arabidopsis NIP5;1 and NIP6;1. In: Jahn T.P., Bienert G.P. (eds) MIPs and Their Role in the Exchange of Metalloids. Advances in Experimental Medicine and Biology, 2010;679:83-96. Springer, New York, NY. doi:https://doi.org/10.1007/978-1-4419-6315-4_7
   Google Scholar
• Johnson KD, Chrispeels MJ. Tonoplast-bound protein kinase phosphorylates tonoplast intrinsic protein. Plant Physiology. 1992;100(4):1787–1795. doi:https://doi.org/10.1104/pp.100.4.1787.
   PubMed Web of Science ®Google Scholar
• Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P. Structural mechanism of plant aquaporin gating. Nature. 2006;439(7077):688–694. doi:https://doi.org/10.1038/nature04316.
   PubMed Web of Science ®Google Scholar
• Santoni V, Verdoucq L, Sommerer N, Vinh J, Pflieger D, Maurel. C. Methylation of aquaporins in plant plasma membrane. Biochemical Journal. 2006;400(1):189–197. doi:https://doi.org/10.1042/BJ20060569.
   PubMedGoogle Scholar
• Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O. HJ Bohnert and O Pantoja. Novel regulation of aquaporins during osmotic stress. Plant Physiology. 2004;135(4):2318–2329. doi:https://doi.org/10.1104/pp.104.044891.
   PubMed Web of Science ®Google Scholar