A Survey of Barley PIP Aquaporin Ionic Conductance Reveals Ca2+-Sensitive HvPIP2;8 Na+ and K+ Conductance
Abstract
:1. Introduction
2. Results
2.1. Ion Transport Activity Was Observed for HvPIP2;8 in Tests Screening for Barley PIP Ionic Conductance
2.2. HvPIP2;8 Monovalent Alkaline Cation Selectivity
2.3. HvPIP2;8 Was not Permeable to Cl−
2.4. Effects of Divalent Cations on HvPIP2;8-Mediated Ion Transport Activity
2.5. Co-Expression of HvPIP2;8 with HvPIP1s Limited HvPIP2;8 Ion Transport Activity
2.6. An HvPIP2;8 S285D Phosphomimic Mutant Had Greater Ionic Conductance Than Wild Type HvPIP2;8
2.7. Expression of HvPIP2;8 in Barley
3. Discussion
4. Materials and Methods
4.1. Plant Materials and Growth Conditions
4.2. Extraction of RNA and Gene Expression Analysis by RT-PCR and Real-Time Quantitative PCR (qPCR)
4.3. Preparation of HvPIP cRNAs
4.4. Expression of HvPIPs in X. laevis Oocytes
4.5. Electrophysiology
4.6. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Maurel, C.; Boursiac, Y.; Luu, D.T.; Santoni, V.; Shahzad, Z.; Verdoucq, L. Aquaporins in plants. Physiol. Rev. 2015, 95, 1321–1358. [Google Scholar] [PubMed]
- Laloux, T.; Junqueira, B.; Maistriaux, L.C.; Ahmed, J.; Jurkiewicz, A.; Chaumont, F. Plant and Mammal Aquaporins: Same but Different. Int. J. Mol. Sci. 2018, 19, 27. [Google Scholar]
- Katsuhara, M.; Shibasaka, M. Barley root hydraulic conductivity and aquaporins expression in relation to salt tolerance. Soil Sci. Plant Nutr. 2007, 53, 466–470. [Google Scholar] [CrossRef]
- Grondin, A.; Rodrigues, O.; Verdoucq, L.; Merlot, S.; Leonhardt, N.; Maurel, C. Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell 2015, 27, 1945–1954. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rodrigues, O.; Reshetnyak, G.; Grondin, A.; Saijo, Y.; Leonhardt, N.; Maurel, C.; Verdoucq, L. Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. Proc. Natl. Acad. Sci. USA 2017, 114, 9200–9205. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, C.; Hu, H.; Qin, X.; Zeise, B.; Xu, D.; Rappel, W.J.; Schroeder, J.I. Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor. Plant Cell 2016, 28, 568–582. [Google Scholar] [CrossRef] [Green Version]
- Katsuhara, M.; Koshio, K.; Shibasaka, M.; Hayashi, Y.; Hayakawa, T.; Kasamo, K. Over-expression of a barely aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants. Plant Cell Physiol. 2003, 44, 1378–1383. [Google Scholar]
- McGaughey, S.A.; Qiu, J.; Tyerman, S.D.; Byrt, C.S. Regulating root aquaporin function in response to changes in salinity. Ann. Plant Rev. Online 2018, 1, 381–416. [Google Scholar]
- Prak, S.; Hem, S.; Boudet, J.; Viennois, G.; Sommerer, N.; Rossignol, M.; Santoni, V. Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: Role in subcellular trafficking of AtPIP2;1 in response to salt stress. Mol. Cell. Proteom. 2008, 7, 1019–1030. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, S.Y.; Fukumoto, T.; Gena, P.; Feng, P.; Sun, Q.; Li, Q.; Ding, X.D. Ectopic expression of a rice plasma membrane intrinsic protein (OsPIP1;3) promotes plant growth and water uptake. Plant J. 2020, 102, 779–796. [Google Scholar] [CrossRef] [PubMed]
- Ikeda, M.; Beitz, E.; Kozono, D.; Guggino, W.B.; Agre, P.; Yasui, M. Characterization of aquaporin-6 as a nitrate channel in mammalian cells—Requirement of pore-lining residue threonine 63. J. Biol. Chem. 2002, 277, 39873–39879. [Google Scholar]
- Byrt, C.S.; Zhao, M.; Kourghi, M.; Bose, J.; Henderson, S.W.; Qiu, J.; Tyerman, S. Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant Cell Environ. 2017, 40, 802–815. [Google Scholar] [CrossRef] [Green Version]
- Kourghi, M.; Nourmohammadi, S.; Pei, J.V.; Qiu, J.; McGaughey, S.; Tyerman, S.D.; Yool, A.J. Divalent cations regulate the ion conductance properties of diverse classes of aquaporins. Int. J. Mol. Sci. 2017, 18, 2323. [Google Scholar] [CrossRef] [Green Version]
- Qiu, J.; McGaughey, S.A.; Groszmann, M.; Tyerman, S.D.; Byrt, C.S. Phosphorylation influences water and ion channel function of AtPIP2;1. Plant Cell Environ. 2020, in press. [Google Scholar] [CrossRef] [PubMed]
- Demidchik, V.; Tester, M. Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol. 2002, 128, 379–387. [Google Scholar] [CrossRef] [PubMed]
- Tyerman, S.D.; Skerrett, M.; Garrill, A.; Findlay, G.P.; Leigh, R.A. Pathways for the permeation of Na+ and Cl− into protoplasts derived from the cortex of wheat roots. J. Exp. Bot. 1997, 48, 459–480. [Google Scholar] [CrossRef]
- Essah, P.A.; Davenport, R.; Tester, M. Sodium influx and accumulation in Arabidopsis. Plant Physiol. 2003, 133, 307–318. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Isayenkov, S.V.; Maathuis, F.J.M. Plant salinity stress: Many unanswered questions remain. Front. Plant Sci. 2019, 10, 80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bienert, M.D.; Diehn, T.A.; Richet, N.; Chaumont, F.; Bienert, G.P. Heterotetramerization of Plant PIP1 and PIP2 Aquaporins Is an Evolutionary Ancient Feature to Guide PIP1 Plasma Membrane Localization and Function. Front. Plant Sci. 2018, 9, 15. [Google Scholar] [CrossRef]
- Zelazny, E.; Borst, J.W.; Muylaert, M.; Batoko, H.; Hemminga, M.A.; Chaumont, F. FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc. Natl. Acad. Sci. USA 2007, 104, 12359–12364. [Google Scholar] [CrossRef] [Green Version]
- Otto, B.; Uehlein, N.; Sdorra, S.; Fischer, M.; Ayaz, M.; Belastegui-Macadam, X.; Kaldenhoff, R. Aquaporin Tetramer Composition Modifies the Function of Tobacco Aquaporins. J. Biol. Chem. 2010, 285, 31253–31260. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vitali, V.; Jozefkowicz, C.; Fortuna, A.C.; Soto, G.; Flecha, F.L.G.; Alleva, K. Cooperativity in proton sensing by PIP aquaporins. FEBS J. 2019, 286, 991–1002. [Google Scholar] [CrossRef] [PubMed]
- Vandeleur, R.K.; Mayo, G.; Shelden, M.C.; Gilliham, M.; Kaiser, B.N.; Tyerman, S.D. The Role of Plasma Membrane Intrinsic Protein Aquaporins in Water Transport through Roots: Diurnal and Drought Stress Responses Reveal Different Strategies between Isohydric and Anisohydric Cultivars of Grapevine. Plant Physiol. 2009, 149, 445–460. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Horie, T.; Kaneko, T.; Sugimoto, G.; Sasano, S.; Panda, S.K.; Shibasaka, M.; Katsuhara, M. Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in Barley roots. Plant Cell Physiol. 2011, 52, 663–675. [Google Scholar] [CrossRef]
- Boursiac, Y.; Chen, S.; Luu, D.T.; Sorieul, M.; van den Dries, N.; Maurel, C. Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol. 2005, 139, 790–805. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boursiac, Y.; Boudet, J.; Postaire, O.; Luu, D.T.; Tournaire-Roux, C.; Maurel, C. Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J. 2008, 56, 207–218. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Wang, X.; Yang, Y.; Li, R.; He, Q.; Fang, X.; Luu, D.T.; Maurel, C.; Lin, J. Single-molecule analysis of PIP2; 1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 2011, 23, 3780–3797. [Google Scholar] [CrossRef] [Green Version]
- Ismail, A.M.; Horie, T. Genomics, Physiology, and Molecular Breeding Approaches for Improving Salt Tolerance. Annu. Rev. Plant Biol. 2017, 68, 405–434. [Google Scholar] [CrossRef] [Green Version]
- Munns, R.; Tester, M. Mechanisms of salinity tolerance. Ann. Rev. Plant Biol. 2008, 59, 651–681. [Google Scholar] [CrossRef] [Green Version]
- Katsuhara, M.; Hanba, Y.T.; Shiratake, K.; Maeshima, M. Expanding roles of plant aquaporins in plasma membranes and cell organelles. Funct. Plant Biol. 2008, 35, 1–14. [Google Scholar] [CrossRef]
- Shibasaka, M.; Sasano, S.; Utsugi, S.; Katsuhara, M. Functional characterization of a novel plasma membrane intrinsic protein2 in barley. Plant Sigal. Behav. 2012, 7, 1648–1652. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hove, R.M.; Ziemann, M.; Bhave, M. Identification and Expression Analysis of the Barley (Hordeum vulgare L.) Aquaporin Gene Family. PLoS ONE 2015, 10, e0128025. [Google Scholar] [CrossRef] [PubMed]
- Kaneko, T.; Horie, T.; Nakahara, Y.; Tsuji, N.; Shibasaka, M.; Katsuhara, M. Dynamic Regulation of the Root Hydraulic Conductivity of Barley Plants in Response to Salinity/Osmotic Stress. Plant Cell Physiol. 2015, 56, 875–882. [Google Scholar] [CrossRef] [PubMed]
- Knipfer, T.; Besse, M.; Verdeil, J.L.; Fricke, W. Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots. J. Exp. Bot. 2011, 62, 4115–4126. [Google Scholar] [CrossRef]
- Besse, M.; Knipfer, T.; Miller, A.J.; Verdeil, J.L.; Jahn, T.P.; Fricke, W. Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves. J. Exp. Bot. 2011, 62, 4127–4142. [Google Scholar] [CrossRef] [Green Version]
- Coffey, O.; Bonfield, R.; Corre, F.; Althea Sirigiri, J.; Meng, D.; Fricke, W. Root and cell hydraulic conductivity, apoplastic barriers and aquaporin gene expression in barley (Hordeum vulgare L.) grown with low supply of potassium. Ann. Bot. 2018, 122, 1131–1141. [Google Scholar] [CrossRef] [Green Version]
- Amtmann, A.; Laurie, S.; Leigh, R.; Sanders, D. Multiple inward channels provide flexibility in Na+/K+ discrimination at the plasma membrane of barley suspension culture cells. J. Exp. Bot. 1997, 48, 481–497. [Google Scholar] [CrossRef]
- Chen, Z.; Pottosin, I.I.; Cuin, T.A.; Fuglsang, A.T.; Tester, M.; Jha, D.; Zepeda-Jazo, I.; Zhou, M.; Palmgren, M.G.; Newman, I.A.; et al. Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol. 2007, 145, 1714–1725. [Google Scholar] [CrossRef] [Green Version]
- Kim, M.J.; Lee, Y.S.; Han, J.K. Modulation of lysophosphatidic acid-induced Cl− currents by protein kinases A and C in the Xenopus oocyte. Biochem. Pharmacol. 2000, 59, 241–247. [Google Scholar] [CrossRef]
- Horie, T.; Karahara, I.; Katsuhara, M. Salinity tolerance mechanisms in glycophytes: An overview with the central focus on rice plants. Rice 2012, 5, 1–18. [Google Scholar] [CrossRef] [Green Version]
- Horie, T.; Costa, A.; Kim, T.H.; Han, M.J.; Horie, R.; Leung, H.Y.; Miyao, A.; Hirochika, H.; An, G.; Schroeder, I.J. Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J. 2007, 26, 3003–3014. [Google Scholar] [CrossRef] [Green Version]
- Davenport, R.J.; Tester, M. A weakly voltage-dependent, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiol. 2000, 122, 823–834. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mori, I.C.; Nobukiyo, Y.; Nakahara, Y.; Shibasaka, M.; Furuichi, T.; Katsuhara, M. A Cyclic Nucleotide-Gated Channel, HvCNGC2-3, Is Activated by the Co-Presence of Na+ and K+ and Permeable to Na+ and K+ Non-Selectively. Plants 2018, 7, 61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chaumont, F.; Tyerman, S.D. Aquaporins: Highly Regulated Channels Controlling Plant Water Relations. Plant Physiol. 2014, 164, 1600–1618. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Byrt, C.S. Genes for Sodium Exclusion in Wheat. Ph.D. Thesis, University of Adelaide, Adelaide, Australia, 2008. Available online: https://digital.library.adelaide.edu.au/dspace/handle/2440/56208 (accessed on 26 September 2020).
- Xu, B.; Hrmova, M.; Gilliham, M. High affinity Na+ transport by wheat HKT1;5 is blocked by K+. BioRxiv 2018. Available online: https://www.biorxiv.org/content/10.1101/280453v2.abstract (accessed on 26 September 2020).
- Yao, X.; Horie, T.; Xue, S.; Leung, H.Y.; Katsuhara, M.; Brodsky, D.E.; Wu, Y.; Schroeder, J.I. Differential sodium and potassium transport selectivities of the rice OsHKT2;1 and OsHKT2;2 transporters in plant cells. Plant Physiol. 2010, 152, 341–355. [Google Scholar] [CrossRef] [Green Version]
- Yool, A.J.; Weinstein, A.M. New roles for old holes: Ion channel function in aquaporin-1. News Physiol. Sci. 2002, 17, 68–72. [Google Scholar] [CrossRef]
- Engh, R.A.; Girod, A.; Kinzel, V.; Huber, R.; Bossemeyer, D. Crystal structures of catalytic subunit of cAMP-dependent protein kinase in complex with isoquinolinesulfonyl protein kinase inhibitors H7, H8, and H89 structural implications for selectivity. J. Biol. Chem. 1996, 271, 26157–26164. [Google Scholar] [CrossRef] [Green Version]
- Nyblom, M.; Frick, A.; Wang, Y.; Ekvall, M.; Hallgren, K.; Hedfalk, K.; Neutze, R.; Tajkhorshid, E.; Törnroth-Horsefield, S. Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J. Mol. Biol. 2009, 387, 653–668. [Google Scholar] [CrossRef]
- Hyder, S.Z.; Greenway, H. Effects of Ca2+ on plant sensitivity to high NaCl concentrations. Plant Soil 1965, 23, 258–260. [Google Scholar] [CrossRef]
- Sanders, D.; Pelloux, J.; Brownlee, C.; Harper, J.F. Calcium at the crossroads of signaling. Plant Cell 2002, 14, S401–S417. [Google Scholar] [CrossRef] [Green Version]
- Choi, W.G.; Toyota, M.; Kim, S.H.; Hilleary, R.; Gilroy, S. Salt stress induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc. Natl. Acad. Sci. USA 2014, 111, 6497–6502. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Horie, T.; Hauser, F.; Schroeder, J.I. HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trend. Plant Sci. 2009, 14, 660–668. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liam, D.; Davies, J. Cell expansion in roots. Curr. Opin. Plant Biol. 2004, 7, 33–39. [Google Scholar]
- Martinez-Ballesta, M.C.; Garcia-Ibañez, P.; Yepes-Molina, L.; Rios, J.J.; Carvajal, M. The expanding role of vesicles containing aquaporins. Cells 2018, 7, 179. [Google Scholar] [CrossRef] [Green Version]
- Katsuhara, M.; Akiyama, Y.; Koshio, K.; Shibasaka, M.; Kasamo, K. Functional analysis of water channels in barley roots. Plant Cell Physiol. 2002, 43, 885–893. [Google Scholar] [CrossRef]
- 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, 688–694. [Google Scholar] [CrossRef]
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Tran, S.T.H.; Horie, T.; Imran, S.; Qiu, J.; McGaughey, S.; Byrt, C.S.; Tyerman, S.D.; Katsuhara, M. A Survey of Barley PIP Aquaporin Ionic Conductance Reveals Ca2+-Sensitive HvPIP2;8 Na+ and K+ Conductance. Int. J. Mol. Sci. 2020, 21, 7135. https://doi.org/10.3390/ijms21197135
Tran STH, Horie T, Imran S, Qiu J, McGaughey S, Byrt CS, Tyerman SD, Katsuhara M. A Survey of Barley PIP Aquaporin Ionic Conductance Reveals Ca2+-Sensitive HvPIP2;8 Na+ and K+ Conductance. International Journal of Molecular Sciences. 2020; 21(19):7135. https://doi.org/10.3390/ijms21197135
Chicago/Turabian StyleTran, Sen Thi Huong, Tomoaki Horie, Shahin Imran, Jiaen Qiu, Samantha McGaughey, Caitlin S. Byrt, Stephen D. Tyerman, and Maki Katsuhara. 2020. "A Survey of Barley PIP Aquaporin Ionic Conductance Reveals Ca2+-Sensitive HvPIP2;8 Na+ and K+ Conductance" International Journal of Molecular Sciences 21, no. 19: 7135. https://doi.org/10.3390/ijms21197135