Ectopic expression of a rice plasma membrane intrinsic protein (OsPIP1;3) promotes plant growth and water uptake.
aquaporin
carbon dioxide
hydraulic conductivity
membrane transport
nitrate
permeability
plant growth
water
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
14
11
2018
revised:
09
11
2019
accepted:
09
12
2019
pubmed:
25
12
2019
medline:
16
2
2021
entrez:
25
12
2019
Statut:
ppublish
Résumé
Plasma membrane intrinsic proteins (PIPs) are known to be major facilitators of the movement of a number of substrates across cell membranes. From a drought-resistant cultivar of Oryza sativa (rice), we isolated an OsPIP1;3 gene single-nucleotide polymorphism (SNP) that is mostly expressed in rice roots and is strongly responsive to drought stress. Immunocytochemistry showed that OsPIP1;3 majorly accumulated on the proximal end of the endodermis and the cell surface around the xylem. Expression of GFP-OsPIP1;3 alone in Xenopus oocytes or rice protoplasts showed OsPIP1;3 mislocalization in the endoplasmic reticulum (ER)-like neighborhood, whereas co-expression of OsPIP2;2 recruited OsPIP1;3 to the plasma membrane and led to a significant enhancement of water permeability in oocytes. Moreover, reconstitution of 10×His-OsPIP1;3 in liposomes demonstrated water channel activity, as revealed by stopped-flow light scattering. Intriguingly, by patch-clamp technique, we detected significant NO
Substances chimiques
Membrane Proteins
0
Plant Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
779-796Informations de copyright
© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd.
Références
Abascal, F., Irisarri, I. and Zardoya, R. (2014) Diversity and evolution of membrane intrinsic proteins. Biochim. Biophys. Acta, 1840, 1468-1481.
Aharon, R., Shahak, Y., Wininger, S., Bendov, R., Kapulnik, Y. and Galilia, G. (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell, 15, 439-447.
Alexandersson, E., Fraysse, L., Sjövall-Larsen, S., Gustavsson, S., Fellert, M., Karlsson, M., Johanson, U. and Kjellbom, P. (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol. Biol. 59, 469-484.
Almeida-Rodriguez, A.M., Cooke, J.E.K., Yeh, F. and Zwiazek, J.J. (2010) Functional characterization of drought-responsive aquaporins in Populus balsamifera and Populus simonii×balsamifera clones with different drought resistance strategies. Physiol. Plant. 140, 321-333.
Baba, A., Hasezawa, S. and Syono, K. (1986) Cultivation of rice protoplasts and their transformation mediated by Agrobacterium spheroplasts. Plant Cell Physiol. 27, 463-471.
Bienert, M.D., Diehn, T.A., Richet, N., Chaumont, F. and Bienert, G.P. (2018) Heterotetramerization of plant PIP1 and PIP2 aquaporins is an evolutionary ancient feature to guide PIP1 plasma membrane localization and function. Front. Plant Sci. 9, 382.
Borgnia, M.J., Kozono, D., Calamita, G., Maloney, P.C. and Agre, P. (1999) Functional reconstitution and characterization of AqpZ, the E. coli water channel protein. J. Mol. Biol. 291, 1169-1179.
Calamita, G., Bishai, W.R., Preston, G.M., Guggino, W.B. and Agre, P. (1995) Molecular cloning and characterization of AqpZ, a water channel from Escherichia coli. J. Biol. Chem. 270, 29063-29066.
Calamita, G., Gena, P., Meleleo, D., Ferri, D. and Svelto, M. (2006) Water permeability of rat liver mitochondria: a biophysical study. Biochim. Biophys. Acta-Biomembr. 1758, 1018-1024.
Chaumont, F., Barrieu, F., Jung, R. and Chrispeels, M.J. (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol. 122, 1025-1034.
Chevalier, A.S. and Chaumont, F. (2015) Trafficking of plant plasma membrane aquaporins: multiple regulation levels and complex sorting signals. Plant Cell Physiol. 56, 819-829.
Clarkson, D.T., Carvajal, M., Henzler, T., Waterhouse, R.N., Smyth, A.J., Cooke, D.T. and Steudle, E. (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J. Exp. Bot. 51, 61-70.
Crozet, P., Margalha, L., Confraria, A., Rodrigues, A., Martinho, C., Adamo, M., Elias, C.A. and Baena-González, E. (2014) Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases. Front. Plant Sci. 5, 190.
Dean, R.M., Rivers, R.L., Zeidel, M.L. and Roberts, D.M. (1999) Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry, 38, 347-353.
Deshmukh, R.K., Sonah, H. and Bélanger, R.R. (2016) Plant aquaporins: genome-wide identification, transcriptomics, proteomics, and advanced analytical tools. Front. Plant Sci. 7, 1896.
Ding, X., Iwasaki, I. and Kitagawa, Y. (2004) Overexpression of a lily PIP1 gene in tobacco increased the osmotic water permeability of leaf cells. Plant Cell Environ. 27, 177-186.
Ding, X., Matsumoto, T., Gena, P. et al. (2013) Water and CO2 permeability of SsAqpZ, the cyanobacterium Synechococcus sp. PCC7942 aquaporin. Biol. Cell, 105, 118-128.
Echevarría, M., Windhager, E.E. and Frindt, G. (1996) Selectivity of the renal collecting duct water channel aquaporin-3. J. Biol. Chem. 271, 25079-25082.
Fetter, K., van Wilder, V., Moshelion, M. and Chaumont, F. (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell, 16, 215-228.
Flexas, J., Ribas-Carbó, M., Hanson, D.T., Bota, J., Otto, B., Cifre, J., McDowell, N., Medrano, H. and Kaldenhoff, R. (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J. 48, 427-439.
Flexas, J., Ortuño, M.F., Ribas-Carbo, M., Diaz-Espejo, A., Flórez-Sarasa, I.D. and Medrano, H. (2007) Mesophyll conductance to CO2 in Arabidopsis thaliana. New Phytol. 175, 501-511.
Flexas, J., Niinemets, U., Gallé, A. et al. (2013a) Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth Res. 117, 45-59.
Flexas, J., Scoffoni, C., Gago, J. and Sack, L. (2013b) Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. J. Exp. Bot. 64, 3965-3981.
Fox, A.R., Maistriaux, L. and Chaumont, F. (2017) Towards understanding of the high number of plant aquaporin isoforms and multiple regulation mechanisms. Plant Sci. 264, 179-187.
Gaspar, M., Bousser, A., Sissoeff, I., Roche, O., Hoarau, J. and Mahe, A. (2003) Cloning and characterization of ZmPIP1-5b, an aquaporin transporting water and urea. Plant Sci. 165, 21-31.
Gena, P., Pellegrini-Calace, M., Biasco, A., Svelto, M. and Calamita, G. (2011) Aquaporin membrane channels: biophysics, classification, functions, and possible biotechnological applications. Food Biophys. 6, 241-249.
Gloser, V., Zwieniecki, M.A., Orians, C.M. and Holbrook, N.M. (2007) Dynamic changes in root hydraulic properties in response to nitrate availability. J. Exp. Bot. 58, 2409-2415.
Grondin, A., Mauleon, R., Vadez, V. and Henry, A. (2016) Root aquaporins contribute to whole plant water fluxes under drought stress in rice (Oryza sativa L.). Plant Cell Environ. 39, 347-365.
Groszmann, M., Osborn, H.L. and Evans, J.R. (2017) Carbon dioxide and water transport through plant aquaporins. Plant Cell Environ. 40, 938-961.
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. and Sigworth, F.J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391, 85-100.
Harley, P.C., Loreto, F., Marco, G.D. and Sharkey, T.D. (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol. 98, 1429-1436.
Hedrich, R. and Geiger, D. (2017) Biology of SLAC1-type anion channels-from nutrient uptake to stomatal closure. New Phytol. 216, 46-61.
van Heeswijk, M.P.E. and van Os, C.H. (1986) Osmotic water permeabilities of brush border and basolateral membrane vesicles from rat renal cortex and small intestine. J. Membr. Biol. 92, 183-193.
Hwang, J.H., Ellingson, S.R. and Roberts, D.M. (2010) Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett. 584, 4339-4343.
Ikeda, M., Beitz, E., Kozono, D., Guggino, W.B., Agre, P. and Yasui, M. (2002) Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63. J. Biol. Chem. 277, 39873-39879.
Ishibashi, K., Morishita, Y. and Tanaka, Y. (2017) The evolutionary aspects of aquaporin family. Adv. Exp. Med. Biol. 969, 35-50.
Jang, J.Y., Kim, D.G., Kim, Y.O., Kim, J.S. and Kang, H. (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol. Biol. 54, 713-725.
Jozefkowicz, C., Rosi, P., Sigaut, L., Soto, G., Pietrasanta, L., Amodeo, G. and Alleva, K. (2013) Loop A is critical for the functional interaction of two Beta vulgaris PIP aquaporins. PLoS ONE, 8, e57993.
Kadam, S., Abril, A., Dhanapal, A.P., Koester, R.P., Vermerris, W., Jose, S. and Fritschi, F.B. (2017) Characterization and regulation of aquaporin genes of sorghum (Sorghum bicolor (L.) Moench) in response to waterlogging stress. Front. Plant Sci. 8, 862.
Kaldenhoff, R. and Fischer, M. (2006) Functional aquaporin diversity in plants. Biochem. Biophy. Acta, 1758, 1134-1141.
Kaldenhoff, R., Grote, K., Zhu, J.J. and Zimmermann, U. (1998) Significance of plasmalemma aquaporins for water-transport in Arabidopsis thaliana. Plant J. 14, 121-128.
Katsuhara, M., Akiyama, Y., Koshio, K., Shibasaka, M. and Kasamo, K. (2002) Functional analysis of water channels in barley roots. Plant Cell Physiol. 43, 885-893.
Kozono, D., Ding, X., Iwasaki, I., Meng, X., Kamagata, Y., Agre, P. and Kitagawa, Y. (2003) Functional expression and characterization of an archaeal aquaporin. AqpM from Methanothermobacter marburgensis. J. Biol. Chem. 278, 10649-10656.
Li, G., Tillard, P., Gojon, A. and Maurel, C. (2016) Dual regulation of root hydraulic conductivity and plasma membrane aquaporins by plant nitrate accumulation and high-affinity nitrate transporter NRT2.1. Plant Cell Physiol. 57, 733-742.
Lian, H.L., Yu, X., Ye, Q., Ding, X., Kitagawa, Y., Kwak, S.S., Su, W.A. and Tang, Z.C. (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol. 45, 481-489.
Lian, H.L., Yu, X., Lane, D., Sun, W.N., Tang, Z.C. and Su, W.A. (2006) Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res. 16, 651-660.
Liu, H.Y., Yu, X., Cui, D.Y., Sun, M.H., Sun, W.N., Tang, Z.C., Kwak, S.S. and Su, W.A. (2007) The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Res. 17, 638-649.
Liu, C., Fukumoto, T., Matsumoto, T. et al. (2013) Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination. Plant Physiol. Biochem. 63, 151-158.
Matsumoto, T., Lian, H.L., Su, W.A., Tanaka, D., Liu, C., Iwasaki, I. and Kitagawa, Y. (2009) Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. Plant Cell Physiol. 50, 216-229.
Matsuo, N., Ozawa, K. and Mochizuki, T. (2009) Genotypic differences in root hydraulic conductance of rice (Oryza sativa L.) in response to water regimes. Plant Soil, 316, 25-34.
Maurel, C., Reizer, J., Schroeder, J.I. and Chrispeels, M.J. (1993) The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes. EMBO J. 12, 2241-2247.
Maurel, C., Verdoucq, L., Luu, D.-T. and Santoni, V. (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu. Rev. Plant Biol. 59, 595-624.
Maurel, C., Boursiac, Y., Luu, D.-T., Santoni, V., Shahzad, Z. and Verdoucq, L. (2015) Aquaporins in plants. Physiol. Rev. 95, 1321-1358.
Maurel, C., Verdoucq, L. and Rodrigues, O. (2016) Aquaporins and plant transpiration. Plant Cell Environ. 39, 2580-2587.
Missner, A., Kügler, P., Saparov, S.M., Sommer, K., Mathai, J.C., Zeidel, M.L. and Pohl, P. (2008) Carbon dioxide transport through membranes. J. Biol. Chem. 283, 25340-25347.
Mori, I.C., Rhee, J., Shibasaka, M., Sasano, S., Kaneko, T., Horie, T. and Katsuhara, M. (2014) CO2 transport by PIP2 aquaporins of barley. Plant Cell Physiol. 55, 251-257.
Murai-Hatano, M., Kuwagata, T., Sakurai, J., Nonami, H., Ahamed, A., Nagasuga, K., Matsunami, T., Fukushi, K., Maeshima, M. and Okada, M. (2008) Effect of low root temperature on hydraulic conductivity of rice plants and the possible role of aquaporins. Plant Cell Physiol. 49, 1294-1305.
Nakhoul, N.L., Davis, B.A., Romero, M.F. and Boron, W.F. (1998) Effect of expressing the water channel aquaporin-1 on the CO2 permeability of Xenopus oocytes. Am. J. Physiol. 43, C543-C548.
Nguyen, M.X., Moon, S. and Jung, K.-H. (2013) Genome-wide expression analysis of rice aquaporin genes and development of a functional gene network mediated by aquaporin expression in roots. Planta, 238, 669-681.
Preston, G.M., Carroll, T.P., Guggino, W.B. and Agre, P. (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science, 256, 385-387.
Qin, X. and Boron, W.F. (2013) Mutation of a single amino acid converts the human water channel aquaporin 5 into an anion channel. Am. J. Physiol. 305, C663-C672.
Rodrigues, O., Reshetnyak, G., Grondin, A., Saijo, Y., Leonhardt, N., Maurel, C. and Verdoucq, L. (2017) Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. Proc. Natl Acad. Sci. USA, 114, 9200-9205.
Schäfer, N., Maierhofer, T., Herrmann, J. et al. (2018) A tandem amino acid residue motif in guard cell SLAC1 anion channel of grasses allows for the control of stomatal aperture by nitrate. Curr. Biol. 28, 1370-1379.
She, J., Guo, J., Chen, Q., Zeng, W., Jiang, Y. and Bai, X. (2018) Structural insights into the voltage and phospholipid activation of mammalian TPC1 channel. Nature, 556, 130-134.
Shen, J., Fu, J., Ma, J., Wang, X., Gao, C., Zhuang, C., Wan, J. and Jiang, L. (2014) Isolation, culture, and transient transformation of plant protoplasts. Curr. Protoc. Cell Biol. 63, 2.8.1-17.
Song, S., Xu, Y., Huang, D., Miao, H., Liu, J., Jia, C., Hu, W., Valarezo, A.V., Xu, B. and Jin, Z. (2018) Identification of a novel promoter from banana aquaporin family gene (MaTIP1;2) which responses to drought and salt-stress in transgenic Arabidopsis thaliana. Plant Physiol. Biochem. 128, 163-169.
Song, Y., Zhang, H., You, H. et al. (2019) Identification of novel interactors and potential phosphorylation substrates of GsSnRK1 from wild soybean (Glycine soja). Plant Cell Environ. 42, 145-157.
Takano, J., Wada, M., Ludewig, U., Schaaf, G., Wirén, N. and Fujiwara, T. (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell, 18, 1498-1509.
Uehlein, N., Lovisolo, C., Siefritz, F. and Kaldenhoff, R. (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature, 425, 734-737.
Vieira, P.M., Santos, M.P., Andrade, C.M., Souza-Neto, O.A., Ulhoa, C.J. and Aragão, F.J.L. (2017) Overexpression of an aquaglyceroporin gene from Trichoderma harzianum improves water-use efficiency and drought tolerance in Nicotiana tabacum. Plant Physiol. Biochem. 121, 38-47.
Wang, Y.H., Garvin, D.F. and Kochian, L.V. (2001) Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiol. 127, 345-59.
Wang, X., Cai, H., Li, Y., Zhu, Y., Ji, W., Bai, X., Zhu, D. and Sun, X. (2015) Ectopic overexpression of a novel Glycine soja stress-induced plasma membrane intrinsic protein increases sensitivity to salt and dehydration in transgenic Arabidopsis thaliana plants. J. Plant Res. 128, 103-113.
Wang, C., Hu, H., Qin, X., Zeise, B., Xu, D., Rappel, W.J., Boron, W.F. and Schroeder, J.I. (2016) Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor. Plant Cell, 28, 568-582.
Wang, L., Li, Q.-T., Lei, Q., Feng, C., Zheng, X., Zhou, F., Li, L., Liu, X. and Kong, J. (2017a) Ectopically expressing MdPIP1;3, an aquaporin gene, increased fruit size and enhanced drought tolerance of transgenic tomatoes. BMC Plant Biol. 17, 246.
Wang, L., Wang, S., Chen, W., Li, H. and Deng, X. (2017b) Physiological mechanisms contributing to increased water-use efficiency in winter wheat under organic fertilization. PLoS ONE, 12, e0180205.
Wu, F., Sheng, P., Tan, J. et al. (2015) Plasma membrane receptor-like kinase leaf panicle 2 acts downstream of the DROUGHT AND SALT TOLERANCE transcription factor to regulate drought sensitivity in rice. J. Exp. Bot. 66, 271-281.
Xu, F., Wang, K., Yuan, W. et al. (2019) Overexpression of rice aquaporin OsPIP1;2 improves yield by enhancing mesophyll CO2 conductance and phloem sucrose transport. J. Exp. Bot. 70, 671-681.
Zhuo, C., Wang, T., Guo, Z. and Lu, S. (2016) Overexpression of MfPIP2-7 from Medicago falcata promotes cold tolerance and growth under NO3- deficit in transgenic tobacco plants. BMC Plant Biol. 16, 138.
Zwiazek, J.J., Xu, H., Tan, X., Navarro-Ródenas, A. and Morte, A. (2017) Significance of oxygen transport through aquaporins. Sci. Rep. 7, 40411.