Abstract
Boron deficiency hampers the productivity of 132 crops in more than 80 countries1. Boron is essential in higher plants primarily for maintaining the integrity of cell walls2,3,4 and is also beneficial and might be essential in animals5 and in yeast6. Understanding the molecular mechanism(s) of boron transport is crucial for alleviating boron deficiency. Here we describe the molecular identification of boron transporters in biological systems. The Arabidopsis thaliana mutant bor1-1 is sensitive to boron deficiency7,8. Uptake studies indicated that xylem loading is the key step for boron accumulation in shoots with a low external boron supply and that the bor1-1 mutant is defective in this process. Positional cloning identified BOR1 as a membrane protein with homology to bicarbonate transporters in animals. Moreover, a fusion protein of BOR1 and green fluorescent protein (GFP) localized to the plasma membrane in transformed cells. The promoter of BOR1 drove GFP expression in root pericycle cells. When expressed in yeast, BOR1 decreased boron concentrations in cells. We show here that BOR1 is an efflux-type boron transporter for xylem loading and is essential for protecting shoots from boron deficiency.
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References
Shorrocks, V. M. The occurrence and correction of boron deficiency. Plant Soil 193, 121–148 (1997)
Dannel, F., Pfeffer, H. & Römheld, V. Update on boron in higher plants – uptake, primary translocation and compartmentation. Plant Biol. 4, 193–204 (2002)
Brown, P. H. et al. Boron in plant biology. Plant Biol. 4, 205–223 (2002)
O'Neill, M. A., Eberhard, S., Albersheim, P. & Darvill, A. G. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294, 846–849 (2001)
Nielsen, F. H. The emergence of boron as nutritionally important throughout the life cycle. Nutrition 16, 512–514 (2000)
Bennett, A., Rowe, R. I., Soch, N. & Eckhert, C. D. Boron stimulates yeast (Saccharomyces cerevisiae) growth. J. Nutr. 129, 2236–2238 (1999)
Noguchi, K. et al. bor1-1, an Arabidopsis thaliana mutant that requires a high level of boron. Plant Physiol. 115, 901–906 (1997)
Takano, J., Yamagami, M., Noguchi, K., Hayashi, H. & Fujiwara, T. Preferential translocation of boron to young leaves in Arabidopsis thaliana regulated by the BOR1 gene. Soil Sci. Plant Nutr. 47, 345–357 (2001)
Dannel, F., Pfeffer, H. & Römheld, V. Characterization of root boron pools, boron uptake and boron translocation in sunflower using the stable isotopes 10B and 11B. Aust. J. Plant Physiol. 27, 397–405 (2000)
Stangoulis, J. C. R., Reid, R. J., Brown, P. H. & Graham, R. D. Kinetic analysis of boron transport in Chara. Planta 213, 142–146 (2001)
Noguchi, K. et al. Defect in root-shoot translocation of boron in Arabidopsis thaliana mutant bor1-1. J. Plant Physiol. 156, 751–755 (2000)
Poirier, Y., Thoma, S., Somerville, C. & Schiefelbein, J. A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol. 97, 1087–1093 (1991)
Gaymard, F. et al. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94, 647–655 (1998)
Dannel, F., Pfeffer, H. & Römheld, V. Compartmentation of boron in roots and leaves of sunflower as affected by boron supply. J. Plant Physiol. 153, 615–622 (1998)
Yasumori, M., et al. Plant Nutrition: Molecular Biology and Genetics (eds Nielsen, G. G. & Jensen, A.) 269–275 (Kluwer, Dordrecht, 1999)
Alper, S. L., Darman, R. B., Chernova, M. N. & Dahl, N. K. The AE gene family of Cl-/HCO3- exchangers. J. Nephrol. 15 suppl. 5, S41–S53 (2002)
Soleimani, M. Na+:HCO3- cotransporters (NBC): Expression and regulation in the kidney. J. Nephrol. 15 suppl. 5, S32–S40 (2002)
Pearson, W. R. & Lipman, D. J. Improved tools for biological sequence comparison. Proc. Natl Acad. Sci. USA 85, 2444–2448 (1988)
Zhao, R. & Reithmeier, R. A. F. Expression and characterization of the anion transporter homologue YNL275w in Saccharomyces cerevisiae. Am. J. Physiol. Cell Physiol. 281, C33–C45 (2001)
Chiu, W. L. et al. Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325–330 (1996)
Raven, J. A. Short- and long-distance transport of boric acid in plants. New Phytol. 84, 231–249 (1980)
Dordas, C., Chrispeels, M. J. & Brown, P. H. Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol. 124, 1349–1361 (2000)
Dordas, C. & Brown, P. H. Permeability and the mechanism of transport of boric acid across the plasma membrane of Xenopus laevis oocytes. Biol. Trace Elem. Res. 81, 127–139 (2001)
Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907 (1987)
Deblaere, R. et al. Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Res. 13, 4777–4788 (1985)
Bechtold, N., Ellis, J. & Pelletier, G. In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C.R. Acad. Sci. Paris Life Sci. 316, 1194–1199 (1993)
Fujiwara, T., Hirai, M. Y., Chino, M., Komeda, Y. & Naito, S. Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia. Plant Physiol. 99, 263–268 (1992)
Winzeler, E. A. et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901–906 (1999)
Sherman, F. Getting started with yeast. Method. Enzymol. 194, 3–21 (1991)
Kyte, J. & Doolittle, R. F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105–132 (1982)
Acknowledgements
We thank S. Naito, N. von Wirén and P. Walch-Liu for critical reading of the manuscript; Y. Niwa for providing the sGFP construct; K. Mukaikawato, M. Hashimoto and M. Sugasawa for technical contributions; and F. Kurisu for use of the facilities of the Research Center for Water Environment Technology in the School of Engineering, the University of Tokyo. RZ119b07 was kindly provided by Kazusa DNA Research Institute; BAC T3D7 clone was kindly provided by the Arabidopsis Biological Resource Center at Ohio State University. This work is supported in part by grants to T.F. from the Japanese Ministry of Education, Sports, Culture, Science, and Technology and the Graduate School of Agricultural Life Sciences, the University of Tokyo.
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T.F. applied for a Japanese patent (application no. 2001-062191) on 6 March 2001.
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Takano, J., Noguchi, K., Yasumori, M. et al. Arabidopsis boron transporter for xylem loading. Nature 420, 337–340 (2002). https://doi.org/10.1038/nature01139
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DOI: https://doi.org/10.1038/nature01139
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