Abstract
Boron, an orphan of the periodic table of the elements, is unique not only in its chemical properties but also in its roles in biology. Its requirement in plants was described more than 80 years ago. Understandings of the molecular basis of the requirement and transport have been advanced greatly in the last decade. This article reviews recent findings of boron function and transport in plants and discusses possible implication to other organisms including humans.
Similar content being viewed by others
References
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, San Diego, CA
Woods WG (1996) Review of possible boron speciation relating to its essentiality. J Trace Elem Exp Med 9:153–163
Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Romheld V (2002) Boron in plant biology. Plant Biol 4:205–223
Devirian TA, Volpe SL (2003) The physiological effects of dietary boron. Crit Rev Food Sci Nutr 43:219–231
WHO (1998) Boron. In: Environmental Health Criteria Monograph 204. Geneva, World Health Organization, ICPCS 1–125
Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193:121–148
Bolanos L, Lukaszewski K, Bonilla I, Blevins D (2004) Why boron? Plant Physiol Biochem 42:907–912
Yan X, Wu P, Ling H, Xu G, Xu F, Hang Q (2006) Plant nutriomics in China: an overview. Ann Bot 98(3):473–482
Yau SK, Nachit MM, Hamblin J, Ryan J (1995) Phenotypic variation in boron-toxicity tolerance at seedling stage in durum wheat (Triticum durum). Euphutica 83:185–191
Warington K (1923) The effect of boric acid and borax on the broad bean and certain other. Ann Bot 27:629–672
Dell B, Huang L (1997) Physiological response of plants to low boron. Plant Soil 193:103–120
Yazbeck C, Kloppmann W, Cottier R, Sahuquillo J, Debotte G, Huel G (2005) Health impact evaluation of boron in drinking water: a geographical risk assessment in northern France. Environ Geochem Health 27:419–427
Loomis WD, Durst RW (1992) Chemistry and biology of boron. Biofactors 3:229–239
Rowe RI, Eckhert CD (1999) Boron is required for zebrafish embryogenesis. J Exp Bot 202:1649–1654
Fort DJ, Propst TL, Stover EL, Strong PL, Murray FJ (1998) Adverse reproductive and developmental effects in Xenopus from insufficient boron. Biol Trace Elem Res 66:237–259
Goldbach HE (1997) A critical review on current hypotheses concerning the role of boron in higher plants: suggestions for further research and methodological requirements. J Trace Micer Techn 15:51–91
Goldbach HE, Yu Q, Wingender R, Schulz M, Wimmer M, Findeklee P, Baluka F (2001) Rapid response reactions of roots to boron deprivation. J Plant Nut Soil Sci 164:173–181
Kobayashi M, Matoh T, Azuma J (1996) Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol 110:1017–1020
O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139
O’Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis. Growth Science 294:846–849
Brown PH, Shelp BJ (1997) Boron mobility in plants. Plant Soil 193:85–101
Brown PH, Hu H (1996) Phloem mobility of boron is species dependent. Evidence for phloem mobility in sorbitol rich species. Ann Bot 77:497–505
Brown PH, Hu H (1998) Boron mobility and consequent management in different crops. Better Crops 82:28–31
Brown PH, Bellaloui N, Hu H, Dandekar A (1999) Transgenically enhanced sorbitol synthesis facilitates phloem boron transport and increases tolerance of tobacco to boron deficiency. Plant Physiol 110:17–20
Noguchi K, Dannel F, Pfeffer H, Romheld V, Hayashi H, Fujiwara T (2000) Defect in root-shoot translocation of boron in Arabidopsis thaliana mutant bor1-1. J Plant Physiol 156:751–755
Takano J, Yamagami M, Noguchi K, Hayashi H, Fujiwara T (2001) Preferential translocation of boron to young leaves in Arabidopsis thaliana regulated by the BOR1 gene. Soil Sci Plant Nutr 47:345–357
Stangolius JC, Brown PH, Bellaloui N, Reid RJ, Graham RD (2001) The efficiency of boron ulitisation in canola. Aust J Plant Physiol 28:1109–1114
Matoh T, Ochiai K (2005) Distribution and partitioning of newly take-up boron in sunflower. Plant Soil 278:351–360
Raven JA (1980) Short- and long-distance transport of boric acid in plants. New Phytol 84:231–249
Dordas C, Brown PH (2000) Permeability of boric acid across lipid bilayers and factors affecting it. J Membr Biol 175:95–105
Dordas C, Brown PH (2001) Evidence for channel mediated transport of boric acid in squash (Cucurbita pepo). Plant Soil 235:95–103
Stangoulis JCR, Reid RJ, Brown PH, Graham RD (2001) Kinetic analysis of boron transport in Chara. Planta 213:142–146
Dannel F, Pfeffer H, Romheld V (2000) 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
Takano J, Noguchi K, Yasumori M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T, Fujiwara T (2002) Arabidopsis boron transporter for xylem loading. Nature 420:337–340
Noguchi K, Yasumori M, Imai T, Naito S, Matsunaga T, Oda H, Hayashi H, Chino M, Fujiwara T (1997) bor1-1, an Arabidopsis thaliana mutant that requires a high level of boron. Plant Physiol 115:901–906
Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. PNAS 102:12276–12281
Nakagawa Y, Hanaoka H, Kobayashi M, Miyoshi K, Miwa K, Fujiwara T (2007) Cell-type specificity of the expression of OsBOR1, a rice efflux boron transporter gene, is regulated in response to boron availability for efficient boron uptake and xylem loading. Plant Cell 19:2624–2635
Park M, Li Q, Shcheynikov N, Zeng W, Muallern S (2004) NaBC1 is a ubiquitous electrogenic Nat-coupled borate transporter essential for cellular boron homeostasis and cell growth and proliferation. Mol Cell 16:331–341
Dordas C, Chrispeels MJ, Brown PH (2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124:1349–1361
Takano J, Wada M, Ludewig U, Schaaf G, von Wiren N, 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
Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194
Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biology Cell 97:397–414
Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysee L, Weig AR, Kjellbom P (2001) 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 Physiol 126:1358–1369
Mauel C (2007) Plant aquaporin: nove functions and regulation properties. FEBS Lett 581:2227–2236
Rivers RL, Dean RM, Chandy G, Hall JE, Roberts DM, Zeidel ML (1997) Functional analysis of nodulin 26, an aquaporin in soybean root nodule symbiosomes. J Biol Chem 272:16256–16261
Wallace IS, Choi WG, Roberts DM (2006) The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochim Biophys Acta 1758:1165–1175
Guenther JF, Chanmanivone N, Galetovic MP, Wallace IS, Cobb JA, Roberts DM (2003) Phosphorylation of nodulin 26 on serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. Plant Cell 15:981–991
Wallace IS, Roberts DM (2002) Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry 44:16826–16834
Wallace IS, Roberts DM (2004) Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins: classification based on the aromatic/arginine selectivity filter. Plant Physiol 135:1059–1068
Wallace IS, Roberts DM (2005) Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry 44:16826–16834
Choi WG, Roberts MD (2007) Arabidopsis NIP2;1: a major intrinsic protein transporter of lactic acid induced by anoxic stress. J Biol Chem 33:24209–24218
Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691
Weig AR, Jakob C (2000) Functional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae. FEBS Lett 481:293–298
Klebl F, Wolf M, Sauer N (2003) A defect in the yeast plasma membrane urea transporter Dur3p is complemented by CpNIP1, a Nod26-like protein from zucchini (Cucurbita pepo L.), and by Arabidopsis thaliana delta-TIP or gamma-TIP. FEBS Lett 547:69–74
Hanaoka H, Fujiwara F (2007) Channel-mediated boron transport in rice. Plant Cell Physiol 48:227
Tsukaguchi H, Shayaku Cl, Berger UV, Mackenzie B, Devidas S, Guggino WB, Hoek AN, Hediger MA (1998) Molecular characterization of a broad selectivity neutral solute channel. J Biol Chem 38:24737–24743
Tsukaguchi H, Weremowicz S, Morton CC, Hediger MA (1999) Functional and molecular characterization of the human neutral solute channel aquaporin-9. Am J Physiol Renal Physiol 277:685–696
Acknowledgements
The present review is in part based on the daily discussion with the members of our laboratory, and we would like to specially thank Drs. Junpei Takano, Hideki Hanaoka, and Kyoko Miwa for sharing thoughts and information.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tanaka, M., Fujiwara, T. Physiological roles and transport mechanisms of boron: perspectives from plants. Pflugers Arch - Eur J Physiol 456, 671–677 (2008). https://doi.org/10.1007/s00424-007-0370-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00424-007-0370-8