Update on Boron in Higher Plants - Uptake, Primary Translocation and Compartmentation

Abstract

This review focuses on the uptake and primary translocation of boron (B), as well as on the subcellular compartmentation of B and its role in cell walls of higher plants. B uptake occurs via passive diffusion across the lipid bilayer, facilitated transport through major intrinsic proteins (MIPs), and energy-dependent transport through a high affinity uptake system. Whereas the first two represent passive uptake systems, which are constitutively present, the latter is induced by low B supply and is able to establish a concentration gradient for B between the root symplasm and the external medium. At high B supply, a substantial retention of B can be observed at xylem loading, and passive processes are most likely responsible for that. At low B supply, another energy-dependent high affinity transport system for B seems to be induced which establishes an additional concentration gradient between root symplasm and the xylem. The possible significance of all these processes at various B supplies is discussed. The role of soluble B complexes in uptake and primary translocation of B has been evaluated, but the few data available do not allow comprehensive conclusions to be drawn. In any case, there are no indications that soluble B complexes play a major role in either uptake or primary translocation of B. The subcellular compartmentation of B still remains a matter of controversy, but it is unequivocally clear that B is present in all subcellular compartments (apoplasm, cell wall, cytosol and vacuole). The relative distribution of B between these is dependent on plant species and experimental conditions and may vary greatly. Recent results on the well-established role of B in cell walls are summarized and their physiological significance discussed.

Boron - cell wall - compartmentation - complexes - translocation - uptake

References

• 01 Agre,  P.,, Bonhivers,  M.,, and Borgnia,  M. J.. (1998);  The aquaporins, blueprints for cellular plumbing systems.  J. Biol. Chem.. 273 14659-14662
• 02 Asad,  A.,, Bell,  R. W.,, Dell,  B.,, and Huang,  L.. (1997);  External boron requirements for canola (Brassica napus L.) in boron buffered solution culture.  Ann. Bot.. 80 65-73
• 03 Bellaloui,  N., and Brown,  P. H.. (1998);  Cultivar differences in boron uptake and distribution in celery (Apium graveolens), tomato (Lycopersicon esculentum) and wheat (Triticum aestivum). .  Plant Soil. 198 153-158
• 04 Bellaloui,  N.,, Brown,  P. H.,, and Dandekar,  A.. (1999);  Manipulation of in vivo sorbitol production alters boron uptake and transport in tobacco.  Plant Physiol.. 119 735-741
• 05 Bennett,  A.,, Rowe,  I.,, Soch,  N.,, and Eckhert,  C. D.. (1999);  Boron stimulates yeast (Saccharomyces cerevisiae) growth.  J. Nutr.. 129 2236-2238
• 06 Brown,  J. C., and Jones,  W. E.. (1971);  Differential transport of boron in tomato.  Plant Physiol.. 25 279-282
• 07 Brown,  P. H.,, Bellaloui,  N.,, Hu,  H.,, and Dandekar,  A.. (1999);  Transgenically enhanced sorbitol synthesis facilitates phloem boron transport and increases tolerance of tobacco to boron deficiency.  Plant Physiol.. 119 17-20
• 08 Brown,  P. H., and Hu,  H.. (1997) Does boron play only a structural role in the growing tissues of higher plants?. Plant Nutrition for Sustainable Food Production and Environment. Ando, T., Fujita, K., Mae, T., Matsumoto, H., Mori, S., and Sekiya, J., eds. Dordrecht, The Netherlands; Kluwer Academic Publishers pp. 63-67
• 09 Brown,  P. H., and Shelp,  B. J.. (1997);  Boron mobility in plants.  Plant Soil. 193 85-101
• 10 Chapman,  V. J.,, Edwards,  D. G.,, Blamey,  F. P. C.,, and Asher,  C. J.. (1997) Challenging the dogma of a narrow supply range between deficiency and toxicity of boron. Boron in Soils and Plants. Bell, R. W. and Rerkasem, B., eds. Dordrecht, The Netherlands; Kluwer Academic Publishers pp. 151-155
• 11 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
• 12 Chuda,  Y.,, Ohnishi-Kameyama,  M.,, and Nagata,  T.. (1997);  Identification of the forms of boron in seaweed by ¹¹B NMR.  Phytochemistry. 46 209-213
• 13 Dannel,  F.,, Pfeffer,  H.,, and Marschner,  H.. (1995);  Isolation of apoplasmic fluid from sunflower leaves and its use for studies on influence of nitrogen supply on apoplasmic pH.  J. Plant Physiol.. 146 273-278
• 14 Dannel,  F.,, Pfeffer,  H.,, and Römheld,  V.. (1997) Effect of pH and boron concentration in the nutrient solution on translocation of boron in the xylem of sunflower. Boron in Soils and Plants. Bell, R. W. and Rerkasem, B., eds. Dordrecht, The Netherlands; Kluwer Academic Publishers pp. 183-186
• 15 Dannel,  F.,, Pfeffer,  H.,, and Römheld,  V.. (1998);  Compartmentation of boron in roots and leaves of sunflower as affected by boron supply.  J. Plant Physiol.. 153 615-622
• 16 Dannel,  F.,, Pfeffer,  H.,, and Römheld,  V.. (1999);  Distribution within the plant or compartmentation does not contribute substantially to the detoxification of excess boron in sunflower (Helianthus annuus). .  Aust. J. Plant Physiol.. 26 95-99
• 17 Dannel,  F.,, Pfeffer,  H.,, and Römheld,  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
• 18 De Boer,  A. H.. (1999);  Potassium translocation into the root xylem.  Plant Biol.. 1 36-45
• 19 Dordas,  C., and Brown,  P. H.. (2000);  Permeability of boric acid across lipid bilayers and factors affecting it.  J. Membrane Biol.. 175 95-105
• 20 Dordas,  C.,, Chrispeels,  M. J.,, and Brown,  P. H.. (2000);  Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots.  Plant Physiol.. 124 1349-1361
• 21 Eckert,  M.,, Biela,  A.,, Siefritz,  F.,, and Kaldenhoff,  R.. (1999);  New aspects of plant aquaporin regulation and specificity.  J. Exp. Bot.. 50 1541-1545
• 22 Fleischer,  A.,, O'Neill,  M. A.,, and Ehwald,  R.. (1999);  The pore size of non-graminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II.  Plant Physiol.. 121 829-838
• 23 Fleischer,  A.,, Titel,  C.,, and Ehwald,  R.. (1998);  The boron requirement and cell wall properties of growing and stationary suspension-cultured Chenopodium album L. cells.  Plant Physiol.. 117 1401-1410
• 24 Gerbeau,  P.,, Güçlü,  J.,, Ripoche,  P.,, and Maurel,  C.. (1999);  Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small solutes.  Plant J.. 18 577-587
• 25 Hu,  H., and Brown,  P. H.. (1994);  Localization of boron in cell walls of squash and tobacco and its association with pectin - Evidence for a structural role of boron in the cell wall.  Plant Physiol.. 105 681-689
• 26 Hu,  H., and Brown,  P. H.. (1997);  Absorption of boron by plant roots.  Plant Soil. 193 49-58
• 27 Hu,  H.,, Brown,  P. H.,, and Labavitch,  J. M.. (1996);  Species variability in boron requirement is correlated with cell wall pectin.  J. Exp. Bot.. 47 227-232
• 28 Hu,  H.,, Penn,  S. G.,, Lebrilla,  C. B.,, and Brown,  P. H.. (1997);  Isolation and characterization of soluble boron complexes in higher plants.  Plant Physiol.. 113 649-655
• 29 Ishii,  T., and Matsunaga,  T.. (1996);  Isolation and characterization of a boron-rhamnogalacturonan-II complex from cell walls of sugar beet pulp.  Carbohydr. Res.. 284 1-9
• 30 Ishii,  T.,, Matsunaga,  T.,, Pellerin,  P.,, O'Neill,  M. A.,, Darvill,  A. G.,, and Albersheim,  P.. (1999);  The plant cell wall polysaccharide rhamnogalacturonan II self-assembles into a covalently cross-linked dimer.  J. Biol. Chem.. 274 13098-13104
• 31 Kobayashi,  M.,, Matoh,  T.,, and 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
• 32 Kobayashi,  M.,, Nakagawa,  H.,, Asaka,  T.,, and Matoh,  T.. (1999);  Borate-Rhamnogalacturonan II bonding reinforced by Ca²⁺ retains pectic polysaccharides in higher-plant cell walls.  Plant Physiol.. 119 199-203
• 33 Kobayashi,  M.,, Ohno,  K.,, and Matoh,  T.. (1997);  Boron nutrition of cultured tobacco BY-2 cells. II. characterization of the boron-polysaccaride complex.  Plant Cell Physiol.. 38 676-683
• 34 Kochian,  L. V., and Lucas,  W. J.. (1982);  Potassium transport in corn roots. I. Resolution of kinetics into a saturable and linear component.  Plant Physiol.. 70 1723-1731
• 35 Lande,  M. B.,, Donovan,  J. M.,, and Zeidel,  M. L.. (1995);  The relationship between membrane fluidity and permeabilities to water, solutes, ammonia, and protons.  J. Gen. Physiol.. 106 67-84
• 36 Lasat,  M. M.,, Baker,  A. J. M.,, and Kochian,  L. V.. (1996);  Physiological characterization of root Zn²⁺ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi.  Plant Physiol.. 112 1715-1722
• 37 Logan,  H.,, Basset,  M.,, Véry,  A.-A.,, and Sentenac,  H.. (1997);  Plasma membrane transport systems in higher plants: From black boxes to molecular physiology.  Physiol. Plant.. 100 1-15
• 38 Loomis,  W. D., and Durst,  R. W.. (1992);  Chemistry and biology of boron.  BioFactors. 3 229-239
• 39 Lutz,  O.,, Humpfer,  E.,, and Spraul,  M.. (1991);  Ascertainment of boric esters in wine by ¹¹B NMR.  Naturwissenschaften. 78 67-69
• 40 Manhart,  J. R., and Palmer,  J. D.. (1990);  The gain of two chloroplast tRNA introns marks the green algal ancestors of land plants.  Nature. 345 268-270
• 41 Marentes,  E.,, Vanderpool,  R. A.,, and Shelp,  B. J.. (1997);  Boron-isotope fractionation in plants.  Can. J. Plant Sci.. 77 627-629
• 42 Marschner,  H.. (1995) Mineral Nutrition of Higher Plants. London; Academic Press
• 43 Martini,  F., and Thellier,  M.. (1993);  Boron distribution in parenchyma cells of clover leaves.  Plant Physiol. Biochem.. 31 777-786
• 44 Matoh,  T.. (1997);  Boron in plant cell walls.  Plant Soil. 193 59-70
• 45 Matoh,  T.,, Ishigaki,  K.,, Mizutani,  M.,, Matsunaga,  W.,, and Takabe,  K.. (1992);  Boron nutrition of cultured tobacco BY-2 cells. I. Requirement for and intracellular localisation of boron and selection of cells that tolerate low levels of boron.  Plant Cell Physiol.. 33 1135-1141
• 46 Matoh,  T.,, Ishigaki,  K.,, Ohno,  K.,, and Azuma,  J.. (1993);  Isolation and characterization of a boron-polysaccharide complex from radish roots.  Plant Cell Physiol.. 34 639-642
• 47 Matoh,  T.,, Kawaguchi,  S.,, and Kobayashi,  M.. (1996);  Ubiquity of a borate-rhamno-galacturonan II complex in the cell walls of higher plants.  Plant Cell Physiol.. 37 636-640
• 48 Matoh,  T., and Kobayashi,  M.. (1998);  Boron and calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls.  J. Plant Res.. 111 179-190
• 49 Matoh,  T.,, Takasaki,  M.,, Kobayashi,  M.,, and Takabe,  K.. (2000);  Boron nutrition of cultured tobacco BY-2 cells. III. Characterization of the boron-rhamnogalacturonan II complex in cells acclimated to low levels of boron.  Plant Cell Physiol.. 41 363-366
• 50 Matsunaga,  T.,, Ishii,  T.,, and Watanabe,  H.. (1996);  Speciation of water-soluble boron compounds in radish roots by size exclusion HPLC/ICP-MS.  Anal. Sci.. 12 673-675
• 51 Matsunaga,  T., and Nagata,  T.. (1995);  In vivo ¹¹B NMR observation of plant tissue.  Anal. Sci.. 11 889-892
• 52 Nable,  R. O.. (1988);  Resistance to boron toxicity amongst several barley and wheat cultivars: A preliminary examination of the resistance mechanism.  Plant Soil. 112 45-52
• 53 Nable,  R. O.,, Banuelos,  G. S.,, and Paull,  J. G.. (1997);  Boron toxicity.  Plant Soil. 193 181-198
• 54 Navari-Izzo,  F.,, Quartacci,  M. F.,, Melfi,  D.,, and Izzo,  R.. (1993);  Lipid composition of plasma membranes isolated from sunflower seedlings grown under water stress.  Physiol. Plant.. 87 508-514
• 55 Nielsen,  F. H.. (2000);  The emergence of boron as nutritionally important throughout the life cycle.  Nutrition. 16 512-514
• 56 Noguchi,  K.,, Dannel,  F.,, Pfeffer,  H.,, Römheld,  V.,, Hayashi,  H.,, and Fujiwara,  T.. (2000);  Defect in root-shoot translocation of boron in Arabidopsis thaliana mutant bor1-1.  J. Plant Physiol.. 156 751-755
• 57 Noguchi,  K.,, Yasumori,  M.,, Imai,  T.,, Naito,  S.,, Matsunaga,  T.,, Oda,  H.,, Hayashi,  H.,, Chino,  M.,, and Fujiwara,  T.. (1997);  bor1-1, an Arabidopsis thaliana mutant that requires a high level of boron.  Plant Physiol.. 115 901-906
• 58 Nuttall,  C. Y.. (2000) Boron Tolerance and Uptake in Higher Plants. University of Cambridge, U.K.; PhD Thesis
• 59 O'Neill,  M. A.,, Warrenfeltz,  D.,, Kates,  K.,, Pellerin,  P.,, Doco,  T.,, Darvill,  A. G.,, and Albersheim,  P.. (1996);  Rhamnogalacturonan II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by borate ester.  J. Biol. Chem.. 271 22923-22930
• 60 Pariot,  C.,, Martini,  F.,, Thellier,  M.,, and Ripoll,  C.. (1994);  Quantitative imaging of the distribution of boron in hypocotyl sections of flax seedlings, using neutron capture radiography.  J. Trace and Microprobe Techniques. 12 61-85
• 61 Pellerin,  P.,, Doco,  T.,, Vidal,  S.,, Williams,  P.,, Brillouet,  J.-M.,, and O'Neill,  M. A.. (1996);  Structural characterization of red wine rhamnogalacturonan II.  Carbohydr. Res.. 290 183-197
• 62 Penn,  S. G.,, Hu,  H.,, Brown,  P. H.,, and Lebrilla,  C. B.. (1997);  Direct analysis of sugar alcohol borate complexes in plant extracts by matrix-assisted laser desorption/ionization Fourier transform mass spectrometry.  Anal. Chem.. 69 2471-2477
• 63 Pfeffer,  H.,, Dannel,  F.,, and Römheld,  V.. (1997) Compartmentation of boron in roots and its translocation to the shoot of sunflower as affected by short term changes in boron supply. Boron in Soils and Plants. Bell, R. W. and Rerkasem, B., eds. Dordrecht, The Netherlands; Kluwer Academic Publishers pp. 203-207
• 64 Pfeffer,  H.,, Dannel,  F.,, and Römheld,  V.. (1999 b);  Are there two mechanisms for boron uptake in sunflower?.  J. Plant Physiol.. 155 34-40
• 65 Pfeffer,  H.,, Dannel,  F.,, and Römheld,  V.. (1999 a);  Isolation of soluble boron complexes and their determination together with free boric acid in higher plants.  J. Plant Physiol.. 154 283-288
• 66 Pfeffer,  H.,, Dannel,  F.,, and Römheld,  V.. (2001);  Boron compartmentation in roots of sunflower plants of different boron status - a study using the stable isotopes ¹⁰B and ¹¹B adopting two independent approaches.  Physiol. Plant. 113 346-351
• 67 Power,  P. P., and Woods,  W. G.. (1997);  The chemistry of boron and its speciation in plants.  Plant Soil. 193 1-13
• 68 Raven,  J. A.. (1980);  Short- and long-distance transport of boric acid in plants.  New Phytol.. 84 231-249
• 69 Reczynski,  W., and Ryczkowski,  M.. (1994);  Boron distribution in the developing ovules of Clivia miniata Regel and Aesculus glabra Willd.  J. Plant Physiol.. 144 623-626
• 70 Sah,  R. N., and Brown,  P. H.. (1997);  Techniques for boron determination and their application to the analysis of plant and soil samples.  Plant Soil. 193 15-33
• 71 Schuler,  I.,, Milon,  A.,, Nakatani,  Y.,, Ourisson,  G.,, Albrecht,  A.-M.,, Benveniste,  P.,, and Hartmann,  M.-A.. (1991);  Differential effects of plant sterols on water permeability and on acyl chain ordering of soybean phosphatidylcholine bilayers.  Proc. Natl. Acad. Sci. USA. 88 6926-6930
• 72 Shelp,  B. J.,, Kitheka,  A. M.,, Vanderpool,  R. A.,, Van Cauwenberghe,  O. R.,, and Spiers,  G. A.. (1998);  Xylem-to-phloem transfer of boron in broccoli and lupin during early reproductive growth.  Physiol. Plant.. 104 533-540
• 73 Sheveleva,  E. V.,, Marquez,  S.,, Chmara,  W.,, Zegeer,  A.,, Jensen,  R. G.,, and Bohnert,  H. J.. (1998);  Sorbitol-6-phosphate dehydrogenase expression in transgenic tobacco. High amounts of sorbitol lead to necrotic lesions.  Plant Physiol.. 117 831-839
• 74 Stangoulis,  J. C. R.,, Reid,  R. J.,, Brown,  P. H.,, and Graham,  R. D.. (2001);  Kinetic analysis of boron transport in Chara. .  Planta. 213 142-146
• 75 Steudle,  E., and Henzler,  T.. (1995);  Water channels in plants: do basic concepts of water transport change?.  J. Exp. Bot.. 46 1067-1076
• 76 Thellier,  M.,, Duval,  Y.,, and Demarty,  M.. (1979);  Borate exchange of Lemna minor as studied with the help of the enriched stable isotopes and of a (n,α) nuclear reaction.  Plant Physiol.. 63 283-288
• 77 Walker,  N. A., and Pitman,  N. A.. (1976) Measurement of fluxes across membranes. Encyclopedia of Plant Physiology, New Series. Lüttge, U. and Pitman, M. G., eds. Berlin; Springer pp. 93-126
• 78 Walker,  N. A.,, Reid,  R. J.,, and Smith,  F. A.. (1993);  The uptake and metabolism of urea by Chara australis: IV. Symport with sodium - a slip model for the high and low affinity uptake systems.  J. Membrane Biol.. 136 263-271
• 79 Wall,  J. R., and Andrus,  C. F.. (1962);  The inheritance and physiology of boron response in the tomato.  Amer. J. Bot.. 49 758-762
• 80 Wann,  E. V., and Hills,  W. A.. (1973);  The genetics of boron and iron transport in the tomato.  Journal of Heredity. 64 370-371
• 81 Weig,  A.,, Deswarte,  C.,, and Chrispeels,  M. J.. (1997);  The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group.  Plant Physiol.. 114 1347-1357
• 82 Wilson,  M. R.,, O'Donohue,  S. I.,, and Walker,  N. A.. (1988);  The transport and metabolism of urea in Chara australis: III. Two specific transport systems.  J. Exp. Bot.. 39 763-774
• 83 Wilson,  M. R., and Walker,  N. A.. (1988);  The transport and metabolism of urea in Chara australis: I. Passive diffusion, specific transport and metabolism of urea, thiourea and methylurea.  J. Exp. Bot.. 39 739-751

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