Boron in Plant Biology

Abstract

The interest of biologists in boron (B) has largely been focused on its role in plants for which B was established as essential in 1923 (Warington, 1923[153]). Evidence that B has a biological role in other organisms was first indicated by the establishment of essentiality of B for diatoms (Smyth and Dugger, 1981[138]) and cyanobacteria (Bonilla et al., 1990[14]; Garcia-Gonzalez et al., 1991[44]; Bonilla et al., 1997[16]). Recently, B was shown to stimulate growth in yeast (Bennett et al., 1999[8]) and to be essential for zebrafish (Danio rerio) (Eckhert and Rowe, 1999[33]; Rowe and Eckhert, 1999[121]) and possibly for trout (Oncorhynchus mykiss) (Eckhert, 1998[32]; Rowe et al., 1998[120]), frogs (Xenopus laevis) (Fort et al., 1998[41]) and mouse (Lanoue et al., 2000[75]). There is also preliminary evidence to suggest that B has at least a beneficial role in humans (Nielsen, 2000[96]).

While research into the role of B in plants has been ongoing for 80 years it has only been in the past 5 years that the first function of B in plants has been defined. Boron is now known to be essential for cell wall structure and function, likely through its role as a stabilizer of the cell wall pectic network and subsequent regulation of cell wall pore size. A role for B in plant cell walls, however, is inadequate to explain all of the effects of B deficiency seen in plants. The suggestion that B plays a broader role in biology is supported by the discovery that B is essential for animals where a cellulose-rich cell wall is not present. Careful consideration of the physical and chemical properties of B in biological systems, and of the experimental data from both plants and animals suggests that B plays a critical role in membrane structure and hence function. Verification of B association with membranes would represent an important advance in modern biology.

For several decades there has been uncertainty as to the mechanisms of B uptake and transport within plants. This uncertainty has been driven by a lack of adequate methodology to measure membrane fluxes of B at physiologically relevant concentrations. Recent experimentation provides the first direct measurement of membrane permeability of B and illustrates that passive B permeation contributes sufficient B at adequate levels of B supply, but would be inadequate at conditions of marginal B supply. The hypothesis that an active, carrier mediated process is involved in B uptake at low B supply is supported by research demonstrating that B uptake can be stimulated by B deprivation, that uptake rates follow a Michaelis-Menton kinetics, and can be inhibited by application of metabolic inhibitors. Since the mechanisms of element uptake are generally conserved between species, an understanding of the processes of B uptake is relevant to studies in both plants and animals.

The study of B in plant biology has progressed markedly in the last decade and we are clearly on the cusp of additional, significant discoveries. Research in this field will be greatly stimulated by the discovery that B is essential for animals, a discovery that will not only encourage the participation of a wider cadre of scientists but will refocus the efforts of plant biologists toward a determination of roles for B outside the plant cell wall. Determination of the function of B in biology and of the mechanisms of B uptake in biological systems, is essential to our understanding and management of B deficiency and toxicity in plants and animals in both agricultural and natural environments. Through an analysis of existing data and the development of new hypotheses, this review aims to provide a vision of the future of research into the biology of boron.

Key words

Boron - function - structure - essentiality - membrane - uptake - transport - cell wall - reproduction

References

• 01 Agarwala,  S.,, Sharma,  P.,, Chatterjee,  C.,, and Sharma,  C.. (1981);  Development and enzymatic changes during pollen development in boron deficient maize plants.  J. Plant Nutr.. 3 329-336
• 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 Baron,  L.. (1973);  The value of boron sprays on filberts.  Nut Growers Soc. Oregon Washington. 58 22-28
• 04 Barone,  L. M.,, Shih,  C.,, and Wasserman,  B. P.. (1997);  Mercury-induced conformational changes and identification of conserved surface loops in plasma membrane aquaporins form higher plants: topology of PMIP 31 form Beta vulgaris L.  J. Biol. Chem.. 272 30672-30677
• 05 Baron-Epel,  O.,, Gharyal,  P. K.,, and Schindler,  M.. (1988);  Pectins as mediators of wall porosity in soybean cells.  Planta. 175 389-395
• 06 Barr,  R.,, Böttger,  M.,, and Crane,  F. L.. (1993);  The effect of boron on plasma membrane electron transport and associated proton secretion by cultured carrot cells.   Biochemistry and Molecular Biology International. 31 (1) 31-39
• 07 Bellaloui,  N.,, Brown,  P. H.,, and Dandekar,  A. M.. (1999);  Manipulation of in vivo sorbitol production alters boron uptake and transport in tobacco.  Plant Physiol.. 119 735-741
• 08 Bennett,  A.,, Rowe,  R. I.,, Soch,  N.,, and Eckhert,  C. D.. (1999);  Boron stimulates yeast (Saccharomyces cerevisiae) growth.  J. Nutr.. 129 2236-2238
• 09 Blaser-Grill,  J.,, Knoppik,  D.,, Amberger,  A.,, and Goldbach,  H. E.. (1989);  Influence of boron on the membrane potential in Elodea densa and Helianthus annuus roots and H⁺ extrusion of suspension cultured Daucus carota cells.  Plant Physiol.. 90 280-284
• 10 Blevins,  D. G., and Lukaszewski,  K. M.. (1998);  Boron in plant structure and function.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. 49 481-500
• 11 Boeseken,  J.. (1949);  The use of boric acid for the determination of the configuration of carbohydrates.  Adv. Carbohydrate Chem.. 4 183-210
• 12 Bolanos,  L.,, Esteban,  E.,, Delorenzo,  C.,, Fernandezpascual,  M.,, Defelipe,  M. R.,, Garate,  A.,, and Bonilla,  I.. (1994);  Essentiality of boron for symbiotic dinitrogen fixation in pea (Pisum sativum) rhizobium nodules.  Plant Physiol.. 104 85-90
• 13 Bolanos,  L.,, Mateo,  P.,, and Bonilla,  I.. (1993);  Calcium-mediated recovery of boron deficient Anabaena Sp PPCC 7119 grown under nitrogen fixing conditions.  J. Plant Physiol.. 142 513-517
• 14 Bonilla,  I.,, Garcia-González,  M.,, and Mateo,  P.. (1990);  Boron requirement in cyanobacteria. Its possible role in the early evolution of photosynthetic organisms.  Plant Physiol.. 94 1554-1560
• 15 Bonilla,  I.,, Mateo,  P.,, and Garate,  A.. (1988);  Accion del boro sobre el metabolismo nitrogenado en Lycopersicum esculentum cv. Dombo, cultivado en hidroponia.  Agrochimica. 32 276-284
• 16 Bonilla,  I.,, Mergold-Villasenor,  C.,, Campos,  M. E.,, Sánchez,  N.,, Pérez,  H.,, López,  L.,, Castrejón,  L.,, Sánchez,  F.,, and Cassab,  G. I.. (1997);  The aberrant cell walls of boron-deficient bean root nodules have no covalently bound hydroxyproline-/proline-rich proteins.  Plant Physiol.. 115 1329-1340
• 17 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
• 18 Brown,  P. H., and Hu,  H. N.. (1994);  Boron uptake by sunflower, squash and cultured tobacco cells.  Physiol. Plant.. 91 435-441
• 19 Brown,  P. H., and Shelp,  B. J.. (1997);  Boron mobility in plants.  Plant and Soil. 193 85-101
• 20 Cakmak,  I.,, Kurz,  H.,, and Marschner,  H.. (1995);  Short-term effects of boron, germanium and high light intensity on membrane permeability in boron deficient leaves of sunflower.  Physiol. Plant.. 95 11-18
• 21 Cakmak,  I., and Römheld,  V.. (1997);  Boron deficiency-induced impairments of cellular functions in plants.  Plant and Soil. 193 71-83
• 22 Carpena,  R. O.,, Garate,  A.,, and Zornoza,  P.. (2000);  Boron and calcium distribution in nitrogen-fixing pea plants.  Plant Science. 151 163-170
• 23 Cleland,  R. E.. (1992);  Auxin-induced growth of Avena coleoptiles involves two mechanisms with different pH Optima.  Plant Physiol.. 99 1556-1561
• 24 Coetzer,  L., and Robbertse,  P.. (1987);  Pollen biology of Persea americana Fuerte.  S. Afr. Avocado Grow Assoc. Yearbook. 10 43-45
• 25 Cresti,  M.,, Ciampolini,  D.,, Mulcahy,  L.,, and Mulcahy,  G.. (1985);  Ultrastructure of Nicotiana alata pollen, its germination and early development.  Amer. J. Bot.. 72 719-727
• 26 Dannel,  F.,, Pfeffer,  H.,, and Römheld,  V.. (2000);  Characterization of root boron pools, boron uptake and boron translocation in sunflower using stable isotopes ¹⁰B and ¹¹B.  Aust. J. Plant Physiol.. 27 397-405
• 27 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
• 28 Dell,  B., and Huang,  L.. (1997);  Physiological response of plants to low boron.  Plant and Soil. 193 103-120
• 29 Dordas,  C., and Brown,  P. H.. (2000);  Permeability of boric acid across lipid bilayers and factors affecting it.  J. Membrane Biol.. 175 95-105
• 30 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
• 31 Dugger,  W. M.. (1983) Boron in plant metabolism. Encyclopedia of Plant Physiology, New Series, Vol. 15. Läuchli, A. and Bieleski, R. L., eds. Berlin; Springer-Verlag pp. 626-650
• 32 Eckhert,  C. D.. (1998);  Boron stimulates embryonic trout growth.  J. Nutr.. 128 2488-2493
• 33 Eckhert,  C. D., and Rowe,  R. I.. (1999);  Embryonic dysplasia and adult retinal dystrophy in boron-deficient zebrafish.  J. Trace Elem. Exp. Med.. 12 213-219
• 34 Ehwald,  R.,, Heese,  P.,, and Klein,  U.. (1991);  Determination of the size limits of membrane separation in vesicle chromatography by fractionation of polydisperse dextran.  Journal of Chromatography. 542 239-245
• 35 Ehwald,  R.,, Woehlecke,  H.,, and Titel,  C.. (1992);  Cell wall microcapsules with different porosity from suspension cultured Chenopodium album. .  Phytochemistry. 31 3033-3038
• 36 El-Shintinawy,  F.. (1999);  Structural and functional damage caused by boron deficiency in sunflower leaves.  Photosynthetica. 36 565-573
• 37 Ferrol,  N.,, Belver,  A.,, Roldan,  M.,, Rodriguezrosales,  M. P.,, and Donaire,  J. P.. (1993);  Effects of boron on proton transport and membrane properties of sunflower (Helianthus annuus L.) cell microsomes.  Plant Physiol.. 103 763-769
• 38 Findeklee,  P., and Goldbach,  H. E.. (1996);  Rapid effects of boron deficiency on cell wall elasticity modulus in Cucurbita pepo roots.  Bot. Acta. 109 463-465
• 39 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
• 40 Fleischer,  A.,, O'Neill,  M. A.,, and Ehwald,  R.. (1999);  The pore size of non-graminaceaous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II.  Plant Physiol.. 121 829-838
• 41 Fort,  D. J.,, Propst,  T. L.,, Stover,  E. L.,, and Strong,  P. L.. (1998);  Adverse reproductive and developmental effects in Xenopus from insufficient boron.  Biol. Trace Elem. Res.. 66 237-259
• 42 Frantzen,  F.,, Grimsrud,  K.,, Heggli,  D.-E.,, and Sundrehagen,  E.. (1995);  Protein-boronic acid conjugates and their binding to low-molecular-mass cis-diols and glycated hemoglobin.  Journal of Chromatography B. 670 37-45
• 43 Friedman,  S.,, Pace,  B.,, and Pizer,  R.. (1974);  Complexation of phenylboronic acid with lactic acid. Stability constant and reaction kinetics.  J. Am. Chem. Soc.. 96 5381-5384
• 44 Garcia-Gonzalez,  M.,, Mateo,  P.,, and Bonilla,  I.. (1991);  Boron requirement for envelope structure and function in Anabaena PCC 7119 heterocysts.  J. Exp. Bot.. 42 925-929
• 45 Gauch,  H. G., and Dugger,  W. M.. (1954);  The physiological action of boron in higher plants: review and interpretation.  University Maryland AES Techn. Bull.. 80 1-43
• 46 Goldbach,  H. E.. (1985);  Influence of boron nutrition on net uptake and efflux of ³²P and ¹⁴C-glucose in Helianthus annuus roots and cell cultures of Daucus carota. .  J. Plant Physiol.. 118 431-438
• 47 Goldbach,  H. E.. (1997);  A critical review on current hypotheses concerning the role of boron in higher plants: suggestions for further research and methodological requirements.  J. Trace and Microprobe Tech.. 15 51-91
• 48 Goldbach,  H. E.,, Hartmann,  D.,, and Rötzer,  T.. (1990);  Boron is required for the stimulation of the ferricyanide-induced proton release by auxins in suspension-cultured cells of Daucus carota and Lycopersican esculentum. .  Physiol. Plant.. 80 114-118
• 49 Gupta,  U. C.. (1979);  Boron nutrition of crops.  Advances in Agronomy. 31 273-307
• 50 Gupta,  U. C.. (1993) Factors affecting boron uptake by plants. Boron and its role in crop production. Gupta, U. C., ed. Boca Raton; CRC Press Inc. pp. 87-104
• 51 Hanson,  E., and Breen,  P.. (1985);  Effects of fall boron sprays and environmental factors on fruit set and boron accumulation in “Italian” prune flowers.  J. Amer. Soc. Hort. Sci.. 110 389-392
• 52 Hanson,  E. J.. (1991 a);  Movement of boron out of tree fruit leaves.  HortScience. 26 271-273
• 53 Hanson,  E. J.. (1991 b);  Sour cherry trees respond to foliar boron applications.  HortScience. 26 1142-1145
• 54 Hanson,  E. J.,, Chaplin,  M. H.,, and Breen,  P. J.. (1985);  Movement of foliar applied boron out of leaves and accumulation in flower buds and flower parts of “Italian” prune.  HortScience. 20 747-748
• 55 Hirsch,  A. M., and Torrey,  J. G.. (1980);  Ultrastructural changes in sunflower root cells in relation to boron deficiency and added auxin.  Can. J. Bot.. 58 856-866
• 56 Hu,  H., and Brown,  P. H.. (1994);  Localization of boron in cell walls of squash and tobacco and its association with pectin.  Plant Physiol.. 105 681-689
• 57 Hu,  H., and Brown,  P. H.. (1997);  Absorption of boron by plant roots.  Plant and Soil. 193 49-58
• 58 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
• 59 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
• 60 Huang,  C., and Graham,  R. D.. (1990);  Resistance of wheat genotypes to boron toxicity is expressed at the cellular level.  Plant and Soil. 126 295-300
• 61 Huang,  L.,, Pant,  J.,, Dell,  B.,, and Bell,  R.. (2000);  Effects of boron deficiency on anther development and floret fertility in wheat (Triticum aestivum L. “Wilgoyne”).  Ann. Bot.. 85 493-500
• 62 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
• 63 Ishii,  T.,, Matsunaga,  T.,, Pellerin,  P.,, O'Neill,  M. A.,, Darvill,  A.,, 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
• 64 Jackson,  J. F.. (1989);  Borate control of protein secretion from Petunia pollen exhibits critical temperature discontinuities.  Sex. Plant Reprod.. 2 11-14
• 65 Jarvis,  B. C.,, Yasmin,  S.,, Ali,  A. H.,, and Hunt,  R.. (1984);  The interaction between auxin and boron in adventitious root development.  New Phytol.. 97 197-204
• 66 Jones,  D. H.. (1984);  Phenylalanine ammonia-lyase: regulation of its induction and its role in plant development.  Phytochemistry. 23 1349-1359
• 67 Kaneko,  S.,, Ishii,  T.,, and Matsunaga,  T.. (1997);  A boron-rhamnogalacturonan-II complex from bamboo shoot cell walls.  Phytochemistry. 44 243-248
• 68 Kastori,  R., and Petrovic,  N.. (1989);  Effect of boron on nitrate reductase activity in young sunflower plants.  J. Plant Nutr.. 12 621-632
• 69 Kastori,  R.,, Plesnicar,  M.,, Pankovic,  D.,, and Sakac,  Z.. (1995);  Photosynthesis, chlorophyll fluorescence and soluble carbohydrates in sunflower leaves as affected by boron deficiency.  J. Plant Nutr.. 18 1751-1763
• 70 Kobayashi,  M.,, Matoh,  T.,, and Azuma,  J.-I.. (1996);  Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls.  Plant Physiol.. 110 1017-1020
• 71 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
• 72 Kobayashi,  M.,, Ohno,  K.,, and Matoh,  T.. (1997);  Boron nutrition of cultured tobacco BY-2 cells. II. Characterization of the boron-polysaccharide complex.  Plant Cell Physiol.. 38 676-683
• 73 Kouchi,  H., and Kumazawa,  K.. (1976);  Anatomical responses of root tips to boron deficiency. III: Effect of boron deficiency on sub-cellular structure of root tips, particularly on morphology of cell wall and its related organelles.  Soil Sci. Plant Nutr.. 22 53-71
• 74 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 Phys.. 106 67-84
• 75 Lanoue,  L.,, Trollinger,  D. R.,, Strong,  P. L.,, and Keen,  C. L.. (2000);  Functional impairments in preimplantation mouse embryos following boron deficiency.  FASEB J.. 14 A 539
• 76 Lawrence,  K.,, Bhalla,  P.,, and Misra,  P. C.. (1995);  Changes in NAD(P)H-dependent redox activities in plasmalemma-enriched vesicles isolated from boron- and zinc-deficient chick pea roots.  J. Plant Physiol.. 146 652-657
• 77 Lee,  S. G., and Aronoff,  S.. (1966);  Investigations on the role of boron in plants. III. Anatomical observations.  Plant Physiol.. 41 1570-1577
• 78 Lewis,  D. H.. (1980);  Boron, lignification and the origin of vascular plants - a unified hypothesis.  New Phytol.. 84 209-229
• 79 Linden,  C. D.,, Wright,  K. L.,, McConnell,  H. M.,, and Fox,  C. F.. (1973);  Lateral phase separations in membrane lipids and the mechanism of sugar transport in Escherichia col. .  Proc. Natl. Acad. Sci. USA. 70 2271-2275
• 80 Liu,  P., and Yang,  Y.-A.. (2000);  Effects of molybdenum and boron on membrane lipid peroxidation and endogenous protective systems of soybean leaves.  Acta Bot. Sin.. 42 461-466
• 81 Loomis,  W. D., and Durst,  R. W.. (1992);  Chemistry and biology of boron.  BioFactors. 3 229-239
• 82 Lovatt,  C. J., and Dugger,  W. M.. (1984) Boron. The Biochemistry of the Essential Ultra Trace Elements. Frieden, E., ed. New York; Plenum pp. 389-421
• 83 Lukaszewski,  K. M., and Blevins,  D. G.. (1996);  Root growth inhibition in boron-deficient or aluminum-stressed squash may be a result of impaired ascorbate metabolism.  Plant Physiol.. 112 1135-1140
• 84 Matoh,  T.,, Ishigaki,  K.-I.,, Mizutani,  M.,, Matsunaga,  W.,, and Takabe,  K.. (1992);  Boron nutrition of cultured tobacco BY-2 cells. I. Requirement for and intracellular localization of boron and selection of cells that tolerate low levels of boron.  Plant Cell Physiol.. 33 (8) 1135-1141
• 85 Matoh,  T.,, Ishigaki,  K.-I.,, Ohno,  K.,, and Azuma,  J.-I.. (1993);  Isolation and characterization of a boron-polysaccharide complex from radish roots.  Plant Cell Physiol.. 34 (4) 639-643
• 86 Matoh,  T.,, Kawaguchi,  S.,, and Kobayashi,  M.. (1996);  Ubiquity of a borate-rhamnogalacturonan II complex in the cell walls of higher plants.  Plant Cell Physiol.. 37 636-640
• 87 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
• 88 Matsunaga,  T.,, Ishii,  T.,, and Watanabe-Oda,  H.. (1997) HPLC/ICP-MS study of metals bound to borate-rhamnogalacturonan-II form plant cell walls. Plant Nutrition for Sustainable Food Production and Environment. Ando, T., Fujita, K., Mae, T., Matsumoto, H., Sori, S., and Sekiya, eds. Dordrecht; Kluwer Academic Publishers pp. 81-82
• 89 Misra,  D., and Patil,  B.. (1987);  Effect of boron on seed yield in lucern Medicago sativa L.  Crop Sci.. 158 34
• 90 Moing,  A.,, Carbonne,  F.,, Rashad,  M. H.,, and Gaudilere,  J. P.. (1992);  Carbon fluxes in mature peach leaves.  Plant Physiol.. 100 1878-1884
• 91 Mouritsen,  O. G.,, Jorgensen,  K.,, and Honger,  T.. (1995) Permeability of lipid bilayers near the phase transition. Permeability and Stability of Lipid Bilayers. Disalvo, S. and Simon, S. A., eds. Boca Raton, Florida; CRC Press pp. 137-157
• 92 Mozafar,  A.. (1993) Role of boron in seed production. Boron and its role in crop production. Gupta, U. C., ed. Boca Raton, Florida; CRC Press pp. 186-206
• 93 Mühling,  K. H.,, Wimmer,  M.,, and Goldbach,  H. E.. (1998);  Apoplastic and membrane-associated Ca²⁺ in leaves and roots as affected by boron deficiency.  Physiol. Plant.. 102 179-184
• 94 Mullins,  G. L., and Sommers,  L. E.. (1986);  Cadmium and zinc influx characteristics by intact corn (Zea mays L.) seedlings.  Plant and Soil. 96 153-164
• 95 Nable,  R. O.,, Banuelos,  G. S.,, and Paull,  J. G.. (1997);  Boron toxicity.  Plant and Soil. 193 181-198
• 96 Nielsen,  F. H.. (2000);  The emergence of boron as nutritionally important throughout the life cycle.  Nutrition. 16 512-514
• 97 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
• 98 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
• 99 Nuttall,  C. Y.. (2000) Boron Tolerance and Uptake in Higher Plants. University of Cambridge, U.K.; PhD Thesis
• 100 Nyomora,  A. M. S.. (1995) The effect of boron deficiency on the reproductive processes of almond (Prunus dulcis [Mill] DA Webb). University of California, Davis; PhD Thesis
• 101 Nyomora,  A. M. S.,, Brown,  P. H.,, and Freeman,  M.. (1997);  Fall foliar-applied boron increases tissue boron concentration and nut set of almond.  J. Amer. Soc. Hort. Sci.. 122 405-410
• 102 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 a borate ester.  J. Biol. Chem.. 271 22923-22930
• 103 Parr,  A. J., and Loughman,  B. C.. (1983) Boron and membrane function in plants. Metals and micronutrients: uptake and utilization by plants. Robb, D. A. and Pierpoint, W. S. A., eds. New York; Academic Press pp. 87-107
• 104 Passioura,  J. B.. (1977);  Grain yield, harvest index and water use of wheat.  J. Aust. Inst. Agric. Sci.. 43 117-120
• 105 Pellerin,  P.,, Doco,  T.,, Vidal,  S.,, Williams,  P.,, Brillouet,  J.-M.,, and O'Neill,  M. A.. (1996);  Structural characterization of red wine rhamnogalacturonan II.  Carbohydrate Research. 290 183-197
• 106 Peter,  J. K., and Stanley,  R. G.. (1974) Boron in pollen and pollen cell fractions. Pollen: Biochemistry and management. Stanley, R. G. and Linskens, H. G., eds. Berlin; Springer
• 107 Pfeffer,  H.,, Dannel,  F.,, and Römheld,  V.. (1999);  Are there two mechanisms for boron uptake in sunflower?.  J. Plant Physiol.. 155 34-40
• 108 Pfeffer,  H.,, Dannel,  F.,, and Römheld,  V.. (1998);  Are there connections between phenol metabolism, ascorbate metabolism and membrane integrity in leaves of boron-deficient sunflower plants?.  Physiol. Plant.. 104 479-485
• 109 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
• 110 Piland,  J. R.,, Ireland,  C. F.,, and Reisenauer,  H. M.. (1944);  The importance of borax in legume seed production in the south.  Soil Sci.. 57 75-84
• 111 Pilbeam,  D. J., and Kirkby,  E. A.. (1983);  The physiological role of boron in plants.  J. Plant Nutr.. 6 (7) 563-582
• 112 Pollard,  A. S.,, Parr,  A. J.,, and Loughman,  B. C.. (1977);  Boron in relation to membrane function in higher plants.  J. Exp. Bot.. 28 831-841
• 113 Rahman,  N. H. H.,, Arima,  Y.,, Watenabe,  K.,, and Sekimoto,  H.. (1999);  Adequate range of boron nutrition is more restricted for root nodule development than for plant growth in young soybean plant.  Soil Sci. Plant Nutr.. 45 287-296
• 114 Ramon,  A. M.,, Ruiz,  R. O.,, and Garate,  A.. (1989);  In vitro stabilization and distribution of nitrate reductase in tomato plants: incidence of boron deficiency.  J. Plant Physiol.. 135 126-128
• 115 Raven,  J. A.. (1980);  Short- and long-distance transport of boric acid in plants.  New Phytol.. 84 231-249
• 116 Rawson,  H. M.. (1996);  The developmental stage during which boron limitation causes sterility in wheat genotypes and the recovery of fertility.  Aust. J. Plant Physiol.. 23 709-717
• 117 Rayle,  D. L., and Cleland,  R. E.. (1992);  The acid growth theory of auxin-induced cell elongation is alive and well.  Plant Physiol.. 99 1271-1274
• 118 Robbertse,  P. J.,, Lock,  J. J.,, Stoffberg,  E.,, and Coetzer,  L. A.. (1990);  Effect of boron on directionality of pollen tube growth in Petunia and Agapanthus. .  S. Afr. J. Bot.. 56 487-492
• 119 Robertson,  G. A., and Loughman,  B. C.. (1974);  Reversible effects of boron on the absorption and incorporation of phosphate in Vicia faba. .  New Phytol.. 73 291-298
• 120 Rowe,  R. I.,, Bouzan,  C.,, Nabili,  S.,, and Eckhert,  C. D.. (1998);  The response of trout and zebrafish embryos to low and high boron concentrations in U-shaped.  Biol. Trace Elem. Res.. 66 261-270
• 121 Rowe,  R. I.,, and Eckhert,  C. D.. (1999);  Boron is required for zebrafish embryogenesis.  J. Exp. Bot.. 202 1649-1654
• 122 Ruiz,  J. M.,, Baghour,  M.,, Bretones,  G.,, Belakbir,  A.,, and Romero,  L.. (1998 a);  Nitrogen metabolism in tobacco plants (Nicotiana tabacum L.): role of boron as a possible regulatory factor.  Int. J. Plant Sci.. 159 121-126
• 123 Ruiz,  J. M.,, Bretones,  G.,, Baghour,  M.,, Belakbir,  A.,, and Romero,  L.. (1998 b);  Relationship between boron and phenolic metabolism in tobacco leaves.  Phytochemistry. 48 269-272
• 124 Ruiz,  J. M.,, Garcia,  P. C.,, Rivero,  R. M.,, and Romero,  L.. (1999);  Response of phenolic metabolism to the application of carbendazim plus boron in tobacco.  Physiol. Plant.. 106 151-157
• 125 Schmucker,  T.. (1932);  Bor als physiologisch entscheidendes Element.  Naturwissenschaften. 20 839
• 126 Schmucker,  T.. (1933);  Zur Blutenbiologie tropischer Nymphaea-Arten. II. (Bor als entscheidender Faktor).  Planta. 18 641-650
• 127 Schmucker,  T.. (1934);  Über den Einfluß von Borsäure auf Pflanzen, insbesondere keimende Pollenkörner.  Planta. 23 264-283
• 128 Schon,  M. K.,, Novacky,  A.,, and Blevins,  D. G.. (1990);  Boron induces hyperpolarization of sunflower root cell membranes and increases membrane permeability to K⁺.  Plant Physiol.. 93 566-571
• 129 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 phospatidylcholine bilayers.  Proc. Natl. Acad. Sci. USA. 88 6926-6930
• 130 Shen,  Z. G.,, Liang,  Y. C.,, and Shen,  K.. (1993);  Effect of boron on the nitrate reductase-activity in oilseed rape plants.  J. Plant Nutr.. 16 1229-1239
• 131 Shorrocks,  V. M.. (1997);  The occurrence and correction of boron deficiency.  Plant and Soil. 193 121-148
• 132 Shrestha,  G. K.,, Thompson,  M. M.,, and Righetti,  T. L.. (1987);  Foliar-applied boron increases fruit set in “barcelona” hazelnut.  J. Amer. Soc. Hort. Sci.. 112 412-416
• 133 Simons,  K., and Ikonen,  E.. (1997);  Functional rafts in cell membranes.  Nature. 387 569-572
• 134 Singh,  Z., and Dhillan,  B. S.. (1989);  Effect of foliar application of boron on vegetative and panicle growth, sex expression, fruit retention and physiochemical characteristics of mango (Mangifera indica cv Dusheri).  Trop. Agric.. 64 305-308
• 135 Slack,  C. R., and Wittington,  W. J.. (1964);  The role of boron in plant growth. III. The effects of differentiation and deficiency on radicle metabolism.  J. Exp. Bot.. 15 495-514
• 136 Smith,  K. W., and Johnson,  S. L.. (1976);  Borate inhibition of yeast alcohol dehydrogenase.  Biochem.. 15 560-564
• 137 Smith,  T. E.,, Stephenson,  R. A.,, Asher,  C. J.,, and Hetherington,  S. E.. (1997) Boron deficiency of avocado. 1. Effects on pollen viability and fruit set. Boron in soils and plants. Bell, R. W. and Rerkasem, B., eds. Dordrecht, The Netherlands; Kluwer Academic Publishers pp. 131-133
• 138 Smyth,  D. A., and Dugger,  W. M.. (1981);  Cellular changes during boron-deficient culture of the diatom Cylindrotheca fusiformis. .  Physiol. Plant.. 51 111-117
• 139 Spurr,  A. R.. (1957);  The effect of boron on cell wall structure in celery.  Amer. J. Bot.. 44 637-650
• 140 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
• 141 Stanley,  R. G., and Linskens,  H. F.. (1974) Boron in pollen and floral organs. Pollen: Biochemistry and management. Stanley, R. G. and Linskens, H. G., eds. Berlin; Springer
• 142 Steer,  M. W., and Steer,  J. M.. (1989);  Tansley review No. 16. Pollen tube growth.  New Phytol.. 111 323-358
• 143 Tate,  S. S., and Meister,  A.. (1978);  Serine-borate complex as a transition-state inhibitor of gamma-glutamyl transpeptidase.  Proc. Natl. Acad. Sci. USA. 75 4806-4809
• 144 Teasdale,  R. D., and Richards,  D. K.. (1990);  Boron deficiency in cultured pine cells.  Plant Physiol.. 93 1071-1077
• 145 Thompson,  A. H., and Batjer,  L. P.. (1950);  The effect of boron in the germination medium on pollen germination and pollen tube growth for several deciduous tree fruits.  Proc. Amer. Soc. Hort. Sci.. 55 227-229
• 146 Torssell,  K.. (1956);  Chemistry of arylboric acids. VI. Effects of arylboric acids on wheat roots and the role of boron in plants.  Physiol. Plant.. 9 652-664
• 147 van Duin,  M.,, Peters,  J. A.,, Kieboom,  A. P. G.,, and VanBekkum,  H.. (1987);  Synergic coordination of calcium in borate-polyhydroxycarboxylate systems.  Carbohydr. Res.. 162 65-78
• 148 Vasil,  I. K.. (1963) Effect of boron on pollen tube germination and pollen tube growth. Pollen Physiology and Fertilisation. Linskens, H. F., ed. Amsterdam, North Holland; Publishing Company pp. 107-119
• 149 Vaughan,  A. K. F.. (1977);  The relation between the concentration of boron in the reproductive and vegetative organs of maize plant and their development.  Rhod. J. Agric. Res.. 15 163-170
• 150 Veltrup,  W.. (1978);  Characteristics of zinc uptake by barley roots.  Physiol. Plant.. 42 243-250
• 151 Vorob'ev,  L. N., and Pelkhanov,  S. E.. (1975);  Possible effect of boron on the potassium-sodium permeability of membranes of the plant cells Nitella syncarpa. .  Chem. Abstr.. 83 97
• 152 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
• 153 Warington,  K.. (1923);  The effect of boric acid and borax on the broad bean and certain other plants.  Ann. Bot.. 37 629-672
• 154 Weig,  A.,, Deswarte,  C.,, and Chrispeels,  M. J.. (1997);  The major intrinstic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group.  Plant Physiol.. 114 1347-1357
• 155 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
• 156 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
• 157 Wimmer,  M. A., and Goldbach,  H. E.. (1999);  Influence of Ca²⁺ and pH on the stability of different boron fractions in intact roots of Vicia faba L.  Plant Biol.. 1 632-637
• 158 Woods,  W. G.. (1996);  Review of possible boron speciation relating to its essentiality.  J. Trace Elem. Exp. Med.. 9 153-163
• 159 Yamagishi,  M., and Yamamoto,  Y.. (1994);  Effects of boron on nodule development and symbiotic nitrogen fixation in soybean plants.  Soil Sci. Plant Nutr.. 40 265-274
• 160 Yamauchi,  T.,, Hara,  T.,, and Sonoda,  Y.. (1986);  Distribution of calcium and boron in the pectin fraction of tomato leaf cell wall.  Plant Cell Physiol.. 27 729-732

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