Advertisement

Plant and Soil

, Volume 193, Issue 1–2, pp 71–83 | Cite as

Boron deficiency-induced impairments of cellular functions in plants

  • Ismail Cakmak
  • Volker Römheld
Article

Abstract

The essentiality of B for growth and development of plants is well-known, but the primary functions of B still remain unknown. Evidence in the literature supports the idea that the major functions of B in growth and development of plants are based on its ability to form complexes with the compounds having cis-diol configurations. In this regard, the formation of B complexes with the constituents of cell walls and plasma membranes as well as with the phenolic compounds seems to be a decisive step affecting the physiological functions of B. Boron seems to be of crucial importance for the maintenance of structural integrity of plasma membranes. This function of B is mainly related to stabilisation of cell membranes by B association with membrane constituents. Possibly, B may also protect plasma membranes against peroxidative damage by toxic O2 species. In B-deficient plants, plasma membranes are highly leaky and lose their functional integrity. Under B-deficient conditions, substantial changes in ion fluxes and proton pumping activity of the plasma membranes were noted. Impairments in phenol metabolism and increases in levels of phenolics and polyphenoloxidase activity are typical indications of B deficiency, particularly in B deficiency-sensitive plant species, such as Helianthus annuus (sunflower). Enhanced oxidation of phenols is responsible for generation of reactive quinones which subsequently produce extremely toxic O2 species, thus resulting in the increased risk of a peroxidative damage to vital cell components such as membrane lipids and proteins. In B-deficient tissues, enhancement in levels of toxic O2 species may also occur as a result of impairments in photosynthesis and antioxidative defence systems. Recent evidence shows that the levels of ascorbic acid, non-protein SH-compounds (mainly glutathione) and glutathione reductase, the major defence systems of cells against toxic O2 species, are reduced in response to B deficiency. There is also increasing evidence that, in the heterocyst cells of cyanobacteria, B is involved in protection of nitrogenase activity against O2 damage.

Keywords

Boron Quinone Glutathione Reductase Helianthus Annuus Typical Indication 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Appel H M 1993 Phenolics in ecological interaction: the importance of oxidation. J. Chem. Ecol. 19, 1521-1552.Google Scholar
  2. Bagchi N, Ernst A and Böger P 1991 The effect of activated oxygen species on nitrogenase of Anabaena variabilis. Z. Naturforsch. 66, 407-415.Google Scholar
  3. Bakker J, Gommers F J, Smits L, Fuchs A and De Vries F W 1983 Photoactivation of isoflavonoid phytoalexins: Involvement of free radicals. Photochem. Photobiol. 38, 323-329.Google Scholar
  4. Barr R, Böttger M and Crane F L 1993 The effect of B on plasma membrane electron transport and associated proton secretion by cultured carrot cells. Biochem. Mol. Biol. Int. 31, 31-39.Google Scholar
  5. Bironaite A D, Cenas N K and Kulys J J 1989 The inhibition of glutathione reductase by quinones. Eur. J. Biochem. 178, 693-703.Google Scholar
  6. Blaser-Grill J, Knoppik D, Amberger A and Goldbach H 1989 Influence of boron on the membrane potential in Elodea densa andHelianthus annuus roots and H+ extrusion of suspension cultured Daucus carota cells. Plant Physiol. 90, 280-284.Google Scholar
  7. Bolaños L, Estaben E, De Lorenzo C, Fernandez-Pascual M, De Felipe 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.Google Scholar
  8. Bolaños L, Brewin N J and Bonilla I 1996 Effect of boron on rhizobium-legume cell-surface interactions and nodule development. Plant Physiol. 110, 1249-1256.Google Scholar
  9. Bolwell G P and Butt V S 1983 Photoinduced changes in o-dyphenol oxidase and p-coumarate hydroxylase activities in spinach beet seedlings and leaves. Phytochem. 22, 37-45.Google Scholar
  10. Bonilla I, Garcia-Gonzàlez M and Mateo P 1990 Boron requirement in cyanobacteria. Its possible role in the early evolution of photosynthetic organisms. Plant Physiol. 94, 1554-1560.Google Scholar
  11. Cakmak I 1994 Activity of ascorbate-dependent H2O2-scavenging enzymes and leaf chlorosis are enhanced in magnesium-and potassium-deficient leaves, but not in phosphorus-deficient leaves. J. Exp. Bot. 45, 1259-1266.Google Scholar
  12. 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.Google Scholar
  13. Chattopadhyay S, Datta S K and Mahato S B 1994 Production of L-DOPA from cell suspension culture of Mucuna pruriens f. pruriens. Plant Cell Rep. 13, 519-522.Google Scholar
  14. Cilliers J J L and Singleton V L 1990 Caffeic acid autoxidation and the effect of thiols 38, 1789-1796.Google Scholar
  15. Coke L and Whittington W J 1968 The role of boron in plant growth, IV. Interrelationships between boron and indol-3-yl acetic acid in the metabolism of bean radicles. J. Exp. Bot. 19, 295-308.Google Scholar
  16. Cordoba-Pedregosa M D C, Gonzalez-Reyes J A, Canadillas M D S, Navas P and Cardoba F 1996 Role of apoplastic and cell wall peroxidases on the stimulation of root elongation by ascorbate. Plant Physiol. 112, 1119-1125.Google Scholar
  17. CoSeteng M Y and Lee C Y 1987 Changes in apple polyphenoloxidase and polyphenol concentrations in relation to degree of browning. J. Food Sci. 52, 985-989.Google Scholar
  18. Dalton D A, Russell S A, Hanus F J, Pascoe G A and Evans H J 1986 Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc. Natl. Acad. Sci. USA 83, 3811-3815.Google Scholar
  19. Desiraju S, Rashmi A and Rathore V S 1993 Influence of boron deficiency on growth, protein and lipid contents in tomato and okra seedlings. Acta Physiol. Plant. 15, 25-30.Google Scholar
  20. Dugger W M 1983 Boron in plant metabolism In Encyclopedia of Plant Physiology, new series, Vol. 15. Eds. A Lauchli and R L Bieleski. pp 626-650 Springer-Verlag, Berlin.Google Scholar
  21. Fackler U, Goldbach H, Weiler E W and Amberger A 1985 Influence of boron deficiency on indol-3yl-acetic acid and abscissic acid levels in root and shoot tips. J. Plant Physiol. 119, 295-299.Google Scholar
  22. Ferrol N and Donaire J P 1992 Effect of boron on plasma membrane proton extrusion and redox activity in sunflower cells. Plant Sci. 86, 41-47.Google Scholar
  23. Ferrol N, Belver A, Roldan M, Rodriguez-Rosales MP and Donaire J R 1993 Effects of boron on proton transport and membrane properties of sunflower (Helianthus annuus L.) cell microsomes. Plant Physiol. 103, 763-769.Google Scholar
  24. Findeklee P and Goldbach H E 1996 Rapid effects of boron defi-ciency on cell wall elasticity modulus in Cucurbita pepo roots. Bot. Acta 109, 463-465.Google Scholar
  25. Foyer C H, Lelandais M and Kunert K J 1994 Photooxidative stress in plants. Physiol. Plant. 92, 696-717.Google Scholar
  26. Garcia-Gonzáles M, Mateo P and Bonilla I 1988 Boron protection for O2 diffusion in heterocysts of Anabaena sp. PCC 7119. Plant Physiol. 87, 785-789.Google Scholar
  27. Garcia-Gonzáles M, Mateo P and Bonilla I 1990 Effect of boron deficiency on photosynthesis and reductant sources and their relationship with nitrogenase activity in Anabaena PCC 7119. Plant Physiol. 93, 560-565.Google Scholar
  28. Garcia-Gonzáles 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.Google Scholar
  29. Glass A D M 1973 Influence of phenolic acids on ion uptake. I. Inhibition of phosphorus uptake. Plant Physiol. 51, 1037-1041.Google Scholar
  30. Glass A D M 1974 Influence of phenolic acids upon ion uptake. III. Inhibition of potassium absorption. J. Exp. Bot. 25, 1104-1113.Google Scholar
  31. Glass A D M and Dunlop J 1974 Influence of phenolic acids on ion uptake. IV Depolarisation of membrane potentials. Plant Physiol. 54, 855-858.Google Scholar
  32. Golan-Goldhirsh A and Whitaker J R 1984 Effect of ascorbic acid, sodium bisulphite, and thiol compounds on mushroom polyphenol oxidase. J. Agric. Food Chem. 32, 1003-1009.Google Scholar
  33. Goldbach H E, Hartmann D and Rötzer T 1990 Boron is required for the ferricyanide-induced proton release by auxins in suspensioncultured cells of Daucus carota and Lycopersicon esculentum. Physiol. Plant. 80, 114-118.Google Scholar
  34. Goldbach H E, Blaser-Grill J, Lindemann N, Porzelt M, Hörmann C, Lupp B and Gessner B 1991 Influence of boron on net proton release and its relation to other metabolic process. Curr. Topics Plant Biochem. Physiol. 10, 195-220.Google Scholar
  35. Gomes-Rodriguez M V, Luna del Castillo de D and Alvarez-Tinaut M C 1987 The evolution of glucose-6P-dehydrogenase and 6P-gluconate-dehydrogenase activities and the ortho-diphenolic content of sunflower leaves cultivated under different boron treatments. J. Plant Nutr. 10, 2211-2229.Google Scholar
  36. Grill D, Esterbauer H and Klösch U 1979 Effect of sulphur dioxide on glutathione in leaves of plants. Environ. Pollut. 19, 187-194.Google Scholar
  37. Heipieper H J, Keweloh H and Rehm H J 1991 Influence of phenols on growth and membrane permeability of free and immobilised Escherichia coli. Appl. Environ. Microbiol. 57, 1213-1217.Google Scholar
  38. 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.Google Scholar
  39. Hirsch A M, Pengelly W L and Torrey J G 1982 Endogenous IAA levels in boron-deficient and control root tips of sunflower. Bot. Gaz. 143, 15-19.Google Scholar
  40. Hu H and Brown P H 1994 Localisation of boron in the cell wall and its association with pectin. Evidence of a structural role of boron in the cell wall. Plant Physiol. 105, 681-689.Google Scholar
  41. Hu H, Brown P B and Labavitch J M 1996 Species variability in boron requirement is correlated with cell wall pectin. J. Exp. Bot. 47, 227-232.Google Scholar
  42. Jiang Y and Miles P W 1993 Generation of H2O2 during enzymic oxidation of catechin. Phytochem. 33, 29-34.Google Scholar
  43. Kappus H 1986 Overview of enzyme systems involved in bioreduction of drugs and in redox cycling 35, 1-6.Google Scholar
  44. Kastori R, Plesnicar M, Pankovic D and Sakac Z 1995 Photosynthesis, chlorophyll fluorescence and soluble carbohydrates in sun-flower leaves as affected by boron deficiency. J. Plant Nutr. 18, 1751-1763.Google Scholar
  45. Larson R A 1986 Insect defences against phototoxic plant chemicals. J. Chem. Ecol. 12, 859-780.Google Scholar
  46. Lee S and Aronoff S 1967 Boron in plants: a biochemical role. Science 158, 798-799.Google Scholar
  47. Lewis D H 1980 Boron, lignification and the origin of vascular plants a unified hypothesis. New Phytol. 84, 209-229.Google Scholar
  48. Liso R, Calabrese G, Bitonti M B and Arrigoni O 1984 Relationship between ascorbic acid and cell division. Exp. Cell Res. 150, 314- 320.Google Scholar
  49. Loomis W D and Durst R W 1991 Boron and cell walls. Curr. Topics Plant Biochem. Physiol. 10, 149-178.Google Scholar
  50. Loomis W D and Durst R W 1992 Chemistry and biology of boron. BioFactors 4, 229-239.Google Scholar
  51. Lukaszewski K M and Blevins D G 1996 Root growth inhibition in boron-deficient or aluminium-stressed squash may be a result of impaired ascorbate metabolism. Plant Physiol. 112, 1135-1140.Google Scholar
  52. Maas F M, DeKok L J, Peters J L and Kuiper P J C 1987 A comparative study on the effects ofH2S andSO2 fumigation on the growth and accumulation of sulphate and sulphydryl compounds in Trifolium pratense L., Glycine max Merr. and Phaseolus vulgaris L. J. Exp. Bot. 38, 1459-1469.Google Scholar
  53. Macheix J-J, Sapis J-C and Fleuriet A 1991 Phenolic compounds and polyphenoloxidase in relation to browning in grapes and wines. Crit. Rev. Food Sci. Nutr. 30, 441-486.Google Scholar
  54. Marschner H 1995 Mineral Nutrition of Higher Plants. pp 379-396. Academic Press, San Diego, USA.Google Scholar
  55. Mason T L and Wasserman B P 1987 Inactivation of red beet ßglucan synthetase by native and oxidised phenolic compounds. Phytochem. 26, 2197-2202.Google Scholar
  56. Mateo P, Bonilla I, Fernandez-Valiente E and Sanchez-Maeso E 1986 Essentiality of boron for dinitrogen fixation in Anabaena sp. PCC 7119. Plant Physiol. 81, 430-433.Google Scholar
  57. Matoh T 1997 Boron in plant cell walls. In Boron in Soils and Plants. Ed. B Dell. pp. 000–000. Kluwer Academic Publishers, Dordrecht, the Netherlands.Google Scholar
  58. 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 localisation of boron and selection of cells that tolerate low levels of boron. Plant Cell Physiol. 33, 1135-1141.Google Scholar
  59. Mole S, Ross J A M and Waterman P G 1988 Light-induced variation in phenolic levels in foliage of rain-forest plants. I. Chemical Changes. J. Chem. Ecol. 14, 1-21.Google Scholar
  60. Monday N I and Munshi C B 1993 Effect of boron on enzymatic discolouration and phenolic and ascorbic acid content of potatoes. J. Agric. Food Chem. 41, 554-556.Google Scholar
  61. Noppakoonwong R N, Bell R L, Dell B and Loneragan J F 1993 An effect of shade on the boron requirement for leaf blade elongation in black gram (Vigna mungo L. Hepper). Plant and Soil 155/156, 317-320.Google Scholar
  62. Obermeyer G, Kriechbaumer R, Strasser D, Maschessnig A and Bentrup F-W 1996 Boric acid stimulates the plasma membrane H+-ATPase of ungerminated lily pollen grains. Physiol. Plant. 98, 281-290.Google Scholar
  63. Parr A J and Loughman B C 1983 Boron and membrane function in plants. In Metals and Micronutrients, Uptake and Utilisation by Plants. Eds. D A Robb and W S Pierpoint. pp 87-107. Academic Press, New York.Google Scholar
  64. Perkins H J and Aronoff S 1956 Identification of the blue-fluorescent compounds in boron-deficient plants. Arch. Biochem. Biophys. 64, 506-507.Google Scholar
  65. Pilbeam D J and Kirkby E A 1983 The physiological role of boron in plants. J. Plant Nutr. 6, 563-582.Google Scholar
  66. Pillinger J M, Cooper J A and Ridge I 1994 Role of phenolic compounds in the antialgal activity of barley straw. J. Chem. Ecol. 20, 1557-1569.Google Scholar
  67. 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.Google Scholar
  68. Poole R J 1978 Energy coupling for membrane transport. Ann. Rev. Plant Physiol. 29, 437-460.Google Scholar
  69. Rajarathnam J A and Lowry J B 1974 The role of boron in the oil-palm (Elaeis guinensis). Ann. Bot. 38, 193-200.Google Scholar
  70. Robertson G A and Loughman B C 1973 Rubidium uptake and boron deficiency in Vicia faba. J. Exp. Bot. 24, 1046-1052.Google Scholar
  71. 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.Google Scholar
  72. Robinson J M 1988 Does O2 photoreduction occur within chloroplasts in vivo? Physiol. Plant. 72, 666-680.Google Scholar
  73. Roldan M, Belver A, Rodriguez-Rosales P, Ferrol N and Donaire J D 1992 In vivo and in vitro effects of boron on the plasma membrane proton pump of sunflower roots. Physiol. Plant. 84, 49-54.Google Scholar
  74. Römheld V and Marschner H 1991 Functions of micronutrients in plants. In Micronutrients in Agriculture, 2nd ed. Eds. J J Mordvedt, F R Cox, L M Shuman and R M Welch pp 297-328. SSSA Book Series, No. 4, Madison, WI, USA.Google Scholar
  75. Roth-Bejerano N and Itai C 1981 Effect of boron on stomatal opening in epidermis strips of Commelina communis. Physiol. Plant. 52, 302-304.Google Scholar
  76. Schon M K, Novacky A and Blevins D G 1990 Boron induces hyperpolarisation of sunflower root cell membranes and increases membrane permeability to K+. Plant Physiol. 93, 566-577.Google Scholar
  77. Shelp B J 1993 Physiology and biochemistry of boron in plants. In Boron and Its Role in Crop Protection. Ed. U C Gupta. pp 53-85. CRC Press, Boca Raton, FL, USA.Google Scholar
  78. Shkol'nik M Y 1984 Trace Elements in Plants. pp. 68-109. Developments in Crop Science (6), Elsevier, New York.Google Scholar
  79. Shkol'nik M Y, Krupnikova T A and Smirnov Y S 1981a Activity of polyphenol oxidase and sensitivity to boron deficiency in monocots and dicots. Fiziol. Rast. 28, 391-397.Google Scholar
  80. Shkol'nik M Y, Krupnikavo T A, Timofeeva S S and Stom D I 1981b Intensification of quinone formation fromexogenous polyphenols by homogenates of the leaves of sunflower plants reared under conditions of boron deficiency. Fiziol. Rast. 28, 541-546.Google Scholar
  81. Serrano R 1989 Structure and function of plasmamembrane ATPase. Ann. Rev. Plant Physiol. 40, 61-94.Google Scholar
  82. Skok J 1957 The substitution of complexing substances for boron in plant growth. Plant Physiol. 32, 308-312.Google Scholar
  83. Smirnov Y S, Krupnikova T A and Shkol'nik M Y 1977 Content of IAA in plants with different sensitivity to boron deficits. Sov. Plant Physiol. 24, 270-276.Google Scholar
  84. Tan K-S and Kubo I 1990 Release of oxidases from the roots of plants. Experientia 46, 478-481.Google Scholar
  85. Tanada T 1983 Localisation of boron in membranes. J. Plant Nutr. 6, 743-749.Google Scholar
  86. Tanada T 1995 Boron as a transducer in some physiological process of plants. J. Plant Nutr. 18, 1743-1750.Google Scholar
  87. Tanaka H 1966 Response of Lemna paucicostata to boron as affected by light intensity. Plant and Soil 25, 425-434.Google Scholar
  88. Tang P M and Dela Fuente R K 1986 The transport of indole-3-acetic acid in boron-and calcium-deficient sunflower hypocotyl segments. Plant Physiol. 81, 646-650.Google Scholar
  89. 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.Google Scholar
  90. Vaughan D and Ord B G 1990 Influence of phenolic acids on morphological changes in roots of Pisum sativum. J. Sci. Food Agric. 52, 289-299.Google Scholar
  91. Vaughan D, Cheshire M V and Ord B G 1994 Exudation of peroxidase from roots of Festuca rubra and its effects on exuded phenolic acids. Plant and Soil 160, 153-155.Google Scholar
  92. Warington K 1923 The effect of boric acid and borax on the broad bean and certain other plants. Ann. Bot. 37, 629-672.Google Scholar
  93. Watanabe R, Skok C J and Wender S H 1964 Effect of boron deficiency on polyphenol production in the sunflower. Phytochemistry 3, 391-393.Google Scholar
  94. Zawistowski J, Biliaderis C G and Eskin N A M 1991 Polyphenol Oxidase. In Oxidative Enzymes in Foods. Eds. D S Robinson and A M Eskin. pp 217-273. Elsevier Science Publishers, England.Google Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Ismail Cakmak
  • Volker Römheld

There are no affiliations available

Personalised recommendations