Plant and Soil

, Volume 193, Issue 1–2, pp 103–120 | Cite as

Physiological response of plants to low boron

  • Bernie Dell
  • Longbin Huang
Article

Abstract

This review focuses on physiological responses in higher plants to B deficiency at the whole plant and organ level. Plants respond to decreasing B supply in soil solutions by slowing down or ceasing growth. Boron deficiency inhibits root elongation through limiting cell enlargement and cell division in the growing zone of root tips. In the case of severe B deficiency, the root cap, quiescent centre and protoderm of root tips disappear and root growth ceases, leading to the death of root tips. Although vascular bundles are weakly developed in B-deficient roots, early effects of B deficiency on their initiation and differentiation is poorly understood. Inhibited leaf expansion by low B indirectly decreases the photosynthetic capacity of plants, though exact roles of B in photosynthesis remain to be explored. The early inhibition of root growth, compared to shoot growth, increases the shoot:root ratio. It is hypothesised that this may enhance the susceptibility of plants to environmental stresses such as marginally deficient supplies of other nutrients and water deficit in soil.

In the field, sexual reproduction is often more sensitive to low soil B than vegetative growth, and marked seed yield reductions can occur without symptoms being expressed during prior vegetative growth. In flowers, low B reduces male fertility primarily by impairing microsporogenesis and pollen tube growth. Post-fertilisation effects include impaired embryogenesis, resulting in seed abortion or the formation of incomplete or damaged embryos, and malformed fruit. However, there is a great diversity of effects of low B on reproductive growth among species, and within the same species between sites and seasons. Much of this diversity is not explained by the current literature. Key processes in reproductive development which may be impaired under B deficiency are proposed and discussed. These include the formation of a diverse array of cell wall types, the supply of carbohydrates for growth and storage reserves, and the production of flavonols. Inflorescence architecture, floral morphology, canopy structure and prevailing weather conditions are suggested as being important for xylem B delivery into flowers because of their impact on transpiration. The extent of phloem translocation of B into reproductive organs has yet to be fully assessed. The timing of B sensitive stages in reproduction of most crop plants need defining in order to facilitate appropriate timing of corrective B treatments.

As most container studies have imposed B deficiency by withholding B, much of the data on severely B-deficient plants requires re-evaluation. Further studies are warranted to understand the effects of realistically low levels of B in solution on the growth of meristematic tissues and floral organs. A B-buffered solution culture system is recommended for some of this work.

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References

  1. Agrawala S C, Sharma P N, Chatterjee C and Sharma C P 1981 Development and enzymatic changes during pollen development in boron deficient maize plants. J. Plant Nutr. 3, 329-336.Google Scholar
  2. Anderson M A, Harris P J, Bonig I and Clarke AE 1987 Immunogold localization of α-L-arabinofuranosyl residue in pollen tubes of Nicotiana alata Link et Otto. Planta 171, 438-442.Google Scholar
  3. Astwood J D and Hill R D 1995 Barley spikelet culture: An effective tool for the analysis of biochemical events in flower development. Plant Cell, Tissue and Organ Culture 40, 93-96.Google Scholar
  4. Becker W M and Deamer D W 1991 The World of the Cell, 2nd ed. The Benjamin/Cummings Publ. Company Inc., Sydney.Google Scholar
  5. Bedinger P 1992 The remarkable biology of pollen. Plant Cell 4, 879-887.Google Scholar
  6. Bell RW, McLay L, Plaskett D, Dell B and Loneragan J F 1990 Internal boron requirements of green gram (Vigna radiata). In Plant Nutrition - Physiology and Application. Ed. M L van Beusichem. pp 275-280. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  7. Bell, RW, McLay L, Plaskett D, Dell B and Loneragan J F 1989 Germination and vigour of black gram (Vigna mungo (L.) Hepper) seed from plants grown with and without boron. Aust. J. Agric. Res. 40, 273-279.Google Scholar
  8. Bergmann W 1992 Nutritional Disorders of Plants - Development, Visual and Analytical Diagnosis. Gustav Fischer Verlag, Jena, Stuttgart.Google Scholar
  9. Birnbaum EH, Beasley C A and Dugger WM 1974 Boron deficiency in underfertilised cotton (Gossypium hirsutum) ovules grown in vitro. Plant Physiol. 54, 931-935.Google Scholar
  10. Bohnsack C W and Albert L S 1977 Early effects of boron deficiency on indoleacetic acid oxidase levels of squash root tips. Plant Physiol. 59, 1047-1050.Google Scholar
  11. Brett C T and Waldron K W 1996 Physiology and Biochemistry of Plant Cell Walls, 2nd ed. Chapman and Hall, London.Google Scholar
  12. Brown P H and Hu H 1996 Phloem mobility of boron is species dependent: Evidence for phloem mobility in sorbitol-rich species. Ann. Bot. 77, 497-505.Google Scholar
  13. Cai G, Moscatelli A and Cresti M 1997 Cytoskeletal organization and pollen tube growth. Trends in Plant Sci. 2, 86-91.Google Scholar
  14. 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
  15. Campbell L C, Miller M H and Loneragan J F 1975 Translocation of boron to plant fruits. Aust. J. Plant Physiol. 2, 481-487.Google Scholar
  16. Chang M T and Neuffer M G 1989 Maize microsporogenesis. Genome 32, 232-244.Google Scholar
  17. Cheung A Y 1996 Pollen-pistil interactions during pollen-tube growth. Trends in Plant Sci. 1, 45-51.Google Scholar
  18. Cheng C and Rerkasem B 1993 Effects of Boron on pollen viability in wheat. Plant and Soil 155/156, 313-315.Google Scholar
  19. Clément C and Audran J-C 1995 Anther wall layers control pollen sugar nutrition in Lilium. Protoplasma 187, 172-181.Google Scholar
  20. Clément C, Chavant L, Burrus M and Audran J-C 1994. Anther starch variations in Lilium during pollen development. Sex Plant Reprod. 7, 347-356.Google Scholar
  21. Clément C, Burrus M and Audran J-C 1996 Floral organ growth and carbohydrate content during pollen development in Lilium. Amer. J. Bot. 83, 459-469.Google Scholar
  22. Coetzer L A and Robbertse P J 1987 Pollen biology of Persea americana Fuerte. S. Afr. Avocado Grow. Assoc. Yearbook 10, 43-45.Google Scholar
  23. Cohen MS and Lepper R Jr 1977 Effects of boron on cell elongation and division in squash roots. Plant Physiol. 59, 884-887.Google Scholar
  24. Cohen M S and Albert L S 1974 Autoradiographic examination of meristems of intact boron-deficient squash roots treated with tritiated thymidine. Plant Physiol. 54, 766-768.Google Scholar
  25. Cresti M and Tiezzi A 1990 Germination and pollen tube formation. In Microspores: Evolution and Ontogeny. Eds. S Blackmore and R B Knox. pp 239-263. Academic Press, London.Google Scholar
  26. Darvill A, McNeil M, Albersheim P and Delmer D P 1980. The primary cell wall of flowering plants. In The biochemistry of plants. A comprehensive treatise. Ed. N E Tolbert. pp 91-161. Academic Press, New York.Google Scholar
  27. de Wet E, Robbertse P J and Groeneveld H T 1989 The influence of temperature and boron on pollen germination in Mangifera indica L. S Afr. J. Plant Soil 6, 228-234.Google Scholar
  28. Dear B S and Lipsett J 1987 The effect of boron supply on the growth and seed production of subterranean clover (Trifolium subterraneum L.). Aust. J. Agric. Res. 38, 537-546.Google Scholar
  29. Dell B 1981 Male sterility and anther wall structure in copper defi-cient plants. Ann. Bot. 48, 599-608.Google Scholar
  30. Dell B and Malajczuk N 1994 Boron deficiency in eucalypt plantations in China. Can. J. For. Res. 24, 2409-2416.Google Scholar
  31. Delvallée I and Dumas C 1988. Anther development in Zea mays: changes in proteins, peroxidase, and esterase patterns. J. Plant Physiol. 132, 210-217.Google Scholar
  32. Derksen J 1996 Pollen tubes - a model system for plant cell growth. Bot. Acta 109, 341-345.Google Scholar
  33. Dhakre G, Singh, J and Chauhan S V S 1994 Analysis of phenolics and boron in the stigma of seedless Campsis grandiflora K. Schum. Indian J. Exp. Biol. 32, 816-818.Google Scholar
  34. Dugger W M 1983 Boron in plant metabolism. In Encyclopedia of Plant Physiology, New Series, vol. 15B. Eds. A Läuchli and R L Bieleski. pp 626-650. Springer-Verlag, Berlin.Google Scholar
  35. Dugger W M and Palmer R L 1980 Effect of boron on the incorporation of glucose into cotton fibers grown in vitro. Plant Physiol. 65, 266-273.Google Scholar
  36. Esau K 1977 Anatomy of Seed Plants, 2nd. ed. John Wiley & Sons, New York.Google Scholar
  37. Galrao E Z and Sousa D M G 1988 Effect of boron on male sterility of wheat in an organic paddy soil. Revista Brasileira de Ciencia do Solo 12, 147-152.Google Scholar
  38. Ganguly B 1979 Note on seedlessness in some wheat varieties caused by boron deficiency. Indian J. Agric. Sci. 49, 384-386.Google Scholar
  39. Garcia-González 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
  40. Garg O K, Sharma A N and Kona G R S S 1979 Effect of boron on the pollen vitality and yield of rice plants (Oryza sativa L. var. Jaya). Plant and Soil 52, 591-594.Google Scholar
  41. Geitmann A, Hudák J, Vennigerholz F and Walles B 1995 Immunogold localization of pectin and callose in pollen grains and pollen tubes of Brugmansia suaveolens - Implications for the self-incompatability reaction. J. Plant Physiol. 147, 225-235.Google Scholar
  42. Goldberg RB, Beals T P and Sanders PM 1993 Anther development: basic principles and practical applications. Plant Cell 5, 1217- 1229.Google Scholar
  43. Graham R D 1975 Male sterility in wheat plants deficient in copper. Nature, Lond. 254, 514-515.Google Scholar
  44. Gupta U C (Ed.) 1993 Boron and its Role in Crop Production. CRC Press, Boca Raton, FL, USA.Google Scholar
  45. Harkness R W 1959 Boron deficiency and alternate bearing in avocados. Proc. Florida State Hort. Soc. 72, 311-317.Google Scholar
  46. Harris H C and Brolman J B 1966a Comparison of calcium and boron deficiencies of the peanut. I. Physiological and yield differences. Agron. J. 58, 575-578.Google Scholar
  47. Harris H C and Brolman J B 1966b Comparison of calcium and boron deficiencies of the peanut. II. Seed quality in relation to histology and viability. Agron. J. 58, 578-582.Google Scholar
  48. Hasegawa Y, Nakamura S, and Nakamura N 1996 Immunocyto-chemical localization of callose in germinated pollen of Camellia japonica. Protoplasma 194, 133-139.Google Scholar
  49. Hirsch A M and Torrey JG 1980 Ultrastructural changes in sunflower root cells in relation to boron deficiency and added auxin. Can. J. Bot. 58, 856-866.Google Scholar
  50. 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
  51. 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.Google Scholar
  52. 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.Google Scholar
  53. Huang L, Ye Z and Bell R 1996a The importance of sampling immature leaves for the diagnosis of boron deficiency in oilseed rape (Brassica napus cv. Eureka). Plant and Soil 183, 187-198.Google Scholar
  54. Huang S R, An Y Q, McDowell, J M, McKinney E C and Meagher R B 1997 The Arabidopsis ACT11 actin gene is strongly expressed in tissues of the emerging inflorescence, pollen, and developing ovules. Plant Mol. Biol. 33, 125-139.Google Scholar
  55. Jackson J F 1991 Borate control of energy-driven protein secretion from pollen and interaction of borate with auxin or herbicide - a possible role for boron in membrane events. Curr. Top. Plant Biochem. Physiol. 10, 221-229.Google Scholar
  56. Jauh G Y and Lord E M 1996 Localization of pectins and arabinogalactan-proteins in lily (Lilium longiflorum L.) pollen tube and style, and their possible roles in pollination. Planta 199, 251-261.Google Scholar
  57. Jewell A W, Murray B G and Alloway B J 1988 Light and electron microscope studies on pollen development in barley (Hordeum vulgare L.) grown under copper-sufficient and deficient conditions. Plant Cell Env. 11, 273-281.Google Scholar
  58. Kamali A R and Childers N F 1970 Growth and fruiting of peach in sand culture as affected by boron and fritted form of trace elements. J. Amer. Soc. Hort. Sci. 95, 652-656.Google Scholar
  59. Kaul M L H 1988 Male Sterility in Higher Plants. Springer-Verlag, Berlin.Google Scholar
  60. Keerati-Kasikorn P, Bell R W and Loneragan J F 1991 Response of two peanut cultivars (Arachis hypogaea) to boron and calcium. Plant and Soil 138, 61-66.Google Scholar
  61. Kehrel B and Wiermann R 1985 Immunochemical localization of phenylalanine ammonia-lyase and chalcone synthase in anthers. Planta 163, 183-190.Google Scholar
  62. Keijzer C J, Leferink-ten Klooster H B and Reinders M C 1996 The mechanics of the grass flower: anther dehiscence and pollen shedding in maize. Ann. Bot. 78, 15-21.Google Scholar
  63. Keijzer C J 1983 Hydration changes during anther development. In Pollen, Biology and Implications for Plant Breeding. Eds. D L Mulcahy and E Ottaviano. pp 197-201. Elsevier Biomedical, New York.Google Scholar
  64. Kirk G J and Loneragan J F 1988 Functional boron requirement for leaf expansion and its use as a critical value for diagnosis of boron deficiency in soybean. Agron. J. 80, 758-762.Google Scholar
  65. Kishitani S, Yomoda A, Konno, N and Tanak Y 1993. Involvement of phenylalanine ammonia-lyase in the development of pollen in broccoli (Brassica oleracea L.). Sex Plant Reprod. 6, 244-248.Google Scholar
  66. Kouchi H and Kumazawa K 1975 Anatomical responses of root tips to boron deficiency II. Effect of boron deficiency on the cellular growth and development in root tips. Soil Sci. Plant Nutr. 21, 137-150.Google Scholar
  67. Leggatt C W 1948 Germination of boron-deficient peas. Sci. Agric. 28, 131-139.Google Scholar
  68. Lewis D H 1980a Boron, lignification and the origin of vascular plants - a unified hypothesis. New Phytol. 84, 209-229.Google Scholar
  69. Lewis D H 1980b Are there inter-relations between the metabolic role of boron, synthesis of phenolic phytoalexins and the germination of pollen? New Phytol. 84, 261-270.Google Scholar
  70. Li B H, Li W H, Kui M C, Chao W S, Jern H P, Li C R, Chu W J and Wang C L 1978 Studies on the cause of sterility of wheat. J. Northeast. Agric. Coll. 3, 1-19 (In Chinese).Google Scholar
  71. Li Y, Faleri C, Geitmann A, Zhang H and Cresti M 1995. Immuno-gold localization of arabinogalactan proteins, unesterified and esterified pectins in pollen grains and pollen tubes of Nicotiana tabacum L. Protoplasma 189, 26-36.Google Scholar
  72. Liu L, Shelp B J and Spiers G A 1993. Boron distribution and retranslocation in field-grown broccoli (Brassica oleracea var. italica). Can. J. Plant Sci. 73, 587-600.Google Scholar
  73. Loomis W D and Durst RW 1992 Chemistry and biology of boron. Biofactors 3, 229-239.Google Scholar
  74. MacInnes C B and Albert L S 1969 Effect of light intensity and plant size on rate of development of early boron deficiency symptoms in tomato root tips. Plant Physiol. 44, 965-967.Google Scholar
  75. Malho R and Trewavas A J 1996 Localized apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell 8, 1935-1949.Google Scholar
  76. Marschner H 1995 Mineral Nutrition of Higher Plants. 2nd ed. Academic Press, London.Google Scholar
  77. Mascarenhas J P 1975 The biochemistry of Angiosperm pollen development. Bot. Rev. 41, 259-314.Google Scholar
  78. Mascarenhas J P 1989 The male gametophyte of flowering plants. Plant Cell 1, 657-664.Google Scholar
  79. Mascarenhas J P 1990 Gene activity during pollen development. Ann. Rev. Plant Physiol. Plant Mol. Biol. 41, 317-338.Google Scholar
  80. Mascarenhas J P 1993 Molecular mechanisms of pollen tube growth and differentiation. Plant Cell 5, 1303-1314.Google Scholar
  81. 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.Google Scholar
  82. McCormick S 1993 Male gametophyte development. Plant Cell 5, 1265-1275.Google Scholar
  83. Meikle P J, Bonig I, Hoogenraad NJ, Clarke AE and Stone BA 1991 The location of (1→3)-β-glucans in the walls of pollen tubes of Nicotiana alata using a (1→3)-β-glucan-specific monoclonal antibody. Planta 185, 1-8.Google Scholar
  84. Moore H M and Hirsch A M 1983 Effects of boron deficiency on mitosis and incorporation of tritiated thymidine into nuclei of sunflower root tips. Amer. J. Bot. 70, 165-172.Google Scholar
  85. Mozafar A 1993 Role of boron in seed production. In Boron and its Role in Crop Production. Ed. UC Gupta, pp 185-206. CRC Press, Boca Raton, FL, USA.Google Scholar
  86. Nakamura N and Yoshida K 1980 A pectic substance extracted from the pollen tube wall of Camellia japonica. Japan J. Palynol. 25, 11-16.Google Scholar
  87. Noppakoonwong R N, Bell RW, Dell B and Loneragan J F 1993 An effect of shade on the boron requirement for leaf blade elongation in black gram (Vigna mungo). Plant and Soil 155/156, 317-320.Google Scholar
  88. Noppakoonwong R N, Rerkasem B, Bell RW, Dell B and Loneragan J F 1997 Prognosis and diagnosis of boron deficiency in black gram (Vigna mungo L. Hepper) in the field by using plant analysis. In Proceeding of Boron in Soils and Plants. Eds. R W Bell and B Rerkasem. pp 00-00. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  89. 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
  90. Owen HA and Makaroff C A 1995 Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185, 7-21.Google Scholar
  91. Pacini E 1996 Types and meaning of pollen carbohydrate reserves. Sex. Plant Reprod. 9, 362-366.Google Scholar
  92. Pollak P E, Hansen K, Astwood J D and Taylor L P 1995 Conditional male fertility in maize. Sex. Plant Reprod. 8, 231-241.Google Scholar
  93. Rae A L, Harris P J, Bacic A and Clarke A E 1985 Composition of the cell walls of Nicotiana alata Link et Otto pollen tubes. Planta 166, 128-133.Google Scholar
  94. Ram S, Bist L D and Sirohi S C 1989 Internal fruit necrosis of mango and its control. Acta Hort. 231, 805-813.Google Scholar
  95. Rawson H M 1996a Parameters likely to be associated with sterility. In Sterility in Wheat in Sub-tropical Asia: Extent, Causes and Solutions. Eds. H M Rawson and K D Subedi. pp 13-31. ACIAR Proc. No. 72.Google Scholar
  96. Rawson H M 1996b The developmental stage during which boron limitation causes sterility in wheat genotypes and the recovery of fertility. Aust. J. Plant Physiol. 23, 709-717.Google Scholar
  97. Rerkasem B 1996 Boron and plant reproductive development. In Sterility inWheat in Sub-tropical Asia: Extent, Causes and Solutions. Eds. H M Rawson and K D Subedi. pp 32-35. ACIAR Proc. No. 72.Google Scholar
  98. Rerkasem B and Loneragan J F 1994 Boron deficiency in two wheat genotypes in a warm, subtropical region. Agron. J. 86, 887-890.Google Scholar
  99. Rerkasem B, Bell RW and Longeragan J F 1990 Effect of seed and soil boron on early seedling growth of black and green gram. In Plant Nutrition - Physiology and Application. Ed. M L Van Beusichem. pp 281–285. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  100. Rerkasem B, Lordkaew S and Dell B 1997a Boron requirement for reproductive development in wheat. Proc. XIII Int. Plant Nutr. Colloq., Tokyo (In press).Google Scholar
  101. Rerkasem B, Bell R W, Lordkaew S and Loneragan J F 1993a Boron deficiency in soybean (Glycine max L. Merr.), peanut (Arachis hypogaea L.), and black gram (Vigna mungo L. Hepper): symptoms in seeds and differences among soybean cultivars in susceptibility to boron deficiency. Plant and Soil 150, 289-294.Google Scholar
  102. Rerkasem B, Bell RW, Lordkaew S, and Loneragan J F 1997b Relationship of seed boron concentration to germination and growth of soybean (Glycine max L. Merr.). Nutr. Cycling in Agroecosystems. (In press).Google Scholar
  103. Rerkasem B, Netsangtip R, Bell R W and Loneragan J F 1988 Comparative species responses to boron on a Typic Tropaqualf in Northern Thailand. Plant and Soil 106, 15-21.Google Scholar
  104. Rerkasem B, Netsangtip R, Lordkaew S and Cheng C 1993b Grain set failure in boron deficient wheat. Plant and Soil 155/156, 309- 312.Google Scholar
  105. Robbertse P J, Lock J J, Stoffberg E and Coetzer L A 1990a Effect of boron on directionality of pollen tube growth in Petunia and Agapanthus. S. Afr. J. Bot. 56, 487-492.Google Scholar
  106. Robbertse P J, Coetzer L A, Bezuidenhou J J, Vorster L and Swart N G N 1990b The influence of boron on fruit set in avocado. Acta Hort. 275, 587-594.Google Scholar
  107. Robertson G A and Loughman B C 1974 Response to boron deficiency: a comparison with responses produced by chemical methods of retarding root elongation. New Phytol. 73, 821-832.Google Scholar
  108. Rodriguez-Rosales M P, Roldan M, Belver A and Donaire J P 1989 Correlation between in vitro germination capacity and proton extrusion in olive pollen. Plant Physiol. Biochem. 27, 723-728.Google Scholar
  109. Schrauwen J A M and Wullems G J 1997 Regulation of flavonol biosynthesis during anther and pistil development, and during pollen tube growth in Solanum tuberosum. Plant J. 11, 105-113.Google Scholar
  110. Schlupmann H, Bacic A and Read SM 1993 A novel callose synthase from pollen tubes of Nicotiana. Planta 191, 470-481.Google Scholar
  111. Sharma P N and Ramchandra T 1990 Water relations and photosynthesis in mustard plants subjected to boron deficiency. Indian J. Plant Physiol. 33, 150-154.Google Scholar
  112. Shelp B J 1993 Physiology and biochemistry of boron in plants. In Boron and Its Role in Crop Production. Ed. UC Gupta. pp 53-85. CRC Press, Boca Raton, FL, USA.Google Scholar
  113. Shelp B J, Marentes E, Kitheka A M and Vivekanandan P 1995 Boron mobility in plants. Physiol. Plant. 94, 356-361.Google Scholar
  114. Shen Z, Zhang X, Wang Z and Shen K 1994 On the relationship between boron nutrition and development of anther (pollen) in rapeseed plant. Scientia Agric. Sinica 27, 51-56.Google Scholar
  115. Sheoran I S and Saini H S 1996 Drought-induced male sterility in rice: changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sex. Plant Reprod. 9, 161-169.Google Scholar
  116. Sherrell C G 1983 Effect of boron application on seed production of New Zealand herbage legumes. New Zealand J. Exp. Agric. 11, 113-117.Google Scholar
  117. Shorrocks V M 1989 Boron Deficiency - its Prevention and Cure. Borax Consolidated, London.Google Scholar
  118. Shorrocks VM 1996 Boron - important for pollen, fertilisation, seed and fruit set. Boron in Agriculture 16, 1-2.Google Scholar
  119. Simojoki P 1972 Boron deficiency, pollen sterility and ergot disease of barley. Ann, Agric. Fenniae 11, 333-341 (In Finnish).Google Scholar
  120. Singh R K and Choudhury B 1988 Differential response of chemicals on sex modification of three genera of cucurbits. Indian J. Hort. 45, 89-99.Google Scholar
  121. Smith T E, Hetherington S E, Asher C J and Stephenson R A 1997 Boron deficiency of avocado. 1. Effects on pollen viability and fruit set. In Proc. Int. Symp. on Boron in Soils and Plants. Eds. R W Bell and B Rerkasem. pp 00-00. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  122. Spurr A R 1957 The effect of boron on cell-wall structure in celery. Amer. J. Bot. 44, 565-636.Google Scholar
  123. Stead A D 1992 Pollination-induced flower senescence - a review. Plant Growth Regul. 11, 13-20.Google Scholar
  124. Steer M W and Steer J M 1989 Tansley Review No.16. Pollen tube growth. New Phytol. 111, 323-358.Google Scholar
  125. Steiglitz H 1977 Role of β-1,3-glucanase in postmeiotic microspore release. Dev. Biol. 57, 87-97.Google Scholar
  126. Takahasi M 1993 Exine initiation and substructure in pollen of Cae-salpinia japonica (Leguminosae: Caesalpinoideae). Amer. J. Bot. 80, 192-197.Google Scholar
  127. Tanaka H 1966 Response of Lemna paucicostata to boron as affected by light intensity. Plant and Soil 25, 425-434.Google Scholar
  128. Trione E J and Stockwell V O 1989 Development of detached wheat spikelets in culture. Plant Cell Tiss. Org. Cult. 17, 161-170.Google Scholar
  129. Tsuchiya T, Toriyama K, Yoshikawa M, Ejiri S, and Hinata K 1995 Tapetum-specific expression of the gene for an endo-beta-1,3-glucanase causes male sterility in transgenic tobacco. Plant Cell Physiol. 36, 487-494.Google Scholar
  130. Utsugi S, Sakamoto W, Ogura Y, Murata M and Motoyoshi F 1996 Isolation and characterization of cDNA clones corresponding to the genes expressed preferentially in floral organs of Arabidopsis thaliana. Plant Mol. Biol. 32, 759-765.Google Scholar
  131. Van Aelst A C and Van Went J L 1992 Ultrastructural immuno-localization of pectins and glycoproteins in Arabidopsis thaliana pollen grains. Protoplasma 168, 14-19.Google Scholar
  132. Vasil I K 1964 Effect of boron on pollen germination and pollen tube growth. In Pollen physiology and fertilisation. Ed. H F Liskens. pp 107-119. North Holland Publishing Company, Amsterdam.Google Scholar
  133. Vaughan A K F 1977 The relation between the concentration of boron in the reproductive and vegetative organs of maize plants and their development. Rhod. J. Agric. Res. 15, 163-170.Google Scholar
  134. Woodbridge C G, Venegas A and Crandall P C 1971. The boron content of developing pear, apple, and cherry flower buds. J. Amer. Soc. Hort. Sci. 96, 613-615.Google Scholar
  135. Worrall D, Hird D L, Hodge R, Paul W, Draper J and Scott R 1992 Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell 4, 759-771.Google Scholar
  136. Xu H, Huang Q, Shen K and Shen Z 1993 Anatomical studies on the effects of boron on the development of stamen and pistil of rape (Brassica napus). Acta Bot. Sinica 35, 453-459.Google Scholar
  137. Ylstra B, Muskens M and van Tunen A J 1996 Flavonols are not essential for fertilisation in Arabidopsis thaliana. Plant Mol. Biol. 32, 1155-1158.Google Scholar
  138. Ylstra B, Toyraev A, Moreno R M B, Stoger E, van Tunen A J, Vicente O, Mol J N M and Heberle-Bors E 1992 Flavonols stimulate development, germination, and tube growth of tobacco pollen. Plant Physiol. 100, 902-907.Google Scholar
  139. Zhang X, Shen Z, and Shen K 1994 The effect of boron on the development of floral organs and seed yield of rape. Acta Pedologica Sinica 31, 146-151. (In Chinese).Google Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Bernie Dell
    • 1
  • Longbin Huang
    • 1
  1. 1.School of Biological and Environmental SciencesMurdoch UniversityPerthAustralia

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