Physiology and Metabalism of Boron in Plants

Boron Modulation of Chilling and Freezing Tolerance in Leaf Cells of Warm Season Species
  • Longbin Huang
  • Richard W. Bell
  • Bernard Dell

Abstract

Historical accounts of possible B roles in the protection of tree and horticulture species against frost damage were reported as early as 1950s, with more field observations and experimental evidence since then. Although the initial reports (Anon 1958; Beltram 1958) were no more than anecdotal evidence due to the lack of proper comparative control experiments, later field and glasshouse studies have provided more reliable evidence about the involvement of B in the protection against frost damage – decreased frost-induced shoot-tip dieback or increased flowering and fruit yield, for example: in subtropical eucalypts Eucalyptus grandis (Cooling 1967; Cooling and Jones 1970) and Eucalyptus grandis x Eucalyptus urophylla (Lu and Huang 2003); apple, pear and blueberry (Blevins et al. 1996; Hanson and Breen 1985; Milovankic et al. 1990) and in birch, Scots pine, and Norway spruce (Braekke 1983). Frost-induced “white top” (bleached young leaves) has been observed in low temperature-sensitive E. urophylla and E. grandis in south China (Xu Daping, pers. comm.) where B deficient soils are common (Dell and Malajczuk 1994). Field observations have also suggested a link between low canopy temperature and enhanced leaf tissue damage (bleached patches) in oilseed rape grown in low B soil in south-east China (Ye et al. 1997).

Keywords

Sucrose Starch Chlorophyll Glutathione Proline 

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References

  1. Allen D.J. and Ort D.R., 2001 Impacts of chilling temperatures on photosynthesis in warm-climate plants. TRENDS in Plant Science 6, 36–42.PubMedCrossRefGoogle Scholar
  2. Anon 1958 Borax as frost protection. Horticultural Advertiser September.Google Scholar
  3. Arato A., Bondarava N., and Krieger-Liszkay A., 2004 Production of reactive oxygen species in chloride and calcium-depleted phtosystem II and their involvement in photoinhibition. Biochimica et Biophysica Acta 1608, 171–180.PubMedCrossRefGoogle Scholar
  4. Barr R. and Bottger 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, 31–39.PubMedGoogle Scholar
  5. Bassil E., Hu H., and Brown P.H., 2004 Use of Phenylboronic Acids to Investigate Boron Function in Plants. Possible Role of Boron in Transvacuolar Cytoplasmic Strands and Cell-to-Wall Adhesion. Plant Physiol. 136, 3383–3395.PubMedCrossRefGoogle Scholar
  6. Bell R.W., 1997 Diagnosis and prediction of boron deficiency for plant production. Plant and Soil 193, 149–168.CrossRefGoogle Scholar
  7. Beltram V., 1958 Bor als frostschutz (Boron as frost protector). Allgemeine Forstzeitschrift 10, 147–148.Google Scholar
  8. Blaser-Grill J., Knoppik D., Amberger A., and Goldbach H., 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 Physiology 90, 280–284.PubMedGoogle Scholar
  9. Blevins D., Scrivner C.L., Reinbott T.M., and Schon M.K., 1996 Foliar boron increases berry number and yield of two highbush blueberry cultivars in Missouri. J. Plant Nutr. 19, 99–113.Google Scholar
  10. Braekke F.H., 1979 Boron deficiency in forest plantations on peatland in Norway. Meddelesar fra Norsk Institutte for Skogforskning 35, 213–236.Google Scholar
  11. Braekke F.H., 1983 Micronutrients-prophylactic use and cure of forest growth disturbances. Proc. Int. Workshop on Growth Disturbances of Forest Trees. Finland, October 1982. Commun. Inst. Forest. Fenniae Helsinki 116, 159–169.Google Scholar
  12. Brown P.H., Bellaloui N., Wimmer M.A., Bassil E., Ruiz J., Hu H., Pfeffer H., Dannel F., and Romheld V., 2002 Boron in plant biology. Plant Biology 4, 205–223.CrossRefGoogle Scholar
  13. Cakmak I. and Romheld V., 1997 Boron deficiency-induced impairments of cellular functions in plants. Plant and Soil 193, 71–84.CrossRefGoogle Scholar
  14. Cleland R.E., 1988 Molecular events of photoinhibitory inactivation in the reaction centre of photosystem II. Australian Journal of Plant Physiology 15, 135–150.CrossRefGoogle Scholar
  15. Cooling E.N., 1967 Frost resistance in Eucalyptus grandis following the application of fertiliser borate. Rhod. Zamb. Mal. J. Agric. Res. 5, 97–100.Google Scholar
  16. Cooling E.N. and Jones B.E., 1970 The importance of boron and NPK fertilisers to eucalypts in the southern province, Zambia. East Afr. Agric. & Forest. J. 36, 185–194.Google Scholar
  17. Dell B. and Malajczuk N., 1994 Boron deficiency in eucalypt plantations in China. Canadian Journal of Forest Research 24, 2409–2416.Google Scholar
  18. El-Shintinawy F., 1999 Structural and functional damage caused by boron deficiency in sunflower leaves. Photosynthetica 36, 565–573.CrossRefGoogle Scholar
  19. Ferrol N. and Donaire J.P., 1992 Effect of boron on plasma membrane proton extrusion and redox activity in sunflower cells. Plant Science 86, 41–47.CrossRefGoogle Scholar
  20. Goldbach H.E., Blaser-Grill J., Lindemann N., Porzelt M., Hörrmann C., Lupp B., and Gesser B., 1991 Influence of boron on net proton release and its relation to other metabolic processes. Current Topics in Plant Biochemistry and Physiology 10, 195–220.Google Scholar
  21. 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 Lycopersicon esculentum. Physiologia Plantarum 80, 114–118.CrossRefGoogle Scholar
  22. Goldbach H.E., Wimmer M.A., Chaumont F., Matoh T., Volkmann D., Baluška F., Wingender R., and Schulz M.Q., 2002 Rapid responses of plants to boron deprivation. In Boron in Plant and Animal Nutrition, Bonn, Germany, 2002. Eds H.E. Goldbach, B. Rerkasem, M. Wimmer, P.H. Brown, M. Thellier and R.W. Bell. pp 167.Google Scholar
  23. Goodwin W., Pallas J.A., and Jenkins G.I., 1996 Transcripts of a gene encoding a putative cell wall-plasma membrane linker protein are specifically cold-induced in Brassica napus. Plant Molecular Biology 31, 771–781.PubMedCrossRefGoogle Scholar
  24. Graham D. and Patterson B.D., 1982 Responses of plants to low, nonfreezing temperatures: proteins, metabolism, and acclimation. Annual Review of Plant Physiology and Plant Molecular Biology 33, 347–372.Google Scholar
  25. Guy C.L., 1990 Cold acclimation and freezing stress tolerance: role of protein metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 41, 187–223.Google Scholar
  26. Hanson E.J. and Breen P.J., 1985 Effects of all boron sprays and environmental factors on fruit set and boron accumulcation in ‘Italian’ prune flowers. Journal of American Society and Horticulture Science 110, 389–392.Google Scholar
  27. Hodges D.M., Andrews C.J., Johnson D.A., and Hamilton R.I., 1996 Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines. Physiologia Plantarum 98, 685–692.CrossRefGoogle Scholar
  28. Huang L., Gherardi M., Bell R.W., and Dell B., 2002 High photon flux density increases external boron (B) requirements for leaf growth of sunflower (Helianthus annuus L. cv. Hysun 25) in B-buffered solution culture. In Boron in Plant and Animal Nutrition, Bonn, Germany, 2002. Eds H.E. Goldbach, B. Rerkasem, M. Wimmer, P.H. Brown, M. Thellier and R W Bell. pp 213.Google Scholar
  29. Huang L., Ye Z., Bell R.W., and Dell B., 2005 Boron Nutrition and Chilling Tolerance of Warm Climate Crop Species. Ann Bot, 96, 755–767.PubMedCrossRefGoogle Scholar
  30. Hughes M.A, and Dunn M.A., 1996 The molecular biology of plant acclimation to low temperature. Journal of Experimental Botany 47, 291–305.CrossRefGoogle Scholar
  31. Kang H.-M. and Saltveit M.E., 2002 Effect of chilling on antioxidant enzymes and DPPH-radical scavenging activity of high and low vigour cucumber seedling radicles. Plant Cell & Environment 25.Google Scholar
  32. Kastori R., Plesnicar M., Pankovic D. and Sakac Z., 1995 Photosynthesis, chlorophyll fluorescence and soluble carbohydrates in sunflower leaves as affected by boron deficiency. Journal of Plant Nutrition 18, 1751–1763.Google Scholar
  33. Kobayashi M., Mutoh T., and Matoh T., 2004 Boron nutrition of cultured tobacco BY-2 cells. IV. Genes induced under low boron supply. J. Exp. Bot. 55, 1441–1443.PubMedCrossRefGoogle Scholar
  34. Kratsch H.A. and Wise R.R., 2000 The ultrastructure of chilling stress. Plant, Cell and Environment 23, 337–350.CrossRefGoogle Scholar
  35. Leonardos E.D., Savitch L.V., Huner N.P.A., Oquist G., and Grodzinski B., 2003 Daily photosynthetic and C-export patterns in winter wheat leaves during cold stress and acclimation. Physiologia Plantarum 117, 521–531.PubMedCrossRefGoogle Scholar
  36. Lu C.-q. and Huang B.-l., 2003 Effects of boron on membrane lipid peroxidation and endogenous protective mechanisms in leaves of Eucalyptus grandis x Eucalyptus urophylla under low temperature. Journal of Tropical and Subtropical Botany 11, 217–222.Google Scholar
  37. Lyons J.M., Graham D., and Raison J.K., 1979 Low Temperature Stress in Crop Plants: The Role of the Membrane. Academic Press, New York.Google Scholar
  38. Marschner H., 1995 Mineral Nutrition of Higher Plants. Academic Press, London.Google Scholar
  39. Melis A., 1999 Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? TRENDS in Plant Science 4, 130–135.CrossRefPubMedGoogle Scholar
  40. Milovankic M., Keserovic Z., and Vasiljevic Z., 1990 Studies on some chemicals used for prevention of frost damage to fertile buds and flowers of fruit crops. Yugoslovensko Vocarstvo 24, 21–27.Google Scholar
  41. Muhling K.H., Wimmer M., and Goldbach H., 1998 Apoplastic and membrane-associated Ca2+ in leaves and roots as affected by boron deficiency. Physiologia Plantarum 102, 179–184.CrossRefGoogle Scholar
  42. 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. Physiologia Plantarum 98, 281–290.CrossRefGoogle Scholar
  43. 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? Physiologia Plantarum 104, 479–485.CrossRefGoogle Scholar
  44. Plesnicar M., Kastori R., Sakac Z., Pankovic D., and Petrovic N., 1997 Boron as limiting factor in photosynthesis and growth of sunflower plants in relation to phosphate supply. Agrochimica 41, 144–154.Google Scholar
  45. Powles S.B. and Critchley C., 1980 The effect of photon flux density during growth on photo-inhibition of intact attached bean leaflets. Plant Physiology 65, 1181–1187.PubMedGoogle Scholar
  46. Roldán M., Belver A., Rodriguez-Rosales M.P., Ferrol N., and Donaire J.P., 1998 In vivo and in vitro effects of boron on the plasmamembrane proton pump of sunflower roots. Physiologia Plantarum 84, 49–54.CrossRefGoogle Scholar
  47. Sakya A.T., Dell B., and Huang L., 2002 Boron requirements for Eucalyptus globulus seedlings. Plant and Soil 246, 87–95.CrossRefGoogle Scholar
  48. Saruyama H. and Tanida M., 1995 Effect of chilling on activated oxygen-scavenging enzymes in low temperature-sensitive and tolerant cultivars of rice (Oryza sativa L.). Plant Science 109, 105–113.CrossRefGoogle Scholar
  49. Savitch L.V., Harney T., and Huner N.P.A., 2000 Sucrose metabolism in spring and winter wheat in response to high irradiance, cold stress and cold acclimation. Physiologia Plantarum 108, 270–278.CrossRefGoogle Scholar
  50. Shinozaki K. and Yamaguchi-Shinozaki K., 2000 Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Current Opinion in Plant Biology 3, 217–223.PubMedGoogle Scholar
  51. Shorrocks V.M., 1997 The occurrence and correction of boron deficiency. Plant and Soil 193, 121–148.CrossRefGoogle Scholar
  52. Sonoike K., 1999 The different roles of chilling temperatures in the photoinhibition of photosystem I and photosystem II. Journal of Photochemistry and Photobiology B: Biology 48, 136–141.CrossRefGoogle Scholar
  53. Tahtiharju S., Sangwan V., Monroy A.F., Dhindsa R.S., and Bor M., 1997 The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. Planta 203, 442–447.PubMedCrossRefGoogle Scholar
  54. Terashima I., Noguchi K., Itoh-Nemoto T., Park Y.-M., Kubo A., and Tanaka K., 1998 The cause of PSI photoinhibition at low temperatures in leaves of Cucumis sativus, a chilling-sensitive plant. Physiologia Plantarum 103, 295–303.CrossRefGoogle Scholar
  55. Thomashow M., 1999 Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571–599.PubMedCrossRefGoogle Scholar
  56. Wang Z.Y., Tang Y.L., Zhang F.S., and Wang H., 1999 Effect of boron and low temperature on membrane integrity of cucumber leaves. Journal of Plant Nutrition 22, 543–550.CrossRefGoogle Scholar
  57. Wimmer M.A., and Goldbach H., 1999 Influence of Ca2+ and pH on the stability of different boron fractions in intact roots of Vicia faba L. Plant Biology 1 632–637.Google Scholar
  58. Wise R.R., McWilliam J., and Naylor A.W., 1983 A comparative study of low temperature-induced ultrastructure alterations of three species with different chilling sensitivities. Plant Cell & Environment 5, 525–535.Google Scholar
  59. Xin Z. and Browse J., 2000 Cold comfort farm: the acclimation of plants to freezing temperatures. Plant, Cell and Environment 2000, 893–902.CrossRefGoogle Scholar
  60. Ye Z., 2005 Effect of low temperature on plant boron nutrition. PhD thesis. Murdoch University, Perth, Australia.Google Scholar
  61. Ye Z., Bell R., Huang L., Yang Y., and Dell B., 1997 Covering winter oilseed rape (Brassica napus cv. Eureka) increases yield on a low boron soil. In The International Symposium on Boron in Soils and Plants, Chiang Mai, Thailand, 7–11 September, 1997, 1997. Eds R. Bell and B. Rerkasem. pp 29–34.Google Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Longbin Huang
    • 1
  • Richard W. Bell
    • 1
  • Bernard Dell
    • 2
  1. 1.School of Land and Food SciencesThe University of QueenslandBrisbaneAustralia
  2. 2.Division of Science and EngineeringMurdoch UniversityAustralia

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