Boron and calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls
- 656 Downloads
Among 16 essential elements of higher plants, Ca2+ and B have been termed as apoplastic elements. This is mainly because of their localization in cell walls, however, it has turned to be highly likely that these two elements significantly contribute to maintain the integrity of cell walls through binding to pectic polysaccharides.
Boron in cell walls exclusively forms a complex with rhamnogalacturonan II (RG-II), and the B-RG-II complex is ubiquitous in higher plants. Analysis of the structure of the B-RG-II complex revealed that the complex contains two molecules boric acid, two molecules Ca2+ and two chains of monomeric RG-II. This result indicates that pectic chains are cross-linked covalently with boric acid at their RG-II regions. The complex was reconstitutedin vitro only by mixing monomeric RG-II and boric acid, however, the complex decomposed spontaneously unless Ca2+ was supplemented. Furthermore, the native complex decomposed when it was incubated withtrans-1,2-diaminocyclohexane-N, N, N′, N′-tetraacetic acid (CDTA) which chelates Ca2+.
When radish root cell walls were washed with a buffered 1.5% (w/v) sodium dodesyl sulfate (SDS) solution (pH 6.5), 96%, 13% and 6% of Ca2+, B and pectic polysaccharides of the cell walls, respectively, were released and the cell wall swelled twice. Subsequent extraction with 50 mM CDTA (pH 6.5) of the SDS-washed cell walls further released 4%, 80% and 61% of Ca2+, B and pectic polysaccharides, respectively. Pectinase hydrolysis of the SDS-treated cell walls yielded a B-RG-II complex and almost all the remaining Ca2+ was recovered in the complex. This result suggests that cell-wall bound Ca2+ is divided into at least two fractions, one anchors the CDTA-soluble pectic polysaccharides into cell walls together with B, and the other may control the properties of the pectic gel.
These studies demonstrate that B functions to retain CDTA-soluble pectic polysaccharides in cell walls through its binding to the RG-II regions in collaboration with Ca2+.
Key wordsBoron Calcium Cell wall Pectic polysaccharide Rhamnogalacturonan II
trans-1,2-diaminocyclohexane-N, N, N′, N′-tetraacetic acid
sodium dodesyl sulfate
Unable to display preview. Download preview PDF.
- Bowen, H.J.M. 1966. Trace Elements in Biochemistry, Academic Press, London, pp. 61–84.Google Scholar
- Da Silva, P.G.P. 1962. On the possibility of substitution of strontium for calcium in maize plants. Agronomia Lusitana24: 133–164.Google Scholar
- Hirsch, A.M. andTorrey, 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
- Hu, H., Brown, P.H. andLabavitch, J.M. 1996. Species variability in boron requirement is correlated with cell wall pectin. J. Exp. Bot.47: 227–232.Google Scholar
- Jarvis, M.C. 1984. Structure and properties of pectin gels in plant cell walls. Plant Cell Environ.7: 153–164.Google Scholar
- Kobayashi, M., Kawaguchi, S., Takasaki, M., Miyagawa, I., Takabe, K. andMatoh, T. 1997a. A borate-rhamnogalacturonan II complex in germinating pollen tubes of lily (Lilium longiflorum).In T. Andoet al.., eds., Plant Nutrition for Sustainable Food Production and Environment. Kluwer Academic Publishers, Netherlands, pp. 89–90.Google Scholar
- Kobayashi, M., Matoh, T. andAzuma, J. 1995. Structure and glycosyl composition of the boron-polysaccharide complex of radish roots. Plant Cell Physiol.36S: 139.Google Scholar
- Kobayashi, M., Nakagawa, H., Asaka, T., and Matoh, T. 1998. Cross-linkage in the rhamnogalacturonan II regions both with boric acid and calcium ion anchors pectic network in cell walls. Plant Physiol. (in press)Google Scholar
- Kobayashi, M., Ohno, K. andMatoh, T. 1997b. Boron nutrition of cultured tobacco BY-2 cells. II. Characterization of the boron-polysaccharide complex. Plant Cell Physiol.38: 676–683.Google Scholar
- Kouchi, H. andKumazawa, K. 1975. Anatomical responses of root tips to boron deficiency II. Effect of boron deficiency on cellular growth and development in root tips. Soil Sci. Plant Nutr.21: 137–150.Google Scholar
- Matoh, T., Ishigaki, K., Mizutani, M., Matsunaga, W. andTakabe, 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: 1135–1141.Google Scholar
- Matoh, T., Ishigaki, K., Ohno, K. andAzuma, J. 1993. Isolation and characterization of a boron-polysaccharide complex from radish roots. Plant Cell Physiol.34: 639–642.Google Scholar
- Matoh, T., Kawaguchi, S. andKobayashi, M. 1996. Ubiquity of a borate-rhamnogalacturonan II complex in the cell walls of higher plants. Plant Cell Physiol.37: 636–640.Google Scholar
- Matoh, T., Takasaki, M., Kawaguchi, S. and Kobayashi, M. 1998. Immunocytochemistry of rhamnogalacturonan II in cell walls of higher plant. Plant Cell Physiol. (in Press).Google Scholar
- Matsunaga, T., Ishii, T. andWatanabe-Oda, H. 1997. HPLC/ICP-MS study of metals bound to borate-rhamnogalacturonan-II from plant cell walls.In T. Andoet al., eds., Plant Nutrition for Sustainable Food Production and Environment. Kluwer Academic Publishers. Netherlands, pp. 81–82.Google Scholar
- McCann, M.C. andRoberts, K. 1991. Architecture of the primary cell wall.InC.W. Lloyd, ed., The Cytoskeletal Basis of Plant Growth and Form, Academic Press, London, pp. 109–129.Google Scholar
- Nye, P.H. andTinker, P.B. 1977. Solute interchange between solid, liquid and gas phases in the soil.In Solute Movement in the Soil-Root System, University of California Press, California, pp. 33–68.Google Scholar
- O'Neill, M.A., Warrenfeltz, D., Kates, K., Pellerin, P., Doco, T., Darvill, A.G. andAlbersheim, P. 1996. Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cells, forms a dimer that is covalently cross-linked by a borate ester. J. Biol. Chem.271: 22923–22930.PubMedCrossRefGoogle Scholar
- Puvanesarajah, V., Darvill, A.G. andAlbersheim, P. 1991. Structural characterization of two oligosaccharide fragments formed by the selective cleavage of rhamnogalacturonan II: evidence for the anomeric configuration and attachment sites of apiose and 3-deoxy-2-heptulosaric acid. Carbohydr. Res.218: 211–222.PubMedCrossRefGoogle Scholar
- Skok, J. 1958. The role of boron in the plant cell.In C.A. Lamb, O.G. Bentley and J.M. Beattie, eds., Trace Elements. Academic Press, London, pp. 227–263.Google Scholar
- Smith, M.E. 1944. The role of boron in plant metabolism. 1. Boron in relation to the absorption and solubility of calcium. Aust. J. Exp. Biol. Med. Sci.22: 257–263.Google Scholar
- 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
- Yamanouchi, M. 1971. The role of boron in higher plants I. The relations between boron and calcium or the pectic substance in plants. J. Soil Sci. Manure Jpn.42: 207–213.Google Scholar
- Yamauchi, T., Hara, T. andSonoda, Y. 1986. Distribution of calcium and boron in the pectin fraction of tomato leaf cell wall. Plant Cell Physiol.27: 729–732.Google Scholar