Abstract
Cell suspension cultures of Populus alba L. (original cells) require at least 10 μM boron for appropriate growth. Using original cells we established a cell line, T-5B, which can grow in a medium containing low levels of boron (5 μM). The level of boron localized in the cell walls of T-5B cells was one-half that found in the cell walls of original cells maintained in medium containing 100 μM boron, and the level of the rhamnogalacturonan II dimer, cross-linked by a borate ester, also decreased in the former. The sugar composition of whole cell walls of the T-5B cell line was similar that of the original cells, however pectic polysaccharides composed of arabinose or galacturonic acid were easily extracted from T-5B cell walls with 50 mM trans-1,2-cyclohexanediamine-N,N,N′,N′-tetraacetic acid. Our results suggest that boron deficiency causes a weakening of the interaction among pectic polysaccharides due to a decrease in boron-rhamnogalacturonanII cross-linkage.
Similar content being viewed by others
Abbreviations
- Ara:
-
Arabinose
- CDTA:
-
Trans-1,2-Cyclohexanediamine-N,N,N′,N′-tetraacetic acid monohydrate
- Fuc:
-
Fucose
- Gal:
-
Galactose
- GalUA:
-
Galacturonic acid
- Glc:
-
Glucose
- GlcUA:
-
Glucuronic acid
- Man:
-
Mannose
- Rha:
-
Rhamnose
- RG-II:
-
Rhamnogalacturonan II
- Xyl:
-
Xylose
References
Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 49:481–500
Blumenkrantz N, Asboe-Hansen HM (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489
Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Romheld V (2002) Boron in plant biology. Plant Biol 4:205–223
Dubois M, Gilles KA, Hamilton JK, Robers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Fleischer A, Titel C, 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
Fleischer A, O’Neill MA, Ehwald R (1999) The pore size of non-graminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiol 121:829–838
Hu H, Brown PH (1994) Localization of boron in cell walls of squash and tobacco and its association with pectin. Plant Physiol 105:681–689
Ishii T, Matsunaga T (1996) Isolation and characterization of a boron-rhamnogalacturonan-II complex from cell walls of sugar beet pulp. Carbohydr Res 284:1–9
Ishii T, Matsunaga T, Hayashi N (2001) Formation of rhamnogalacturonan II-borate dimer in pectin determines cell wall thickness of pumpkin tissue. Plant Physiol 126:1698–1705
Kakegawa K, Edashige Y, Ishii T (2000) Metabolism of cell wall polysaccharides in cell suspension cultures of Populus alba in relation to cell growth. Physiol Plant 108:420–425
Kaneko S, Ishii T, Matsunaga T (1997) A boron-rhamnogalacturonan-II complex from bamboo shoot cell walls. Phytochemistry 44:243–248
Kobayashi M, Matoh T, Azuma J (1995) Structure and glycosyl composition of the boron-polysaccharide complex of radish roots. Plant Cell Physiol 36S:139
Kobayashi M, Matoh T, Azuma J (1996) Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell wall. Plant Physiol 110:1017–1020
Loomis WD, Durst RW (1992) Chemistry and biology of boron. Biofactors 3:229–239
Matoh T, Ishigaki K, Mizutani M, Matsunaga W, 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 33:1135–1141
Matoh T, Ishigaki K, Ohno K, Azuma J (1993) Isolation and characterization of boron-polysaccharide complex from radish roots. Plant Cell Physiol 34:639–642
Matoh T, Kawaguchi S, Kobayashi M (1996) Ubiquity of a borate-rhamnogalacturonan II complex in the cell walls of higher plants. Plant Cell Physiol 37:636–640
Matoh T, Takasaki M, Kobayashi M, 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
Matoh T, Matsuda A, Akaike R, Hara Y, Kobayashi M (2001) Increased supply of boron to swiss chard plants did not affect the level of boron in a cell wall-bound form: a possible application to the diagnosis of B nutrition of plants. Soil Sci Plant Nutr 47:779–784
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497
O’Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darvill AG, Albersheim 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
O’Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294:846–849
Pellerin P, Doco T, Vidal S, Williams P, Brillouet J-M, O’Neill MA (1996) Structural characterization of red wine rhamnogalacturonan II. Carbohydr Res 290:183–197
Selvendran RR, O’Neill MA (1987) Isolation and analysis of cell walls from plant material. Methods Biochem Anal 32:25–153
Selvendran RR, Ryden P (1990) Isolation and analysis of plant cell walls. In: Dey PM (ed) Methods in plant biochemistry, vol 2. Carbohydrates. Academic Press, London, pp 549–579
Shimokawa T, Ishii T, Matsunaga T (1999) Isolation and characterization of rhamnogalacturonan II-borate complex from Pinus densiflora. J Wood Sci 45:435–439
Titel CH, Ehwald R (1999) Permeability limits of cell walls in suspension cultures: biotechnological and physiological aspects. Russ J Plant Physiol 46:739–744
York WS, Darvill AG, McNeil M, Albersheim P (1986) Isolation and characterization of plant cell wall and plant cell components. Methods Enzymol 118:3–40
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by F. Sato
Rights and permissions
About this article
Cite this article
Kakegawa, K., Ishii, T. & Matsunaga, T. Effects of boron deficiency in cell suspension cultures of Populus alba L.. Plant Cell Rep 23, 573–578 (2005). https://doi.org/10.1007/s00299-004-0878-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-004-0878-8