Plant Biol (Stuttg) 2002; 4(1): 46-52
DOI: 10.1055/s-2002-20435
Original Paper
Georg Thieme Verlag Stuttgart ·New York

Callose in Frankia-Infected Tissue of Datisca glomerata is an Artifact of Specimen Preparation[*]

K. R. Jacobsen 1,2 , A. M. Berry 3
  • 1 Department of Agronomy and Range Science, University of California, Davis, CA 95616, USA
  • 2 Present address: Department of Botany, University of Wisconsin, Madison, WI 53706, USA
  • 3 Department of Environmental Horticulture, University of California, Davis, CA 95616, USA
Further Information

Publication History

June 18, 2001

January 02, 2002

Publication Date:
28 February 2002 (online)

Abstract

Callose, or β-1,3-glucan, is a plant cell wall polysaccharide that occurs endogenously at distinct sites in a variety of tissues. Callose is also formed in response to stress involving cell membrane perturbation. In sections of chemically-fixed nodule tissue of the actinorhizal host, Datisca glomerata, callose was cytochemically detected within the Frankia-infected cortical cells, as an extensive network of wall material surrounding the microsymbiont, but not in uninfected cortical cells. Callose formation was completely inhibited within the infected cells when 2-deoxy-D-glucose, an inhibitor of callose formation, was included in the tissue fixative. The study concludes that callose deposition in the Datisca nodule infected zone is apparently a stress response to tissue preparation and fixation. However, the rapidity and extent of callose deposition primarily at the symbiotic interface in Frankia-infected cells suggests an unusual predisposition to biosynthesis of β-1,3-glucan in the nodule cortical cells that is related to their interaction with the microsymbiont.

1 Dedicated to Professor Walter Eschrich for his 75th birthday

References

  • 01 Aist,  J. R.. (1976);  Papillae and related wound plugs of plant cells.  Annual Review of Phytopathology. 14 145-163
  • 02 Amor,  Y.,, Haigler,  C. H.,, Johson,  S.,, Wainscott,  M.,, and Delmer,  D. P.. (1995);  A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants.  Proceedings of the National Academy of Sciences of the United States of America. 92 9353-9357
  • 03 Berg,  R. H.,, Langenstein,  B.,, and Silvester,  W. B.. (1999);  Development in the Datisca-Coriaria nodule type.  Canadian Journal of Botany. 77 1334-1350
  • 04 Berry,  A. M.,, McIntyre,  L.,, and McCully,  M. E.. (1986);  Fine structure of root hair infection leading to nodulation in the Frankia-Alnus symbiosis.  Canadian Journal of Botany. 64 292-305
  • 05 Chang,  Y. C.,, Yamamoto,  Y.,, and Matsumoto,  H.. (1999);  Enhancement of callose production by a combination of aluminum and iron in suspension-cultured tobacco (Nicotiana tabacum) cells.  Soil Science and Plant Nutrion. 45 337-347
  • 06 Currier,  H. B., and Webster,  D. H.. (1964);  Callose formation and subsequent disappearance: Studies in ultrasound stimulation.  Plant Physiology. 39 843-847
  • 07 Dahiya,  P., and Brewin,  N. J.. (2000);  Immunogold localization of callose and other cell wall components in pea nodule transfer cells.  Protoplasma. 214 210-218
  • 08 Delmer,  D. P.. (1977) The biosynthesis of cellulose and other plant cell wall polysaccharides. Advances in Phytochemistry. The Structure, Biosynthesis and Degradation of Wood, Vol. 2. Loewus, F. A., Runeckle, V. C., eds. New York; Plenum pp. 45-77
  • 09 Eschrich,  W.. (1956);  Kallose. (Ein kritischer Sammelbericht).  Protoplasma. 47 487-530
  • 10 Eschrich,  W.. (1957);  Callosebildung in plasmolysierten Allium cepa-Epidermen.  Planta. 48 578-586
  • 11 Eschrich,  W.. (1965);  Physiology der Siebröhrencallose.  Planta. 65 280-300
  • 12 Eschrich,  W.. (1975) Sealing systems in phloem. Transport in Plants I. Phloem Transport. Encyclopedia of Plant Physiology. New Series, Vol. 1. Zimmermann, M. H. and Milburn, J. A., eds. Berlin, Heidelberg, New York; Springer-Verlag pp. 39-56
  • 13 Eschrich,  W., and Heyser,  W.. (1975) Biochemistry of Phloem Constituents. Transport in Plants I. Phloem Transport. Encyclopedia of Plant Physiology. New Series, Vol. 1. Zimmermann, M. H. and Milburn, J.A., eds. Berlin, Heidelberg, New York; Springer-Verlag pp. 101-136
  • 14 Fink,  J.,, Jeblick,  W.,, Blaschek,  W.,, and Kauss,  H.. (1987);  Calcium ions and polyamines activate the plasma membrane-located 1,3-β-glucan synthase.  Planta. 171 130-135
  • 15 Galway,  M. E., and McCully,  M. E.. (1987);  The time course of the induction of callose in wounded pea roots.  Protoplasma. 139 77-91
  • 16 Gibeaut,  D. M., and Carpita,  N. C.. (1994);  Biosynthesis of plant cell wall polysaccharides.  FASEB Journal. 8 904-915
  • 17 Hayashi,  T.,, Read,  S. M.,, Bussel,  J.,, Thelen,  M.,, Lin,  F.-C.,, Brown,  R. M.,, and Delmer,  D. P.. (1987);  UDP-glucose: (1,3)-β-glucan synthases from mung bean and cotton: differential effects of Ca2+ and Mg2+ on enzyme properties, and on macromolecular structure of the glucan product.  Plant Physiology. 83 1054-1062
  • 18 Hughes,  J. E., and Gunning,  B. E. S.. (1980);  Glutaraldehyde-induced deposition of callose.  Canadian Journal of Botany. 58 250-258
  • 19 Jaffe,  M. J., and Leopold,  A. C.. (1984);  Callose deposition during gravitropism of Zea mays and Pisum sativum and its inhibition by 2-deoxy-D-glucose.  Planta. 161 20-26
  • 20 Johansen,  D. A.. (1940) Plant Microtechnique. New York, London; McGraw-Hill 523 p.
  • 21 Kauss,  H.. (1985);  Some aspects of calcium-dependent regulation in plant metabolism.  Annual Review of Plant Physiology. 38 47-72
  • 22 Kauss,  H.. (1987);  Callose-Synthese. Regulation durch induzierten Ca2+-Einstrom in Pflanzenzellen.  Naturwissenschaften. 74 275-281
  • 23 Kauss,  H.. (1996) Callose Synthesis. Membranes: Specialized Functions in Plants. Smallwood, M., Knox, J. P., Bowles, D. J., eds. Oxford; BIOS Scientific Publishers pp. 77-92
  • 24 Kauss,  H.,, Köhle,  H.,, and Jeblick,  W.. (1983);  Proteolytic activation and stimulation by Ca2+ of glucan synthase from soybean cells.  FEBS. 158 84-88
  • 25 Köhle,  H.,, Jeblick,  W.,, Poten,  F.,, Blaschek,  W.,, and Kauss,  H.. (1985);  Chitosan-elicited callose synthesis in soybean cells as a Ca2+-dependent process.  Plant Physiology. 77 544-551
  • 26 Lalonde,  M., and Knowles,  R.. (1975);  Ultrastructure, composition, and biogenesis of the encapsulation material surrounding the endophyte in Alnus crispa var. mollis root nodules.  Canadian Journal of Botany. 53 1951-1971
  • 27 Lian,  C. L.,, Oiwake,  Y.,, Yokota,  H.,, and Wang,  G.. (1998);  Effect of aluminum on callose synthesis in root tips of tea (Camellia sinensis L.) plants.  Soil Science and Plant Nutrition. 44 695-700
  • 28 Liu,  Q., and Berry,  A. M.. (1991);  Localization and characterization of pectic polysaccharides in roots and root nodules of Ceanothus spp. during intercellular infection by Frankia. .  Protoplasma. 163 93-101
  • 29 Majumder,  S. K., and Leopold,  A. C.. (1967);  Callose formation in response to low temperature.  Plant Cell Physiology. 8 775-778
  • 30 Meinert,  M. C., and Delmer,  D. P.. (1977);  Changes in biochemical composition of the cell wall of the cotton fiber during development.  Plant Physiology. 59 1088-1097
  • 31 Massot,  N.,, Llugany,  M.,, Poschenrieder,  C.,, and Barcelo,  J.. (1999);  Callose production as indicator of aluminum toxicity in bean cultivars.  Journal of Plant Nutrition. 22 1-10
  • 32 McDonald,  K. L.. (1999);  High pressure freezing for preservation of high resolution fine structure and antigenicity for immunolabeling.  Methods in Molecular Biology. 117 77-97
  • 33 McNairn,  R. B.. (1972);  Phloem translocation and heat-induced callose formation in field-grown Gossypium hirsutum L.  Plant Physiology. 50 369-380
  • 34 Matheson,  N. K., and Myers,  D. K.. (1998);  Inhibition of germination by glucose analogues that are hexokinase substrates.  Phytochemistry. 48 241-248
  • 35 Newcomb,  W., and Wood,  S. M.. (1987);  Morphogenesis and fine structure of Frankia (Actinomycetales): The microsymbiont of nitrogen-fixing actinorhizal root nodules.  International Review of Cytology. 109 1-88
  • 36 Pak,  J.-Y.,, Fukuhara,  T.,, and Nitta,  T.. (1995);  Discrete subcellular localization of membrane-bound ATPase activity in marine angiosperms and marine algae.  Planta. 196 15-22
  • 37 Pate,  J. S., and Gunning,  B. E. S.. (1972);  Transfer cells.  Annual Review of Plant Physiology. 23 173-196
  • 38 Radford,  J. E.,, Vesk,  M.,, and Overall,  R. L.. (1998);  Callose deposition at plasmodesmata.  Protoplasma. 201 30-37
  • 39 Schreiner,  K. A.,, Hoddinott,  J.,, and Taylor,  G. J.. (1994);  Aluminum-induced deposition of (1,3)-β-glucans (callose) in Triticum aestivum L.  Plant and Soil. 162 273-280
  • 40 Schwarz,  R. T., and Datema,  R.. (1980);  Inhibitors of protein glycosylation.  Trends in biochemical sciences. 5 65-67
  • 41 Shimoura,  T., and Dijkstra,  J.. (1975);  The occurence of callose during the process of local lesion formation.  Netherlands Journal of Plant Pathology. 81 107-121
  • 42 Sivaguru,  M.,, Fujiwara,  T.,, Samaj,  J.,, Baluka,  F.,, Yang,  Z.,, Osawa,  H.,, Maeda,  T.,, Mori,  T.,, Volkmann,  D.,, and Motsumoto,  H.. (2000);  Aluminum-induced 1,3-β-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants.  Plant Physiology. 124 991-1006
  • 43 Tighe,  D. M., and Heath,  M. C.. (1982);  Callose induction in cowpea by uridine diphosphate glucose and calcium phosphate-boric acid treatments.  Plant Physiology. 69 366-370
  • 44 van Caeseele,  L.,, Klingner,  B.,, and Summer,  M. J.. (1996);  The immunolocalization of plasma membrane H+-ATPase in the transfer cell region of Brassica napus (Brassicaceae) ovules.  American Journal of Botany. 83 1386-1390
  • 45 Zhang,  G. C.,, Hoddinott,  J.,, and Taylor,  G. J.. (1994);  Characterization of 1,3-β-D-glucan (callose) synthesis in roots of Triticum aestivum in response to aluminum toxicity.  Journal of Plant Physiology. 144 229-234

1 Dedicated to Professor Walter Eschrich for his 75th birthday

A. M. Berry

Department of Environmental Horticulture
University of California

One Shields Ave.
Davis, CA 95616
USA

Email: amberry@ucdavis.edu

Section Editor: A. Läuchli

    >