Plant Biol (Stuttg) 2004; 6(4): 402-407
DOI: 10.1055/s-2004-817959
Original Paper

Georg Thieme Verlag Stuttgart KG · New York

The Cell Wall-Modifying Xyloglucan Endotransglycosylase/Hydrolase LeXTH1 is Expressed during the Defence Reaction of Tomato against the Plant Parasite Cuscuta reflexa

M. Albert1 , M. Werner1 , P. Proksch2 , S. C. Fry3 , R. Kaldenhoff1
  • 1TU Darmstadt, Botanisches Institut, Darmstadt, Germany
  • 2Heinrich-Heine-Universität Düsseldorf, Institut für Pharmazeutische Biologie, Universitätsstr. 1, 40225 Düsseldorf, Germany
  • 3The Edinburgh Cell Wall Group, Institute of Cell and Molecular Biology, The University of Edinburgh, Daniel Rutherford Building, The King's Buildings, Edinburgh EH9 3JH, UK
Further Information

Publication History

Publication Date:
12 July 2004 (online)

Abstract

A suppressive subtractive hybridization technique was used to identify genes, which were induced during the early phases of the interaction between dodder (Cuscuta reflexa), a phanerogamic parasite, and its incompatible host plant tomato. One of the identified genes encodes a tomato xyloglucan endotransglycosylase/hydrolase (XTH) - an enzyme involved in cell wall elongation and restructuring. The corresponding LeXTH1 mRNA accumulated 6 h after attachment of the parasite. In contrast, wounding did not influence the expression level. Subsequent to LeXTH1 mRNA accumulation, an increase in XTH activity at the infection sites as well as in adjacent tissues was observed. The effect of IAA on LeXTH1 expression was analyzed because the concentration of this phytohormone is known to increase in the tomato tissue during the interaction with the parasite. LeXTH1 mRNA accumulation was in fact induced by external application of auxin. However, in the auxin-insensitive tomato mutant diageotropica, Cuscuta induced LeXTH1-mRNA accumulated with a time course similar to wild type tomato. Thus, auxin appears not to be an essential signal for infection-induced LeXTH1 activation. Our data suggest a role for xyloglucan transglycosylation in defence reactions associated with the incompatible tomato-Cuscuta interaction.

References

  • 1 Antosiewicz D. M., Purugganan M. M., Polisensky D. H., Braam J.. Cellular localization of Arabidopsis xyloglucan endotransglycosylase-related proteins during development and after wind stimulation.  Plant Physiology. (1997);  115 1319-1328
  • 2 Aubert D., Herzog M.. A new cDNA encoding a xyloglucan endotransglycosylase-related polypeptide (AtXTR8) preferentially expressed in seedling, root and stem of Arabidopsis thaliana. .  Plant Science. (1996);  121 187
  • 3 Capdepon M., Fer A., Ozenda P.. Sur un Système Inédit de Rejet d'un Parasite: Exemple de la Cuscute sur Cotonnier (C. lupuliformis Krock. sur Gossypium hirsutum L.) Paris; C. R. Acad. Sc. (1985): 227-232
  • 4 Catala C., Rose J. K., Bennett A. B.. Auxin regulation and spatial localization of an endo-1,4-β-d-glucanase and a xyloglucan endotransglycosylase in expanding tomato hypocotyls.  Plant J.. (1997);  12 417-426
  • 5 Catala C., Rose J. K., Bennett A. B.. Auxin-regulated genes encoding cell wall-modifying proteins are expressed during early tomato fruit growth.  Plant Physiol.. (2000);  122 527-534
  • 6 Chomczynski P., Sacchi N.. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol chloroform extraction.  Anal. Biochem.. (1987);  162 156-159
  • 7 Cosgrove D. J.. Enzymes and other agents that enhance cell wall extensibility.  Annual Review of Plant Physiology and Plant Molecular Biology. (1999);  50 391-417
  • 8 Fry S. C.. Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals.  Biochemical Journal. (1998);  332 507-515
  • 9 Fry S. C., Smith R. C., Renwick K. F., Martin D. J., Hodge S. K., Matthews K. J.. Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants.  Biochem. J.. (1992);  282 821-828
  • 10 Fry S. C., York W. S., Albersheim P., Darvill A., Hayashi T., Joseleau J.-P., Kato Y., Lorences E. P., Maclachlan G. A., McNeil M., Mort A. J., Reid J. S. G., Seitz H. U., Selvendran R. R., Voragen A. G. J., White A. R.. An unambiguous nomenclature for xyloglucan-derived oligosaccharides.  Physiologia Plantarum,. (1993);  89 1-3
  • 11 Fry S. C.. The Growing Plant Cell Wall: Chemical and Metabolic Analysis. Reprint Edition (ISBN 1-93066-508-3). Caldwell, New Jersey, USA; The Blackburn Press (2000)
  • 12 Gertz O.. Über die Schutzmittel einiger Pflanzen gegen schmarotzende Cuscuta. .  Jb. Wiss. Bot.. (1915);  56 123-154
  • 13 Hayashi T.. Xyloglucans in the primary cell wall.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. (1989);  40 139-168
  • 14 Ihl B., Tutakhil N., Hagen A., Jacob F.. Studien an Cuscuta reflexa Roxb. VII. Zum Abwehrmechanismus von Lycopersicon esculentum Mill.  Flora. (1988);  181 383-393
  • 15 Kelly M. O., Bradford K. J.. Insensitivity of the diageotropica tomato Lycopersicon esculentum mutant to auxin.  Plant Physiol.. (1986);  82 713-717
  • 16 Kollmann R., Dörr I.. Parasitische Blütenpflanzen.  Naturwissenschaften,. (1987);  74 12-21
  • 17 Löffler C., Czygan F.-C., Proksch P.. Role of indole-3-acetic acid in the interaction of the phanerogamic parasite Cuscuta and host plants.  Plant Biol.. (1999);  1 613-617
  • 18 Manning K.. Isolation of nucleic acids from plants by differential solvent precipitation.  Anal. Biochem.. (1991);  195 45-50
  • 19 Nagar R., Singh M., Sanwal G. G.. Cell-wall degrading enzymes in Cuscuta reflexa and its hosts.  J. Exp. Bot.. (1984);  35 1104-1112
  • 20 Nishitani K.. Construction and restructuring of the cellulose-xyloglucan framework in the apoplast as mediated by the xyloglucan-related protein family - a hypothetical scheme.  Journal of Plant Research. (1998);  111 159-166
  • 21 Oh M. H., Romanow W. G., Smith R. C., Zamski E., Sasse J., Clouse S. D.. Soybean BRU1 encodes a functional xyloglucan endotransglycosylase that is highly expressed in inner epicotyl tissues during brassinosteroid-promoted elongation.  Plant and Cell Physiology. (1998);  39 124-130
  • 22 Okazawa K., Sato Y., Nakagawa T., Asada K., Kato I., Tomita E., Nishitani K.. Molecular cloning and cDNA sequencing of endoxyloglucan transferase, a novel class of glycosyltransferases that mediates molecular grafting between matrix polysaccharides in plant cell walls.  J. Biol. Chem.. (1993);  268 25364-25368
  • 23 Otto B., Grimm B., Ottersbach P., Kloppstech K.. Circadian control of the accumulation of mRNA for light- and heat-inducible chloroplast proteins in pea.  Plant Physiol.. (1988);  88 21-25
  • 24 Potter I., Fry S. C.. Xyloglucan endotransglycosylase activity in pea internodes. Effects of applied gibberellic acid.  Plant Physiol.. (1993);  103 235-241
  • 25 Pritchard J., Hetherington P. R., Fry S. C., Tomos A. D.. Xyloglucan endotransglycosylase activity, microfibril orientation and the profiles of cell wall properties along growing regions of maize roots.  Journal of Experimental Botany. (1993);  44 1281-1289
  • 26 Rayle D. L., Cleland R. E.. The acid growth theory of cell elongation is alive and well.  Plant Physiol.. (1992);  99 1271-1274
  • 27 Saab I. N., Sachs M. M.. A flooding-induced xyloglucan endotransglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma.  Plant Physiology. (1996);  112 385-391
  • 28 Sahm A., Pfanz H., Grünsfelder M., Czygan F.-C., Proksch P.. Anatomy and phenylpropanoid metabolism in the incompatible interaction of Lycopersicon esculentum and Cuscuta reflexa. .  Bot. Acta. (1995);  108 358-364
  • 29 Schlenzka B.. Hibiscus rosa-sinensis/Cuscuta odorata: Beispiel einer inkompatiblen Wirts-Parasiten-Beziehung. Ph.D. Thesis. Kiel; Christian-Albrechts-Universität (1992)
  • 30 Singh A., Singh M.. Incompatibility of Cuscuta haustoria with the resistant hosts - Ipomea batatas L. and Lycopersicon esculentum Mill.  J. Plant Physiol.. (1997);  150 592-596
  • 31 Smith R. C., Matthews P. R., Schünmann P. H. D., Chandler P. M.. The regulation of leaf elongation and xyloglucan endotransglycosylase by gibberellin in “Himalaya” barley (Hordeum vulgare L.).  Journal of Experimental Botany. (1996);  47 1395-1404
  • 32 Smith R. C., Fry S. C.. Endotransglycosylation of xyloglucans in plant cell suspension cultures.  Biochemical Journal. (1991);  279 529-535
  • 33 Stürzl M., Roth K.. “Run off” synthesis and application of defined single-stranded DNA hybridization probes.  Anal. Biochem.. (1990);  185 164-169
  • 34 Thompson J. E., Fry S. C.. Evidence for covalent linkage between xyloglucan and acidic pectins in suspension-cultured rose cells.  Planta. (2000);  211 275-286
  • 35 Thompson J. E., Smith R. C., Fry S. C.. Xyloglucan undergoes inter-polymeric transglycosylation during binding to the plant cell wall in vivo: evidence from 13C/3H dual labelling and isopycnic centrifugation in caesium trifluoroacetate.  Biochemical Journal. (1997);  327 699-708
  • 36 Thompson J. E., Fry S. C.. Restructuring of wall-bound xyloglucan by transglycosylation in living plant cells.  Plant Journal. (2001);  26 23-34
  • 37 Vissenberg K., Martinez-Vilchez I. M., Verbelen J.-P., Miller J. G., Fry S. C.. In vivo co-localization of xyloglucan endotransglycosylase activity and its donor substrate in the elongation zone of Arabidopsis roots.  The Plant Cell. (2000);  12 1299-1237
  • 38 Werner M., Uehlein N., Proksch P., Kaldenhoff R.. Characterization of two tomato aquaporins and expression during the incompatible interaction of tomato with the plant parasite Cuscuta relexa. .  Planta. (2001);  213 550-555
  • 39 Xu W., Campbell P., Vargheese A. K., Braam J.. The Arabidopsis XTH-related gene family: environmental and hormonal regulation of expression.  Plant Journal. (1996);  9 879-889

R. Kaldenhoff

Botanisches Institut
TU Darmstadt

Schnittspahnstraße 10

64287 Darmstadt

Germany

Email: kaldenhoff@bio.tu-darmstadt.de

Section Editor: G. Thiel