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

M. Albert; M. Werner; P. Proksch; S. C. Fry; R. Kaldenhoff

doi:10.1055/s-2004-817959

Plant Biology, Inhaltsverzeichnis

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

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.

Key words

Plant interaction - Cuscuta reflexa - tomato - xyloglucan endotransglycosylase/hydrolase.

Volltext

Referenzen

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