First published online October 19, 2004; 10.1105/tpc.104.024968
The Plant Cell 16:3020-3032 (2004)
© 2004 American Society of Plant Biologists
ß-1,3 Glucan Sulfate, but Not ß-1,3 Glucan, Induces the Salicylic Acid Signaling Pathway in Tobacco and Arabidopsis
Rozenn Ménarda,
Susanne Albanb,1,
Patrice de Ruffraya,
Frank Jamoisc,
Gerhard Franzb,
Bernard Fritiga,
Jean-Claude Yvinc and
Serge Kauffmanna,2
a Institut de Biologie Moléculaire des Plantes du Centre National de la Recherche Scientifique, Université Louis Pasteur, 67084 Strasbourg, France
b Institute of Pharmacy, University of Regensburg, 93040 Regensburg, Germany
c Laboratoires Goëmar, 35400 Saint Malo, France
2 To whom correspondence should be addressed. E-mail serge.kauffmann{at}ibmp-ulp.u-strasbg.fr; fax 33-388-614442.
Sulfate substituents naturally occurring in biomolecules, such as oligosaccharides and polysaccharides, can play a critical role in major physiological functions in plants and animals. We show that laminarin, a ß-1,3 glucan with elicitor activity in tobacco (Nicotiana tabacum), becomes, after chemical sulfation, an inducer of the salicylic acid (SA) signaling pathway in tobacco and Arabidopsis thaliana. In tobacco cell suspensions, the oxidative burst induced by the laminarin sulfate PS3 was Ca2+ dependent but partially kinase independent, whereas laminarin triggered a strickly kinase-dependent oxidative burst. Cells treated with PS3 or laminarin remained fully responsive to a second application of laminarin or PS3, respectively, suggesting two distinct perception systems. In tobacco leaves, PS3, but not laminarin, caused electrolyte leakage and triggered scopoletin and SA accumulation. Expression of different families of Pathogenesis-Related (PR) proteins was analyzed in wild-type and mutant tobacco as well as in Arabidopsis. Laminarin induced expression of ethylene-dependent PR proteins, whereas PS3 triggered expression of ethylene- and SA-dependent PR proteins. In Arabidopsis, PS3-induced PR1 expression was also NPR1 (for nonexpressor of PR genes1) dependent. Structure-activity analysis revealed that (1) a minimum chain length is essential for biological activity of unsulfated as well as sulfated laminarin, (2) the sulfate residues are essential and cannot be replaced by other anionic groups, and (3) moderately sulfated ß-1,3 glucans are active. In tobacco, PS3 and curdlan sulfate induced immunity against Tobacco mosaic virus infection, whereas laminarin induced only a weak resistance. The results open new routes to work out new molecules suitable for crop protection.
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