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A Key Enzyme of the Leloir Pathway Is Involved in Pathogenicity of Leptosphaeria maculans Toward Oilseed Rape

June 2009 , Volume 22 , Number  6
Pages  725 - 736

E. Remy,1 M. Meyer,1 F. Blaise,1 U. K. Simon,2 D. Kuhn,3 M. H. Balesdent,1 and T. Rouxel1

1INRA, UMR 1290 BIOGER, Route de Saint-Cyr, F-78026 Versailles cedex, France; 2Institute for Plant Sciences, Dept. Plant Physiology, Karl-Franzens-University Graz, Schubertstr. 51, 8010 Graz, Austria; 3Lehrstuhl Spezielle Botanik und Mykologie, Universität Tübingen, Auf der Morgenstelle 1, 72076 Tübingen, Germany

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Accepted 10 February 2009.

Agrobacterium tumefaciens-mediated random insertional mutagenesis was used to investigate pathogenicity determinants in Leptosphaeria maculans. One tagged nonpathogenic mutant, termed m186, is analyzed in detail here. Microscopic analyses of infected plant tissues revealed that m186 is specifically blocked at the invasive growth phase after an unaffected initial penetration stage and is unable to switch to the necrotrophic lifestyle. In addition, m186 exhibits an altered cell wall and seems to be affected in its ability to produce cell-wall-degrading enzymes. The T-DNA insertion occurs in the intergenic region between two head-to-tail genes, leading to a constitutive upregulation of their expression. Complementation experiments showed that only one of these two genes, Lmepi, fully accounts for the mutant phenotype. Bioinformatics and expression analyses along with functional studies suggested that the Lmepi gene encodes for the highly conserved UDP-glucose-4-epimerase, a key enzyme of the Leloir pathway involved in galactose metabolism. For the third time, this study highlights the intimate connection between primary metabolism and pathogenicity in L. maculans. This finding, along with similar data obtained from the related species Stagonospora nodorum, indicates the importance of in planta nutrition for the success of infection of plants by fungi belonging to class Dothideomycete.

© 2009 The American Phytopathological Society