Aphanomyces euteiches cell wall fractions containing novel glucan-chitosaccharides induce defense genes and nuclear calcium oscillations in the plant host Medicago truncatula

Amaury Nars (1) , Claude Lafitte (1) , Mireille Chabaud (2) , Sophie Drouillard (3) , Hugo Mélida (4) , Saïda Danoun (1) , Tinaig Le Costaouec (3) , Thomas Rey (1) , Julie Benedetti (2, 1) , Vincent Bulone (4) , David Barker (2) , Jean-Jacques Bono (2) , Bernard Dumas (5) , Christophe Jacquet (6) , Laurent Heux (3) , Judith Fliegmann (2, 1) , Arnaud Bottin (1)

1 LRSV - Laboratoire de Recherche en Sciences Végétales
2 Unité mixte de recherche interactions plantes-microorganismes
3 CERMAV - Centre de Recherches sur les Macromolécules Végétales
4 Albanova University Center
5 Interactions Microbiennes dans la Rhizosphère et les Racines
6 Evolution des Interactions Plantes-Microorganismes

N-acetylglucosamine-based saccharides (chitosaccharides) are components of microbial cell walls and act as molecular signals during host-microbe interactions. In the legume plant Medicago truncatula, the perception of lipochitooligosaccharide signals produced by symbiotic rhizobia and arbuscular mycorrhizal fungi involves the Nod Factor Perception (NFP) lysin motif receptor-like protein and leads to the activation of the so-called common symbiotic pathway. In rice and Arabidopsis, lysin motif receptors are involved in the perception of chitooligosaccharides released by pathogenic fungi, resulting in the activation of plant immunity. Here we report the structural characterization of atypical chitosaccharides from the oomycete pathogen Aphanomyces euteiches, and their biological activity on the host Medicago truncatula. Using a combination of biochemical and biophysical approaches, we show that these chitosaccharides are linked to beta-1,6-glucans, and contain a beta-(1,3; 1,4)-glucan backbone whose beta-1,3-linked glucose units are substituted on their C-6 carbon by either glucose or N-acetylglucosamine residues. This is the first description of this type of structural motif in eukaryotic cell walls. Glucan-chitosaccharide fractions of A. euteiches induced the expression of defense marker genes in Medicago truncatula seedlings independently from the presence of a functional Nod Factor Perception protein. Furthermore, one of the glucan-chitosaccharide fractions elicited calcium oscillations in the nucleus of root cells. In contrast to the asymmetric oscillatory calcium spiking induced by symbiotic lipochitooligosaccharides, this response depends neither on the Nod Factor Perception protein nor on the common symbiotic pathway. These findings open new perspectives in oomycete cell wall biology and elicitor recognition and signaling in legumes.

Domaines: Sciences du Vivant [q-bio]; Biologie végétale

Amaury Nars, Claude Lafitte, Mireille Chabaud, Sophie Drouillard, Hugo Mélida, et al.. Aphanomyces euteiches cell wall fractions containing novel glucan-chitosaccharides induce defense genes and nuclear calcium oscillations in the plant host Medicago truncatula. PLoS ONE, 2013, 8 (9), ⟨10.1371/journal.pone.0075039⟩. ⟨hal-02648518⟩