Identification of a multigene family encoding putative β-glucan-binding proteins in Medicago truncatula

Leclercq, Julie; Fliegmann, Judith; Tellström, Verena; Niebel, Andréas; Cullimore, Julie V.; Niehaus, Karsten; Küster, H.; Ebel, Jürgen; Mithöfer, Axel

doi:10.1016/j.jplph.2007.02.008

Cited by 8 publications

(4 citation statements)

References 40 publications

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“…Fungal cell wall β‐glucans and chitins have also been reported as MAMPs that evoke primary immune responses in plant cells (Ryan and Farmer, 1991; Felix et al ., 1993; Zhang et al ., 2002; Altenbach and Robatzek, 2007; de Wit, 2007). β‐glucan binding proteins have been identified as components of a proposed receptor complex that detects branched β‐glucan derivatives from oomycetes in soybean ( Glycine max ), French bean ( Phaseolus vulgaris ) and barrel medic ( Medicago truncatula ) (Mithofer et al ., 1996; 1999; Leclercq et al ., 2008). Recently, a pattern‐recognition receptor for chitin oligosaccharides was identified in rice ( Oryza sativa ) (Kaku et al ., 2006).…”

Section: Introductionmentioning

confidence: 99%

Dynamics of cell wall components of Magnaporthe grisea during infectious structure development

Fujikawa

Kuga

Yano

et al. 2009

Molecular Microbiology

136

169

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SummaryOligosaccharides derived from cell wall of fungal pathogens induce host primary immune responses. To understand fungal strategies circumventing the host plant immune responses, cell wall polysaccharide localization was investigated using fluorescent labels during infectious structure differentiation in the rice blast fungus Magnaporthe grisea. a-1,3-glucan was labelled only on appressoria developing on plastic surfaces, whereas it was detected on both germ tubes and appressoria on plant surfaces. Chitin, chitosan and b-1,3-glucan were detected on germ tubes and appressoria regardless of the substrate. Major polysaccharides labelled at accessible surface of infectious hyphae were a-1,3-glucan and chitosan, but after enzymatic digestion of a-1,3-glucan, b-1,3-glucan and chitin became detectable. Immunoelectron microscopic analysis showed a-1,3-glucan and b-1,3-glucan intermixed in the cell wall of infectious hyphae; however, a-1,3-glucan tended to be distributed farther from the fungal cell membrane. The fungal cell wall became more tolerant to chitinase digestion upon accumulation of a-1,3-glucan. Accumulation of a-1,3-glucan was dependent on the Mps1 MAP kinase pathway, which was activated by a plant wax derivative, 1,16-hexadecanediol. Taken together, a-1,3-glucan spatially and functionally masks b-1,3-glucan and chitin in the cell wall of infectious hyphae.Thus, a dynamic change of composition of cell wall polysaccharides occurs during plant infection in M. grisea.

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Section: Introductionmentioning

confidence: 99%

Dynamics of cell wall components of Magnaporthe grisea during infectious structure development

Fujikawa

Kuga

Yano

et al. 2009

Molecular Microbiology

136

169

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“…Since the outermost layer of fungal cell surface glycans mainly consists of β-1,3-glucans (Wanke et al, 2021), hydrolysis by β-1,3-glucanases renders the inner chitin layer more accessible to secreted plant chitinases. Although GH81 family members are not categorized as PR-2 proteins, previous studies focusing on GBPs from soybean and other legumes have shown their importance in defense against oomycetes (Fliegmann et al, 2004;Leclercq et al, 2008). To better understand the contribution of GBP1 to hydrolysis of fungal surface glycan substrates, we performed substrate characterization assays with heterologously purified barley GBP1.…”

Section: Discussionmentioning

confidence: 99%

A GH81-type β-glucan-binding protein facilitates colonization by mutualistic fungi in barley

Wanke

Boerdonk

Mahdi

et al. 2023

Preprint

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Cell walls are important interfaces of plant-fungal interactions. Host cell walls act as robust physical and chemical barriers against fungal invaders, making them an essential line of defense. Upon fungal colonization, plants deposit phenolics and callose at the sites of fungal penetration to reinforce their walls and prevent further fungal progression. Alterations in the composition of plant cell walls significantly impact host susceptibility. Furthermore, plants and fungi secrete glycan hydrolases acting on each other's cell walls. These enzymes release a wide range of sugar oligomers into the apoplast, some of which trigger the activation of host immunity via host surface receptors. Recent characterization of cell walls from plant-colonizing fungi have emphasized the abundance of β-glucans in different cell wall layers, which makes them suitable targets for recognition. To characterize host components involved in immunity against fungi, we performed a protein pull-down with the biotinylated β-glucan laminarin. Thereby, we identified a glycoside hydrolase family 81-type glucan-binding protein (GBP) as the major β-glucan interactor. Mutation of GBP1 and its only paralogue GBP2 in barley led to decreased colonization by the beneficial root endophytes Serendipita indica and S. vermifera, as well as the arbuscular mycorrhizal fungus Rhizophagus irregularis. The reduction of symbiotic colonization was accompanied by enhanced responses at the host cell wall. Moreover, GBP mutation in barley also increased resistance to fungal infections in roots and leaves by the hemibiotrophic pathogen Bipolaris sorokiniana and the obligate biotrophic pathogen Blumeria graminis f. sp. hordei, respectively. These results indicate that GBP1 is involved in the establishment of symbiotic associations with beneficial fungi, a role that has potentially been appropriated by barley-adapted pathogens.

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“…In addition, we unequivocally show that cell wall glucan-chitosaccharide fractions are defense gene elicitors, and that they can trigger nuclear-associated calcium oscillations independent of the well-characterized CSP signal transduction pathway used by endosymbiotic microbes. The fact that the activation of defense genes by glucan-chitosaccharide fractions was independent of NFP suggests that they are perceived by one or several other receptors, which might belong either to the LysM or glucan-binding protein families [32], [65], for which most members have unknown biochemical functions in M. truncatula . Furthermore, the loss of resistance in nfp mutants suggests a regulatory role for NFP in immunity, rather than direct elicitor recognition.…”

Section: Discussionmentioning

confidence: 99%

Aphanomyces euteiches Cell Wall Fractions Containing Novel Glucan-Chitosaccharides Induce Defense Genes and Nuclear Calcium Oscillations in the Plant Host Medicago truncatula

et al. 2013

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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 β-1,6-glucans, and contain a β-(1,3;1,4)-glucan backbone whose β-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.

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Identification of a multigene family encoding putative β-glucan-binding proteins in Medicago truncatula

Cited by 8 publications

References 40 publications

Dynamics of cell wall components of Magnaporthe grisea during infectious structure development

Dynamics of cell wall components of Magnaporthe grisea during infectious structure development

A GH81-type β-glucan-binding protein facilitates colonization by mutualistic fungi in barley

Aphanomyces euteiches Cell Wall Fractions Containing Novel Glucan-Chitosaccharides Induce Defense Genes and Nuclear Calcium Oscillations in the Plant Host Medicago truncatula

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