Non‐branched β‐1,3‐glucan oligosaccharides trigger immune responses in Arabidopsis

Abstract

SUMMARYFungal cell walls, which are essential for environmental adaptation and host colonization by the fungus, have been evolutionarily selected by plants and animals as a source of microbe-associated molecular patterns (MAMPs) that, upon recognition by host pattern recognition receptors (PRRs), trigger immune responses conferring disease resistance. Chito-oligosaccharides [b-1,4-N-acetylglucosamine oligomers, (GlcNAc) n ] are the only glycosidic structures from fungal walls that have been well-demonstrated to function as MAMPs in plants. Perception of (GlcNAc) 4-8 by Arabidopsis involves CERK1, LYK4 and LYK5, three of the eight members of the LysM PRR family. We found that a glucan-enriched wall fraction from the pathogenic fungus Plectosphaerella cucumerina which was devoid of GlcNAc activated immune responses in Arabidopsis wild-type plants but not in the cerk1 mutant. Using this differential response, we identified the non-branched 1,3-b-D-(Glc) hexasaccharide as a major fungal MAMP. Recognition of 1,3-b-D-(Glc) 6 was impaired in cerk1 but not in mutants defective in either each of the LysM PRR family members or in the PRR-co-receptor BAK1. Transcriptomic analyses of Arabidopsis plants treated with 1,3-b-D-(Glc) 6 further demonstrated that this fungal MAMP triggers the expression of immunity-associated genes. In silico docking analyses with molecular mechanics and solvation energy calculations corroborated that CERK1 can bind 1,3-b-D-(Glc) 6 at effective concentrations similar to those of (GlcNAc) 4 . These data support that plants, like animals, have selected as MAMPs the linear 1,3-b-D-glucans present in the walls of fungi and oomycetes. Our data also suggest that CERK1 functions as an immune co-receptor for linear 1,3-b-D-glucans in a similar way to its proposed function in the recognition of fungal chito-oligosaccharides and bacterial peptidoglycan MAMPs.

Plant cell wall‐mediated immunity: cell wall changes trigger disease resistance responses

“…Recent results also indicate that insoluble polymers are not able to induce immune responses in plants, and that these polymers should be shortened to smaller entities (oligosaccharides) to get active DAMPs recognized by their corresponding PRRs (Mélida et al ., ). Thus, oligosaccharide production by the enzymatic machinery from either the host or the invader is necessary for DAMP release.…”

“…CERK1 is also implicated in PGN perception (probably as a co‐receptor), forming heteromeric complexes with LYM1 and LYM3 RLPs (Willmann et al ., ). Moreover, CERK1 has recently been shown to be necessary for 1,3‐β‐ d ‐glucan‐triggered immune responses (Mélida et al ., ). The 1,3‐β‐ d ‐glucans are an important component of fungal and oomycete cell walls but are also present in plant cells, although in minute amounts, thus suggesting that CERK1 might also be a DAMP receptor (Mélida et al ., ).…”

“…Moreover, CERK1 has recently been shown to be necessary for 1,3‐β‐ d ‐glucan‐triggered immune responses (Mélida et al ., ). The 1,3‐β‐ d ‐glucans are an important component of fungal and oomycete cell walls but are also present in plant cells, although in minute amounts, thus suggesting that CERK1 might also be a DAMP receptor (Mélida et al ., ). The central role of CERK1 in Arabidopsis immunity is supported by its role in resistance against fungi such as Alternaria brassicicola , G. cichoracearum and P. cucumerina (Miya et al ., ; Wan et al ., ; Mélida et al ., ), the bacterium P. syringae (Gimenez‐Ibanez et al ., ) and the oomycete H. arabidopsidis (Mélida et al ., ).…”

“…Despite pioneering work and recently regained momentum (Nothnagel et al, 1983;Doares et al, 1995;Willmann et al, 2011;Liu et al, 2012;Cao et al, 2014;M elida et al, 2018), knowledge about the specific mechanisms of plant defence activation by carbohydrate-based patterns (MAMPs and DAMPs) clearly lags behind the animal field, where different types of receptors have been described to bind carbohydrate-based ligands (Figure 3; Erwig and Gow, 2016). Also, our current knowledge of carbohydratebased pattern recognition by plants is clearly behind that of peptidic-based MAMP perception by the plant immune system (recently reviewed by Tang et al, 2017).…”

FGB1 and WSC3 are in planta‐induced β‐glucan‐binding fungal lectins with different functions

“…Additionally, CW integrity plays a role in the response to other microbes in the soil. To avoid recognition of CW-derived polysaccharides and to limit stimulation of plant defense responses, fungi have evolved different strategies such as CW remodeling, masking, shielding and manipulation of glycaninduced host defense signaling (El Gueddari et al, 2002;van den Burg et al, 2006;de Jonge et al, 2010;Marshall et al, 2011;Fujikawa et al, 2012;Mentlak et al, 2012;Oliveira-Garcia & Deising, 2013Sanchez-Vallet et al, 2013;Fesel & Zuccaro, 2016a;Takahara et al, 2016;Wawra et al, 2016;Melida et al, 2018). Whereas several mechanisms of chitin masking/ shielding and avoidance of plant host immune perception are known, fungal mechanisms dedicated to the modulation of bglucan recognition have only been described recently (Emsley & Cowtan, 2004;Oliveira-Garcia & Deising, 2013Wawra et al, 2016).…”