Structural signatures in EPR3 define a unique class of plant carbohydrate receptors

Abstract

Receptor-mediated perception of surface-exposed carbohydrates like lipo-and exopolysaccharides (EPS) is important for non-self recognition and responses to microbial associated molecular patterns in mammals and plants. In legumes, EPS are monitored and can either block or promote symbiosis with rhizobia depending on their molecular composition. To establish a deeper understanding of receptors involved in EPS recognition, we determined the structure of the Lotus japonicus (Lotus) exopolysaccharide receptor 3 (EPR3) ectodomain. EPR3 forms a compact structure built of three putative carbohydrate-binding modules (M1, M2 and LysM3). M1 and M2 have unique βαββ and βαβ folds that have not previously been observed in carbohydrate binding proteins, while LysM3 has a canonical βααβ fold. We demonstrate that this configuration is a structural signature for a ubiquitous class of receptors in the plant kingdom. We show that EPR3 is promiscuous, suggesting that plants can monitor complex microbial communities though this class of receptors.

Reprogramming sphingolipid glycosylation is required for endosymbiont persistence in Medicago truncatula

“…The significance of this within the context of symbiosis is not immediately clear but likely reflects important structural, biophysical, or signaling properties. In this regard, it is interesting to note that GlcNAc-containing molecules have prominent roles in symbiosis signaling, [59][60][61][62] and the cell surface of bacteria and fungi is rich in GlcNAc-containing polymers.…”

Rhizobial Exopolysaccharides: Genetic Regulation of Their Synthesis and Relevance in Symbiosis with Legumes

“…Recent results show that EPS3 is also expressed at the root cortex and nodule primordia, suggesting that EPS recognition is reiterated during symbiotic interaction, and it is also involved in intercellular cortical infection [19]. Recently, it has been shown that EPR3-like receptors, which present a structure that is quite different from that of LysM receptors involved in chitooligosaccharide (NF) perception, are ubiquitous in plants, suggesting that they might be surveillance receptors monitoring carbohydrates from different microbes associated with plant roots [186]. However, in the indeterminate-nodule-forming-legume M. truncatula, the orthologue of eps3 (Mtlyk10), although playing a relevant role in symbiosis, appears to be uninvolved in the perception of the S. meliloti EPS I [187].…”

Recent development and new insight of diversification and symbiosis specificity of legume rhizobia: mechanism and application

“…Similarly, extracellular polysaccharides (EPSs) secreted by rhizobia are precepted by legume's receptor-like kinase ERP3 (Kawaharada et al 2015) and mediate the root hair colonization and infection thread formation (Kawaharada et al 2017). While EPSs can either inhibit or promote the symbiosis depending on their molecular composition (Wong et al 2020). It is clear that all the host specificity related molecules, especially the NFs, belonged to the MAMPs, which are conserved elicitor molecules, such as chitin and chitooligosaccharides in fungi, peptidoglycan, flagellin epitope (flg22) and lipopolysaccharides (LPS) in bacteria (Boller and Felix 2009;Zipfel and Oldroyd 2017).…”