Arabidopsis immune responses triggered by cellulose‐ and mixed‐linked glucan‐derived oligosaccharides require a group ofleucine‐rich repeat malectinreceptor kinases

Abstract

SUMMARY The plant immune system perceives a diversity of carbohydrate ligands from plant and microbial cell walls through the extracellular ectodomains (ECDs) of pattern recognition receptors (PRRs), which activate pattern‐triggered immunity (PTI). Among these ligands are oligosaccharides derived from mixed‐linked β‐1,3/β‐1,4‐glucans (MLGs; e.g. β‐1,4‐D‐(Glc)2‐β‐1,3‐D‐Glc, MLG43) and cellulose (e.g. β‐1,4‐D‐(Glc)3, CEL3). The mechanisms behind carbohydrate perception in plants are poorly characterized except for fungal chitin oligosaccharides (e.g. β‐1,4‐d‐(GlcNAc)6, CHI6), which involve several receptor kinase proteins (RKs) with LysM‐ECDs. Here, we describe the isolation and characterization of Arabidopsis thaliana mutants impaired in glycan perception (igp) that are defective in PTI activation mediated by MLG43 and CEL3, but not by CHI6. igp1–igp4 are altered in three RKs – AT1G56145 (IGP1), AT1G56130 (IGP2/IGP3) and AT1G56140 (IGP4) – with leucine‐rich‐repeat (LRR) and malectin (MAL) domains in their ECDs. igp1 harbors point mutation E906K and igp2 and igp3 harbor point mutation G773E in their kinase domains, whereas igp4 is a T‐DNA insertional loss‐of‐function mutant. Notably, isothermal titration calorimetry (ITC) assays with purified ECD‐RKs of IGP1 and IGP3 showed that IGP1 binds with high affinity to CEL3 (with dissociation constant KD = 1.19 ± 0.03 μm) and cellopentaose (KD = 1.40 ± 0.01 μM), but not to MLG43, supporting its function as a plant PRR for cellulose‐derived oligosaccharides. Our data suggest that these LRR‐MAL RKs are components of a recognition mechanism for both cellulose‐ and MLG‐derived oligosaccharide perception and downstream PTI activation in Arabidopsis.

BERBERINE BRIDGE ENZYME-LIKE OXIDASES OF CELLODEXTRINS AND MIXED-LINKED Β-Glucans CONTROL SEED COAT FORMATION

“…Notably, both CELLOXs and the receptor kinases IMPAIRED IN GLYCAN PERCEPTION 1 and 4 (IGP1 and IGP4) recognize as substrates and ligands, respectively, cellulose fragments but not MLG that has a β-(1,3)-linked glucose at the reducing end (Martín-Dacal et al, 2022). IGP1 is also known as the Cello-Oligomer Receptor Kinase 1 (CORK1), required for CD3 perception and PTI activation in Arabidopsis (Tseng et al, 2022).…”

Signals and Their Perception for Remodelling, Adjustment and Repair of the Plant Cell Wall

“…Xyloglucan breakdown products activate signaling cascades which are similar to those activated by oligogalacturonides (OGs), the breakdown products of pectin ( Table 1 ) [ 21 ]. Degradation of mixed-linkage glucan polysaccharides from, e.g., Poaceae hemicellulose, generates the elicitor-active mixed-linkage β-1,3/β-1,4 glucan oligosaccharides ([ 7 ], and ref. therein) ( Table 1 ).…”

“…Furthermore, as components of the cell wall surveillance system, they activate cell wall repair processes by stimulating the biosynthesis of one or more polysaccharides. OGs from pectin [ 123 ], short-chain xyloglucans [ 21 ], mixed-linkage glucans [ 7 ] and arabinoxylan [ 17 ] and mannan oligosaccharides from secondary cell walls of gymnosperms [ 22 ] were identified and characterized as elicitor-active compounds in various species ( Table 1 ).…”

The damage-associated molecular pattern cellotriose alters the phosphorylation pattern of proteins involved in cellulose synthesis and trans -Golgi trafficking in Arabidopsis thaliana

“… 13 Cellooligomers from cellulose breakdown require the malectin-domain (MD) receptor kinase (RK) CORK1 for intracellular signaling. 1 , 14 Therefore, breakdown products of the three cell wall polysaccharides are recognized by pattern recognition receptors (PRR)s.…”