Alteration of cell wall xylan acetylation triggers defense responses that counterbalance the immune deficiencies of plants impaired in the β‐subunit of the heterotrimeric G‐protein

Abstract

Summary Arabidopsis heterotrimeric G protein complex modulates Pathogen Associated Molecular Pattern-triggered immunity (PTI) and disease resistance responses to different type of pathogens. It also plays a role in plant cell wall integrity as mutants impaired in the Gβ (agb1-2) or Gγ subunits have an altered wall composition compared to wild-type plants. Here we performed a mutant screen to identify suppressors of agb1-2 (sgb) that restore susceptibility to pathogens to wild-type levels. Out of the four sgb mutants (sgb10-sgb13) identified, sgb11 is a new mutant allele of ESKIMO1 (ESK1), which encodes a plant-specific polysaccharide O-acetyltransferase involved in xylan acetylation. Null alleles (sgb11/esk1-7) of ESK1 restore to wild-type levels the enhanced susceptibility of agb1-2 to the necrotrophic fungus Plectosphaerella cucumerina BMM (PcBMM), but not to the bacterium Pseudomonas syringae pv. tomato DC3000, nor to the oomycete Hyaloperonospora arabidopsidis. The enhanced resistance to PcBMM of the agb1-2 esk1-7 double mutant was not the result of the re-activation of deficient PTI responses in agb1-2. Alteration of cell wall xylan acetylation caused by ESK1 impairment is accompanied by an enhanced accumulation of abscisic acid, the constitutive expression of genes encoding antibiotic peptides and enzymes involved in the biosynthesis of tryptophan-derived metabolites, and the accumulation of disease resistance-related secondary metabolites and different osmolites. These esk1-mediated responses counterbalance the defective PTI and PcBMM susceptibility of agb1-2 plants, and explain the enhanced drought resistance of esk1 plants. These results suggest that a deficient PTI-mediated resistance is partially compensated by the activation of specific cell wall-triggered immune responses.

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

“…Three‐week‐old Arabidopsis plants were used to determine production of ROS after treatments using the luminol assay (Escudero et al ., ) and a VariosKan Lux luminescence reader (Thermo Scientific). In vivo quantification of RbohD promoter‐driven luciferase was performed using Arabidopsis transgenic lines pRbohD::LUC (Morales et al ., ).…”

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

“…Remodelling of primary and secondary cell walls by impairing the function of CESA genes has a specific impact on pathogen resistance and tolerance to abiotic stresses. Arabidopsis irregular xylem ( irx ) 5/3/1 cell wall mutants defective in CESA subunits (CESA4/7/8, respectively) required for secondary cell wall formation show enhanced resistance to different pathogens, including the necrotrophic fungi Plectosphaerella cucumerina and Botrytis cinerea , the vascular bacterium Ralstonia solanacearum and the vascular fungus Fusarium oxysporum (Table , Figure b; Hernández‐Blanco et al ., ; Escudero et al ., ). In line with these results, an Arabidopsis mutant defective in the MYB46 transcription factor that directly regulates the expression of several secondary cell wall‐related genes, including CESA4 / 7 / 8 , also showed enhanced resistance to necrotrophic fungi (Table ; Ramírez et al ., ).…”

“…The disease resistance phenotype of irx5 , irx3 , irx1 and myb46 plants is in part explained by the constitutive activation of plant immune responses, such as the abscisic acid (ABA) signalling pathway and the synthesis of antimicrobial compounds like peptides and tryptophan‐derived metabolites (Figure b; Hernández‐Blanco et al ., ; Escudero et al ., ). The constitutive activation of these defensive pathways in irx1 / 3 / 5 plants probably explains their trade‐off phenotypes (dwarf plants and reduced seed yield) (Hernández‐Blanco et al ., ; Sánchez‐Vallet et al ., ; Ramírez et al ., ).…”

“…In this case, the alterations in the degree of acetylation were minor, illustrating that subtle CWI impairments are sensed and trigger defence responses. Such impairment in xylan acetylation was accompanied by enhanced accumulation of ABA, the constitutive expression of genes encoding antimicrobial peptides and enzymes involved in the biosynthesis of tryptophan‐derived metabolites, and the accumulation of disease resistance‐related secondary metabolites and different osmolites, which might help explain the enhanced freezing, drought and salinity resistance phenotype of esk1 plants (Xin et al ., ; Lugan et al ., ; Xu et al ., ; Escudero et al ., ). Some of the transcriptional and metabolomic changes observed in esk1‐7 overlapped with those observed in the irx1‐6 mutant and might contribute to explaining the restoration to wild‐type levels of the defective PTI responses of agb1‐2 plants observed in abg1‐2 esk1‐7 and agb1‐2 irx1‐6 double mutants (Escudero et al ., ).…”

“…Some of the transcriptional and metabolomic changes observed in esk1‐7 overlapped with those observed in the irx1‐6 mutant and might contribute to explaining the restoration to wild‐type levels of the defective PTI responses of agb1‐2 plants observed in abg1‐2 esk1‐7 and agb1‐2 irx1‐6 double mutants (Escudero et al ., ). Despite the similarities of the constitutively activated defence responses of esk1‐7 and irx1‐6 , the first showed enhanced resistance to P. cucumerina but not to H. arabidopsidis , which contrasted with the increased resistance of irx1‐6 to both pathogens (Table ; Hernández‐Blanco et al ., ; Escudero et al ., ).…”