Assembly of cell wall polysaccharides into specific patterns is required for plant growth. A complex of RAPID ALKALINIZATION FACTOR 4 (RALF4) and its cell wall–anchored LEUCINE-RICH REPEAT EXTENSIN 8 (LRX8)–interacting protein is crucial for cell wall integrity during pollen tube growth, but its molecular connection with the cell wall is unknown. Here, we show that LRX8-RALF4 complexes adopt a heterotetrametric configuration in vivo, displaying a dendritic distribution. The LRX8-RALF4 complex specifically interacts with demethylesterified pectins in a charge-dependent manner through RALF4’s polycationic surface. The LRX8-RALF4-pectin interaction exerts a condensing effect, patterning the cell wall’s polymers into a reticulated network essential for wall integrity and expansion. Our work uncovers a dual structural and signaling role for RALF4 in pollen tube growth and in the assembly of complex extracellular polymers.

Aims: High salinity stress impairs plant growth and development. Trehalose metabolism has been implicated in sugar signaling, and enhanced trehalose metabolism can positively regulate abiotic stress tolerance. However, the molecular mechanism(s) of the stress-related trehalose pathway and the role of individual trehalose biosynthetic enzymes for stress tolerance remain unclear. Results: Trehalose-6-phosphate phosphatase (TPP) catalyzes the final step of trehalose metabolism. Investigating the subcellular localization of the Arabidopsis thaliana TPP family members, we identified AtTPPD as a chloroplast-localized enzyme. Plants deficient in AtTPPD were hypersensitive, whereas plants overexpressing AtTPPD were more tolerant to high salinity stress. Elevated stress tolerance of AtTPPD overexpressors correlated with high starch levels and increased accumulation of soluble sugars, suggesting a role for AtTPPD in regulating sugar metabolism under salinity conditions. Biochemical analyses indicate that AtTPPD is a target of post-translational redox regulation and can be reversibly inactivated by oxidizing conditions. Two cysteine residues were identified as the redox-sensitive sites. Structural and mutation analyses suggest that the formation of an intramolecular disulfide bridge regulates AtTPPD activity. Innovation: The activity of different AtTPP isoforms, located in the cytosol, nucleus, and chloroplasts, can be redox regulated, suggesting that the trehalose metabolism might relay the redox status of different cellular compartments to regulate diverse biological processes such as stress responses. Conclusion: The evolutionary conservation of the two redox regulatory cysteine residues of TPPs in spermatophytes indicates that redox regulation of TPPs might be a common mechanism enabling plants to rapidly adjust trehalose metabolism to the prevailing environmental and developmental conditions. Antioxid. Redox Signal. 21, 1289–1304.

Complex cell-to-cell communication between the male pollen tube and the female reproductive organs is required for plant fertilization. A family ofCatharanthus roseusreceptor kinase 1-like (CrRLK1L) membrane receptors has been genetically implicated in this process. Here, crystal structures of theCrRLK1Ls ANXUR1 and ANXUR2 are reported at 1.48 and 1.1 Å resolution, respectively. The structures reveal a novel arrangement of two malectin-like domains connected by a short β-hairpin linker and stabilized by calcium ions. The canonical carbohydrate-interaction surfaces of related animal and bacterial carbohydrate-binding modules are not conserved in plantCrRLK1Ls. In line with this, the binding of chemically diverse oligosaccharides to ANXUR1 and HERCULES1 could not be detected. Instead,CrRLK1Ls have evolved a protein–protein interface between their malectin domains which forms a deep cleft lined by highly conserved aromatic and polar residues. Analysis of the glycosylation patterns of differentCrRLK1Ls and their oligomeric states suggests that this cleft could resemble a binding site for a ligand required for receptor activation ofCrRLK1Ls.

Pathogens target and degrade the extracellular matrix surrounding plant cells. A central question is how cell wall–derived damage-associated molecular patterns (DAMPs) are recognized and integrated to trigger immune responses. We address this question by determining the structure of the multidomain receptor IGP1 in both apo form and bound to the cellulose-derived DAMP cellotriose. Structural analyses reveal that constitutive Leucine Rich Repeat–malectin interactions preconfigure IGP1 for ligand recognition and that the receptor features a highly specific sugar-binding pocket in the LRR domain capable of distinguishing fine variations in glycan structures. By directly sensing cello-oligomers, IGP1 acts as a cell wall sentinel that links pathogen-induced wall degradation to immune alerting, equipping plants to mount rapid and robust defense responses.

Pathogens target and degrade the extracellular matrix surrounding plant cells. A central question is how cell wall–derived damage-associated molecular patterns (DAMPs) are recognized and integrated to trigger immune responses. We address this question by determining the structure of the extracellular multidomain of the impaired in glycan perception 1 (IGP1) receptor in both apo form and bound to the cellulose-derived DAMP cellotriose. Structural analyses reveal that constitutive interactions of leucine-rich repeat (LRR)–malectin domains preconfigure IGP1 for ligand recognition and that the receptor features a highly specific sugar-binding pocket in the LRR domain capable of distinguishing fine variations in glycan structures. By directly sensing cello-oligomers, IGP1 operates as a cell wall surveillance receptor that links pathogen-induced wall degradation to immune alerting, equipping plants to mount rapid and robust defense responses.