CSLB4 modulates primary cell wall architecture and resistance to Brevicoryne brassicae in Arabidopsis thaliana

Abstract The plant cell wall (CW) is a key determinant of plant defense; however, the extent to which natural variation in primary CW architecture contributes to resistance against phloem-feeding insects remains unclear. Here, we combined genome-wide association studies (GWAS) with functional analyses to identify genetic determinants of resistance against the specialist aphid Brevicoryne brassicae in Arabidopsis thaliana. GWAS identified a significant locus on chromosome 2 associated with aphid performance. Integration of haplotype and epidermis-specific expression data prioritized CSLB4, a member of the cellulose synthase-like B family. Loss-of-function analysis using two independent T-DNA insertion alleles reduced B. brassicae offspring by 39-56%, indicating enhanced resistance, whereas performance of the generalist aphid Myzus persicae was unaffected. Electrical penetration graph analyses revealed that cslb4 mutants reached sustained phloem ingestion earlier than wild type despite reduced performance, indicating that their enhanced resistance was not associated with impaired phloem access. Biochemical, immunolocalization, and transcriptional analyses revealed constitutive alterations in primary CW architecture and aphid-induced defense responses, including changes in pectin composition, increased xyloglucan epitope accessibility, reduced callose deposition, and attenuated induction of defense-related genes. Together, these findings identify CSLB4 as a modulator of primary CW architecture and plant susceptibility to B. brassicae.