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Rapid climate change has led to enhanced soil salinity, one of the major determinants of land degradation, resulting in low agricultural productivity. This has a strong negative impact on food security and environmental sustainability. Plants display various physiological, developmental and cellular responses to deal with salt stress. Recent studies highlight the root cap as the primary stress sensor, which also plays a crucial role in halotropism. The root cap is the forefront of the primary root meristem, is the first cell type to sense and respond to soil salinity, and relays the signal to the neighbouring cell types. However, how root cap cells perceive and contribute to the salt stress response is elusive. To address this, we conducted a root cap cell-specific proteomics study to identify changes in the proteome caused by salt stress. The study revealed a very specific salt stress response pattern in the root cap cells as compared to non-root cap cells and identified several novel proteins unique to the root cap. Root cap-specific protein-protein interaction (PPI) networks derived by superimposing proteomics data onto known global PPI networks reveal that the endoplasmic reticulum (ER) stress pathway is specifically activated in root cap cells upon salt stress. Importantly, we identified root cap-specific Jacalin-associated lectins (JALs) expressed in response to salt stress. A JAL10-GFP fusion protein is shown to be localized to the ER. Analysis of jal10mutants indicated a role for JAL10 in regulating the ER stress pathway in response to salt. Taken together, our study highlights the participation of specific root cap proteins in salt stress response pathways. Further, root cap-specific JAL proteins and their role in salt-mediated ER stress pathway opens a new avenue for exploring tolerance mechanisms and devise better strategies for increasing plant salinity tolerance and enhancing agricultural productivity.