The mechanisms regulating cell-layer organisation in developing plant organs are fundamental to plant growth, but remain largely un-investigated. In order to understand the signalling pathways potentially involved in this process, the receptor kinase-encoding Arabidopsis Crinkly 4 (ACR4) gene was studied. ACR4 expression is restricted to the L1/outside cell-layer of most meristems and organ primordial, including those of the ovule integuments. Mutant analysis shows that ACR4 is required for regulation of cellular organisation during the development of sepal margins an ovule integument outgrowth. ACR4 encodes a protein that in ovules, and possibly other tissues, is abundant in anticlinal and the inner periclinal plasma membrane of “outside” cells. It is proposed that ACR4 may be involved in maintaining L1 cell-layer integrity in aerial organs by receiving and transmitting signals from neighbouring L1 cells and/or from underlying cell layers. In order to discover additional components involved in this process a mutagenesis screen based on the acr4 line was carried out. Potential enhancers of the acr4 phenotype were identified and selected for future analysis. In order to further investigate the molecular mechanism of ACR4 function a comprehensive functional dissection of the ACR4 protein was carried out, based on the ability of deletion derivatives to complement in mutant phenotype. This has permitted identification of functionally important domains of ACR4 and the formulation of a functional model for ACR4 as a partially redundant component of a developmentally crucial signalling pathway involved in the maintenance of L1-layer integrity throughout Arabidopsis development.