Root Cap Cuticle: Divergent Biosynthetic Pathways for the formation of a Unique Protective Barrier

Until recently, the cuticle, a cutin-based protective structure on the surface of the epidermis, was thought to be exclusive to aerial plant organs. However, the discovery of a root cap cuticle (RCC) in Arabidopsis and other species challenged this paradigm and expanded our understanding of root anatomy, development, and physiology (Berhin et al., 2019). The RCC covers the outermost root cap cells of young primary and lateral roots, forming an electron-dense layer similar to the leaf cuticle of Arabidopsis. Acting as a diffusion barrier, the RCC protects the root meristem from toxic compounds during seedling establishment and prevents organ adhesions, which may delay lateral root emergence. The composition of the RCC-polyester of the primary root of Arabidopsis is distinct from that of shoot cuticles because it contains not only oxygenated fatty acids, such as C18:2 dicarboxylic acid, but also unsubstituted very-long-chain fatty acids (VLCFAs), which are atypical for cutin. We have identified two largely independent pathways involved in the biosynthesis of this special polyester: GPAT4 and GPAT8, two glycerol-3-phosphate acyltransferases with an active intrinsic phosphatase domain generating monoacylglycerols, are required for the incorporation of oxygenated fatty acids, together with LACS2, a long-chain acyl-CoA synthetase. Furthermore, GPAT2, a GPAT with an inactive phosphatase domain, that forms lysophosphatidic acids is needed for the incorporation of very-long-chain fatty acids. Both types of GPATs contribute thus non-redundantly to the barrier and surface properties of the RCC in the primary root. LACS2 plays an additional role for the biosynthesis of cutin of outgrowing lateral roots, whereas GPAT2 has only a minor role in this process possibly indicating a different cutin composition in outgrowing lateral roots. These findings highlight how root cap cuticle biosynthesis is fine-tuned through distinct metabolic pathways that selectively incorporate different fatty acids.