In C. elegans, the male animals have nine pairs of bilateral sensory rays as part of the peripheral neural tissues in their tails. Morphogenesis of these sensory rays occurs at the late L4 stage involving the papillus formation, tail retraction and ray stabilization. Each ray is composed of four cells, the hypodermis, a structural cell and two neuronal cells. This simple cellular composition makes ray differentiation an ideal model for studying tissue morphogenesis....[ Read more ]

In C. elegans, the male animals have nine pairs of bilateral sensory rays as part of the peripheral neural tissues in their tails. Morphogenesis of these sensory rays occurs at the late L4 stage involving the papillus formation, tail retraction and ray stabilization. Each ray is composed of four cells, the hypodermis, a structural cell and two neuronal cells. This simple cellular composition makes ray differentiation an ideal model for studying tissue morphogenesis.

There are a number of genetic loci, ram (ray morphology abnormal), known to control this complex glycosylation dependent morphogenetic process. Cloning and characterization of these ram genes are pivotal steps towards a better understanding of the mechanism guiding this process.

In this study, two of the ram genes have been characterized. ram-5 encodes a novel transmembrane protein expressed in the structural cell. Domain analysis of RAM-5 reveals that two extracellular domains, CUT-1 and D1, function as an interaction interface. The RAM-5 residence at the ray tip of the structural cell is guided by the D1 and the transmembrane domains. N-glycosylation modification on the CUT-1 domain modulates the RAM-5 biological activities, both its mutant rescue activity and its distribution on the structural cell surface. Exclusive expression of the ram-5 in the structural cell and yet having cellular defects in both the hypodermis and structural cell imply that reciprocal communication between these two cells is required in this morphogenetic event.

ram-4 encodes a collagen as a constituent component of the extracellular matrix. Mutations in this gene result in the morphological abnormalities, such as cell swelling and cellular process branching, found in all ray cell processes. RAM-4 collagen is preferentially expressed in the posterior hypodermis of male during the onset of the ray retraction. We demonstrate that RAM-4 collagen in the extracellular matrix physically associates with the RAM-5 molecule on the structural cell surface. We postulate that such an interaction constitutes a step in the N-glycosylation dependent morphogenetic process during the ray formation. A mechanistic model of their biological roles of these two ram products will be proposed and discussed.