During animal development, precise cellular morphologies are established that enable polarized cells to perform specialized functions within the organism. For instance, the C. elegans excretory-canal cell has four hollow processes (or canals) that extend from the cell soma along the left and right lateral body regions to collect fluid for osmoregulation. Similarly, neurons project processes to connect with appropriate targets. Heparan sulfate proteoglycans (HSPGs) are conserved glycoproteins that play diverse roles, including to regulate interactions between morphogens and guidance cues and their corresponding receptors to elicit cellular responses and orchestrate morphogenetic events. The heparan sulfate (HS) chains attached to HSPG core proteins are polymerized by glycosyltransferases of the exostosin (EXT) family, whose loss causes morphogenetic defects and embryonic lethality across species. Viable hypomorphic mutants of
rib-1 and
rib-2, which encode the C. elegans HS copolymerase, display the striking phenotype of having supernumerary cellular extensions in a number of polarized cells: several monopolar neurons can develop two full neurites, and the excretory-canal cell can form up to eight projections in these mutants. We define one key HSPG that cell-autonomously controls the number of canals formed by the excretory-canal cell, and find that chemical modifications of its HS chains are important for this function. The supernumerary canals observed in these mutants display the hallmarks of normal canals: they develop at the same time as normal ones, arise from the cell body, and display normal lumen and cytoskeletal (F-actin and microtubule) organization. Through genetic analysis we demonstrate that HSPGs and specific guidance cues and receptors (of the
unc-6 and
slt-1 pathways) cooperate to regulate the number of formed processes; we also define genetic interactions between HSPGs and downstream Rho-family GTPases known to regulate the cytoskeleton. Our results provide insight into a cellular system operating to guarantee that the proper number of cellular projections is established during polarized cell development, and contribute to understanding the roles of conserved HSPGs in cellular morphogenetic events.