Surrounding tissues canalize motile cardiopharyngeal progenitors towards collective polarity and directed migration

Collectively migrating cells maintain group polarity and interpret external cues to reach their destination. The cardiogenic progenitors (also known as trunk ventral cells, TVCs) of the ascidian Ciona intestinalis provide a simple chordate model with which to study collective migration. Bilateral pairs of associated TVCs undergo a stereotyped polarized migration away from the tail towards the ventral trunk, arguably constituting the simplest possible example of directed collective migration. To identify tissues contributing to TVC polarity and migration, we quantified the contact between TVCs and surrounding tissues, and blocked the secretory pathway in a tissue-specific manner. Even though TVCs normally migrate as an invariably determined leader-trailer polarized pair of adherent cells, they are capable of migrating individually, albeit a shorter distance and with altered morphology. The mesenchyme contacts newborn TVCs and contributes to robust specification of the trailer but appears to have only minor effects on directed migration. The notochord does not contact the TVCs but contributes to the onset of migration. The trunk endoderm first contacts the leader TVC, then ‘encases’ both migrating cells and provides the inputs maintaining leader-trailer polarity. Migrating TVCs adhere to the epidermis and need this contact for their cohesion. These phenomenological studies reveal that inherently motile cardiopharyngeal progenitors are channeled into stereotyped behaviors by interactions with surrounding tissues.