The developmentally regulated ECM glycoprotein ISG plays an essential rolein organizing the ECM and orienting the cells of Volvox

Volvox is one of the simplest multicellular organisms with only two cell ty pes, yet it has a surprisingly complex extracellular matrix (ECM) containin g many region-specific morphological components, making Volvox suitable as a model system for ECM investigations. ECM deposition begins shortly after inversion, which is the process by which the embryo turns itself right-side -out at the end of embryogenesis. It was previously shown that the gene enc oding an ECM glycoprotein called ISG is transcribed very transiently during inversion. Here we show that the developmentally controlled ISG accumulate s at the bases of the flagella right after inversion, before any morphologi cally recognizable ECM structures have yet developed. Later, ISG is abundan t in the 'flagellar hillocks' that encircle the basal ends of all flagella, and in the adjacent 'boundary zone' that delimits the spheroid. Transgenic Volvox were generated which express a truncated form of ISG, These transge nics exhibit a severely disorganized ECM within which the cells are embedde d in a highly chaotic manner that precludes motility, A synthetic version o f the C-terminal decapeptide of ISG has a similar disorganizing effect, but only when it is applied during or shortly after inversion. We postulate th at ISG plays a critical role in morphogenesis and acts as a key organizer o f ECM architecture; at the very beginning of ECM formation ISG establishes an essential initial framework that both holds the somatic cells in an adap tive orientation and acts as the scaffold upon which the rest of the ECM ca n be properly assembled, assuring that somatic cells of post-inversion sphe roids are held in orientations and locations that makes adaptive swimming b ehavior possible.