The ascidian notochord forms through simultaneous invagination and convergent extension of a monolayer

Understanding how global patterns of tissue movement and deformation emerge from the combined activities of many individual cells remains a central unsolved problem in developmental biology. We consider this problem in the context of ascidian notochord formation, in which simultaneous invagination and convergent extension transforms a monolayer plate of 40 cells into a cylindrical rod (Munro and Odell, 2002). Active crawling of basolateral notochord cell edges across the faces of their adjacent neighbors accompanies this transformation and probably drives it. Basolateral crawling is biased both within the plane of the notochord plate and along the apical-basal axis in a way that could account for both invagination and convergent extension. But the source of this bias is unknown. Experimental and theoretical studies have identified many possible sources of patterned cellular behavior within tissues and these fall into two classes. First, pre-existing cytoplasmic asymmetries and/or spatial pre-patterns in the expression of “morphoregulatory” genes could determine spatial patterns of intrinsic motile and adhesive behavior before any morphogenetic movements occur. For example, pre-existing gradients of adhesivity along a specific embryonic axis might be resolved by active cell movements into oriented tissue extension (Gergen et al., 1986; Irvine and Wieschaus, 1994; Mittenthal and Mazo, 1983; Nardi and Kafatos, 1976a; Nardi and Kafatos, 1976b; Wieschaus et al., 1991). Second, interactions with surrounding tissues during morphogenesis could trigger or otherwise influence patterned cell behavior. For example, recent studies in Xenopus and Fundulus embryos suggest signals emanating from localized specific cell populations or tissue boundaries could propagate through cell populations and thereby polarize motile and adhesive behaviors within them (Domingo and Keller, 1995; Shih and Keller, 1992; Trinkaus, 1998; Trinkaus et al., 1992). Alternatively, local interactions occurring at tissue boundaries could bias the directionality of cell extension or movement, for example through contact-dependent inhibition or stabilization of protrusive behavior at planar tissue boundaries (Jacobson and Moury, 1995; Jacobson et al., 1986; Keller et al., 1989; Keller et al., 1992), or interactions with an oriented extracellular matrix at vertical tissue boundaries (Keller et al., 1991; Nakatsuji et al., 1982; Nakatsuji and Johnson, 1983; Shih and Keller, 1992). Here, we exploit the relatively simple organization and development of the ascidian embryo to assess the relative 1 Development 129, 1-12 (2002) Printed in Great Britain © The Company of Biologists Limited 2002 DEV5936