Shavenbaby Couples Patterning to Epidermal Cell Shape Control

Abstract

It is well established that developmental programs act during embryogenesis to determine animal morphogenesis. How these developmental cues produce specific cell shape during morphogenesis, however, has remained elusive. We addressed this question by studying the morphological differentiation of the Drosophila epidermis, governed by a well-known circuit of regulators leading to a stereotyped pattern of smooth cells and cells forming actin-rich extensions (trichomes). It was shown that the transcription factor Shavenbaby plays a pivotal role in the formation of trichomes and underlies all examined cases of the evolutionary diversification of their pattern. To gain insight into the mechanisms of morphological differentiation, we sought to identify shavenbaby's downstream targets. We show here that Shavenbaby controls epidermal cell shape, through the transcriptional activation of different classes of cellular effectors, directly contributing to the organization of actin filaments, regulation of the extracellular matrix, and modification of the cuticle. Individual inactivation of shavenbaby's targets produces distinct trichome defects and only their simultaneous inactivation prevent trichome formation. Our data show that shavenbaby governs an evolutionarily conserved developmental module consisting of a set of genes collectively responsible for trichome formation, shedding new light on molecular mechanisms acting during morphogenesis and the way they can influence evolution of animal forms.

Conserved regulatory architecture underlies parallel genetic changes and convergent phenotypic evolution

“…First, svb acts as a single master regulator of larval trichome development. svb function is both required for development of these trichomes and sufficient to induce expression of a large set of downstream genes that regulate and contribute to trichome development (20,29). Thus, manipulation of the svb expression pattern can, on its own, generate diversity of trichome patterns.…”

“…Thus, manipulation of the svb expression pattern can, on its own, generate diversity of trichome patterns. It is not clear that any other single gene can cause such a specific morphological change without disrupting other aspects of larval development (29). svb expression is regulated by a large number of signaling pathways and transcription factors, and manipulations of these factors can alter trichome patterns (30).…”

The structure and evolution ofcis-regulatory regions: theshavenbabystory

“…The embryonic expression pattern of svb is generated by the integration of many signalling pathways (Wnt, EFG-r, Hedgehog and Notch; [15]). In turn, Svb regulates directly or indirectly dozens of genes that participate in trichome morphogenesis [16,17], a complex cellular processes that involves the actin cytoskeleton [16]. The regulatory network governing trichome development thus resembles an 'hourglass' [11,18], with svb occupying a bottleneck, or master control position, in the flow of regulatory information.…”

The flare Gene, Which Encodes the AIP1 Protein of Drosophila, Functions to Regulate F-Actin Disassembly in Pupal Epidermal Cells

“…The activity of the fz-based planar/tissue polarity system restricts hair initiation to the distal-most part of the apical surface of cells (Wong and Adler 1993). Temporal control of hair initiation is likely to involve the turn on of expression of shavenoid/kojak (He and Adler 2002;Ren et al 2006), perhaps due to its expression being regulated by the shavenbaby and/or grainy head transcription factors (Lee and Adler 2004;Chanut-Delalande et al 2006). The planar cell polarity (PCP) proteins are known to become restricted to the proximal and distal sides of cells and it is generally believed that feedback interactions between these proteins lead to the formation of these two protein domains (Tree et al 2002;Amonlirdviman et al 2005).…”