Abstract

During animal development, accurate control of tissue specification and growth are critical to generate organisms of reproducible shape and size. The eye-antennal disc epithelium of Drosophila is a powerful model system to identify the signaling pathway and transcription factors that mediate and coordinate these processes. We show here that the Yorkie (Yki) pathway plays a major role in tissue specification within the developing fly eye disc epithelium at a time when organ primordia and regional identity domains are specified. RNAi-mediated inactivation of Yki, or its partner Scalloped (Sd), or increased activity of the upstream negative regulators of Yki cause a dramatic reorganization of the eye disc fate map leading to specification of the entire disc epithelium into retina. On the contrary, constitutive expression of Yki suppresses eye formation in a Sd-dependent fashion. We also show that knockdown of the transcription factor Homothorax (Hth), known to partner Yki in some developmental contexts, also induces an ectopic retina domain, that Yki and Scalloped regulate Hth expression, and that the gain-of-function activity of Yki is partially dependent on Hth. Our results support a critical role for Yki- and its partners Sd and Hth - in shaping the fate map of the eye epithelium independently of its universal role as a regulator of proliferation and survival.

Highlights

  • Animal body size and shape is genetically determined by evolutionarily conserved signaling pathways that control patterning and growth

  • We propose that these activities reflect a function of the Hpo/Yki pathway in tissue specification that is distinct from its activity in regulating tissue growth and survival, and that partner-specificity, in addition to Yki activity levels, contributes in a significant way to the differential activity of Yki in specification versus proliferation in different regions of the eye disc

  • In the course of an RNAi-based genetic screen [Zhang & Pignoni, unpublished] to identify early players in the patterning and development of the fly eye, we discovered that the disc-wide knock-down of Yki or its partner Sd induced a dramatic reorganization of the eye-disc fate map

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Summary

Introduction

Animal body size and shape is genetically determined by evolutionarily conserved signaling pathways that control patterning and growth. The activity of these pathways is integrated to produce organisms of similar dimensions and body pattern for a given biological species. How different signaling pathways contribute to these processes is intensely studied in the imaginal discs of Drosophila, including the eye-antennal disc epithelium. There is significant overlap in the control of tissue specification and growth within the larval eye epithelium, a primary role can be ascribed to most signaling pathways such that they contribute in a predominant fashion to either patterning or proliferation. Changes in the level or distribution of the secreted morphogen Decapentaplegic (Dpp), a BMP 2/4 type factor, affects proliferation within the disc. The most striking effect of changes in Dpp expression is on the early fate map with dramatic changes in the location, size, and even ectopic gain of organ primordial [2,3,4,5]

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