CNS midline cells contribute to maintenance of the initial dorsoventral patterning of theDrosophila ventral neuroectoderm

Abstract

Dorsoventral patterning of the Drosophila ventral neuroectoderm is established by the expression of three evolutionarily conserved homeodomain genes: ventral nervous system defective (vnd), intermediate neuroblasts defective (ind), and muscle segment homeobox (msh) in the medial, intermediate, and lateral columns of the ventral neuroectoderm, respectively. It was not clear whether extrinsic factor(s) from the CNS midline cells influence the initial dorsoventral patterning by controlling the expression of the dorsoventral patterning genes. We show here that the CNS midline cells, specified by single-minded (sim), are essential for maintaining expression of the dorsoventral patterning genes. Ectopic expression of sim in the ventral neuroectoderm during the blastoderm stage repressed expression of the three homeodomain genes in the ventral neuroectoderm. This indicates that the identity of the CNS midline cells is established by a series of repressions of the three homeodomain genes in the ventral neuroectoderm. Ectopic expression of sim in the ventral neuroectoderm during initial neurogenesis induced ectopic ind expression in the medial column in addition to that in the intermediate column via EGFR signaling between the ventral neuroectoderm and midline cells. In contrast, it repressed the expression of vnd and msh in the medial and lateral columns, respectively. Our findings demonstrate that the CNS midline cells provide extrinsic positional information via EGFR signaling that maintains the initial subdivision of the ventral neuroectoderm into three dorsoventral columns during initial neurogenesis.

Conserved and novel roles for the Gsh2 transcription factor in primary neurogenesis

“…Similarly, the expression of Xenopus Nkx6.1 and Nkx6.2 is somewhat lower in the most medial cells, which are fated to form the floor plate of the neural tube. In Drosophila, medial exclusion of vnd expression is mediated by the indirect action of the Sim (single-minded) transcription factor (Estes et al, 2001;Kim et al, 2005). Although a sim homologue is expressed during early Xenopus development, expression is broad throughout the CNS, suggesting that this regulatory interaction is not conserved (Coumailleau et al, 2000).…”

Conservation of enhancer location in divergent insects

“…EGF signals pattern the ventral neurogenic ectoderm in Drosophila (18,19). These signals arise from 2 separate sources.…”

Cephalochordata

“…The developing Drosophila CNS has three anterior-posterior columns of neuroblasts. The lateral one expresses Msh , the intermediate one ind , and the medial one vnd (Kim et al 2005 ). This is precisely the same order as in amphioxus and vertebrates if one takes into consideration that the Drosophila CNS is ventral and inverted compared to chordate CNS (Fig.…”

“…( N , R ) and ( P , T ) reprinted from Wu et al ( 2011 )) and extended anteriorly to form the somites, while the notochord cells involuted posteriorly. Other authors have copied Conklin's fate map (Browder et al 1991 ;Khanna 2004 ;Bhatnagar and Bansal 2008 ) (e.g., while some have made minor variations (Gerhart and Kirschner 1997 ;Chea et al 2005 ). Conklin's erroneous fate map also appears prominently on the web ( http://www.biozoomer.…”