The neuroblast timer gene nubbin exhibits functional redundancy with gap genes to regulate segment identity in Tribolium.

Olivia R A Tidswell,Michael Akam,Matthew A Benton

doi:10.1242/dev.199719

Abstract

ABSTRACTThe neuroblast timer genes hunchback, Krüppel, nubbin and castor are expressed in temporal sequence in neural stem cells, and in corresponding spatial sequence along the Drosophila blastoderm. As canonical gap genes, hunchback and Krüppel play a crucial role in insect segmentation, but the roles of nubbin and castor in this process remain ambiguous. We have investigated the expression and functions of nubbin and castor during segmentation in the beetle Tribolium. We show that Tc-hunchback, Tc-Krüppel, Tc-nubbin and Tc-castor are expressed sequentially in the segment addition zone, and that Tc-nubbin regulates segment identity redundantly with two previously described gap/gap-like genes, Tc-giant and Tc-knirps. Simultaneous knockdown of Tc-nubbin, Tc-giant and Tc-knirps results in the formation of ectopic legs on abdominal segments. This homeotic transformation is caused by loss of abdominal Hox gene expression, likely due to expanded Tc-Krüppel expression. Our findings support the theory that the neuroblast timer series was co-opted for use in insect segment patterning, and contribute to our growing understanding of the evolution and function of the gap gene network outside of Drosophila.

Highlights

The gap gene network of Drosophila is arguably one of the best characterised gene regulatory networks in developmental biology
We used hybridisation chain reaction (HCR) RNA in situ hybridisation (ISH) (Choi et al, 2018) to examine the expression patterns of Tc-hb, Tc-Kr, Tc-nub and Tc-cas in Tribolium embryos spanning the stages of segment addition [8-22 h after egg lay (AEL) at 30°C]
We found that these four genes are expressed sequentially in the segment addition zone (SAZ) in largely the same order as they are expressed in neuroblasts, and that this sequential expression results in their being expressed in spatial order along the anterior-to-posterior (AP) axis of the embryonic trunk (Fig. 2)

Summary

Introduction

The gap gene network of Drosophila is arguably one of the best characterised gene regulatory networks in developmental biology. Gap genes mediate two central processes in Drosophila segmentation – the formation of segment boundaries and the assignment of segment identities – through direct regulation of pairrule and Hox genes, respectively (reviewed by Jaeger, 2011). Homologs of many Drosophila gap genes regulate segment patterning in other insect species (Bucher and Klingler, 2004; Cerny et al, 2005; Liu and Kaufman, 2004b; Liu and Patel, 2010; Marques-Souza et al, 2008; Mito et al, 2005, 2006). Recent attention has turned to understanding how gap genes interact and function outside of Drosophila, in order to better.

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