Differential and redundant functions of gooseberry and gooseberry neuro in the central nervous system and segmentation of the Drosophila embryo

Abstract

The gooseberry locus of Drosophila consists of two homologous Pax genes, gooseberry neuro (gsbn) and gooseberry (gsb). Originally characterized by genetics as a single segment-polarity gene, its role in segmentation has been enigmatic, as only deficiencies uncovering both genes showed a strong segmentation phenotype while mutants of gsb did not. To solve this conundrum and assay for differential roles of gsbn and gsb, we have obtained by homologous recombination for the first time null mutants of either gene as well as a deficiency inactivating only gsbn and gsb. Our analysis shows that (i) gsbn null mutants are subviable while all surviving males and most females are sterile; (ii) gsb and gsbn share overlapping functions in segmentation and the CNS, in which gsbn largely, but not completely depends on the transcriptional activation by the product of gsb; (iii) as a consequence, in the absence of gsbn, gsb becomes haploinsufficient for its function in the CNS, and gsbn(-/-)gsb(-/+) mutants die as larvae. Such mutants display defects in the proper specification of the SNa branch of the segmental nerve, which appears intact in gsbn(-/-) mutants. Lineage analysis in the embryonic CNS showed that gsbn is expressed in the entire lineage derived from NB5-4, which generates 4 or 5 motoneurons whose axons are part of the SNa branch and all of which except one also express BarH1. Analysis of gsbn(-/-)gsb(-/+) clones originating from NB5-4 further suggests that gsb and gsbn specify the SNa fate and concomitantly repress the SNc fate in this lineage and that their products activate BarH1 transcription. Specification of the SNa fate by Gsb and Gsbn occurs mainly at the NB and GMC stage. However, the SNa mutant phenotype can be rescued by providing Gsbn as late as at the postmitotic stage. The hierarchical relationship between gsb and gsbn, the haploinsufficiency of gsb in gsbn mutants, and their redundant roles in the epidermis and CNS are discussed. A model is proposed how selection for both genes occurred after their duplication during evolution.

Bridging the gap between postembryonic cell lineages and identified embryonic neuroblasts in the ventral nerve cord ofDrosophila melanogaster

“…The secondary neurons match lineage 20/22 which are indistinguishable by their morphology ( Truman et al, 2004 ). Both postembryonic lineages express Gsb ( Li et al, 2014 ) and BarH1 ( Lacin et al, 2014b ), which fits the embryonic expression of the NB5-4 clone ( He and Noll, 2013 ). Moreover, they share a high degree of CRMs ( Li et al, 2014 ).…”

Transcription factor expression uniquely identifies most postembryonic neuronal lineages in the Drosophila thoracic central nervous system

“…S12B,C). In the embryo, these neurons derive from NB 5-4 (He and Noll, 2013). Thus, we speculate that embryonic NB 5-4 produces either postembryonic lineage 20 or 22.…”

Arthropod segmentation

“…In some cases, these functions have become distributed between multiple paralogues, e.g. prd/gooseberry/gooseberry-neuro in Drosophila (He and Noll, 2013), or the three copies of eve in Strigamia (Green and Akam, 2013). Across species, there can be considerable variation in both the number of paralogues present in the genome and the degree of subfunctionalisation between them, complicating the interpretation of genetic perturbations.…”