The ecdysone receptor and ultraspiracle regulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis

Abstract

Ecdysteroids regulate insect metamorphosis through the edysone receptor complex, a heterodimeric nuclear receptor consisting of the ecdysone receptor (EcR) and its partner ultraspiracle (USP). Differentiation in the Drosophila ovary at metamorphosis correlates with colocalization of USP and the EcR-A isoform in all but one of eight mesoderm-derived somatic cell types. The one exception is the larval terminal filament (TF) cells, in which only USP is detectable during cell differentiation. In cells destined to form the basal stalks and anterior oviduct, USP colocalizes with what appears to be the EcR-B2 isoform. Flies heterozygous for a deletion of the EcR gene exhibit several defects in ovarian morphogenesis, including a heterochronic delay in the onset of terminal filament differentiation. Flies heterozygous for a strong usp allele exhibit accelerated TF differentiation. Flies simultaneously heterozygous for both EcR and usp have additional phenotypes, including several heterochronic shifts, delayed initiation and completion of terminal filament morphogenesis and delayed ovarian differentiation during the first day of metamorphosis. Terminal filament morphogenesis is severely disrupted in homozygous usp clones. Our results demonstrate that proper expression of the ecdysone receptor complex is required to maintain the normal progression and timing of the events of ovarian differentiation in Drosophila. These findings are discussed in the context of a developmental and evolutionary role for the ecdysone receptor complex in regulating the timing of ovarian differentiation in dipteran insects.

Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus. I. Ovary morphogenesis, amplification of viral DNA and ecdysteroid titres

“…However, the titre data shown here do not support this hypothesis, since at stage 3b, when excised viral DNA first appears, 20E has already decreased and continues to drop, whereas polydnavirus replication is most intense up to stage 6. The level of 20E is highest when the reproductive tract is in a phase of intensive cell proliferation and differentiation, which suggests a role in early ovarian morphogenesis, as has been reported for Drosophila (Audit-Lamour & Busson, 1981;Hodin & Riddiford, 1998). Furthermore, ecdysteroid titres were also highest shortly after pupation in pupae of an ichneumonid ectoparasitoid, which does not harbour polydnaviruses (Gelman et al, 2000).…”

Activin signaling balances proliferation and differentiation of ovarian niche precursors and enables adjustment of niche numbers

“…This corroborates a previous pulse-chase study that indicated a first wave of proliferation at 68-72 h AEL, in which BrdU-retaining somatic cells contributed ∼50% of all TF cells throughout the larval ovary. A second wave of proliferation during third instar occurred gradually and resulted in labeled TF cells that appeared from the medial to the lateral side of the ovary (SahutBarnola et al, 1996), matching the topology of mature filament appearance (Gancz et al, 2011;Godt and Laski, 1995;Hodin and Riddiford, 1998;Sahut-Barnola et al, 1996.…”

“…Ecdysone is another hormonal cue that promotes TF formation (Gancz and Gilboa, 2013a;Gancz et al, 2011;Hodin and Riddiford, 1998;Konig et al, 2011). At early larval stages, ecdysone receptors act as repressors of TF differentiation, whereas in the second part of the third instar they become activators of TF differentiation.…”

Insulin and Target of rapamycin signaling orchestrate the development of ovarian niche-stem cell units in Drosophila

“…The first is Epidermal growth factor (EGF), which coordinates PGC proliferation rates with intermingled cell (IC) numbers in the ovary (Gilboa and Lehmann, 2006). The second is ecdysone, which initiates both somatic niches and PGC differentiation (Gancz et al, 2011;Hodin and Riddiford, 1998).…”