Cooperative Control of Ecdysone Biosynthesis in Drosophila by Transcription Factors Séance, Ouija Board, and Molting Defective

Abstract

Ecdysteroids are steroid hormones that control many aspects of development and physiology. During larval development, ecdysone is synthesized in an endocrine organ called the prothoracic gland through a series of ecdysteroidogenic enzymes encoded by the Halloween genes. The expression of the Halloween genes is highly restricted and dynamic, indicating that their spatiotemporal regulation is mediated by their tight transcriptional control. In this study, we report that three zinc finger-associated domain (ZAD)-C2H2 zinc finger transcription factors—Séance (Séan), Ouija board (Ouib), and Molting defective (Mld)—cooperatively control ecdysone biosynthesis in the fruit fly Drosophila melanogaster. Séan and Ouib act in cooperation with Mld to positively regulate the transcription of neverland and spookier, respectively, two Halloween genes. Remarkably, loss-of-function mutations in séan, ouib, or mld can be rescued by the expression of neverland, spookier, or both, respectively. These results suggest that the three transcription factors have distinct roles in coordinating the expression of just two genes in Drosophila. Given that neverland and spookier are located in constitutive heterochromatin, Séan, Ouib, and Mld represent the first example of a transcription factor subset that regulates genes located in constitutive heterochromatin.

Innovation of heterochromatin functions drives rapid evolution of essential ZAD-ZNF genes in Drosophila

“…The Nnk-null larval arrest phenotype is reminiscent of previous findings with the ZAD-ZNF genes Séance, Ouija Board and Molting Defective , which encode proteins necessary for expression of the Spookier and Neverland genes required for ecdysone biosynthesis ( Uryu et al, 2018 ; Neubueser et al, 2005 ; Komura-Kawa et al, 2015 ). Defects in any of the Séance, Ouija Board and Molting Defective ZAD-ZNF genes leads to arrest of larval development and death ( Uryu et al, 2018 ; Neubueser et al, 2005 ; Komura-Kawa et al, 2015 ). However, this lethality can be rescued by supplementing the diet with ecdysone or by overexpression of ecdysone biosynthetic enzymes, bypassing the requirement for these three ZAD-ZNF genes.…”

“…Similarly, ZAD-ZNF gene Grauzone promotes cortex expression and is necessary for meiotic progression during oogenesis ( Chen et al, 2000 ; Harms et al, 2000 ; Page and Orr-Weaver, 1996 ). Finally ZAD-ZNF genes Molting Defective, Ouija Board, and Séance encode proteins that promote the transcription of heterochromatin-embedded genes, Spookier and Neverland, required for larval progression ( Uryu et al, 2018 ). In contrast, other ZAD-ZNF proteins repress rather than drive transcription.…”

Snail synchronizes endocycling in a TOR-dependent manner to coordinate entry and escape from endoreplication pausing during the Drosophila critical weight checkpoint

“…Several zinc finger transcription factors have been shown to specifically regulate the expression of single or a group of ecdysone biosynthetic genes in the PG [78][79][80]. Further studies are required to assess whether Snail directly controls the transcription of any of the six major ecdysone biosynthetic genes.…”

Effects of lipopolysaccharide and juvenile hormone III treatments on cell growth and gene expression in the Ceratitis capitata (Diptera: Tephritidae) CCE/CC128 cell line

“…JHIII may possibly also generate a positive response in ecdysone synthesis to ensure normal growth and the survival of the embryonic cell culture. However, the ecdysone biosynthetic pathways are quite complex and not completely understood (Ou et al, ; Uryu et al, ). They involve many tissues and enzymes, and therefore, this information regarding Shade expression may contribute to clarifying the role of this gene in the C. capitata cell line.…”