The Drosophila orb gene is predicted to encode sex-specific germline RNA-binding proteins and has localized transcripts in ovaries and early embryos

Abstract

We report the identification of a new gene, orb, which appears to be expressed only in the germline and encodes ovarian- and testis-specific transcripts. The predicted proteins contain two regions with similarity to the RRM family of RNA-binding proteins but differ at their amino termini. In testes, orb RNA accumulates in the primary spermatocytes and at the caudal ends of the spermatid bundles. In ovaries, orb transcripts display an unusual spatial pattern of accumulation in the oocyte. Preferential accumulation in the oocyte of orb RNA is first detected in region 2 of the germarium and is dependent on Bicaudal-D and egalitarian. While in stage 7 egg chambers orb RNA is localized posteriorly in the oocyte, during stages 8–10 it is localized at the anterior of the oocyte, asymmetrically along the dorsal-ventral axis. In embryos the transcripts accumulate at the posterior end and are included in the pole cells. This pattern of localization and the similarity to RNA-binding proteins suggest that the orb gene product may mediate the localization of maternal RNAs during oogenesis and early embryogenesis.

Orb-dependent polyadenylation contributes to PLP expression and centrosome scaffold assembly

“…Drosophila encodes two CPEB proteins, oo18 RNA-binding protein (Orb) and Orb2 (Lantz et al, 1992;Hafer et al, 2011). While Orb2 functions are best defined in the testis and central nervous system (Keleman et al, 2007;Mastushita-Sakai et al, 2010;Hafer et al, 2011;Xu et al, 2012), Orb regulates RNA localization and translation during oogenesis and early embryogenesis (Lantz et al, 1992;Christerson and McKearin, 1994;Chang et al, 2001;Castagnetti and Ephrussi, 2003;Rojas-Ríos et al, 2015).…”

“…Drosophila encodes two CPEB proteins, oo18 RNA-binding protein (Orb) and Orb2 (Lantz et al, 1992;Hafer et al, 2011). While Orb2 functions are best defined in the testis and central nervous system (Keleman et al, 2007;Mastushita-Sakai et al, 2010;Hafer et al, 2011;Xu et al, 2012), Orb regulates RNA localization and translation during oogenesis and early embryogenesis (Lantz et al, 1992;Christerson and McKearin, 1994;Chang et al, 2001;Castagnetti and Ephrussi, 2003;Rojas-Ríos et al, 2015). Orb is orthologous to mammalian CPEB1 and similarly promotes polyadenylation to regulate the stability and translation of its target mRNAs, including oskar (osk), gurken (grk), and Autophagy-related 12 (Atg12) mRNAs (Christerson and McKearin, 1994;Chang et al, 1999;Chang et al, 2001;Castagnetti and Ephrussi, 2003;Norvell et al, 2015;Rojas-Ríos et al, 2015;Davidson et al, 2016).…”

Quantitative models for building and growing fated small cell networks

“…Perhaps the most obvious of these is cytoplasmic, characterized by the accumulation of several specific mRNAs and proteins in one of the two cells with four ring canals (the pro-oocytes)-presumably the future oocyte. Examples of such mRNAs include orb, egalitarian (egl) and BicaudalD (BicD), which are initially uniformly distributed throughout the cyst before progressively localizing to one cell [178,179]. Nuclear asymmetries also arise: the synaptonemal complex that underlies the beginning of meiosis first appears in the pro-oocytes in early region 2 of the germarium, spreads to the two cells with three ring canals, and is finally restricted to one of the two cells with four ring canals towards the end of region 2 [180][181][182][183] (figure 1b,d).…”

“…Orb is among the earliest cytoplasmic markers for oocyte identity: in the early regions of the germarium, orb mRNA is expressed uniformly in low amounts in all cells of the cyst, yet as the cyst progresses through the germarium, orb mRNA is gradually restricted to the pro-oocytes, and finally to the presumptive oocyte [35,191]. Egg chambers with strong loss-of-function orb alleles form 16-cell cysts but fail to specify an oocyte, while orb nulls fail to form a 16-cell cyst at all [178]. Furthermore, Orb's regulatory targets include the mRNAs of BicD, Egl and Cup-proteins with key roles in oocyte specification [191][192][193].…”

The careful control of Polo kinase by APC/C-Ube2C ensures the intercellular transport of germline centrosomes during Drosophila oogenesis

“…During this process, germline centrosomes of the 16 cystocytes exhibit a very peculiar behaviour: virtually, all the 32 centrosomes intercellularly migrate within the cyst to eventually accumulate in one cell, the future oocyte [7]. This migration coincides with the events that mark the specification of the oocyte: the concentration of fate determinants such as Bicaudal-D (BicD), Egalitarian (Egl) and Oo18 RNA-binding protein (Orb) [10][11][12][13], and the restriction of synaptonemal complexes to the oocyte [14]. These observations suggest potential involvement of germline centrosomes in the specification and/ or the subsequent differentiation of the oocyte [6].…”