A Proximal Centriole-Like Structure Is Present in Drosophila Spermatids and Can Serve as a Model to Study Centriole Duplication

Abstract

Most animals have two centrioles in spermatids (the distal and proximal centrioles), but insect spermatids seem to contain only one centriole (Fuller 1993), which functionally resembles the distal centriole. Using fluorescent centriolar markers, we identified a structure near the fly distal centriole that is reminiscent of a proximal centriole (i.e., proximal centriole-like, or PCL). We show that the PCL exhibits several features of daughter centrioles. First, a single PCL forms near the proximal segment of the older centriole. Second, the centriolar proteins SAS-6, Ana1, and Bld10p/Cep135 are in the PCL. Third, PCL formation depends on SAK/PLK4 and SAS-6. Using a genetic screen for PCL defect, we identified a mutation in the gene encoding the conserved centriolar protein POC1, which is part of the daughter centriole initiation site (Kilburn et al. 2007) in Tetrahymena. We conclude that the PCL resembles an early intermediate structure of a forming centriole, which may explain why no typical centriolar structure is observed under electron microscopy. We propose that, during the evolution of insects, the proximal centriole was simplified by eliminating the later steps in centriole assembly. The PCL may provide a unique model to study early steps of centriole formation.

The Y Chromosome Modulates Splicing and Sex-Biased Intron Retention Rates in Drosophila

“…As expected, Piwi expression is higher in ovary and matched by a lower rate of retention of the forth intron, whereas Piwi expression is lower in testis and accompanied by a much higher IR rate. We also observed that some other interesting genes important for oogenesis such as Medea (XIE AND SPRADLING 1998) and Tho2 (JAGUT et al 2013) had lower IR rates and higher abundance in the ovary; conversely, genes important for spermatogenesis such as Boule (CASTRILLON et al 1993) and ana1 (BLACHON et al 2009) had lower IR rates and higher abundance in the testis. Hence, IR negatively impacts the abundance of transcripts in one of the sexes and contributes to sexbiased gene expression.…”

DrosophilaCep135/Bld10 maintains proper centriole structure but is dispensable for cartwheel formation

“…In Chlamydomonas and Paramecium the centriolar protein Bld10 (Cep135 in vertebrates) is essential for cartwheel formation, and so for centriole duplication (Hiraki et al, 2007;Jerka-Dziadosz et al, 2010); Cep135 also appears to be required for efficient centriole duplication in human and Drosophila cells in culture (Dobbelaere et al, 2008;Kleylein-Sohn et al, 2007). Surprisingly, flies that lack detectable Cep135/Bld10 are viable and exhibit only mild centriole defects (Blachon et al, 2009;Carvalho-Santos et al, 2010;Mottier-Pavie and Megraw, 2009). Centriole duplication and centrosome formation appeared unperturbed, and mutant flies were not uncoordinated, indicating that the sensory cilia in the type I sensory neurons (the only ciliated cells in the adult fly) were functional.…”

Drosophila Hook-Related Protein (Girdin) Is Essential for Sensory Dendrite Formation

“…Furthermore, we observed that the dendritic sheath, which did not contain a sensory cilium with the tubular body, displayed dramatic defects ( Figure 1I). This phenotype is distinct from that observed in centriole or cilium mutants, which have inner segments but fail to form the centrioles and the cilium (Avidor-Reiss et al 2004;Blachon et al 2008Blachon et al , 2009. The absence of the tubular body in mecA 101 is unlikely due to defects in tubular body formation itself since DCX-EMAP mutant flies that cause specific defects in tubular body formation show no other anatomical defects (Bechstedt et al 2010).…”

“…UAS-GFP-a1-tubulin84B line was provided by A. Spradling (Grieder et al 2000). Ana1-tdtomato was previously described (Blachon et al 2008(Blachon et al , 2009). …”

“…The cilium at the tip of a mechanosensory dendrite is formed using the typical protein machinery essential for ciliogenesis including centriolar, connecting cilium, and IFT proteins (Avidor-Reiss et al 2004;Martinez-Campos et al 2004;Rodrigues-Martins et al 2007;Blachon et al 2008Blachon et al , 2009Basiri et al 2014). The tip of the mechanosensory cilium associates with two cuticular structures: the bristle and the socket ( Figure 1A), each of which is formed by a unique support cell.…”