Abstract
Typical centrioles are made of microtubules organized in ninefold symmetry. Most animal somatic cells have two centrioles for normal cell division and function. These centrioles originate from the zygote, but because the oocyte does not provide any centrioles, it is surprising that the zygotes of many animals are thought to inherit only one centriole from the sperm. Recently, in the sperm of Drosophila melanogaster, we discovered a second centriolar structure, the proximal centriole-like structure (PCL), which functions in the zygote. Whether the sperm of other insects has a second centriolar structure is unknown. Here, we characterized spermiogenesis in the red flour beetle, Tribolium castaneum. Electron microscopy suggests that Tribolium has one microtubule-based centriole at the tip of the axoneme and a structure similar to the PCL, which lacks microtubules and lies in a cytoplasmic invagination of the nucleus. Immunostaining against the orthologue of the centriole/PCL protein, Ana1, also recognizes two centrioles near the nucleus during spermiogenesis: one that is microtubule-based at the tip of the axoneme, suggesting it is the centriole; and another that is more proximal and appears during early spermiogenesis, suggesting it is the PCL. Together, these findings suggest that Tribolium sperm has one microtubule-based centriole and one microtubule-lacking centriole.
Highlights
The centriole is a cellular organelle that is essential for fertilization and embryo development
Our findings suggest that Tribolium sperm has two centriolar structures: the first is an axoneme-attached centriole with nine doublet microtubules that was previously described in many insect studies, and the second is a new type of centriole that lacks microtubules and has a unique structure that is similar, but not identical, to the Drosophila proximal centriole-like structure (PCL)
We examined the centrioles of Tribolium during spermatogenesis and found that Tribolium sperm has two centrioles: (i) as described previously, a centriole made of doublet microtubules instead of triplet microtubules, and (ii) a previously undescribed atypical centriole, the Tribolium PCL, that is made of a 100 nm electron-dense core surrounded by electron-translucent material
Summary
The centriole is a cellular organelle that is essential for fertilization and embryo development (reviewed in [1]). Most somatic cells have a pair of centrioles, each consisting of microtubules arranged in ninefold radial symmetry. The older centriole is known as the mother centriole, and it forms the axoneme (a microtubule-based subcellular skeletal structure) of the cilium (aka flagellum) during interphase. The younger centriole, known as the daughter centriole, matures into a mother centriole in preparation for cell division. The centrioles duplicate (each centriole serves as a platform for the formation of a single new centriole nearby) to have four centrioles, and two are inherited by each daughter cell [2,3,4]. Since two centrioles are required for normal cell division, a fundamental question in reproductive biology is from where the first two centrioles in a zygote arise [5]
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