Centrioles are conserved, self-replicating, microtubule-based 9-fold symmetric subcellular organelles that are essential for proper cell division and functions. Most cells have two centrioles and maintaining this number of centrioles is important for animal development. However, how animals gain their first two centrioles during reproduction is only partially understood. It is well established that in most animals, the centrioles are contributed to the zygote by the sperm. However, in humans, insects, and many other animals, the sperm centrioles are modified in their structure and protein composition, or they appear to be missing altogether. In these animals, the origin of the first centrioles is not clear.
We have discovered that Drosophila melanogaster sperm has a novel and atypical second centriolar structure that we named the proximal centriole-like structure (PCL). The PCL contains centriolar proteins but lacks microtubules and has a structure distinct from a typical centriole. Nevertheless, the PCL functions analogously to a centriole in the zygote; after fertilization, it recruits PCM, forms astral microtubules and found in one of the spindle pole, and provides a platform for the formation of a new centriole. Therefore, our data suggests that insect sperm provides two centrioles and suggest a universal mechanism of centriole inheritance among animals that include atypical centrioles.
We have also discovered that both the typical and atypical centrioles of Drosophila melanogaster sperm centrioles are remodeled during spermiogenesis. The ultrastructure and protein composition of the two centrioles is modified during spermiogenesis, resulting with two atypical centrioles in the spermatozoa. Paternal protein mutants that regulate this remodeling affect the resulting embryo. Altogether, our findings demonstrate that atypical paternal centrioles play a role in pre- and post-fertilization to ensure embryogenesis.