Atypical centrioles are present in Tribolium sperm

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.

Rapid Evolution of Sperm Produces Diverse Centriole Structures that Reveal the Most Rudimentary Structure Needed for Function

“…Since centrioles do not normally have central microtubules, it was later proposed that the base of the axoneme of Tribolium is not an axoneme, but rather a centriole. This hypothesis was confirmed when it was shown that the base of the axoneme contains the centriole specific protein Ana1 [ 10 ].…”

“…Such minimal centrioles were recently identified in the spermatozoon of insects and non-rodent mammals ( Figure 3 ) [ 9 , 10 , 11 , 12 ]. These centrioles are smaller, have reduced protein composition, and have either no microtubules or have microtubules that lack nine-fold symmetry.…”

“…However, multiple groups of animals evolved a sperm neck with one or no typical centrioles ( Figure 1 and Figure 2 a). Recent studies suggest that some of the species that were thought to have only one centriole actually have a second centriole with an atypical structure (atypical centriole) ( Figure 3 ) [ 9 , 10 , 11 , 12 ]. In this manuscript, we will describe centriole evolution by focusing on sperm that has one typical centriole and one atypical centriole.…”

“…This difference caused some investigators to conclude that the Tribolium axoneme has lost the centriole at its base. However, the end of the axoneme base in Tribolium lacks the central pair of microtubules that are necessary for motile axoneme function [ 10 , 32 ]. Since centrioles do not normally have central microtubules, it was later proposed that the base of the axoneme of Tribolium is not an axoneme, but rather a centriole.…”

“…However, recent studies of centriole localization proteins suggest that an atypical proximal centriole (PCL) is present in the spermatid and spermatozoon of Drosophila melanogaster [ 11 ]. Recent detailed electron microscopy studies of two additional insect species identified such a PCL with some structural differences [ 10 , 12 , 42 ].…”