Centrosome Remodelling in Evolution.

Daisuke Ito,Mónica Bettencourt-Dias

doi:10.3390/cells7070071

Abstract

The centrosome is the major microtubule organizing centre (MTOC) in animal cells. The canonical centrosome is composed of two centrioles surrounded by a pericentriolar matrix (PCM). In contrast, yeasts and amoebozoa have lost centrioles and possess acentriolar centrosomes—called the spindle pole body (SPB) and the nucleus-associated body (NAB), respectively. Despite the difference in their structures, centriolar centrosomes and SPBs not only share components but also common biogenesis regulators. In this review, we focus on the SPB and speculate how its structures evolved from the ancestral centrosome. Phylogenetic distribution of molecular components suggests that yeasts gained specific SPB components upon loss of centrioles but maintained PCM components associated with the structure. It is possible that the PCM structure remained even after centrosome remodelling due to its indispensable function to nucleate microtubules. We propose that the yeast SPB has been formed by a step-wise process; (1) an SPB-like precursor structure appeared on the ancestral centriolar centrosome; (2) it interacted with the PCM and the nuclear envelope; and (3) it replaced the roles of centrioles. Acentriolar centrosomes should continue to be a great model to understand how centrosomes evolved and how centrosome biogenesis is regulated.

Highlights

In 1887, the German biologist Theodor Boveri first described and named the structure at the pole of a mitotic spindle as “centrosome” [1]
Has been formed by a step-wise process; (1) an spindle pole body (SPB)-like precursor structure appeared on the ancestral centriolar centrosome; (2) it interacted with the pericentriolar matrix (PCM) and the nuclear envelope; and (3) it replaced the roles of centrioles
To better understand centrosome evolution in animal and fungi, we analysed the conservation of the molecular components of the centrosome, searching for orthologues of the known human centrosome proteins required for centriole assembly (SAS-6, CPAP, CEP135) and the PCM. ln addition, to understand how the SPB originated, we searched for orthologues of the fission yeast SPB components: the core scaffold proteins

Summary

Introduction

In 1887, the German biologist Theodor Boveri first described and named the structure at the pole of a mitotic spindle as “centrosome” [1]. Fungi and amoebozoa show great structural diversity in their centrosomes, suggesting very distinct remodelling during evolution [6,7] Within these groups, the yeasts and slime moulds have no centriole and possess highly remodelled acentriolar centrosome, the spindle pole body (SPB) and the nucleus-associated body (NAB), respectively [8,9]. It is likely that the common ancestor of animals, fungi and amoebozoa had centrioles to form cilia and a centriole-containing centrosome with a PCM structure and parallel to the loss of centriole, the remodelled acentriolar centrosomes were acquired in some species such as yeasts and D. discoideum.

Common Components in Centrosome

Common Regulations in Centrosome Biogenesis

Common regulators of centrosome biogenesis

How Did the SPB Evolve?

Speculated scenario of of centrosome

Conclusions and Perspective