Centrosome Remodelling in Evolution

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.

Parental centrioles are dispensable for deuterosome formation and function during basal body amplification

“…Centriole biogenesis in cycling cells is tightly controlled . In G1 phase of the cell cycle, each cell contains a centrosome with a pair of parental centrioles: the mother and daughter centrioles.…”

“…Both the older and younger mother centrioles are then allowed to assemble one nascent daughter centriole from a Cep63‐ and Cep152‐containing platform , located around their basolateral walls, by restricting the levels and location of a critical protein kinase Plk4 . Plk4 recruits and phosphorylates Stil, which then recruits SAS6 to initiate centriole biogenesis . The SAS6‐containing cartwheel further primes the assembly of other components such as the centriolar microtubules and Centrin into a procentriole .…”

Dealing with several flagella in the same cell

“…This could be achieved by at least three means, relying on the difference in age and on the particular anatomy of the base of the flagellum (Figure 3a). First, the molecular composition of the pericentriolar matrix, the matrix surrounding basal bodies (Ito & Bettencourt-Dias, 2018), could be different with the one associated to the old flagellum being nonpermissive to tubulin access (Figure 3b).…”

Centrin-anchored hydrodynamic shape changes underpin active nuclear rerouting in branched hyphae of an oomycete pathogen

“…Assembly of a functional mitotic spindle also requires precise coordination between the nuclear cycle and the major microtubule organizing centre, also known as the centrosome (Leo et al, 2012) . A canonical centrosome is composed of two centrioles surrounded by an electron-dense protein-containing matrix 25 (pericentriolar matrix), which nucleates microtubules (Ito and Bettencourt-Dias, 2018) . All fungi except Chytridiomycota possess an acentriolar centrosome termed the spindle pole body (SPB) (Powell, 1980;Ito and Bettencourt-Dias, 2018) .…”

“…A canonical centrosome is composed of two centrioles surrounded by an electron-dense protein-containing matrix 25 (pericentriolar matrix), which nucleates microtubules (Ito and Bettencourt-Dias, 2018) . All fungi except Chytridiomycota possess an acentriolar centrosome termed the spindle pole body (SPB) (Powell, 1980;Ito and Bettencourt-Dias, 2018) . The SPB is embedded in the nuclear envelope and nucleates spindle microtubules inside the nucleus as well as astral microtubules toward the cytoplasmic side (Ito and Bettencourt-Dias, 2018) .…”