Structural inheritance in Paramecium: ultrastructural evidence for basal body and associated rootlets polarity transmission through binary fission^⋆

Abstract

One main difference between basal bodies and centrioles resides in the expression of their polarity: centrioles display a structural nine-fold radial symmetry, whereas basal bodies express a circumferential polarity, thanks to their asymmetric set of rootlets. The origin of this polarity during organelle duplication still remains under debate: is it intrinsic to the nine-fold structure itself (i.e. the nine microtubular triplets are not equivalent) or imposed by its immediate environment at time of assembly? We have reinvestigated this problem using the Ciliate Paramecium, in which the pattern of basal body duplication is well known. In this cell, all basal bodies produced within ciliary rows appear immediately anterior to parental ones. Observations on cells fixed with the tannic acid protocol suggest that, to be competent for basal body assembly, parental basal bodies have to be individually associated with a complete set of rootlets (monokinetid structure). During pro-basal body assembly, full microtubular triplets were detected according to a random circumferential sequence; during the whole process, the new basal body and its associated rootlets maintained structural relations with the parental monokinetid structure by way of specific links. These results strongly suggest that basal body and associated rootlets (kinetid) polarity is driven by its immediate environment and provide a basis for the structural heredity property observed by Sonneborn some decades ago.

Choosing sides – asymmetric centriole and basal body assembly

“…Mother centrioles instruct the positioning of new basal bodies, the nucleus, and polarized structures within Chlamydomonas cells (Holmes and Dutcher, 1989;Feldman et al, 2007). Similar to algal systems, new basal body assembly in ciliates follows a fixed profile for positioning new basal bodies (Beisson, 2008;Dippell, 1968;Iftode and Fleury-Aubusson, 2003;Wloga and Frankel, 2012).…”

“…In Paramecium and other ciliates, nascent basal bodies form anteriorly and adjacent to preexisting mother basal bodies whose polarized appendage structures define the basal body assembly site (Fig. 2) (Beisson and Jerka-Dziadosz, 1999;Iftode and Fleury-Aubusson, 2003;Kirschner et al, 2000;). The position of new ciliary units is dictated by the local architecture of the parental ciliary unit from which each new cilium develops.…”

“…In Tetrahymena this is the kinetodesmal fiber, in Paramecium the striated rootlet, and in Chlamydomonas the striated microtubuleassociated fiber (Fig. 2) (Allen, 1969;Holmes and Dutcher, 1989;Iftode and Fleury-Aubusson, 2003;Jerka-Dziadosz et al, 1995;Lechtreck and Melkonian, 1991;Munn, 1970;Sperling et al, 1991). Striated fibers extend from a defined triplet microtubule site on the basal body at the base of mature basal bodies and, as their name suggests, are composed of fibers with striations of ,30-nm periodicity.…”

“…It has been suggested that, in Paramecium, the striated fibers are important for basal body triplet microtubule assembly mainly based on three observations (Iftode and Fleury-Aubusson, 2003). First, new basal body assembly occurs in the immediate proximity of striated fibers (Allen, 1969;Iftode and FleuryAubusson, 2003;Lechtreck and Grunow, 1999).…”

“…Second, ctubulin is required for basal body assembly and associates with both basal bodies and striated fibers (Ruiz et al, 1999;Shang et al, 2002). Third, triplet microtubules adjacent to the striated fiber are longer and more mature compared with those distal to the striated fiber (Iftode and Fleury-Aubusson, 2003). However, it remains to be determined how exactly the striated fiber promotes the assembly of basal body microtubules.…”