What Do Genic Mutations Tell Us about the Structural Patterning of a Complex Single-Celled Organism?

Abstract

PROLOGUE: FROM THE CYTOPLASM TO THE NUCLEUSStructural inheritance in the ciliate cortex. Ciliates make up a distinctive group of unicellular organisms characterized by dualism of germ line and somatic nuclei, sex by reciprocal exchange of gametic nuclei with subsequent replacement of the somatic nucleus, and an extraordinarily complex organization of the cell surface layer. This organization is dominated by cytoskeletal structures, including rows of basal bodies, cilia, and accessory fibrillar structures, and is perpetuated by longitudinal extension of these structural ensembles during clonal growth.This mode of perpetuation provides an ideal opportunity for the demonstration and analysis of cellular heredity at a nongenic level. This opportunity was seized by three gifted biologists, the comparative zoologist Emmanuel Fauré-Fremiet, the experimental embryologist Vance Tartar, and the geneticist Tracy Sonneborn, who together led the way in establishing the principle that structural variations of nongenic origin in the ciliate cortex can indeed be faithfully transmitted to progeny over numerous cell generations.Although this review is primarily devoted to the contribution of genic mutations to the understanding of the ciliate cortex, the interpretation of some of the more interesting of these mutations becomes more meaningful against a background of the three major arenas of nongenic structural inheritance in the ciliate cortex, all of which were solidly established before the genetic approach was initiated.The best-known form of structural inheritance is the organization of the longitudinal ciliary rows that cover the surfaces of most ciliates. This was first demonstrated by Beisson and Sonneborn (12), who showed that an inversion (180°rotation) of one or more ciliary rows of Paramecium tetraurelia (then Paramecium aurelia, syngen 4) (Fig. 1A) could be nongenically inherited; Sonneborn gave the name "cytotaxis" to "this ordering and arranging of new structures under the influence of pre-existing cell structure" (137). This demonstration was later repeated for Tetrahymena thermophila (then Tetrahymena pyriformis, syngen 1) (118) and for other ciliates (62,63,71). It was extended by Nanney's observation that the preexisting number of ciliary rows in T. thermophila tended to be conserved (103, 104), presumably due to the same structural constraints that conserve the geometrical organization of these rows.A second form of structural inheritance is demonstrated by the propagation of the number of complete sets of cortical structures. This was investigated in detail by 32), who noted that ciliates that became fused side by side, as a consequence of blockage of division followed by anterior sliding of the presumptive posterior daughter cell, could propagate their duality. Later, Vance Tartar (147) demonstrated that microsurgically constructed Siamese-twin doublets in the large ciliate Stentor coeruleus could perpetuate their doublet condition. In both cases, the way in which the doublets were created virtually rules o...

Sfr1, a Tetrahymena thermophila Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies

“…The observed overproduction of basal bodies upon the loss of Sfr1 was rescued by reintroducing Sfr1 under the control of an inducible promoter, thus revealing a direct role for Sfr1 in the modulation of basal body production along cortical rows. Tetrahymena cells are strikingly capable of maintaining a nearly constant number of cortical row basal bodies by adjusting basal body density relative to the number of cortical rows (52, 54–58). Basal body number constancy has been shown to be regulated on the basis of the cellular corticotype (the number of cortical rows).…”

Mob1: defining cell polarity for proper cell division

“…In fact, the presence of cortical gradients in Tetrahymena was previously postulated based on the spatial patterns of basal body proliferation that precede cleavage furrow constriction (Kaczanowski, 1978;Kaczanowska et al, 1999). In addition, studies of structural pattern mutants (Frankel, 2008) and on fenestrin localization below the fission line and accumulating at the anterior region in dividing cells (Nelsen et al, 1994;Cole et al, 2008) indicate the existence of an asymmetry in the cleavage furrow region.…”

“…1C,D) or abolished (Fig. 1E), suggesting that the new oral apparatus was either assembled at a wrong place or had migrated towards the old oral apparatus during the elongation process (Frankel, 2008). The oral apparatus being an anterior polarity landmark in Tetrahymena, the occurrence of these Mob1-KD phenotypes suggested that these cells possess altered polarity, which compromised the correct definition of the division plane.…”

The cytoplasmic structure hypothesis for ribosome assembly, vertical inheritance, and phylogeny

“…Cellular descendents inherit the new orientation of cilia. Bornens (32) and Frankel (36) have written valuable recent reviews of this remarkable process.…”