Electron-opaque annular structure girdling the constricting isthmus of the dividing chloroplasts ofHeterosigma akashiwo (Raphidophyceae, Chromophyta)

Abstract

Summary.The plastokinesis (kinesis of chloroplasts) of a raphidophyte alga, Heterosigma akashiwo, was studied by electron microscopy using rapid freezing and freeze-substitution techniques. The chloroplasts are enveloped by two pairs of tightly appressed double membranes, the inner and the cytoplasmic outer pair. The inner pair constricts to divide in advance of the outer pair. By observation of serial sections an electron-opaque, annular structure (plastid-dividing ring) was observed at the isthmus of constricting chloroplasts, girdling the periplastidal outer surlhce of the inner pair of the four surrounding membranes. These observations suggest that the mechanisms underlying the constriction of the inner and outer pair may differ from each other. The localization of the annular structure (plastid-dividing ring) suggests that the inner pair of the surrounding membranes may be homologous to the double envelope membranes of the chloroplasts of Chlorophyta and Rhodophyta. In addition these findings provide a new evidence supporting the secondary endosymbiosis hypothesis for the origin of the chloroplasts in chromophyte algae.

Mechanism of Plastid Division: From a Bacterium to an Organelle

“…The outermost membrane is connected with the outer nuclear envelope directly or indirectly through rough endoplasmic reticulum. In certain lineages of the stramenopiles, the filamentous outer PD ring has been observed at the cytosolic surface of the second innermost membrane (Hashimoto, 1998(Hashimoto, , 2005Weatherill et al, 2007). The genome of the nucleomorph, a remnant of the engulfed red algal nucleus in cryptophytes, encodes an FtsZ protein (Fraunholz et al, 1998).…”

“…In certain lineages, the outer pair of membranes divides in the same plane as the inner pair, but the constriction of the outer pair takes place behind that of the inner pair. In addition, spherical vesicles have been observed in the space between the two pairs of membranes (called the periplastid compartment) at the division site (Hashimoto, 1998(Hashimoto, , 2005. In rare cases, such as in Synchroma, the division of the inner and the outer pair is not coupled.…”

Orderly formation of the double ring structures for plastid and mitochondrial division in the unicellular red alga Cyanidioschyzon merolae

“…Subsequently, Hashimoto (1986) revealed that in Avena sativa the PD ring is composed of concentric double rings (PD ring doublet): an outer ring present on the cytoplasmic face of the outer envelope membrane, and an inner ring present on the stromal face of the inner envelope membrane. A PD ring or PD ring doublet has been detected in a variety of terrestrial plants (Hashimoto 1986;Tewinkel and Volkmann 1987;Hashimoto and Possingham 1989;Oross and Possingham 1989;Duckett and Ligrone 1993a,b) and algae (Mita et al 1986;Mita and Kuroiwa 1988;Chida and Ueda 1991;Kuroiwa et al 1993;Hashimoto 1997) and is believed to be ubiquitous in plants (for reviews, see Kuroiwa 1991;Kuroiwa et al 1998). In all plants except for the primitive red algae C. caldarium and Cyanidioschyzon merolae (Kuroiwa et al 1993), and the primitive green alga Nannochloris bacillaris (Ogawa et al 1995), PD rings are only detected in the late phase of plastid division.…”

The timing and manner of disassembly of the apparatuses for chloroplast and mitochondrial division in the red alga Cyanidioschyzon merolae

“…A few earlier studies reported structures in the constriction zone of chloroplasts (Suzuki and Ueda 1975;Chaly and Possingham 1981;Leech et al 1981) but, as described elsewhere in detail (Kuroiwa 1989), their interpretations of the ultrastructure and location were inaccurate. The PD ring has been detected in several species of Chlorophyta (green algae and terrestrial plants) (Hashimoto 1986;Tewinkel and Volkmann 1987;Hashimoto and Possingham 1989;Oross and Possingham 1989;Chida and Ueda 1991;Duckett and Ligrone 1993a, b;Ogawa et al 1995;Robertson et al 1996), Rhodophyta (Mita et al 1986;Suzuki et al 1994) and Chromophyta (Hashimoto 1997;Beech and Gilson 2000), and is thought to be ubiquitous in the plant kingdom (summarized in Kuroiwa et al 1998). The PD ring is formed by the nuclear genome (Hashimoto and Possingham 1989) and consists of three rings, one on the cytosolic face of the outer envelope (outer ring), one on the stromal face of the inner envelope (inner ring) (Hashimoto 1986) and one in the inter-membrane space (middle ring) (Miyagishima et al 1998b).…”