Chloroplast Division in Higher Plants Requires Members of Two Functionally Divergent Gene Families with Homology to Bacterial ftsZ

Abstract

The division of plastids is critical for viability in photosynthetic eukaryotes, but the mechanisms associated with this process are still poorly understood. We previously identified a nuclear gene from Arabidopsis encoding a chloroplast-localized homolog of the bacterial cell division protein FtsZ, an essential cytoskeletal component of the prokaryotic cell division apparatus. Here, we report the identification of a second nuclear-encoded FtsZ-type protein from Arabidopsis that does not contain a chloroplast targeting sequence or other obvious sorting signals and is not imported into isolated chloroplasts, which strongly suggests that it is localized in the cytosol. We further demonstrate using antisense technology that inhibiting expression of either Arabidopsis FtsZ gene (AtFtsZ1-1 or AtFtsZ2-1) in transgenic plants reduces the number of chloroplasts in mature leaf cells from 100 to one, indicating that both genes are essential for division of higher plant chloroplasts but that each plays a distinct role in the process. Analysis of currently available plant FtsZ sequences further suggests that two functionally divergent FtsZ gene families encoding differentially localized products participate in chloroplast division. Our results provide evidence that both chloroplastic and cytosolic forms of FtsZ are involved in chloroplast division in higher plants and imply that important differences exist between chloroplasts and prokaryotes with regard to the roles played by FtsZ proteins in the division process.

An Arabidopsis Homolog of the Bacterial Cell Division Inhibitor SulA Is Involved in Plastid Division[W]

“…Three independent T2 lines were analyzed for both AtFtsZ1-1 and AtFtsZ2-1. We observed more or less severe inhibition of plastid division in the transgenic plants, consistent with previous results (Osteryoung et al, 1998;McAndrews et al, 2001). Figure 6 shows control cells (mesophyll, Figure 6A; bundle sheath, Figure 6B) and cells displaying little or no plastid division defects ( Figures 6C, 6G, and 6H) (;55% of the observed plants, Table 2), intermediate phenotypes (15% of the plants), or very severe phenotypes ( Figures 6D, 6E, 6F, 6I, and 6J) (22% of the plants).…”

“…In these experiments, plastid division was more or less severely affected in the different lines. Indeed, ;20% of the plants were similar to the wild type, whereas ;40% could contain as few as a single greatly enlarged plastid in mesophyll cells and ;40% had an intermediate phenotype (Osteryoung et al, 1998;McAndrews et al, 2001). These authors have shown that the severity of plastid division defects correlates with the protein abundance.…”

“…Indeed, the first plastid division proteins to be isolated were homologs of the bacterial division protein FtsZ (Osteryoung et al, 1998). FtsZ is a tubulin-related protein (Erickson, 1997) that polymerizes at midcell, forming a ring that shrinks until division is completed (Rothfield and Justice, 1997).…”

“…FtsZ is a tubulin-related protein (Erickson, 1997) that polymerizes at midcell, forming a ring that shrinks until division is completed (Rothfield and Justice, 1997). Involvement of FtsZ homologs in plastid division has been clearly established in Arabidopsis (AtFtsZ1-1 and AtFtsZ2-1) and the moss Physcomitrella patens (Osteryoung et al, 1998;Strepp et al, 1998;McAndrews et al, 2001).…”

FtsZ and the division of prokaryotic cells and organelles

“…Normal chloroplast fission and distribution require FtsZ, as shown by the dramatically enlarged organelles after the inhibition of FtsZ 101 . The protein machine of chloroplasts, unlike that of bacteria, can be observed in electron micrographs of thin sections.…”