Transcription of the ftsZ gene and cell division in Escherichia coli

Abstract

TheftsZ gene of Escherichia coli, which lies in a cluster of cell division genes at 2 min on the genetic map, codes for a protein which is thought to play a key role in triggering cell division. Using an ftsZ::lacZ operon fusion, we have studied the transcription of the ftsZ gene under conditions in which cell division was either inhibited or synchronized in the bacterial population. InftsZ, ftsA, ftsQ, and ftsl (or pbpB) mutants, there was no change in the differential rate of expression of the ftsZ gene in nonpermissive conditions, when cell division was completely blocked. Although the FtsZ protein is thought to be limiting for cell division, in synchronized cultures theftsZ gene was expressed not only at the moment of septation initiation but throughout the cell cycle. Its expression, however, was not exponential but linear, with a rapid doubling in rate at a specific cell age; this age, about 20 min after division in a 60-min cycle, was different from the age at which the ftsZ::lacZ operon was duplicated. However, it was close to the age at which replication initiated and at which the rate of phospholipid synthesis doubled. During the transient division inhibition after a nutritional shift-up, ftsZ transcription again became linear, with two doublings in rate at intervals equal to the mass doubling time in the rich medium; it adopted the exponential rate typical of rich medium about 60 min after the shift-up, just before the bacterial population resumed cell division. The doubling in the rate of ftsZ transcription once per cycle in synchronized cultures and once per mass doubling time during the transition period after a nutritional shift-up reflects a new cell cycle event.Although a large number of apparent cell division genes have been identified in Escherichia coli and many have been cloned and sequenced, little is known of the precise role of their products (4). The ftsI (or pbpB) gene product, penicillin-binding protein 3, is the only one for which an activity is known (11).Considerable work has been done on one of these division genes, the ftsZ gene, for which a unique temperaturesensitive allele, ftsZ84, provided the demonstration of its role in an early stage of cell division, possibly the initiation of septum formation (22,33). Further evidence for a direct role of the FtsZ protein in septation was provided by the observation (12, 21) that it is the target of the division inhibitor SfiA (or SulA), whose expression is induced by DNA damage as part of the SOS response (9, 10); in this role, FtsZ is a key element of a system coupling cell division to DNA replication.TheftsZ gene lies in a cluster of cell division genes located at 2 min on the E. coli genetic map (22). Its transcriptional organization is complex, with promoters situated in the coding sequences of the adjacentftsA andftsQ genes (29,32,35,36) (see Fig. 1), suggesting possible regulatory interactions among the products of these three genes; certain authors have postulated the existence of a septation complex including all of these protein...

Expression of an early gene in the flagellar regulatory hierarchy is sensitive to an interruption in DNA replication

“…In that case, premature termination of DNA synthesis induces the SOS response, which affects the expression of a number of genes. In E. coli, the SOS response leads to an inhibition of cell division by blocking FtsZ activity (51). It has also been observed that flagellar biosynthesis in E. coli is inhibited at nonpermissive temperatures in temperature-sensitive cell division mutants, mediated through flagellar gene transcription (42).…”

Analysis of the effect of ppGpp on the ftsQAZ operon in Escherichia coli

“…Other estimates of the relative strength of these promoters, based on studies with transcriptional fusions (Yi et al, 1985;Wang et al, 1991;Flä rdh et al, 1997), found about 60% of the total ftsZ mRNA species started from pZ4-pZ3-pZ2-'pZ1', compared with 92% in our study (Table 4). However, the strength of several of these promoters has been shown to vary considerably with growth rate and with growth phase (Dewar et al, 1989;Aldea et al, 1990;Robin et al, 1990;García-Lara et al, 1996;Flärdh et al, 1997). We therefore suspect that the differences in values found by various groups are likely to result from differences in growth phase.…”

Penicillin-binding protein 2 inactivation in Escherichia coli results in cell division inhibition, which is relieved by FtsZ overexpression

“…FtsZ is distributed randomly in the cytoplasm between successive divisions but condenses to form a ring around the cell center at the onset of septation (4). The relative rate of ftsZ expression is inversely correlated with growth rate: when the growth rate decreases, ftsZ expression increases (2,17,38). The ppGpp pool size is also inversely correlated with growth rate (10) minimal medium (33) supplemented with glucose (0.4%), thiamine (10 ,ug/ml), thymine (100 ,ug/ml), and serine, glycine, and methionine (100 ,ug/ml each); relA mutants cannot grow on this medium unless isoleucine and valine (100 ,ug/ml each) are added (49,50).…”

“…2) shows that all the genes can be transcribed from two promoters located in the ddlB gene, and ftsZ has four additional promoters within the ftsA gene (2,39,40). The expression of ftsZ is inversely correlated with growth rate (2,17,38). The P01 promoter contains a so-called "gearbox" sequence, which is found in other promoters inversely regulated by growth rate (1) and, in one case, has been shown to be essential for this regulation (2).…”

“…The P01 promoter contains a so-called "gearbox" sequence, which is found in other promoters inversely regulated by growth rate (1) and, in one case, has been shown to be essential for this regulation (2). The PZ4-PZ3 promoters, studied together in a gene fusion, also exhibit inverse growth rate regulation (17,38 (38).…”