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J Bacteriol, March 1998, p. 1389-1395, Vol. 180, No. 6
Department of Molecular Biology, School of
Health Sciences, Kyorin University, 476 Miyashita, Hachioji, Tokyo
192, Japan
Received 25 August 1997/Accepted 13 January 1998
A divE mutant, which has a temperature-sensitive
mutation in the tRNA1Ser gene, exhibits
differential loss of the synthesis of certain proteins, such as
The divE mutant of
Escherichia coli K-12 exhibits differential loss of the
synthesis of certain proteins at nonpermissive temperatures
(24). When a culture of the divE mutant grown at 30°C was shifted to 42°C, cell growth first continued and then gradually stopped after an about twofold increase in the amount of bulk
proteins. The rates of synthesis of most cellular protein were not
affected by the temperature shift up, but the synthesis of particular
proteins, such as The divE gene is located at 22 min on the genetic map
(32), and nucleotide sequence determination of the cloned
gene revealed that the divE gene product is
tRNA1Ser and that the divE42
mutation is a base substitution of A10 for G10
in the D stem of tRNA1Ser (35).
Among six serine codons, the UCA codon is recognized only by
tRNA1Ser in E. coli (14,
34). In the divE mutant, some genes containing UCA
codons, such as recA and trpED, are expressed
normally after the temperature shift to 42°C. Therefore, it is
unlikely that a defect in the synthesis of certain proteins at 42°C
is simply caused by a deficiency of the mutant
tRNA1Ser decoding function. Furthermore, Yamada
and Ishikura reported that the serine acceptor activity of mutant
tRNA1Ser (ts-tRNA1Ser)
measured experimentally in vitro is not temperature sensitive (37).
It has been shown that in the divE mutant, the defect in
When a multicopy plasmid containing the mutant divE gene was
transformed into the divE mutant, the defect in
lacZ gene expression was completely reversed
(37), but a single-copy plasmid containing the mutant
divE gene cannot complement the defect. These results indicate that lacZ gene expression at 42°C is dependent on
the cellular concentration of tRNA1Ser.
To elucidate the molecular mechanism of the defect in lacZ
gene expression in the divE mutant, we investigated whether
inactivation of the mRNA degradation pathways could restore
the defect in lacZ gene expression. Arraiano et al. have
shown that two exoribonucleases, polynucleotide phosphorylase
(PNPase) and RNase II, and an endoribonuclease, RNase E, are
directly involved in mRNA degradation in E. coli (3). Therefore, we constructed isogenic divE
mutants containing rne-1, rnb-500, and
pnp-7 mutations in various combinations and examined whether
the defect in lacZ gene expression was suppressed by these
mutations. Our results indicate that Bacterial strains.
All of the strains used in this study are
described in Table 1. To introduce the
divE42 mutation into various strains, we inserted a
transposable drug resistance element, Tn5, adjacent to the
divE gene.
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
An rne-1 pnp-7 Double Mutation
Suppresses the Temperature-Sensitive Defect of lacZ Gene
Expression in a divE Mutant
ABSTRACT
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
-galactosidase and succinate dehydrogenase, at nonpermissive
temperatures. In Escherichia coli, the UCA codon is
recognized only by tRNA1Ser. Several genes
containing UCA codons are normally expressed after a temperature shift
to 42°C in the divE mutant. Therefore, it is unlikely
that the defect in protein synthesis at 42°C is simply caused by a
defect in the decoding function of the mutant
tRNA1Ser. In this study, we sought to determine
the cause of the defect in lacZ gene expression in the
divE mutant. It has also been shown that the defect in
lacZ gene expression is accompanied by a decrease in the
amount of lacZ mRNA. To examine whether inactivation of mRNA degradation pathways restores the defect in lacZ gene
expression, we constructed divE mutants containing
rne-1, rnb-500, and pnp-7 mutations
in various combinations. We found that the defect was almost completely
restored by introducing an rne-1 pnp-7 double mutation into
the divE mutant. Northern hybridization analysis showed
that the rne-1 mutation stabilized lacZ mRNA,
whereas the pnp-7 mutation stabilized mutant
tRNA1Ser, at 44°C. We present a mechanism
that may explain these results.
INTRODUCTION
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
-galactosidase and succinate dehydrogenase,
stopped immediately (26, 32, 38). It has also been reported
that when cells exposed to 42°C were returned to a permissive
temperature, they started to grow and divided synchronously
(25).
-galactosidase synthesis at 42°C is accompanied by a decrease in the amount of lacZ mRNA (26). We also found, by
S1 mapping, that the initiation of lacZ gene transcription
was almost normal at 42°C (unpublished data). Therefore, the lower
level of lacZ mRNA may be caused by either premature
transcriptional termination or increased degradation of the transcript
by RNases.
-galactosidase expression in
the divE mutant was almost completely reversed by introducing rne-1 pnp-7 double mutations. We also present
results showing how individual RNases are involved in this process.
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
467 ( b221
rex::Tn5 cI857 Oam29 Pam80) was used for random insertion of Tn5 into the chromosome of
strain KY2329#6 (pyrD+ divE42)
(5, 7). P1vir phage grown on this library was
used to transduce strain KY2504 (pyrD34 divE42), and the
pyrD+ Kmr transductant was selected.
We refer to it as KYR25. In KYR25, a Kmr marker was
inserted adjacent to divE42 because pyrD is
located at 21 min, adjacent to the divE gene (22 min) on the
genetic map (32). A P1vir lysate grown on KYR25
was used to transduce the divE42 allele into various
RNase-deficient strains. The divE gene is 52%
cotransducible with Tn5. Transductants were screened by Southern hybridization analysis to detect the replacement of base G10 with A10 in
tRNA1Ser.
TABLE 1.
E. coli strains used in this study
Assay of -galactosidase.
M9 minimal medium supplemented
with thymine at 25 µg/ml, Casamino Acids at 1% (wt/vol), and
glycerol at 0.2% (wt/wt) was used (17). Kanamycin was added
to the medium at 20 µg/ml to maintain the Kmr marker.
Cells were grown to mid-log phase at 30°C.
Isopropyl--D-thiogalactopyranoside (IPTG) was then added
to the culture at 2 mM, and an aliquot of the culture was immediately
shifted to 44°C while another was kept at 30°C for further growth.
Samples were removed every 6 min until 30 min after the temperature
shift, and enzymatic activity was assayed as previously described
(29). One unit of enzyme activity was defined as that which
hydrolyzes 1 µmol of
o-nitrophenyl--D-thiogalactopyranoside (ONPG)
per h.
Northern hybridization. Cells were grown as described above and harvested 30 min after the induction and the temperature shift, and then total RNAs were extracted with hot phenol as described by Aiba et al. (2).
For analysis of lacZ mRNA, a 1.5% agarose gel containing 6% formaldehyde was used. Samples (5 µg) of total RNAs were fractionated by electrophoresis at 20 V overnight. RNAs were then blotted onto a nylon membrane (Hybond N; Amersham) and fixed by UV irradiation. The 300-bp DNA fragment containing a lac promoter sequence and the coding sequence for the N-terminal 53 amino acids of-galactosidase was used as a probe. The labelling reactions
were performed with [
-32P]dCTP and the Multiprime DNA
labelling system (Amersham). The radioactivity of each band in the
Northern hybridization was quantified by using a BAS2000 Imaging
Analyzer (Fuji). The amount of 3.1-kb lacZ mRNA was
precisely quantified from the same duplicate Northern blots.
For analysis of tRNA, 2-µg samples of total RNAs were electrophoresed
on an 8% polyacrylamide gel containing 8 M urea and transferred by
electroblotting to a nylon membrane (Clear Blot Membrane-N; Atto) in
1× TAE (10 mM Tris-HCl [pH 7.8], 5 mM sodium acetate, 0.5 mM EDTA).
A 32P-labelled 359-bp fragment containing the coding
sequence for tRNA1Ser and a putative
-independent transcriptional termination signal was used as a probe.
For determination of the half-life of tRNA1Ser,
cells were grown at 30°C to mid-log phase, and then rifampin was
added at 500 µg/ml, and at the same time, an aliquot of the culture
was shifted to 44°C. The radioactivity that remained on bands of
88-nucleotide (nt) mature tRNA1Ser was
quantified.
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RESULTS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Triple mutation of the RNase genes restores repression of
lacZ gene expression in the divE mutant.
We constructed the isogenic divE mutant containing the
rne-1, pnp-7, and rnb-500 alleles to
examine whether the RNA degradation pathway participates in the
decrease in lacZ mRNA at nonpermissive temperatures. In
wild-type strain SKR207, inducible synthesis of -galactosidase at
42°C was about the same as at 30°C (data not shown), while in
divE mutant strain SKR319, synthesis of -galactosidase was barely detected at a nonpermissive temperature (42°C), as reported previously (26). Not only divE42
mutations, but also rne-1 and rnb-500 mutations,
are temperature sensitive, and the nonpermissive temperature for
rne-1 and rnb-500 mutations is 44°C (3, 8,
28). We then used a temperature shift from 30 to 44°C to
examine the effect of a triple mutation on expression of the
lacZ gene in a divE mutant. Growth rates of the
rne-1 pnp-7 rnb-500 triple mutant, either with or without a
divE42 mutation, decreased gradually about 30 min after the
shift to 44°C in M9 medium. To minimize the effects of the triple
mutation on various cellular functions, all samples were removed within
30 min after the temperature shift to 44°C.
-galactosidase at 44°C was somewhat (about 60%) lower than
that at 30°C in strain SKR207. -Galactosidase was hardly
synthesized at 44°C in the divE mutant containing the
wild-type RNase genes (SKR319) (Fig. 1B). Introduction of the triple
mutation into strain SKR207 had no significant effect on
-galactosidase synthesis (Fig. 1C), while in SKR104 (divE42
rne-1 rnb-500 pnp-7), synthesis of -galactosidase was obviously
restored (Fig. 1D) and the level of -galactosidase at 44°C in
SKR104 was comparable to that in SKR101 (divE+
rne-1 rnb-500 pnp-7).
|
,
30°C; 
, 44°C. O.D.530nm; optical density at 530 nm.
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rne-1 mutation stabilized lacZ mRNA in the
divE mutant.
RNase E is known as one of the major
processing endoribonucleases (9, 11, 19, 22, 23, 36). It
also has a general role in mRNA turnover (4, 21) and affects
the stability of specific transcripts in E. coli (3,
6). Yarchuk et al. reported that RNase E participated in the
degradation of lacZ mRNA under conditions that interfered
with synchronization of transcription and translation in E. coli (39). Thus, we subsequently constructed an
isogenic divE mutant containing rne-1. Inducible
synthesis of -galactosidase is shown in Fig.
3, together with the results obtained by
Northern hybridization. It appeared that synthesis of -galactosidase
at 44°C was not restored at all by introduction of the
rne-1 mutation, whereas the lacZ mRNA level at
44°C in SKR615 (rne-1 divE42) was restored up to about
46% compared to that at 30°C (Fig. 3C and Table 2). These results
indicate that for the restoration of lacZ gene expression,
it was not enough to stabilize lacZ mRNA by introduction of
the rne-1 mutation and that mutation of exoribonuclease
genes pnp and/or rnb might have functions other
than the stabilization of the lacZ mRNA in the rne-1
pnp-7 rnb-500 triple mutant.
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Contribution of other mutant alleles of RNase to the restoration of
lacZ gene expression.
To define the minimum set of
alleles necessary to restore lacZ gene expression in the
divE mutant, we constructed a series of divE
mutant strains which carried one or two mutant alleles of the three
RNase genes and analyzed the resulting lacZ gene expression
(Table 2). There was no mutant allele which completely restored
lacZ gene expression by itself. In strain SKR911
(pnp-7 divE42), synthesis of -galactosidase at 44°C was
half of that in the divE+ strain containing the
pnp-7 allele (SKR913), while no significant restoration of
the level of lacZ mRNA at 44°C was observed in this
strain. In SKR711 (rne-1 pnp-7 divE42), -galactosidase
synthesis and the level of lacZ mRNA at 44°C were
completely restored, in comparison with SKR712 (rne-1 pnp-7
divE+). Introduction of the rnb-500
mutation or the rnb-500 pnp-7 double mutation into the
divE mutant did not contribute to the restoration of
-galactosidase synthesis at 44°C. These results demonstrate that
the minimum set of mutant alleles necessary to restore lacZ gene expression was the combination of rne-1 and
pnp-7.
Steady-state levels of tRNA1Ser in various divE mutants. PNPase and RNase E are RNases which participate in the maturation of tRNA molecules (19, 23, 30). It is reasonable to assume that the mutations of RNases affect not only the stability of the lacZ mRNA but also the stability of the divE gene product, tRNA1Ser, especially in case of ts-tRNA1Ser. We next examined the steady-state level of tRNA1Ser by Northern hybridization. The relative amount of tRNA1Ser was calculated from the density of a band positioned at 88 nt (indicated by a solid arrow in Fig. 4). The amount of wild-type tRNA1Ser was not significantly changed by the temperature shift from 30 to 44°C in all strains (Fig. 4, lanes 1, 2, 5, 6, 9, 10, 13, 14, 17, and 18). In strain SKR319 carrying wild-type RNases, the amount of ts-tRNA1Ser at 44°C was about 25% of that at 30°C (Fig. 4, lanes 3 and 4) and it corresponds to approximately 14% of the amount of wild-type tRNA1Ser in strain SKR207 at 44°C (lanes 2 and 4). Steady-state levels of tRNA were raised by introduction of a pnp-7 mutation into the divE mutant strain (lanes 19 and 20). The amount of ts-tRNA1Ser at 44°C became almost half of the level at 30°C when the pnp-7 (in strain SKR911) and pnp-7 and rne-1 (in strain SKR711) alleles were introduced into the divE mutant (lanes 19 and 20 and lanes 11 and 12, respectively). In strain SKR104 (rne-1 pnp-7 rnb-500 divE42) (lanes 7 and 8), the amount of ts-tRNA1Ser at 44°C was completely recovered, while in SKR615 (rne-1 divE42), the amount of ts-tRNA1Ser at 44°C was not restored at all (lane 16). In strains carrying the rne-1 allele, a band migrating slower than mature tRNA1Ser (indicated by the open arrow) was observed. This ~130-nt band was detected in all strains but was most abundant in RNase E-deficient strains. This molecule seems to be a precursor species of tRNA1Ser. Ray and Apirion have reported that RNase E participates in the processing events at the 3' end of the immature tRNA1Ser (30). Our results agree with their observations and indicate that, instead of mature tRNA1Ser, the precursor was produced after the shift to 44°C in rne-1 mutant strains. This precursor molecule seemed to be stable at 44°C, even if it had a base substitution of ts-tRNA1Ser.
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DISCUSSION |
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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In this report, we propose that the defect in lacZ gene
expression at nonpermissive temperatures was almost completely restored by introducing an rne-1 pnp-7 double mutation into the
divE mutant. The rne-1 single mutation restored
the steady-state levels of lacZ mRNA at 44°C to up to 46%
of that at 30°C, but -galactosidase synthesis was not restored at
all. Introduction of a pnp-7 single mutation resulted in
50% recovery of -galactosidase synthesis at 44°C compared to that
of the isogenic divE+ strain, but the amount of
lacZ mRNA was not restored significantly. Northern
hybridization analysis of tRNA1Ser demonstrated
that ts-tRNA1Ser becomes extremely unstable
(half-life, ~1 min) at 44°C and the pnp-7 mutation, but
not the rne-1 and rnb-500 mutations, stabilizes ts-tRNA1Ser. These results indicate that
efficient expression of the lacZ gene in the divE
mutant can be achieved only when lacZ mRNA, as well as
ts-tRNA1Ser, is stabilized by RNase mutations.
From these results, we assume that ts-tRNA1Ser
can decode UCA codons but its decoding efficiency is somewhat lower
than that of wild-type tRNA1Ser at 44°C. The
lacZ gene has eight UCA codons. In the divE
mutant, translating ribosomes might stall at one or several UCA codons at 44°C, resulting in desynchronization of transcription and
translation. The transcribing RNA polymerase might create naked mRNA
behind itself, and if this region has a latent RNase E recognition
site, lacZ mRNA might be cleaved, leading to reduced
-galactosidase synthesis.
There have been several reports indicating that synchronization of
transcription and translation is an important factor for efficient gene
expression in E. coli (1, 4, 10, 16, 18, 20, 33,
39). Yarchuk et al. reported that when the ribosome binding site
(RBS) of the lacZ gene was replaced with RBSs from various
genes or artificial RBSs, strain-to-strain variation in
-galactosidase synthesis was paralleled by nearly equivalent variations in steady-state levels of lacZ mRNA
(39). Moreover, it was demonstrated that inefficient
initiation of translation decreased the stability of lacZ
mRNA and that RNase E was involved in the rate-limiting step of the
degradation of lacZ mRNA. Iost and Dreyfus have shown that
the lacZ mRNA transcribed by T7 RNA polymerase yields less
-galactosidase than does that transcribed by E. coli RNA
polymerase and that the lower yield reflects its lower stability
(13). They proposed that T7 RNA polymerase transcribes the
lacZ gene faster than does the E. coli enzyme and
that this higher speed unmasks an RNase E cleavage site which is
normally shielded by ribosomes (12).
When the ts-tRNA1Ser gene is cloned into a multicopy plasmid and introduced into a divE mutant, expression of the lacZ gene normally occurs at a nonpermissive temperature and it is unnecessary to stabilize lacZ mRNA by use of an rne-1 mutation. The translating ribosomes probably do not stall at UCA codons under these conditions. As reported previously, there are several genes which have UCA codons and whose expression is not affected by a divE mutation (26). According to our model, it is unlikely that there are latent RNase E cleavage sites downstream of the UCA codons in these genes. The translating ribosomes might stall at UCA codons temporarily but could eventually complete translation. Low levels of ts-tRNA1Ser at nonpermissive temperatures seem to be enough to sustain normal levels of translation. Further work is needed to prove this assumption.
As shown in Table 2, the amount of lacZ mRNA was restored by an rne-1 mutation but restoration was not complete. There is a possibility that transcriptional polarity is also one of the causes of lower levels of lacZ gene expression in the divE mutant. Ruteshouser and Richardson reported that the lacZ gene contained several latent transcriptional terminators in its coding region and that transcription terminated at these sites in vivo when the transcript was not properly translated, either by the polar mutation or by amino acid starvation (31).
In this study, we also demonstrated that mutant tRNA1Ser is strikingly unstable at nonpermissive temperatures. The divE42 mutation is a base substitution of A10 for G10 which disrupts one base pairing in the D stem of tRNA1Ser (35). This base pairing seems to be important for the stability of tRNA1Ser. A base substitution of T25 for C25 in the D stem, which restores the A-T base pairing instead of the G-C pair of wild-type tRNA1Ser, is one of the efficient intragenic suppressors of the divE42 mutation (27).
As shown in Fig. 5, introduction of the pnp-7 mutation to the divE mutant increased the stability of ts-tRNA1Ser at 44°C about fourfold. We did not determine the half-life of ts-tRNA1Ser in rne-1 pnp-7 double and rne-1 pnp-7 rnb-500 triple mutants. If mature ts-tRNA1Ser was not synthesized at 44°C in these strains due to the presence of the rne-1 allele, and the half-life was about the same as that in the pnp-7 mutant, the amount of ts-tRNA1Ser remaining 30 min after the temperature shift to 44°C became less than 5% of that at 30°C. However, Northern hybridization analysis showed that the amounts of ts-tRNA1Ser at 44°C in the double and triple mutants were 50 and 100% of that at 30°C, respectively. These results might be explained by the following two possibilities; one is that ts-tRNA1Ser is more stable in these mutants than in the pnp-7 mutant, and the other is that mature ts-tRNA1Ser is synthesized in spite of the presence of the rne-1 mutation.
Northern hybridization analysis showed that in the rne-1
mutant, a band which migrated slower than mature
tRNA1Ser accumulated at 44°C. This band,
about 130 nt in length, was also detected in the wild-type strain,
although the amount was less than that in the rne-1 strain.
This species seems to be an unprocessed precursor of mature
tRNA1Ser. In contrast to mature
ts-tRNA1Ser, it is as stable as the wild-type
one at 44°C. From nucleotide sequence data on the divE
gene, it is reasonable to assume that the transcription starts 5 bases
upstream of the 5' end of the mature tRNA1Ser
and terminates at -independent transcription terminators located downstream of the 3' end (35). It produces an about 130-nt
transcript, which corresponds well to the size of our predicted
precursor of tRNA1Ser. Ray and Apirion reported
that in a temperature-sensitive rne-3071 mutant, a precursor
molecule of tRNA1Ser accumulated which had
eight and five extra nucleotides at the 5' and 3' ends of mature
tRNA1Ser, respectively (30). We have
no explanation for the disparity between these observations and our
results, but it may be due to the difference in genetic background
between the strains used. In connection with this, it is worth
mentioning that the strains used in this study have a one-base deletion
in the rph gene encoding RNase PH, which is also known as
one of the RNases involved in the maturation of tRNA (15).
It has been reported that divE mutant cells exposed to 42°C, when returned to permissive temperatures, started to grow and divide synchronously (25). This indicates that divE mutant cells arrested at a specific stage of the cell cycle at nonpermissive temperatures. Work is in progress to determine which gene is primarily involved in this step and whether the same regulatory mechanism is involved in this case as in that of the lacZ gene.
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ACKNOWLEDGMENTS |
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We are grateful to Sidney R. Kushner for helpful information, as
well as for the donation of a series of RNase-deficient strains. We
also thank Takashi Sato for the divE mutant strains and C. Wada for 467.
This work was supported in part by a grant-in-aid from the Science Research Promotion Fund, Japan Private School Promotion Foundation, and by a project research grant from Kyorin University.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Molecular Biology, School of Health Sciences, Kyorin University, 476 Miyashita, Hachioji, Tokyo 192, Japan. Phone: 81 426 91 0011. Fax: 81 426 91 1094. E-mail: taisokyo{at}cb.mbn.or.jp.
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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J Bacteriol, March 1998, p. 1389-1395, Vol. 180, No. 6
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