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Multiple Mechanisms for Degradation of Bacteriophage T4 soc mRNA
Toshie Kai1,a and Tetsuro Yonesakiaa Department of Biology, Graduate School of Science, Osaka University, Osaka 560-0043, Japan
Corresponding author: Tetsuro Yonesaki, Graduate School of Science, Osaka University, 1-16 Machikaneyama-cho, Toyonaka-shi, Osaka 560-0043, Japan., yonesaki{at}bio.sci.osaka-u.ac.jp (E-mail)
Communicating editor: G. R. SMITH
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The dmd gene of bacteriophage T4 is required for regulation of mRNA stability in a stage-dependent manner during infection. When this gene is mutated, late genes are globally silenced because of rapid degradation of mRNAs. To investigate the mechanism of such mRNA degradation, we analyzed the late gene soc transcripts. The degradation of soc mRNA was remarkably stabilized when its ability to be translated was impaired; either disruption of translation initiation signals or elimination of termination codons was effective in stabilization of soc mRNA and removal of elongation modestly stabilized it. Even in the absence of translation, however, the residual activity was still significant. These results suggested that the degradation of soc transcripts was promoted by two different mechanisms; one is dependent on translation and the other independent of translation. We found several cleavages introduced into soc RNA specifically when the dmd gene was mutated; some of them could be linked to polypeptide chain elongation and termination, suggesting the correlation with ribosomal action, and the others were independent of translation.
BACTERIOPHAGE T4 expresses its hundreds of genes separately at early, middle, and late stages of infection primarily by differential transcription from stage-specific promoters (
To investigate the molecular mechanism of the dmd-mediated discrimination and degradation of mRNAs, it would be essential to characterize the mRNA-degrading activity. Analysis of degradation intermediates of late-gene mRNA in a dmd mutant reveals that the degradation occurs in a dmd mutant-specific manner. It was, however, too rapid and extensive to detect the full-length transcripts, ranging from 1.8 to 5 kb, of late genes 23, 37, and 51 (
In the present study, we focused on the late gene soc for three reasons. First, the soc gene is transcribed from its own late promoter as a monocistronic mRNA that is only 300 nucleotides long (MCDONALD et al. 1984) and may be the shortest among T4 late gene mRNAs. Second, since the soc protein is one of the major components of the T4 phage capsid (
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Bacteria and phage: growth and infection conditions:
We routinely used the E. coli K12 strains MH1 (hsdR- supo) as a nonpermissive host and CR63 (supD) as a permissive host. MH1 cells were also used for cloning T4 genes. Wild-type bacteriophage T4 is T4D. The T4 amSF16 phage contains a nonsense mutation in the dmd gene (
Northern blot analysis:
Total RNA from a 1.5-ml culture of infected cells was isolated as described previously (
-32P]ATP (HAS, 259 TBq/mmol).
Primer extension:
Primer extension was carried out as follows. A total of 1 pmol of DNA primer 1 or 2 (refer to Fig 1) was labeled with 32P at the 5' end and mixed with 5 µg of purified RNA in 2 µl of 50 mM Tris-HCl (pH 8.3) containing 60 mM NaCl and 10 mM dithiothreitol (DTT). After incubation for 3 min at 60°, the mixture was quickly chilled on ice. For analysis of soc-nst RNA, the incubation was conducted for 3 min at 50°, and then the temperature was gradually lowered to 43°. Avian myeloblastosis virus reverse transcriptase (1.4 units) was then added to the mixture, and the final volume was brought to 5 µl by the addition of 50 mM Tris-HCl (pH 8.3) containing 60 mM NaCl, 10 mM DTT, 6 mM Mg(OAc)2, and a 0.4 mM concentration of each 2'-deoxyribonucleoside 5'-triphosphate. The DNA primer was extended at 37° for 3 min and then at 54° for an additional 20 min. The reaction was terminated by the addition of 10 µl of a solution containing 0.1% (w/v) xylene cyanol, 0.1% (w/v) bromophenol blue, 10 mM EDTA (pH 8.0), and 95% (v/v) deionized formaldehyde. The reaction products were denatured by boiling for 2 min and analyzed by electrophoresis through a 5% polyacrylamide gel containing 7 M urea.
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Construction of plasmid and phage mutants for soc gene:
A DNA fragment containing the entire soc gene was amplified by PCR using T4 DNA as a template with the primers soc5' and soc3' and ligated into the PstI site of pBlueScript KS- (Stratagene, La Jolla, CA) to construct pTK40. Plasmids containing various base-substituted soc alleles were pTK50, -61, -70, -80, and -90, harboring the soc-als, soc-sls, soc-nel, soc-hlf, and soc-nst alleles, respectively. These were constructed by PCR with pTK40 as a template and mutagenic oligonucleotide primers. Briefly, PCR was performed with each mutagenic primer and the soc3' primer and then with the DNA fragment amplified by the first PCR and the soc5' primer. The mutagenic oligonucleotides used were the following: for pTK50, 5'-aaaggagaattacatcgatagtactcgcggtta; for pTK61, 5'-gtaatttaaataaagcttaattacatggctagt; for pTK70, 5'-ccgcgagtttattacatgtaat; for pTK80, 5'-tgagcgccttattatttgtgaa; and for pTK90, 5'-aactggttctagactcaagg. The base substitutions introduced into soc alleles are summarized in Fig 1.
The deletion mutants soc
-1, soc-2, soc-3, and soc-4 were also constructed by PCR with pTK40 as a template and deletion-generating primers in the same manner as above: for pI/Ssoc-1, 5'-tactcacccgtccgccactc; for pI/Ssoc-2, 5'-aaccgcgagtacatgattat; for pI/Ssoc-3, 5'-taaccgcgagtttatttaaa; and for pI/Ssoc-4, 5'-aatttctgctcaaattttatttaaattaca. The thus constructed deletion mutants lacked 57 nucleotides from position 3 to 59, inclusive, of the soc mRNA in soc-1; 31 nucleotides from position 3 to 33 in soc-2; 20 nucleotides from position 14 to 33 in soc-3; and 45 nucleotides from position 15 to 59 in soc-4 (refer to Fig 1).
Each soc allele in a plasmid was transferred into the phage genome by the insertion/substitution method (
| RESULTS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Northern blot analysis of soc transcripts:
Northern blot analysis of soc transcripts at a late stage (19 min) of wild-type infection unexpectedly detected two major transcripts (Fig 2A). The slower migrating species (0.3 kb) was the full-length monocistronic soc mRNA transcribed from a late promoter just upstream of the soc coding region, as revealed by primer extension analysis (Fig 2B; also refer to Fig 6A). In agreement with transcription from the stage-specific promoter, this species was undetectable at an early stage (4 min). Moreover, it was much reduced in gene 55--infected cells, indicating that its transcription depended highly on gene 55, which encodes a T4 sigma factor required for the recognition of late promoters (
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, dmd-; 
, dmd- soc-sls; 
, dmd- soc
, dmd- soc
, dmd- soc
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Consistent with the idea that the activity of dmd mutant-specific degradation correlates with mRNA length, we were able to detect full-length soc mRNA even in dmd--infected cells (Fig 2A). Its abundance in dmd--infected cells was, however, only one-fifth of that in wild-type phage-infected cells, reflecting the instability of this RNA caused by a dmd mutation. In contrast to full-length soc mRNA, the 5'-truncated RNA did not appear to suffer from dmd mutant-specific degradation and remained as abundant in dmd- as in the wild type. In fact, the half-life of this truncated RNA was not affected by a dmd mutation and was 10-fold greater than that of the full-length soc mRNA in dmd- (see below). The 5'-truncated RNA must be untranslatable, because this truncation removed the Shine-Dalgarno (SD) sequence, which is required for ribosome binding, and the translation initiation codon of the soc gene (Fig 1). Therefore, the above results raised the possibility that the degradation of soc mRNA was dependent on its ability to be translated.
Translation-dependent degradation of soc RNA:
To investigate the above possibility, we disrupted the signals of translation initiation by base substitutions (Fig 1) to examine the abundance of soc RNA (Fig 3). By disruption of either the SD sequence (soc-sls) or the initiation codon (soc-als), the abundance of full-length soc RNA in dmd- relative to that in dmd+ was markedly increased from 22 to 85–90% of that in the wild type, suggesting an increase in stability.
The effects of translation on soc RNA stability were further evaluated by the decay rates of RNA. This experiment involved an additional mutant, soc-3 (Fig 4A), which lacked both the SD and initiation codon. We measured the decay rate of soc RNA in the presence of rifampicin, a transcription inhibitor. After transcription was blocked by addition of rifampicin at 18 min postinfection, total RNA was extracted from T4-infected cells at 20, 26, and 32 min. The abundance of each full-length soc RNA at these time points was examined by Northern blotting (Fig 4B) and its half-life was determined by plotting the relative abundance (Fig 4C). The half-life of the full-length soc mRNA was 26 min in wild-type-infected cells, and it was 2.7 min in dmd--infected cells. As expected, the soc-sls full-length RNA had a fourfold longer half-life (11 min) than wild-type soc mRNA in dmd--infected cells. Similarly, the full-length RNA of soc-3 had a threefold longer half-life (8.5 min). These results strongly suggest that the rapid degradation of soc mRNA in the dmd mutant is dependent on translation, that is, that translation of soc mRNA triggered the degradation of the template RNA.
Effects of translation phase on soc RNA stability:
Translation consists of three phases, i.e., initiation, elongation, and termination. To estimate the contributions of elongation and termination to translation-dependent RNA degradation, we eliminated each of these phases: Two termination codons were placed in tandem immediately downstream of the initiation codon to eliminate the elongation phase (soc-nel) or the original termination codon was disrupted to eliminate the termination phase (soc-nst; Fig 1). As shown in Fig 5, the relative abundance of the full-length soc-nst transcript in dmd- was threefold (77%) greater than that (24%) of the wild-type soc full-length transcript, suggesting a large contribution of translation termination to the degradation process. Removal of the elongation phase also increased the relative abundance of the full-length soc-nel transcript to 37%. Although this increase was modest, it was reproducibly observed in several independent experiments. We also constructed soc-hlf, in which nonsense codons were placed to terminate translation prematurely (Fig 1). When assessed by Northern blotting, the soc-hlf mutation had an effect on the stability of full-length soc RNA as modest as that of the soc-nel mutation (data not shown). These results reveal that translation-dependent degradation of soc mRNA depends on both elongation and termination. This conclusion, however, does not exclude the possibility that translation initiation by itself also contributes to translation-dependent degradation of soc mRNA. Unfortunately, this possibility cannot be tested under the present circumstances.
Translation-independent degradation of soc RNA:
Although the blockade of translation was effective in the stabilization of soc RNA, such an effect could not account for all of the dmd mutant-specific RNA-degrading activity; soc-sls and soc-3 full-length RNAs were still degraded two- to threefold faster in dmd- than soc mRNA in wild-type-infected cells (Fig 4). Therefore, an activity independent of translation was also suggested to contribute to the soc RNA degradation. The truncated RNA lacking the 5'-terminal 59 nucleotides had a half-life of 
30 min, regardless of the dmd mutation and soc allele (Fig 4B; data not shown), and was threefold longer than those of soc-sls and soc-3 full-length RNAs in dmd-. This observation suggested that the 5'-terminal 59 nucleotides are required for the RNA-degrading activity independent of translation. To investigate this possibility, we constructed other soc deletion mutants, soc-1, soc-2, and soc-4. All of these mutants lacked both the SD and initiation codon and differed in length of sequence deleted from the 5'-terminal 57 nucleotides of soc mRNA (Fig 4A). When the 5' or 3' moiety of this region was deleted in soc-2 or soc-4, the half-lives of their full-length RNAs were 12 min for soc-2 (Fig 4C) and 14 min for soc-4 (data not shown), respectively, as short as that of soc-sls. soc-1 had the largest deletion and its primary structure was similar to that of the 5'-truncated transcript except for an extra 5'-terminal GU. We were not able to determine the half-life of full-length soc-1 RNA by Northern blotting because it comigrated with its 5'-truncated form during gel electrophoresis (Fig 4B). To calculate the half-life of full-length soc-1 RNA, we performed primer extension using the same RNA preparation and analyzed the products through a sequencing gel to estimate the relative abundance of full-length and 5'-truncated RNA (refer to Fig 6B). The ratio of cDNA corresponding to full-length soc-1 RNA to that of its 5'-truncated form was 2.0, 1.8, and 1.5 at 20, 26, and 32 min, respectively. On the basis of these values and the combined signal intensity of full-length and 5'-truncated soc-1 RNA in Fig 4B, we deduced the abundance of full-length soc-1 RNA at each time point and plotted the relative abundance in Fig 4C. The estimated half-life of full-length soc-1 RNA was 30 min: Thus, this species was more stable than full-length soc-2 and -4 RNA and as stable as the 5'-truncated RNA. These results suggest that the 5'-terminal 57 nucleotides deleted in soc-1 RNA are required for the translation-independent degradation.
Cleavage of soc RNA:
In prokaryotes, degradation of mRNA is usually initiated by endonucleolytic cleavage (
A cDNA fragment common to all phage, indicated by the letter F in Fig 6, corresponds to full-length soc RNA. The band indicated by the letter T, which was also detected with all phage, corresponds to 5'-truncated transcripts. In addition, comparison of cDNAs from dmd- infection (even-numbered lanes) with those from dmd+ infection (odd-numbered lanes) revealed several cDNAs associated only with dmd- infection, corresponding to the dmd mutant-specific cleavages. Two cDNAs, designated as TC1 and TC2, were detected for wild-type soc (lane 4). Although the intensities of these cDNAs were rather weak, their detection was highly reproducible. Interestingly, these bands were also detected for soc-nst (lane 2), while they were insignificant with the RNA of soc-sls (lane 6), soc-als (lane 8), soc-nel (lane 10), and soc-hlf (lane 12). Since both cleavages at TC1 and TC2 are located in a region that is translatable in soc-nst as well as in wild type but not in the others (Fig 1), they appear to be linked with polypeptide chain elongation.
The present experiment did not permit detection of cleavages in the vicinity of the termination codon of the wild-type soc gene because the termination codon was located within the sequence used for the primer (Fig 1). This situation arose because of the region downstream from the primer; since it contains a transcriptional terminator with a strong secondary structure (
A band indicated by TU was common to all soc alleles when dmd was mutated (even-numbered lanes). This band was also detected for all deletion mutants in dmd--infected cells (data not shown; refer to Fig 6B). In addition to TU, two bands indicated by U1 and U2 were occasionally detected, although very weakly, for all soc alleles in dmd--infected cells (even-numbered lanes). Accordingly, these cleavages are suggested to be independent of translation. In spite of the fact that the cleavage at TU was prominent, its contribution to degradation of soc RNA at late stages was unclear, because it was observed even for rather stable soc-1 RNA; it seemed possible that this cleavage occurred before late stages, like the 5' truncation. To clarify whether or not this cleavage can occur at late stages, we isolated RNAs of soc-1, soc-2, and soc-4 after rifampicin was added at 18 min postinfection and analyzed them by primer extension analysis. Fig 6B shows a kinetic change in the quantity of full-length, 5'-truncated or TU-cleaved RNA of each soc allele. The intensity of each full-length or 5'-truncated RNA decreased with time, roughly consistent with the decay rate assessed by Northern blotting (Fig 4 and data not shown). On the other hand, the amounts of TU-cleaved RNA of all soc alleles apparently increased from 20 to 30 min and thereafter decreased. This result clearly indicated that the cleavage at TU occurred during late stages.
| DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Our present study was conducted to investigate the mechanism of rapid mRNA degradation that leads many T4 late genes to become silenced in dmd mutant-infected cells. For this purpose, we chose the short mRNA of the soc gene. The full-length soc RNA was remarkably stabilized when its ability to be translated was impaired either by disruption of the translation signals (soc-sls and soc-als) or by removal of them (soc-2 to -4). However, soc RNA-degrading activity was still significant even in the absence of translation. Therefore, two different mechanisms, one dependent on, and the other independent of, translation, may account for the rapid degradation of soc mRNA in the dmd mutant-infected cells. The translation-dependent mechanism was further dissected into two categories depending on elongation or termination. Elimination of termination codons in soc-nst was effective in stabilization of soc mRNA. In contrast, removal of the elongation phase in soc-nel modestly stabilized soc mRNA. However, since an elongation-dependent activity would correlate with the length of the mRNA, this activity should contribute more to degradation of long mRNAs.
Among untranslatable soc RNAs, soc-1 was more stable than soc-2, soc-3, soc-4, and soc-sls. Accordingly, it is likely that the 57-nucleotide sequence from position 3 to 59, which was deleted in soc-1 RNA, has a role as a destabilizer of soc RNA and that it is required for the translation-independent mechanism. A translation-independent cleavage at site TU was detected during the late stages of dmd mutant-infection. The quantity and kinetic change of TU-cleaved RNA was very similar in the soc-1, soc-2, and soc-4 mutants, indicating that the cleavage at TU was little affected in soc-1 RNA in comparison to more unstable soc-2 or soc-4 RNA. These facts strongly suggest that this cleavage occurs apart from the destabilizing effect of the 5' region as discussed above. Accordingly, the translation-independent mechanism for degradation of soc RNA can be comprised of two categories, one accompanying the cleavage at TU and the other independent of this cleavage, the latter of which should be inactive against soc-1 RNA.
Cleavages of soc RNA at several specific sites (HL, NE, TC1, and TC2) were detected when the recognition of RNA for translation by ribosomes was allowed (Fig 1). Site NE is 23 bases downstream of the first termination codon introduced into soc-nel RNA, and site HL is 6 bases downstream of the first termination codon introduced into soc-hlf RNA. The E. coli 70S ribosome covers >30 nucleotides of mRNA (
All the cleavages introduced in the cis-translation-dependent manner are between dinucleotides with sequence 5'-YR or 5'-YY (Fig 1), where Y is a pyrimidine and R is a purine. This preference is especially interesting for elongation-dependent cleavages at sites TC1 and TC2. If we assume that the sequence preference of elongation-dependent cleavage for soc mRNA is the same for other late-gene mRNAs, then we can easily explain the previous results in which dmd mutant-specific cleavages in the coding region of gene 23 mRNA occurred between the dinucleotides 5'-YR or 5'-YY (
Regardless of whether dmd was normal or mutated, the 5'-truncated soc RNA was produced. Our results suggest that the truncated RNA originated from early and middle transcripts. The soc gene can be transcribed as a part of a long polycistronic mRNA from upstream early and middle promoters, but it is not expressed until late stages, when this gene is transcribed from its own late promoter (
This study suggests that multiple mechanisms of RNA degradation lead T4 late genes to become silenced in dmd mutant-infected cells. The extensive degradation may be originally aimed at middle-gene mRNAs when they finish their mission, and the dmd may have a role in discriminating middle- and late-gene mRNAs (
| FOOTNOTES |
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1 Present address: Carnegie Institution of Washington, Department of Embryology, 115 W. University Pkwy., Baltimore, MD 21210. 
| ACKNOWLEDGMENTS |
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We thank the staff of the Radioisotope Research Center at Toyonaka, Osaka University, for facilitation of our research; all of our experiments using radioisotopes were carried out at the center.
Manuscript received July 23, 2001; Accepted for publication October 29, 2001.
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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