Molecular basis of the ‘<i>box</i> effect’

Labouesse, Michel; Netter, Pierre; Schroeder, Renée

doi:10.1111/j.1432-1033.1984.tb08434.x

Cited by 60 publications

(36 citation statements)

References 49 publications

(36 reference statements)

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“…As there are no other candidates for RNA processing factors in the well-described and small chloroplast genome, it was suggested that matK is responsible for splicing these introns. If true, MatK would be an example of a group II intron maturase that has left the strict association with just a single target intron, joined by the group I intron maturase BI4 from yeast mitochondria, which supports splicing of two group I introns (17).…”

mentioning

confidence: 99%

An organellar maturase associates with multiple group II introns

Zoschke

Nakamura

Liere

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

156

207

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Bacterial group II introns encode maturase proteins required for splicing. In organelles of photosynthetic land plants, most of the group II introns have lost the reading frames for maturases. Here, we show that the plastidial maturase MatK not only interacts with its encoding intron within trnK-UUU, but also with six additional group II introns, all belonging to intron subclass IIA. Mapping analyses of RNA binding sites revealed MatK to recognize multiple regions within the trnK intron. Organellar group II introns are considered to be the ancestors of nuclear spliceosomal introns. That MatK associates with multiple intron ligands makes it an attractive model for an early trans-acting nuclear splicing activity.roup II introns are highly structured ribozymes, found in bacteria and organellar genomes of plants, fungi, protists, and some animals. They catalyze their own excision from precursor RNAs (1). In addition, bacterial group II introns are mobile genetic elements. These features, as well as structural similarities with nuclear introns, have led to the proposition that ancestors of modern group II introns have crossed kingdoms from prokaryotes to eukaryotes via eubacterial endosymbionts, and eventually evolved into nuclear introns (2). Whereas nuclear introns are removed by a large ribonucleoprotein complex called the spliceosome, each bacterial intron encodes a distinct maturase protein facilitating its splicing. The evolutionary transition from the highly specific, maturase-driven splicing toward the complex transacting spliceosomal machinery is unclear. Without any "living fossils" with a protospliceosome, a key question is how the emerging intron diversification was accompanied by a splicing machinery with the ability to act on multiple targets. At least initially, the already existing splicing factors encoded by the invading group II introns, i.e., modified maturases, may have fulfilled this task.In present day organelles, maturase genes can be found in fungal and plant mitochondria as well as in plant chloroplasts. Although mitochondria are not directly amenable to transgenic studies, there are a number of plant species, foremost tobacco, for which directed mutagenesis of chloroplast genomes is possible (3). All land plant chloroplasts with the exception of some parasitic species in the genus Cuscuta (4, 5) contain a single maturase gene called matK in the intron of the lysine tRNA-K (UUU) gene. matK is expressed at least in green tissue (6-8). Sequence and structural homologies are found to the RNA binding motif (domain X) and the reverse transcriptase domain typically found in bacterial maturases (9, 10). Both domains are involved in splicing. By contrast, domains required for the mobility of group II introns are missing in MatK.The function of matK in chloroplasts is so far unknown, but its position inside the trnK gene suggests a role for splicing the trnK precursor. Importantly, it has been suggested that other chloroplast introns are targeted by MatK as well: firstly, several chloroplast genomes o...

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mentioning

confidence: 99%

An organellar maturase associates with multiple group II introns

Zoschke

Nakamura

Liere

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

156

207

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“…In the yeast mitochondria, it is also critical for enabling splicing of the bI4 and aI4␣ introns from the cob and cox1␣ genes, respectively (2)(3)(4). LeuRS 4 forms a ternary complex with the bI4 maturase to confer splicing activity to the group I intron (5).…”

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confidence: 99%

Functional Divergence of a Unique C-terminal Domain of Leucyl-tRNA Synthetase to Accommodate Its Splicing and Aminoacylation Roles

Hsu

Rho²,

Vannella³

et al. 2006

Journal of Biological Chemistry

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Leucyl-tRNA synthetase (LeuRS) performs dual essential roles in group I intron RNA splicing as well as protein synthesis within the yeast mitochondria. Deletions of the C terminus differentially impact the two functions of the enzyme in splicing and aminoacylation in vivo. Herein, we determined that a fiveamino acid C-terminal deletion of LeuRS, which does not complement a null strain, can form a ternary complex with the bI4 intron and its maturase splicing partner. However, the complex fails to stimulate splicing activity. The x-ray co-crystal structure of LeuRS showed that a C-terminal extension of about 60 amino acids forms a discrete domain, which is unique among the LeuRSs and interacts with the corner of the L-shaped tRNA Leu . Interestingly, deletion of the entire yeast mitochondrial LeuRS C-terminal domain enhanced its aminoacylation and amino acid editing activities. In striking contrast, deletion of the corresponding C-terminal domain of Escherichia coli LeuRS abolished aminoacylation of tRNALeu and also amino acid editing of mischarged tRNA molecules. These results suggest that the role of the leucine-specific C-terminal domain in tRNA recognition for aminoacylation and amino acid editing has adapted differentially and with surprisingly opposite effects. We propose that the secondary role of yeast mitochondrial LeuRS in RNA splicing has impacted the functional evolution of this critical C-terminal domain.

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“…Thus, it should not be surprising that mRNAs that are extended in length at the 5Ј-end, many nucleotides away from the ribosome entry site, can be translated. It has been known for some years that unspliced precursor mRNAs are translated; translation of the maturases in the introns of COB and COX1 is required for subsequent excision of the introns (15).…”

Section: Discussionmentioning

confidence: 99%

“…Translation of an intron-excision maturase, encoded in the fourth intron of COB (bi4), is required for splicing of the bi4 intron and also for splicing of the fourth intron of COX1. Therefore, if bi4 maturase is not translated from the COB precursor RNA containing introns, fully spliced COX1 mRNA is not produced, and Cox1 protein cannot be translated (15).…”

Section: Figmentioning

confidence: 99%

Cbp1 Is Required for Translation of the Mitochondrial Cytochromeb mRNA of Saccharomyces cerevisiae

Islas-Osuna¹,

Ellis²,

Marnell³

et al. 2002

Journal of Biological Chemistry

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Expression of the yeast mitochondrial cytochrome b gene (COB) is controlled by at least 15 nuclear-encoded proteins. One of these proteins, Cbp1, is required for COB mRNA stability. ⌬cbp1 null strains fail to accumulate mature COB mRNA and cannot respire. Since ⌬cbp1 null strains lack mature COB transcripts, the hypothesis that Cbp1 also plays a role in translation of these mRNAs could not be tested previously. 5-End trimming of precursor COB RNA and other mitochondrial transcripts is dependent on Pet127. pet127 mutants accumulate high levels of precursor COB mRNA and have no mature mRNA. pet127 mutants respire well; this phenotype implies that COB precursor RNA is translated efficiently. With the expectation that a ⌬cbp1⌬pet127 strain might accumulate substantial levels of COB RNA, the double null strain was constructed and analyzed to test the hypothesis that Cbp1 is required for translation of COB RNA. The ⌬cbp1⌬pet127 strain does accumulate levels of COB precursor mRNA that are ϳ60% of the level of COB mRNA in the wild-type strain. However, cytochrome b protein is not synthesized, and thus the ⌬cbp1⌬pet127 strain does not respire. These results suggest that Cbp1 is required for translation of COB RNAs.The expression of mitochondrial genes at the level of transcription, RNA processing, translation, post-translational modification, and complex assembly depends on many nuclearencoded proteins that are synthesized in the cytoplasm and imported into mitochondria (1-3). Mutations in these nuclear genes often lead to respiratory deficiency, termed the pet 1 phenotype because colonies are petite in size on fermentable glucose medium. To understand how mitochondrial gene expression is regulated, the function of these nuclear PET genes must first be understood.The nuclear PET gene CBP1 encodes a protein that is imported into mitochondria and is required for the stability of the mitochondrial cytochrome b (COB) mRNA (4, 5). COB mRNA is co-transcribed with the upstream tRNA glu . The tRNA is processed from the initial transcript by mitochondrial RNaseP and tRNA 3Ј-endonuclease, leaving a transcript we have called the COB precursor RNA. The precursor is further shortened at the 5Ј-end to produce what we have called the mature COB mRNA. In a wild-type strain, there is approximately five times more mature than precursor COB RNA. In a cbp1 null strain, the mature COB mRNA is undetectable, and precursor RNA is reduced 2-to 5-fold from wild-type levels ( Fig. 1) (6). cbp1 null strains are respiratory-deficient, and no apocytochrome b is synthesized, which suggests that: the 5Ј-extension on the precursor RNA inhibits translation, the abundance of the precursor is below the threshold required for respiration (about 4% of the levels of mature mRNA in the wild-type strain), or Cbp1 is required for translation of COB RNAs. Evidence that precursor COB RNAs can be translated has come from studies of Pet127, a nuclear-encoded protein that is localized to mitochondria, where it plays a role in RNA processing. A ⌬pet127 null strain exh...

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Molecular basis of the ‘box effect’

Cited by 60 publications

References 49 publications

An organellar maturase associates with multiple group II introns

An organellar maturase associates with multiple group II introns

Functional Divergence of a Unique C-terminal Domain of Leucyl-tRNA Synthetase to Accommodate Its Splicing and Aminoacylation Roles

Cbp1 Is Required for Translation of the Mitochondrial Cytochromeb mRNA of Saccharomyces cerevisiae

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