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Group II intron splicing factors in plant mitochondria.

Brown GG, Colas des Francs-Small C, Ostersetzer-Biran O - Front Plant Sci (2014)

Bottom Line: Recently, we established the roles of two of these paralogs in Arabidopsis, nMAT1 and nMAT2, in the splicing of mitochondrial introns.In addition to the nMATs, genetic screens led to the identification of other genes encoding various factors, which are required for the splicing and processing of mitochondrial introns in plants.In this review we will summarize recent data on the splicing and processing of mitochondrial introns and their implication in plant development and physiology, with a focus on maturases and their accessory splicing cofactors.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, McGill University Montreal, QC, Canada.

ABSTRACT
Group II introns are large catalytic RNAs (ribozymes) which are found in bacteria and organellar genomes of several lower eukaryotes, but are particularly prevalent within the mitochondrial genomes (mtDNA) in plants, where they reside in numerous critical genes. Their excision is therefore essential for mitochondria biogenesis and respiratory functions, and is facilitated in vivo by various protein cofactors. Typical group II introns are classified as mobile genetic elements, consisting of the self-splicing ribozyme and its intron-encoded maturase protein. A hallmark of maturases is that they are intron specific, acting as cofactors which bind their own cognate containing pre-mRNAs to facilitate splicing. However, the plant organellar introns have diverged considerably from their bacterial ancestors, such as they lack many regions which are necessary for splicing and also lost their evolutionary related maturase ORFs. In fact, only a single maturase has been retained in the mtDNA of various angiosperms: the matR gene encoded in the fourth intron of the NADH-dehydrogenase subunit 1 (nad1 intron 4). Their degeneracy and the absence of cognate ORFs suggest that the splicing of plant mitochondria introns is assisted by trans-acting cofactors. Interestingly, in addition to MatR, the nuclear genomes of angiosperms also harbor four genes (nMat 1-4), which are closely related to maturases and contain N-terminal mitochondrial localization signals. Recently, we established the roles of two of these paralogs in Arabidopsis, nMAT1 and nMAT2, in the splicing of mitochondrial introns. In addition to the nMATs, genetic screens led to the identification of other genes encoding various factors, which are required for the splicing and processing of mitochondrial introns in plants. In this review we will summarize recent data on the splicing and processing of mitochondrial introns and their implication in plant development and physiology, with a focus on maturases and their accessory splicing cofactors.

No MeSH data available.


Related in: MedlinePlus

Model for mis-splicing of mitochondrial group II introns. A schematic illustration of a model for the splicing and mis-splicing of angiosperm nad5 transcripts based on the model of Elina and Brown (2010). The cis-splicing of introns 1 and 4 proceeds normally. If the trans-splicing intron 3 assembles prior to the assembly of the trans-splcing intron 2, it splices correctly, and intron 2 can assemble and splice correctly to generate a properly spliced and functional mRNA. If intron 2 assembles first, however, a sequence at the 3' end of intron 3a (the portion of the intron co-transcribed with exon c) base pairs with a sequence within exon a, preventing correct positioning of the 5' splice site of intron 2. This results in the joining of exon c to sites within exon b to form mis-spliced, non-functional transcripts composed of exon a, a portion of exon b, exon c, and intron 3a; these transcripts do not engage in further splicing. A hybrid lariat mis-splicing product composed of intron 2 and a portion of exon b is also formed.
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Figure 3: Model for mis-splicing of mitochondrial group II introns. A schematic illustration of a model for the splicing and mis-splicing of angiosperm nad5 transcripts based on the model of Elina and Brown (2010). The cis-splicing of introns 1 and 4 proceeds normally. If the trans-splicing intron 3 assembles prior to the assembly of the trans-splcing intron 2, it splices correctly, and intron 2 can assemble and splice correctly to generate a properly spliced and functional mRNA. If intron 2 assembles first, however, a sequence at the 3' end of intron 3a (the portion of the intron co-transcribed with exon c) base pairs with a sequence within exon a, preventing correct positioning of the 5' splice site of intron 2. This results in the joining of exon c to sites within exon b to form mis-spliced, non-functional transcripts composed of exon a, a portion of exon b, exon c, and intron 3a; these transcripts do not engage in further splicing. A hybrid lariat mis-splicing product composed of intron 2 and a portion of exon b is also formed.

Mentions: The nad5 gene in most angiosperms contains four group II introns, of which the second and third flank a small, 22 bp exon and splice in “trans.” The formation of a mature nad5 mRNA therefore involves the production of three independently transcribed transcripts and two distinct RNA-RNA associations through which the functional second and third introns assemble and splice. Analysis of partially spliced products generated when only one of the two trans-splicing events had occurred, revealed that these reactions must take place in a particular sequence (see Figure 3). When the splicing of the third intron precedes that of the second, a properly trans-spliced intermediate is formed that is competent to correctly engage in the other trans-splicing event. If the two portions of the second intron associate prior to the removal of the third intron, however, in a number of monocot and dicot plants, including plants of the Arabidopsis, Brassica, Beta, Zea, and Triticum genera, a variety of mis-spliced products are generated in which the correct 3' splice site is joined to any of a number of sites present in exon b (Elina and Brown, 2010). A model to explain these surprising results was formulated based on the observation that the 3' end of the portion of the third intron co-transcribed with exon c contained a sequence that was potentially capable of forming an extended duplex with the first exon. It was proposed that when the initial base-pairing interactions between the two portions of the second intron occurred, the sequences from the third intron and exon a annealed. This interaction sterically hindered the 3' splice site from assuming a position where it could join the correct 5' splice site; instead the 3' splice site joined to a variety of alternative sites within the upstream exon.


Group II intron splicing factors in plant mitochondria.

Brown GG, Colas des Francs-Small C, Ostersetzer-Biran O - Front Plant Sci (2014)

Model for mis-splicing of mitochondrial group II introns. A schematic illustration of a model for the splicing and mis-splicing of angiosperm nad5 transcripts based on the model of Elina and Brown (2010). The cis-splicing of introns 1 and 4 proceeds normally. If the trans-splicing intron 3 assembles prior to the assembly of the trans-splcing intron 2, it splices correctly, and intron 2 can assemble and splice correctly to generate a properly spliced and functional mRNA. If intron 2 assembles first, however, a sequence at the 3' end of intron 3a (the portion of the intron co-transcribed with exon c) base pairs with a sequence within exon a, preventing correct positioning of the 5' splice site of intron 2. This results in the joining of exon c to sites within exon b to form mis-spliced, non-functional transcripts composed of exon a, a portion of exon b, exon c, and intron 3a; these transcripts do not engage in further splicing. A hybrid lariat mis-splicing product composed of intron 2 and a portion of exon b is also formed.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 3: Model for mis-splicing of mitochondrial group II introns. A schematic illustration of a model for the splicing and mis-splicing of angiosperm nad5 transcripts based on the model of Elina and Brown (2010). The cis-splicing of introns 1 and 4 proceeds normally. If the trans-splicing intron 3 assembles prior to the assembly of the trans-splcing intron 2, it splices correctly, and intron 2 can assemble and splice correctly to generate a properly spliced and functional mRNA. If intron 2 assembles first, however, a sequence at the 3' end of intron 3a (the portion of the intron co-transcribed with exon c) base pairs with a sequence within exon a, preventing correct positioning of the 5' splice site of intron 2. This results in the joining of exon c to sites within exon b to form mis-spliced, non-functional transcripts composed of exon a, a portion of exon b, exon c, and intron 3a; these transcripts do not engage in further splicing. A hybrid lariat mis-splicing product composed of intron 2 and a portion of exon b is also formed.
Mentions: The nad5 gene in most angiosperms contains four group II introns, of which the second and third flank a small, 22 bp exon and splice in “trans.” The formation of a mature nad5 mRNA therefore involves the production of three independently transcribed transcripts and two distinct RNA-RNA associations through which the functional second and third introns assemble and splice. Analysis of partially spliced products generated when only one of the two trans-splicing events had occurred, revealed that these reactions must take place in a particular sequence (see Figure 3). When the splicing of the third intron precedes that of the second, a properly trans-spliced intermediate is formed that is competent to correctly engage in the other trans-splicing event. If the two portions of the second intron associate prior to the removal of the third intron, however, in a number of monocot and dicot plants, including plants of the Arabidopsis, Brassica, Beta, Zea, and Triticum genera, a variety of mis-spliced products are generated in which the correct 3' splice site is joined to any of a number of sites present in exon b (Elina and Brown, 2010). A model to explain these surprising results was formulated based on the observation that the 3' end of the portion of the third intron co-transcribed with exon c contained a sequence that was potentially capable of forming an extended duplex with the first exon. It was proposed that when the initial base-pairing interactions between the two portions of the second intron occurred, the sequences from the third intron and exon a annealed. This interaction sterically hindered the 3' splice site from assuming a position where it could join the correct 5' splice site; instead the 3' splice site joined to a variety of alternative sites within the upstream exon.

Bottom Line: Recently, we established the roles of two of these paralogs in Arabidopsis, nMAT1 and nMAT2, in the splicing of mitochondrial introns.In addition to the nMATs, genetic screens led to the identification of other genes encoding various factors, which are required for the splicing and processing of mitochondrial introns in plants.In this review we will summarize recent data on the splicing and processing of mitochondrial introns and their implication in plant development and physiology, with a focus on maturases and their accessory splicing cofactors.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, McGill University Montreal, QC, Canada.

ABSTRACT
Group II introns are large catalytic RNAs (ribozymes) which are found in bacteria and organellar genomes of several lower eukaryotes, but are particularly prevalent within the mitochondrial genomes (mtDNA) in plants, where they reside in numerous critical genes. Their excision is therefore essential for mitochondria biogenesis and respiratory functions, and is facilitated in vivo by various protein cofactors. Typical group II introns are classified as mobile genetic elements, consisting of the self-splicing ribozyme and its intron-encoded maturase protein. A hallmark of maturases is that they are intron specific, acting as cofactors which bind their own cognate containing pre-mRNAs to facilitate splicing. However, the plant organellar introns have diverged considerably from their bacterial ancestors, such as they lack many regions which are necessary for splicing and also lost their evolutionary related maturase ORFs. In fact, only a single maturase has been retained in the mtDNA of various angiosperms: the matR gene encoded in the fourth intron of the NADH-dehydrogenase subunit 1 (nad1 intron 4). Their degeneracy and the absence of cognate ORFs suggest that the splicing of plant mitochondria introns is assisted by trans-acting cofactors. Interestingly, in addition to MatR, the nuclear genomes of angiosperms also harbor four genes (nMat 1-4), which are closely related to maturases and contain N-terminal mitochondrial localization signals. Recently, we established the roles of two of these paralogs in Arabidopsis, nMAT1 and nMAT2, in the splicing of mitochondrial introns. In addition to the nMATs, genetic screens led to the identification of other genes encoding various factors, which are required for the splicing and processing of mitochondrial introns in plants. In this review we will summarize recent data on the splicing and processing of mitochondrial introns and their implication in plant development and physiology, with a focus on maturases and their accessory splicing cofactors.

No MeSH data available.


Related in: MedlinePlus