A small chloroplast RNA may be required for trans-splicing in chlamydomonas reinhardtii

Goldschmidt-Clermont, Michel; Choquet, Yves; Girard‐Bascou, Jacqueline; Michel, François; Schirmer-Rahire, Michele; Rochaix, Jean‐David

doi:10.1016/0092-8674(91)90415-u

Cited by 188 publications

(143 citation statements)

References 24 publications

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“…Recent analysis of the nuclear pre-mRNA processing machinery revealed that proteins involved in RNA 3Ј-end processing are integral components of supraspliceosomes (44). This is reminiscent of the function of psaA splicing factors Rat2 and Raa1, which are both involved in 3Ј-end processing of the tscA RNA (15,22).…”

Section: Discussionmentioning

confidence: 99%

“…The psaA gene is split into three dispersed exons, which are flanked by truncated group II intron sequences (14). Whereas the second intron (psaA-i2) is bipartite, the first intron (psaA-i1) is tripartite, and the missing group II intron secondary structure is delivered in trans by the chloroplastencoded tscA RNA (15). After separate transcription, two group II introns are built up by base pairing, followed by two transsplicing reactions and, ultimately, formation of the mature psaA mRNA.…”

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confidence: 99%

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A Ribonucleoprotein Supercomplex Involved in trans-Splicing of Organelle Group II Introns

Reifschneider¹,

Marx²,

Jacobs³

et al. 2016

Journal of Biological Chemistry

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In the chloroplast of the green alga Chlamydomonas reinhardtii, two discontinuous group II introns, psaA-i1 and psaAi2, splice in trans, and thus their excision process resembles the nuclear spliceosomal splicing pathway. Here, we address the question whether fragmentation of trans-acting RNAs is accompanied by the formation of a chloroplast spliceosome-like machinery. Using a combination of liquid chromatographymass spectrometry (LC-MS), size exclusion chromatography, and quantitative RT-PCR, we provide the first characterization of a high molecular weight ribonucleoprotein apparatus participating in psaA mRNA splicing. This supercomplex contains two subcomplexes (I and II) that are responsible for trans-splicing of either psaA-i1 or psaA-i2. We further demonstrate that both subcomplexes are associated with intron RNA, which is a prerequisite for the correct assembly of subcomplex I. This study contributes further to our view of how the eukaryotic nuclear spliceosome evolved after bacterial endosymbiosis through fragmentation of self-splicing group II introns into a dynamic, protein-rich RNP machinery.The spliceosome is a dynamic RNP machinery that participates in the excision of mRNA introns in eukaryotes. This machinery consists of five small nuclear RNAs (snRNAs; U1, U2, U4, U5, and U6) and a large number of spliceosomal proteins (1, 2). It is generally accepted that spliceosomal snRNAs were derived from ancient group II introns, which were introduced into the eukaryotic cell after endosymbiosis (3, 4). Group II introns occur frequently in bacteria and organelles of fungi, algae, and higher plants but are rare in archaea and absent from nuclear genomes. Comparable with spliceosomal introns, the splicing reaction includes two transesterification reactions, yielding spliced exons and an excised intron lariat RNA.Despite the lack of significant sequence similarities, group II introns share a common secondary structure with six helical domains (D1-D6) surrounding a central wheel. During intron excision, these domains take over specific functions, and remarkably, they show plenty of functional and structural similarities to spliceosomal snRNAs (5-7). These similarities led to the assumption that during evolution of the nuclear splicing apparatus, group II introns fragmented and degenerated to spliceosomal snRNAs (3,8,9).In contrast to bacterial group II introns, most organelle group II introns display variant forms of degeneration and fragmentation (9). For example, many of the plant group II introns have mispaired domain structures (10, 11). Moreover, group II introns are able to split into autonomous fragments due to rearrangements of organelle genomes (12, 13). Consequently, they are transcribed independently, and association of precursor RNAs by base pairing generates a catalytically active group II intron structure that is finally processed by trans-splicing. Such degenerated and fragmented group II introns along with the interplay of discrete RNAs during the splicing reaction serve to demonstrate how snRNAs...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

A Ribonucleoprotein Supercomplex Involved in trans-Splicing of Organelle Group II Introns

Reifschneider¹,

Marx²,

Jacobs³

et al. 2016

Journal of Biological Chemistry

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“…A further step in fragmentation is represented by the psaA gene (of Chlamydomonas chloroplasts), which has a group II intron split into at least three parts, with a separately transcribed central fragment encoded by the tscA gene (Goldschmidt-Clermont et al 1991). The tscA fragment is thus analogous to an snRNA, being a small RNA that operates in trans in a splicing reaction.…”

Section: Fragmentation Of a Catalytic Intron Into Transacting Snrnasmentioning

confidence: 99%

On the Possibility of Constructive Neutral Evolution

1999

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Abstract. The neutral theory often is presented as a theory of "noise" or silent changes at an isolated "molecular level," relevant to marking the steady pace of divergence, but not to the origin of biological structure, function, or complexity. Nevertheless, precisely these issues can be addressed in neutral models, such as those elaborated here with regard to scrambled ciliate genes, gRNA-mediated RNA editing, the transition from selfsplicing to spliceosomal splicing, and the retention of duplicate genes. All of these are instances of a more general scheme of "constructive neutral evolution" that invokes biased variation, epistatic interactions, and excess capacities to account for a complex series of steps giving rise to novel structures or operations. The directional and constructive outcomes of these models are due not to neutral allele fixations per se, but to these other factors. Neutral models of this type may help to clarify the poorly understood role of nonselective factors in evolutionary innovation and directionality.

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“…However, others are split into two components, located with adjacent exons at widely separated positions in the mtDNA molecule. It is postulated that generation of mature transcripts involves a trans-splicing mechanism (Wolstenholme et al, , 1993Wissinger et al, 1990Wissinger et al, , 1991Bonen et al, 1990;Conklin et al, 1990;Chapdelaine and Bonen, 1991), such as that earlier described for chloroplast genes of Chlamydomonas, Nicontiana and Marchantia (Choquet et al, 1988;Hildebrand et al, 1988;Goldschmidt-Clermont et al, 1991).…”

Section: Introductionmentioning

confidence: 99%

The plant mitochondrial mat-r gene/nad1 gene complex

Wolstenhome¹

1996

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Abstract' s.We have completed sequencing segments of the maize mitochondrial (ret) DNA that contains all five of the exons (A-E) of the gene (nadl) for subunit I of the respiratory chain NADH dehydrogenase. Analysis of these sequences indicates that exons B and C are joined by a continuous group 11intron, but the remaining exons are associated with partial group H introns and are encoded at widely separated locations in the maize mtDNA molecule. Production of mature nadl gene transcripts is postulated to involve both cis-splicing of the b/c intron and trans-splicing of each of the other three introns. In the partial We intron upstream from exon E is encoded a gene (mat-r) for a protein related to fungal maturases. From comparison of the maize split d/e intron, and the soybean continuous d/e intron it was found that the location at which the maize dle intron underwent rearrangement is marked by a repeated 8 nt sequence on each intron half. Interestingly, there is a 9 or 10 nt repeat on each of the two halves of the a/b and c/d introns. We have shown that mature transcripts of the maize nadl gene contain 23 edited (CŨ ) nucleotides and that transcripts of maize and soybean mat-r genes contain 15 and 14 C~U edits, respectively. The majority of edits in nadl transcripts result in amino acid replacements that increase similarity between the maize NAD1 protein and NAD1 proteins of other plant species and of animal species. Edits in mat-r transcripts result in an increase in amino acid similarity of the maize and soybean MAT-R proteins to each other, and of each of these proteins to fungal and bryophyte maturases.We found that the intron between exons b and c is not edited. Edits in other introns are rare and have so far been detected only in domain 6 regions. Unspliced transcripts of exon C and of exon E are partially edited, confirming that editing can precede both cis-and trans-splicing.From data obtained using PCR and sequencing we have shown that transcripts containing all possible exon combinations exist in maize mitochondria. This supports the view that splicing of maize nadl exons can occur in any order, Wd that mans-splicing of exons can occur in advance of cis-splicing of exons B and C. Also, we obtained evidence that the relative rates of splicing are greater for B+C and C+D exons, than for A+B and D+E exons.Attempts made to induce cis-splicing in vitro of the B and C exons by excision of the continuous intron between them have been unsuccessful.Comparisons of nadl, nad2 and nad5 intron sequences have been made to gain information on intron interrelationships. DISCLAIMERPortions of this document may be illegible in electronic image products.Images are produced from the best available original document. * .A pseudo-mat-r gene was detected (using degenerate primers and PCR reactions), sequenced, and mapped on the maize (normal) mtDNA molecule. : 7-10-92 to 7-9-96 Objectives of the Proposed WorkThe major objective for the work outline at the time of the original application was to learn about the structur...

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A small chloroplast RNA may be required for trans-splicing in chlamydomonas reinhardtii

Cited by 188 publications

References 24 publications

A Ribonucleoprotein Supercomplex Involved in trans-Splicing of Organelle Group II Introns

A Ribonucleoprotein Supercomplex Involved in trans-Splicing of Organelle Group II Introns

On the Possibility of Constructive Neutral Evolution

The plant mitochondrial mat-r gene/nad1 gene complex

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