Spliceosomal genes in the D. discoideum genome: a comparison with those in H. sapiens, D. melanogaster, A. thaliana and S. cerevisiae

Yu, Bing; Fey, Petra; Kestin-Pilcher, Karen E.; Fedorov, Alexei; Prakash, Ashwin; Chisholm, Rex L.; Wu, Jane Y.

doi:10.1007/s13238-011-1052-z

Cited by 9 publications

(12 citation statements)

References 45 publications

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“…3. Although exon-skipping has been previously demonstrated at similarly low frequency in other unicellular organisms (15)(16)(17), no such examples of this type of alternative splicing had been previously demonstrated in this organism. More importantly, however, is the demonstration here that several of the S. pombe exons that were identified as subject to skipping are highly conserved across eukaryotic species spanning several major eukaryotic lineages, and that experimental evidence exists for the alternative splicing of the orthologous exons in mammalian species.…”

Section: Discussionmentioning

confidence: 68%

“…Two "smoking guns" that would corroborate early functional exon skipping have been previously suggested: environmentally or developmentally regulated exon skipping in a unicellular eukaryote, and conservation of a particular exonskipping pattern across eukaryotic kingdoms (11,14). Although examples of exon skipping in a few unicellular eukaryotes have been published (15)(16)(17), to our knowledge there are no published examples of either evolutionarily conserved or environmentally regulated exon-skipping events in any unicellular eukaryote.…”

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confidence: 80%

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Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolutionarily conserved with humans

Awan

Manfredo

Pleiss

2013

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

114

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Alternative splicing is a potent regulator of gene expression that vastly increases proteomic diversity in multicellular eukaryotes and is associated with organismal complexity. Although alternative splicing is widespread in vertebrates, little is known about the evolutionary origins of this process, in part because of the absence of phylogenetically conserved events that cross major eukaryotic clades. Here we describe a lariat-sequencing approach, which offers high sensitivity for detecting splicing events, and its application to the unicellular fungus, Schizosaccharomyces pombe, an organism that shares many of the hallmarks of alternative splicing in mammalian systems but for which no previous examples of exon-skipping had been demonstrated. Over 200 previously unannotated splicing events were identified, including examples of regulated alternative splicing. Remarkably, an evolutionary analysis of four of the exons identified here as subject to skipping in S. pombe reveals high sequence conservation and perfect length conservation with their homologs in scores of plants, animals, and fungi. Moreover, alternative splicing of two of these exons have been documented in multiple vertebrate organisms, making these the first demonstrations of identical alternative-splicing patterns in species that are separated by over 1 billion y of evolution.pre-mRNA splicing | post-transcriptional gene regulation | phylogeny T he protein coding regions of eukaryotic genes are typically interrupted by noncoding introns that must be removed to produce a translatable mRNA. The removal of introns, catalyzed by the spliceosome, offers a powerful opportunity for an organism to regulate gene expression. In mammals, where individual genes are often interrupted by multiple introns, it is now abundantly clear that the process of intron removal provides a critical regulatory control point for both qualitative and quantitative aspects of gene expression (1). By changing the identity of the exons that are included within the final mRNA, the process of alternative splicing plays a critical role in expanding the diversity of proteins that can be synthesized within a cell (2). Moreover, alternative splicing can direct the production of isoforms of genes that are directly targeted to cellular decay pathways, providing a mechanism to quantitatively regulate gene expression (3, 4).In mammalian organisms the predominant form of alternative splicing is exon skipping, wherein different combinations of exons are included in the final transcript. In contrast, exon skipping is far less prevalent in simpler eukaryotes (5, 6); however, recent studies suggest that splicing in the last eukaryotic common ancestor was similar in many respects to splicing in vertebrates, in so much as it was intron-dense (7-9), had degenerate splice site sequences (10), and likely had many of the proteins involved in alternative splicing (11,12). Intron density correlates positively with the prevalence of alternative splicing across the eukaryotic kingdoms (13), and thus it has...

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Section: Discussionmentioning

confidence: 68%

mentioning

confidence: 80%

Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolutionarily conserved with humans

Awan

Manfredo

Pleiss

2013

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

114

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“…The N-terminal domain contains RDR and RS repeats, which is a signature of SR proteins in D . discoideum [11], and can be subdivided into a RS-domain (aa 1–220) followed by a basic domain (aa 221–400). The DdDUF926 domain (aa 401–510) is highly conserved and shows ~70% identity with the one in mammalian NKAP.…”

Section: Resultsmentioning

confidence: 99%

“…In a large sequence survey using dictybase (http://dictybase.org/index.html) high sequence similarity was found between human and D . discoideum spliceosomal proteins including SR proteins [11]. The RS domains in D .…”

Section: Introductionmentioning

confidence: 99%

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The C-Terminal SynMuv/DdDUF926 Domain Regulates the Function of the N-Terminal Domain of DdNKAP

et al. 2016

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NKAP (NF-κB activating protein) is a highly conserved SR (serine/arginine-rich) protein involved in transcriptional control and splicing in mammals. We identified DdNKAP, the Dictyostelium discoideum ortholog of mammalian NKAP, as interacting partner of the nuclear envelope protein SUN-1. DdNKAP harbors a number of basic RDR/RDRS repeats in its N-terminal domain and the SynMuv/DUF926 domain at its C-terminus. We describe a novel and direct interaction between DdNKAP and Prp19 (Pre mRNA processing factor 19) which might be relevant for the observed DdNKAP ubiquitination. Genome wide analysis using cross-linking immunoprecipitation-high-throughput sequencing (CLIP-seq) revealed DdNKAP association with intergenic regions, exons, introns and non-coding RNAs. Ectopic expression of DdNKAP and its domains affects several developmental aspects like stream formation, aggregation, and chemotaxis. We conclude that DdNKAP is a multifunctional protein, which might influence Dictyostelium development through its interaction with RNA and RNA binding proteins. Mutants overexpressing full length DdNKAP and the N-terminal domain alone (DdN-NKAP) showed opposite phenotypes in development and opposite expression profiles of several genes and rRNAs. The observed interaction between DdN-NKAP and the DdDUF926 domain indicates that the DdDUF926 domain acts as negative regulator of the N-terminus.

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Non-coding RNAs in Dictyostelium discoideum and Other Dictyostelid Social Amoebae

2013

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Spliceosomal genes in the D. discoideum genome: a comparison with those in H. sapiens, D. melanogaster, A. thaliana and S. cerevisiae

Cited by 9 publications

References 45 publications

Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolutionarily conserved with humans

Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolutionarily conserved with humans

The C-Terminal SynMuv/DdDUF926 Domain Regulates the Function of the N-Terminal Domain of DdNKAP

Non-coding RNAs in Dictyostelium discoideum and Other Dictyostelid Social Amoebae

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