Integrating Phylogenetics With Intron Positions Illuminates the Origin of the Complex Spliceosome

Vosseberg, Julian; Stolker, Daan; Dunk, Samuel Hermann Alexander Von Der; Snel, Berend

doi:10.1093/molbev/msad011

Cited by 13 publications

(13 citation statements)

References 101 publications

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“…Increased intron density may have facilitated some of the genome-wide tendencies that will be described below, such as increased reorganisation of composite genes for example. Even if the mechanisms that initially led to an increased prevalence of introns are likely to have been neutral 19 , this increase will have provided scope for alternative splicing and domain reorganisation that may have played an important role in the acquisition of developmental complexity 17,20–22 .…”

Section: Resultsmentioning

confidence: 99%

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Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Denoeud,

Godfroy,

Cruaud

et al. 2024

Preprint

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SUMMARYBrown seaweeds are keystone species of coastal ecosystems, often forming extensive underwater forests, that are under considerable threat from climate change. Despite their ecological and evolutionary importance, this phylogenetic group, which is very distantly related to animals and land plants, is still poorly characterised at the genome level. Here we analyse 60 new genomes that include species from all the major brown algal orders. Comparative analysis of these genomes indicated the occurrence of several major events coinciding approximately with the emergence of the brown algal lineage. These included marked gain of new orthologous gene families, enhanced protein domain rearrangement, horizontal gene transfer events and the acquisition of novel signalling molecules and metabolic pathways. The latter include enzymes implicated in processes emblematic of the brown algae such as biosynthesis of the alginate-based extracellular matrix, and halogen and phlorotannin biosynthesis. These early genomic innovations enabled the adaptation of brown algae to their intertidal habitats. The subsequent diversification of the brown algal orders tended to involve loss of gene families, and genomic features were identified that correlated with the emergence of differences in life cycle strategy, flagellar structure and halogen metabolism. We show that integration of large viral genomes has had a significant impact on brown algal genome content and propose that this process has persisted throughout the evolutionary history of the lineage. Finally, analysis of microevolutionary patterns within the genusEctocarpusindicated that deep gene flow between species may be an important factor in genome evolution on more recent timescales.

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Section: Resultsmentioning

confidence: 99%

“…, this increase will have provided scope for alternative splicing and domain reorganisation that may have played an important role in the acquisition of developmental complexity 17,[20][21][22] .…”

mentioning

confidence: 99%

Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Denoeud,

Godfroy,

Cruaud

et al. 2024

Preprint

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“…Human RBM41 is a ∼47 kDa protein with a single annotated domain, an RNA recognition motif (RRM) near the C-terminus of the protein (at positions 309–387) (Figure 1A). While no specific cellular function has been assigned to RBM41, it has been listed as a paralog of the U11/U12-65K protein ( RNPC3 ), a structural component of the U11/U12 di-snRNP complex in the minor spliceosome (Benecke et al ., 2005; Vosseberg et al ., 2023). The paralog assignment is based on the local sequence similarity between the C-terminal regions of the two proteins, that encompass the core RRM and its N-terminal expansion (Figure 1B, 1C) which in the U11/U12-65K is essential for the stability of the C-terminal RRM and its interaction with the U12 snRNA (Netter et al ., 2009).…”

Section: Resultsmentioning

confidence: 99%

“…To compare the phylogenetic similarity, we computed cosine distances between the phylogenetic profile of each automatically generated OG and RBM41. As we suspected that RBM41 was part of the minor spliceosome, we also compared the phylogenetic profile of RBM41 to the profiles of other known spliceosome proteins obtained from Vosseberg et al . (2023).…”

Section: Methodsmentioning

confidence: 99%

Distinct functions for the paralogous RBM41 and U11/U12-65K proteins in the minor spliceosome

Norppa,

Chowdhury,

van Rooijen

et al. 2023

Preprint

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In this work, we identify RBM41 as a novel unique protein component of the minor spliceosome. RBM41 has no previously recognized cellular function but has been identified as a paralog of the U11/U12-65K protein, a known unique component of the minor spliceosome that functions during the early steps of minor intron recognition as a component of the U11/U12 di-snRNP. We show that both proteins use their highly similar C-terminal RRMs to bind to 3’-terminal stem-loops in U12 and U6atac snRNAs with comparable affinity. Our BioID data indicate that the unique N-terminal domain of RBM41 is necessary for its association with complexes containing DHX8, an RNA helicase, which in the major spliceosome drives the release of mature mRNA from the spliceosome. Consistently, we show that RBM41 associates with excised U12-type intron lariats, is present in the U12 mono-snRNP, and is enriched in Cajal bodies, together suggesting that RBM41 functions in the post-splicing steps of the minor spliceosome assembly/disassembly cycle. This contrasts with the U11/U12-65K protein, which uses the N-terminal region to interact with U11 snRNP during the intron recognition step. Finally, we show that while RBM41 knockout cells are viable, they show alterations in the splicing of U12-type introns, particularly differential U12-type 3’ splice site usage. Together, our results highlight the role 3’-terminal stem-loop of U12 snRNA as a dynamic binding platform for the paralogous U11/U12-65K and RBM41 proteins, which function at distinct stages of minor spliceosome assembly/disassembly cycle.

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“…A variety of other insights into splicing evolution have come from studying organisms beyond humans and S. cerevisiae . Phylogenetic analysis of splicing proteins revealed that early spliceosomes were similarly complex to current plant and animal spliceosomes ( Roy and Irimia 2014 ), and that many spliceosomal proteins are derived from ribosomal proteins and evolved after intron proliferation ( Vosseberg et al 2023 ). Phylogenetic analysis of introns showed that there had already been substantial intron loss by the time of the Last Eukaryotic Common Ancestor (LECA) ( Vosseberg et al 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Spliceosome assembly and regulation: insights from analysis of highly reduced spliceosomes

Black

Whelan

Garside

et al. 2023

RNA

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Pre-messenger RNA splicing is catalyzed by the spliceosome, a multi-megadalton RNA-protein complex that assembles in a highly-regulated process on each intronic substrate. Most studies of splicing and spliceosomes have been carried out in human or S. cerevisiae model systems. There exists, however, a large diversity of spliceosomes, particularly in organisms with reduced genomes, that suggests a means of analyzing the essential elements of spliceosome assembly and regulation. In this review, we characterize changes in spliceosome composition across phyla, describing those that are most frequently observed and highlighting an analysis of the reduced spliceosome of the red alga Cyanidioschyzon merolae. We used homology modelling to predict what effect splicing protein loss would have on the spliceosome, based on currently available cryo-EM structures. We observe strongly correlated loss of proteins that function in the same process, e.g. in interacting with the U1 snRNP (which is absent in C. merolae), regulation of Brr2, or coupling transcription and splicing. Based on our observations, we predict splicing in C. merolae to be inefficient, inaccurate, and post-transcriptional, consistent with the apparent trend towards its elimination in this lineage. This work highlights the striking flexibility of the splicing pathway and the spliceosome when viewed in the context of eukaryotic diversity.

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Integrating Phylogenetics With Intron Positions Illuminates the Origin of the Complex Spliceosome

Cited by 13 publications

References 101 publications

Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Distinct functions for the paralogous RBM41 and U11/U12-65K proteins in the minor spliceosome

Spliceosome assembly and regulation: insights from analysis of highly reduced spliceosomes

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