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      Comprehensive database and evolutionary dynamics of U12-type introns

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          Abstract

          During nuclear maturation of most eukaryotic pre-messenger RNAs and long non-coding RNAs, introns are removed through the process of RNA splicing. Different classes of introns are excised by the U2-type or the U12-type spliceosomes, large complexes of small nuclear ribonucleoprotein particles and associated proteins. We created intronIC, a program for assigning intron class to all introns in a given genome, and used it on 24 eukaryotic genomes to create the Intron Annotation and Orthology Database (IAOD). We then used the data in the IAOD to revisit several hypotheses concerning the evolution of the two classes of spliceosomal introns, finding support for the class conversion model explaining the low abundance of U12-type introns in modern genomes.

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          The origins of genome complexity.

          Michael Lynch, John Conery (2003)
          Complete genomic sequences from diverse phylogenetic lineages reveal notable increases in genome complexity from prokaryotes to multicellular eukaryotes. The changes include gradual increases in gene number, resulting from the retention of duplicate genes, and more abrupt increases in the abundance of spliceosomal introns and mobile genetic elements. We argue that many of these modifications emerged passively in response to the long-term population-size reductions that accompanied increases in organism size. According to this model, much of the restructuring of eukaryotic genomes was initiated by nonadaptive processes, and this in turn provided novel substrates for the secondary evolution of phenotypic complexity by natural selection. The enormous long-term effective population sizes of prokaryotes may impose a substantial barrier to the evolution of complex genomes and morphologies.
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            A catalogue of splice junction sequences.

            S M Mount (1982)
            Splice junction sequences from a large number of nuclear and viral genes encoding protein have been collected. The sequence CAAG/GTAGAGT was found to be a consensus of 139 exon-intron boundaries (or donor sequences) and (TC)nNCTAG/G was found to be a consensus of 130 intron-exon boundaries (or acceptor sequences). The possible role of splice junction sequences as signals for processing is discussed.
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              Rates of in situ transcription and splicing in large human genes

              Jarnail Singh, Richard A. Padgett (2009)
              Transcription and splicing must proceed over genomic distances of hundreds of kilobases in many human genes. However, the rates and mechanisms of these processes are poorly understood. We have used the compound 5,6-Dichlorobenzimidazole 1-b-D-ribofuranoside (DRB) that reversibly blocks gene transcription in vivo combined with quantitative RT-PCR to analyze the transcription and RNA processing of several long human genes. We found that the rate of RNA polymerase II transcription over long genomic distances is about 3.8 kb per minute and is nearly the same whether transcribing long introns or exon rich regions. We also determined that co-transcriptional pre-mRNA splicing of U2-dependent introns occurs within 5–10 minutes of synthesis irrespective of intron length between 1 kb and 240 kb. Similarly, U12-dependent introns were co-transcriptionally spliced within 10 minutes of synthesis confirming that these introns are spliced within the nuclear compartment. These results show that the expression of large genes is surprisingly rapid and efficient.
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                Author and article information

                Contributors
                Devlin C Moyer
                Graham E Larue:
                ORCID: http://orcid.org/0000-0001-7881-7203
                Courtney E Hershberger
                Scott W Roy:
                ORCID: http://orcid.org/0000-0001-7354-6459
                Richard A Padgett
                Journal
                Journal ID (nlm-ta): Nucleic Acids Res
                Journal ID (iso-abbrev): Nucleic Acids Res
                Journal ID (publisher-id): nar
                Title: Nucleic Acids Research
                Publisher: Oxford University Press
                ISSN (Print): 0305-1048
                ISSN (Electronic): 1362-4962
                Publication date (Print): 27 July 2020
                Publication date (Electronic): 02 June 2020
                Publication date PMC-release: 02 June 2020
                Volume: 48
                Issue: 13
                Pages: 7066-7078
                Affiliations
                Department of Cardiovascular and Metabolic Sciences, Lerner Research Institute, Cleveland Clinic Lerner College of Medicine, Cleveland Clinic and Department of Molecular Medicine, Case Western Reserve University , Cleveland, OH 44106, USA
                Department of Molecular and Cell Biology, University of California, Merced , Merced, CA 95343, USA
                Department of Cardiovascular and Metabolic Sciences, Lerner Research Institute, Cleveland Clinic Lerner College of Medicine, Cleveland Clinic and Department of Molecular Medicine, Case Western Reserve University , Cleveland, OH 44106, USA
                Department of Biology, San Francisco State University , San Francisco, CA 94132, USA
                Department of Cardiovascular and Metabolic Sciences, Lerner Research Institute, Cleveland Clinic Lerner College of Medicine, Cleveland Clinic and Department of Molecular Medicine, Case Western Reserve University , Cleveland, OH 44106, USA
                Author notes
                To whom correspondence should be addressed. Tel: +1 831 420 7720; Email: egrahamlarue@ 123456gmail.com
                Correspondence may also be addressed to Devlin C. Moyer. Email: devmoy@ 123456gmail.com
                Correspondence may also be addressed to Scott W. Roy. Email: scottwroy@ 123456gmail.com
                Correspondence may also be addressed to Richard A. Padgett. Email:  padgetr@ 123456ccf.org

                The authors wish it to be known that, in their opinion, the first two authors should be regarded as Joint First Authors.

                Author information
                http://orcid.org/0000-0001-7881-7203
                http://orcid.org/0000-0001-7354-6459
                Article
                Publisher ID: gkaa464
                DOI: 10.1093/nar/gkaa464
                PMC ID: 7367187
                PubMed ID: 32484558
                SO-VID: f1bef31a-e99b-408a-989f-43797ab144e3
                Copyright © © The Author(s) 2020. Published by Oxford University Press on behalf of Nucleic Acids Research.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Date accepted : 20 May 2020
                Date revision received : 19 May 2020
                Date received : 07 April 2020
                Page count
                Pages: 13
                Funding
                Funded by: National Institutes of Health, DOI 10.13039/100000002;
                Award ID: R01GM104059
                Award ID: R01GM133989
                Funded by: National Science Foundation, DOI 10.13039/100000001;
                Award ID: 1616878
                Award ID: 1751372
                Categories
                Subject: AcademicSubjects/SCI00010
                Subject: Computational Biology

                ScienceOpen disciplines: Genetics
                Data availability:
                ScienceOpen disciplines: Genetics

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