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Mutualism Between Self‑Splicing Introns and Their Hosts

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Mutualism Between Self‑Splicing Introns and Their Hosts www.biomedcentral.com/bmcbiol U A A A U U A - U P9.1 G - C G - C U - G P9.2 A U U A C A C A U G C A G G G G U A A G G - - - - - - - A - - - - - - - U C U A U U C U G U A C G U C G C G C G P9 A A A 3’ C A P12 exon2 P9.0a A G U td c U U U C U U c A C G A A - U 60 A G a A P9.0b G U A P10 u G - C P5 A A U G - C U - G c A - U A - U 5’SS G - U - C - G C C u G AC P7.2 C P1 g - C 10 C - G U - G 70 A A g - C 3’SS U - A P7 C - G A A g G - C G A U - G u A - U A - U C - G exon1 U - A A G td U P4 C - G A A C - G UA G - C C U U - A A C C - G 5’ IMAGEA C - G C - G P7.1 U - A C - G G - A P6 C G A - U U G C - A U P3 G U - A U U 80 U U A C - G A A U - G U A A U - A A A G - U G A A 860 A - U U U G - C G - C U - A U - A U - A U - A G - C A - U P2 G - C P8 P6a U - A U - A A - U A - U A - U A - U G - C 20 A - U C - G 90 G - U G - C A C A - U G A A U C - G U G U - G 850 U U F I-TevI OR Learning to live together: mutualism between self‑splicing introns and their hosts David Edgell, Venkata R Chalamcharla & Marlene Belfort Editorial Office BMC Biology BioMed Central Ltd Floor 6, 236 Gray’s Inn Road London WC1X 8HB United Kingdom Tel: +44 (0) 20 3192 2000 Fax: +44 (0) 20 3192 2011 Email: [email protected] Editor: Miranda Robertson Deputy Editors: Penelope Austin, Ann Le Good Assistant Editor: Kester Jarvis Editorial Assistant: Alice Plane Senior Journal Development Editor: Ciaran O’Neill Editorial Administrators: Gaby Anderson, Vikki Bean Production Manager: Caroline Hering Production staff: Eddy Baker, Rahila Esposito, Ross Hopkins Editorial Board Michael Adams (USA) Susan Gasser (Switzerland) Julian Lewis (UK) Paolo Sassone-Corsi (USA) John Aitchison (Canada) Ronald N Germain (USA) Tomas Lindahl (UK) Alexander Schier (USA) Michael Akam (UK) Dave Goeddel (USA) Andrew Lumsden (UK) Dirk Schübeler (Switzerland) Richard W Aldrich (USA) Joseph L Goldstein (USA) Nancy Maizels (USA) Frank Slack (USA) Brenda J Andrews (Canada) Corey Goodman (USA) James L Manley (USA) Lukas Sommer (Switzerland) John Archibald (Canada) Douglas Green (USA) Philippa Marrack (USA) Ralf Sommer (Germany) Michael Ashburner (UK) Rachel Green (USA) Mark Marsh (UK) Nahum Sonenberg (Canada) Naama Barkai (Israel) Gillian Griffiths (UK) Bruce J Mayer (USA) Stephen R Sprang (USA) Konrad Basler (Switzerland) James Gusella (USA) Malcolm McConville (Australia) David L Stern (USA) David Baulcombe (UK) Stephen Harrison (USA) Jacopo Meldolesi (Italy) Paul Sternberg (USA) Stephen J Benkovic (USA) Richard Henderson (UK) Elliot Meyerowitz (USA) Charles F Stevens (USA) William Bentley (USA) Michael O Hengartner Christopher Miller (USA) Brigitta Stockinger (UK) Sally Blower (USA) (Switzerland) Danesh Moazed (USA) Kevin Struhl (USA) John Brookfield (UK) Rolf Hilgenfeld (Germany) Cesare Montecucco (Italy) Michael P Stryker (USA) Michael Brown (USA) Toshio Hirano (Japan) Dino Moras (France) Masatoshi Takeichi (Japan) Patrick O Brown (USA) Hermann-Georg Holzhütter David O Morgan (USA) Guenter Theissen (Germany) Anne Calof (USA) (Germany) Keith E Mostov (USA) Julie A Theriot (USA) George M Church (USA) H Robert Horvitz (USA) Sean Munro (UK) Masaru Tomita (Japan) James E Cleaver (USA) Jonathan Howard (Germany) Shuh Narumiya (Japan) Mathias Uhlen (Sweden) Philip T Cohen (UK) Tim Hunt (UK) Claus Nielsen (Denmark) Frank Uhlmann (UK) Philip A Cole (USA) Laurence D Hurst (UK) Brian Oliver (USA) Gijsbertus T.J. van der Horst Martha Constantine-Paton Philip W Ingham (Singapore) Zoltan Oltvai (USA) (Netherlands) (USA) Paul Insel (USA) Jan Pawlowski (Switzerland) Ulrich H von Andrian (USA) Roland Contreras (Belgium) Nancy Ip (China) Tony Pawson (Canada) Leslie B Vosshall (USA) Nancy L Craig (USA) Thomas Jessell (USA) Gregory A Petsko (USA) Virginia Walbot (USA) Antoine Danchin (France) Alexander Johnson (USA) Gerd Pfeifer (USA) Peter Walter (USA) Ivan Dikic (Germany) Cynthia Kenyon (USA) David Pimentel (USA) James L Weber (USA) Richard Durbin (UK) Alan R Kimmel (USA) Mu-ming Poo (USA) Robin A Weiss (UK) Dieter Ebert (Switzerland) Mary-Claire King (USA) Martin Raff (UK) Jonathan S Weissman (USA) Michael B Eisen (USA) Marc Kirschner (USA) Dagmar Ringe (USA) James Wells (USA) Adrian Elcock (USA) Eugene Koonin (USA) John Rossi (USA) Jamie Williamson (USA) Sarah C Elgin (USA) Anders Krogh (Denmark) Steven Salzberg (USA) Bruce R Zetter (USA) James Ferrell (USA) Angus I Lamond (UK) Joshua R. Sanes (USA) Michael Zhang (USA) Wolf B. Frommer (USA) Arthur D Lander (USA) Carmen Sapienza (USA) Arturo Zychlinsky (Germany) Edgell DR et al. BMC Biology 2011, 9:22 http://www.biomedcentral.com/1741-7007/9/22 review Open Access Learning to live together: mutualism between self‑splicing introns and their hosts David R Edgell1*, Venkata R Chalamcharla2,3 and Marlene Belfort2* Abstract data argue that the relationship is more elaborate than previously appreciated. Group I and II introns can be considered as molecular parasites that interrupt protein-coding and structural Mobile introns: ribozymes with baggage RNA genes in all domains of life. They function as self- One group of mobile genetic elements comprises the group I splicing ribozymes and thereby limit the phenotypic and II introns. These sequences interrupt protein-coding and costs associated with disruption of a host gene while structural RNA genes in all domains of life and can be con­ they act as mobile DNA elements to promote their sidered as molecular parasites. When the gene is trans­cribed spread within and between genomes. Once considered into RNA, the intron sequence acts as a ribozyme (an RNA purely selfish DNA elements, they now seem, in the with enzymatic activity), which removes the intron sequence light of recent work on the molecular mechanisms from the primary RNA transcript, thus limiting the regulating bacterial and phage group I and II intron phenotypic cost associated with insertion of the element into dynamics, to show evidence of co-evolution with their a host gene and promoting their maintenance in the genome. hosts. These previously underappreciated relationships In the case of group I and II introns, the host-parasite serve the co-evolving entities particularly well in times relationship is enriched by the fact that the introns of environmental stress. themselves have been invaded by smaller parasitic elements – genes that encode mobility-promoting activities that enable the DNA element to move within and between One of the most intricate relationships in biology is that genomes [10]. Thus, at least two levels of parasitism exist for between a host and a parasite. Almost all organisms mobile introns: the intron in the host gene it interrupts, and studied so far harbor mobile genetic elements and/or the invading gene in the intron. Collectively, the intron and their derivatives. At the genomic level, the traditional its encoded mobility protein (often termed an intron- view of mobile elements is that they provide seemingly encoded protein, IEP) collaborate to form a composite little or no benefit to the host while parasitizing the host’s mobile element that utilizes host DNA replication, recombi­ cellular machinery to promote element mobility through nation and repair pathways to spread [11], while the ribozyme complex molecular pathways [1,2]. The host’s response to activity ensures that it does not disrupt the function of genes these elements is primarily defensive, as evidenced by the into which it is inserted. Accordingly, it has become evident many forms of negative regulation that downregulate the that there is an extraordinary degree of co-evolution among activity of mobile elements [3-8]. The persistence of a IEPs, the introns that house them, and the host organism. mobile element in a given population is thus the result of This review highlights several recent studies probing the a delicate balance between an excessive mutational interplay among self-splicing introns in bacterial and phage burden on the host caused by the element’s unrestricted genomes, their genes, and their bacterial and phage hosts. activity, and excessive negative regulation imposed by the host on the element to limit mobility. While the Group I introns relationship between host and mobile element is often Group I introns commonly inhabit bacterial, organellar, viewed as a molecular arms race [9], recent experimental bacteriophage and viral genomes, and the ribosomal RNA genes (rDNA) of eukaryotes, and produce a self- splicing RNA [12]. Group II introns have a similar *Correspondence: [email protected], [email protected] 1Department of Biochemistry, Schulich School of Medicine and Dentistry, distribution, except that they are not found in eukaryotic The University of Western Ontario, London, Ontario, Canada N6A 5C1 nuclear genes. Group I and group II introns show little Full list of author information is available at the end of the article primary sequence conservation, yet their RNAs each © 2010 Author et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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