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Group II Intron Retroelements: Function and Diversity

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Group II Intron Retroelements: Function and Diversity Diversity of Retrotransposable Elements Cytogenet Genome Res 110:589–597 (2005) DOI: 10.1159/000084992 Group II intron retroelements: function and diversity A.R. Robart, S. Zimmerly Department of Biological Sciences, University of Calgary, Calgary, Alberta (Canada) Manuscript received 16 October 2003; accepted in revised form for publication by J.-N. Volff 8 December 2003. Abstract. Group II introns are a class of retroelements capa- and bacterial introns with regard to structures, insertion pat- ble of carrying out both self-splicing and retromobility reac- terns and inferred behaviors. We also discuss the evolution of tions. In recent years, the number of known group II introns has group II introns, as they are the putative ancestors of spliceoso- increased dramatically, particularly in bacteria, and the new mal introns and possibly non-LTR retroelements, and may information is altering our understanding of these intriguing have played an important role in the development of eukaryote elements. Here we review the basic properties of group II genomes. introns, and summarize the differences between the organellar Copyright © 2005 S. Karger AG, Basel Group II introns are a unique type of genetic element with catalytic core of the ribozyme (Fig. 1A) (Michel and Ferat, two remarkable properties. They are catalytic RNAs, or ribo- 1995; Qin and Pyle, 1998). Domain I is the largest domain and zymes, that can excise themselves from pre-mRNA without the is also important for catalysis, while domain VI contains the aid of proteins. They are also retroelements that encode reverse bulged A that forms the branch site in the spliced product. transcriptases (RTs) and can insert themselves into new loca- RNA structures are divided into two major classes, IIA and IIB, tions. Group II introns are present in mitochondria and chloro- with class IIC being a minor class of bacterial introns. plasts of plants and fungi, where they are relatively abundant The ORF is encoded within the loop of domain IV (Fig. 1A) (Michel et al., 1989), and they are also found in about 25% of and has four functionally defined domains: RT (reverse trans- eubacterial genomes, in either full-length or truncated forms criptase activity, with sub-domains 0–7), X (maturase activity (Ferat and Michel, 1993; Dai and Zimmerly, 2002). Recently, associated with intron splicing), D (non-conserved DNA-bind- they were found even in some archaebacterial species (Dai and ing domain) and En (endonuclease activity) (Fig. 1B) (Zimmer- Zimmerly, 2003; Rest and Mindell, 2003; Toro, 2003). Due to ly et al., 2001; Belfort et al., 2002; San Filippo and Lambowitz, the burgeoning information from the genome projects, our 2002). The protein serves two functions for the intron. It assists knowledge about the introns has increased significantly in the intron splicing in vivo through an activity associated with the X past few years, and this review emphasizes this new genomic domain (maturase activity), and it also allows the intron to act and comparative perspective. as a mobile element and invade intronless sites, a process which The typical group II intron consists of a conserved intron involves all four of the ORF domains, as well as the catalytic RNA structure and an RT ORF. The RNA structure is com- RNA activity. prised of six domains, of which domain V is believed to be the Self-splicing reaction Ribozyme activity was the first property assigned to group Supported by the Canadian Institutes of Health Research (CIHR) and by Alberta II introns (van der Veen et al., 1986; Peebles et al., 1987). Self- Heritage Foundation for Medical Research (AHFMR). splicing is accomplished by two transesterifications (Fig. 2A). Request reprints from Dr. Steven Zimmerly In the first step, the 5) exon is defined through two base-pairing Department of Biological Sciences, University of Calgary 2500 University Dr. NW, Calgary, AB T2N 1N4 (Canada) interactions, in which the intron binding sequences (IBS) 1 and telephone: (403) 220-7933; fax: (403) 289-9311; e-mail: [email protected] 2 pair to their corresponding exon binding sequences (EBS) Fax + 41 61 306 12 34 © 2005 S. Karger AG, Basel Accessible online at: ABC E-mail [email protected] 1424–8581/05/1104–0589$22.00/0 www.karger.com/cgr www.karger.com Fig. 1. Basic group II intron structure. (A) Simplified secondary structure of IIB introns, composed of six structural domains, with the ORF located in domain IV. The intron is shown by black lines, exons by thick gray lines, and the ORF by a dotted black line. Black dots indicate individual nucleotides involved in base pairing tertiary interactions. The most important tertiary interactions are IBS1,2,3/EBS1,2,3, Á–Á) and ‰–‰), which are indicated by gray lines and arrows. For IIA introns, ‰) is located at the first nucleotide of Fig. 2. Reactions performed by group II introns. (A) Self-splicing reac- the 3) exon rather than in domain I, and there is no IBS3/EBS3 pairing. See tion. Self-splicing is catalyzed by the intron RNA structure through two Toor et al. (2001) for detailed information about RNA structural subclasses. transesterification reactions, yielding spliced exons and intron lariat. The (B) Intron-encoded ORF domains. The ORF consists of an RT domain (out- bulged A branch site that attacks the 5)-splice site is shown in domain VI of lined gray boxes; reverse transcriptase with sub-domains 0–7), domain X Fig. 1A. (B) Basic mechanism of group II intron mobility. The intron lariat in (solid box; maturase domain), domain D (hatched box; DNA binding an RNP particle (lariat+RT) reverse splices into the top strand of the DNA domain, not conserved in sequence among different ORFs), and the En target site. The bottom strand is cleaved by the En domain, and the intron is domain (double-hatched box; endonuclease domain). Exons are dark gray, reverse transcribed. Recombination and repair activities complete the inser- and intron RNA structure light gray. tion. 1 and 2 (Fig. 1A). The two interactions position the 5) splice site bond of the 3) junction, resulting in exon ligation and release of in proximity to the bulged adenosine in DVI (Jacquier and the intron lariat (Fig. 2A). Because the number of phosphate Michel, 1987). The 2)-OH of the adenosine acts as a nucleo- bonds broken and created during the reaction is equal, splicing phile, attacking the phosphodiester bond of the 5) junction to is energetically neutral and reversible, and does not require break the bond and form a lariat intermediate with a 2)–5) link- energy sources such as ATP. age (Fig. 2A). The self-splicing reaction in vitro requires relatively ex- In the second splicing step, the 3) exon is defined by two, treme reaction conditions of salt, magnesium and sometimes single-base-pair interactions, which vary for the RNA structur- temperature (e.g., 500 mM KCl, 100 mM MgCl2, 45°C) (Jarrell al classes. For IIA introns, the base pairs are Á–Á) and ‰–‰), et al., 1988), and it is known that protein factors are required while for IIB and IIC introns, they are Á–Á) and IBS3-EBS3 for splicing of introns in vivo. For many introns, the most (Fig. 1A) (Jacquier and Michel, 1990; Costa et al., 2000). The important splicing factor is the intron-encoded protein. Upon second transesterification is similar to the first, but with the transcription, the protein is translated from unspliced mRNA, now free 3)-OH of the 5) exon attacking the phosphodiester and binds to a high affinity binding site in domain IVA in un- 590 Cytogenet Genome Res 110:589–597 (2005) spliced intron (Fig. 1A) (Wank et al., 1999). Combined with markers (Eskes et al., 2000). The pathways differ with regard to contacts with other regions of the intron RNA, the protein the role of double-strand break repair (DSBR) activities that induces structural changes that stimulate self-splicing (Matsuu- complete the insertion event. In bacteria, group II introns have ra et al., 2001; Noah and Lambowitz, 2003), to yield spliced not been observed to coconvert exon markers, and mobility exons and a ribonucleoprotein (RNP) particle consisting of a occurs in RecA– strains, indicating independence from a gener- lariat with the protein still attached. This RNP is the entry mol- al DSBR system during retrohoming (Mills et al., 1997; Cousi- ecule to the mobility pathway. neau et al., 1998; Martı´nez-Abarca and Toro, 2000). Interestingly, many bacterial introns do not encode En domains (Fig. 3B), yet appear to be mobile. The best studied of The basic intron mobility reaction these is the Sinorhizobium intron RmInt1 (Martı´nez-Abarca et al., 2000; Muñoz-Adelantado et al., 2003), which is efficiently Mobility of group II introns occurs through a simple yet spe- mobile in vivo even though it does not have an En domain. A cialized mechanism. In the predominant event, retrohoming, similar process was characterized for an Ll.ltrB intron with a the introns invade double-stranded DNA targets with high site mutated En domain (Zhong and Lambowitz, 2003). The data specificity (Moran et al., 1995). Non-site-specific mobility, or suggested a mechanism in which the intron reverse splices into retrotransposition, also occurs (see below) (Mueller et al., 1993; the double-stranded DNA target, and cDNA synthesis is Sellem et al., 1993; Cousineau et al., 2000; Martı´nez-Abarca primed by the 3) end of a DNA at the replication fork, rather and Toro, 2000), but the majority of characterized introns than priming by cleaved target DNA. home to consistent and predictable locations. A final variation of mobility is insertion into noncognate Homing is initiated by recognition of the DNA target site by sites, known as retrotransposition.
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