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Mass migration of a group I intron: promiscuity on a grand scale (Gray, 1998)

This article from Michael Gray gives some background information about the group I introns. The title is interesting since any engineer should be reluctant to accept mass migrations of DNA. Let’s also see what he means by ‘promiscuity’, a teleological term not fit for evolutionary science because it implies intent. The concept of homing is not entire clear to me, as it also implies intent and I wonder if it is relevant to mitochondria since there would be no cross-over between mitochondrial and nuclear DNA. This seems to be ignored although crucial for this process.

Both genetically and biochemically, group I introns are rather special. At the RNA level, they are inherently autocatalytic, mediating their own removal from transcripts containing them and effecting the ligation of flanking exons (self-splicing) (1). Many group I introns are mobile elements, able to spread in genetic crosses to alleles that do not contain them via a process known as intron homing (2). Homing is initiated by a site-specific endonuclease encoded by the intron. Additionally, several group I introns specify protein cofactors (maturases) that function in the splicing of the intron RNA that encodes them (1, 2). Although a given group I intronic reading frame almost always specifies either endonuclease or maturase activity, there are a few cases known in which the encoded protein can perform both functions (3, 4).

To date, most studies of group I intron mobility have dealt with intraorganismal transfer occurring between intron+ and intron alleles of particular genes during genetic crosses. Little is known about the frequency and extent of horizontal transfer of group I introns between organisms that do not mate. Most such identified cases involve transfer into the same genome (e.g., mitochondrial) in taxa that at least belong to the same phylum (see ref. 5). There is, however, one reported instance in which interphylum (and interorganellar) transfer of group I introns appears to have occurred (6). Even so, nothing remotely approaching the extraordinary intron radiation reported by Cho et al. in this issue of the Proceedings (5) has been documented previously.

This is the commentary on another article that showa that a common intron position between a fungal nuclear (?) donor and a plant mitochondrial gene. This is interpreted as wide-spread intron insertion but can be easily explained by a loss in most but a few, and in more agreement with an original gene that possessed introns.

What these workers have uncovered is an explosive invasion of plant mitochondrial DNA (mtDNA) by a particular group I intron. The authors were led to the present study by a previous finding (7) of this curious intron in the gene encoding subunit 1 of cytochrome oxidase (cox1) in the mtDNA of an angiosperm (flowering plant), Peperomia polybotrya. Not only is this the sole group I intron so far reported in the mtDNA of vascular plants (in contrast to the frequent presence of group II introns in plant mtDNA), it clearly is of a different evolutionary origin than the gene in which it resides. In fact, phylogenetic evidence suggests that this intron arose recently by horizontal transfer from a fungal donor species (7). In the initial study (7), the intron was not found in cox1 from 19 other diverse plant species, and a follow-up investigation (8) indicated that it was restricted to the single genus Peperomia within the order Piperales. […] From this survey, the authors infer 32 separate cases of intron acquisition among the 278 genera and 281 species of angiosperm examined in the botanical equivalent of a “zoo blot.” Extrapolating to angiosperms as a whole, Cho et al. (5) come to the startling conclusion that this intron has invaded the cox1 gene >1,000 times among the >13,500 genera and >300,000 species of extant flowering plants.

Here a nice example of circular reasoning: the article proposes that extensive intron homing is necessary, but for intron homing, the genes need to be in the same physical location, but they are not. So instead of concluding that intron homing is not possible, he concludes that the genes had to be in physical proximity since intron homing was observed and simply calls this promiscuity. And he continues with ‘that being the case …’.

(ii) How does horizontal transfer actually take place at the cellular level? For intron homing to occur, both the intron-containing donor DNA and the intronless recipient DNA must be in the same physical location; the intron+ DNA must be satisfactorily transcribed; and the encoded endonuclease must be correctly translated. Because cox1 is encoded in the mitochondrial genome, this implies that the cox1 intron homing described by Cho et al. (5) takes place within mitochondria. That being the case, the mitochondrial transcription and translation systems…

 

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