Molecular Biology and Evolution 17:1760-1768 (2000)
© 2000 Society for Molecular Biology and Evolution
ARTICLE |
Double-Hairpin Elements in the Mitochondrial DNA of Allomyces: Evidence for Mobility
Program in Evolutionary Biology, Canadian Institute for Advanced Research, Département de Biochimie, Université de Montréal, Montreal, Quebec, Canada
 |
Abstract |
|---|
 TOP Abstract IntroductionMaterials and MethodsResults and DiscussionAcknowledgementsliterature cited |
|---|
The mitochondrial DNA (mtDNA) of the chytridiomycete fungus Allomyces macrogynus contains 81 G+C-rich sequence elements that are 26–79 bases long and can be folded into a unique secondary structure consisting of two stem-loops. At the primary sequence level, the conservation of these double-hairpin elements (DHEs) is variable, ranging from marginal to complete identity. Forty of these DHEs are inserted in intergenic regions, 35 in introns, and 6 in variable regions of rRNA genes. Ten DHEs are inserted into other DHE elements (twins); two even form triplets. A comparison of DHE sequences shows that loop regions contain more sequence variation than helical regions and that the latter often contain compensatory base changes. This suggests a functional importance of the DHE secondary structure. We further identified nine DHEs in a 4-kb region of Allomyces arbusculus, a close relative of A. macrogynus. Eight of these DHEs are highly similar in sequence (90%–100%) to those in A. macrogynus, but only five are inserted at the same positions as in A. macrogynus. Interestingly, DHEs are also found in the mtDNAs of other chytridiomycetes, as well as certain zygomycete and ascomycete fungi. The overall distribution pattern of DHEs in fungal mtDNAs suggests that they are mobile elements.
|
Introduction |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResults and DiscussionAcknowledgementsliterature cited |
|---|
Mitochondrial genomes are extremely variable in both size and sequence, and their coding capacity (including introns and intron open reading frames [ORFs]) ranges from as much as 96% in the ciliate Paramecium aurelia to only 47% in the choanoflagellate Monosiga brevicollis (Gray et al. 1998
). mtDNAs with relatively low coding content are often loaded with repetitive sequences of variable size and primary sequence (e.g., in Saccharomyces cerevisiae [de Zamaroczy and Bernardi 1986
], Neurospora crassa [Yin, Heckman, and RajBhandary 1981
], Podospora anserina [Koll et al. 1996
], the chlorophyte alga Pedinomonas minor [Turmel et al. 1999
], and several Chlamydomonas species [Nedelcu and Lee 1998
]). These elements are usually located in intergenic regions but can also occur in introns, in variable domains of rRNA genes, and, exceptionally, in protein coding genes (Butow, Perlman, and Grossman 1985
; Wenzlau and Perlman 1990
). Depending on the case, classes of repetitive sequence elements are defined by similarities at the primary sequence level, conserved secondary structure, or both. The most frequent forms of repeats are (1) tandem repeats of the macro- or minisatellite type, (2) dispersed repeats of variable length (sometimes leading to inverted repeats), and (3) short elements with conserved secondary structure.
In most instances, the significance of such repeat sequences and structural elements for mitochondrial function remains unknown. With biochemical experiments being difficult to perform for mitochondria, especially for nonmodel species, valuable hints as to the nature of such motifs have emerged from the comparison of mtDNA sequences from closely related species (e.g., de Zamaroczy and Bernardi 1986
; Lang, O'Kelly, and Burger 1998
; Nedelcu and Lee 1998
). They might serve as control elements, involved in regulation of transcription, translation, or replication, and be conserved during evolution. Alternatively, they might simply result from errors of the mitochondrial DNA replication and DNA repair machinery or transposition of mobile elements. In any case, the accumulation of repeat elements likely favors recombination events that lead to mitochondrial genome reorganization.
Families of tandem repeats of varying complexity occur in the divergent regions of the maxicircle (mitochondrial) genomes of Leishmania tarentolae and Trypanosoma brucei, forming arrays of up to 3 kb (Muhich, Neckelmann, and Simpson 1985
; Simpson et al. 1987
). In the mtDNA of the green alga Pedinomonas minor, a 9-kb region contains exclusively repeat elements (13 families of 6–389 bp of dispersed repeats forming an elaborate superstructure), occupying more than a third of the genome (Turmel et al. 1999
). The mtDNA of another chlorophyte alga, that of Prototheca wickerhamii, also contains families of repeats consisting of nine sequence motifs of 30–200 nt in length. In this case, instead of being organized in large arrays, the repeats are dispersed throughout the genome (Wolff et al. 1994
). The mtDNA of the fungus Podospora anserina contains a large number of short repeats, dispersed mostly in single units throughout the genome (Koll et al. 1996
). Finally, the mtDNA of the red alga Porphyra purpurea contains two inverted copies of a sequence unit of 291 bp, located opposite each other on the 37-kb circular mapping mtDNA (Burger et al. 1999
). None of these repeats has an obvious cellular function; however, some if not all are recombinogenic, favoring genomic rearrangements (Muhich, Neckelmann, and Simpson 1985
; Koll et al. 1996
; Burger et al. 1999
).
Structural sequence elements constitute a second class of repetitive sequences. In the mtDNA of the fungus N. crassa, inverted repeats forming long, highly stable hairpins have been identified (Yin, Heckman, and RajBhandary 1981
). These Pst palindromes (so-called for the presence of PstI restriction sites in their primary sequence) are scattered throughout intergenic spacers and introns of the genome. In the mtDNA of the yeast S. cerevisiae, stretches of G+C-rich sequences are dispersed throughout the genome. These G+C-rich clusters have been subdivided into eight families according to their sequence similarities, and many of them can be folded into a variety of stem-and-loop structures (deZamaroczy and Bernardi 1986). They have been characterized as preferential recombination sites (Dieckmann and Gandy 1987
; Clark-Walker 1989
; Weiller, Schueller, and Schweyen 1989
; Weiller et al. 1991
), and their presence in replication origins may serve regulatory functions (deZamaroczy and Bernardi 1986). In addition, some G+C-rich clusters are unidirectionally transmitted at the DNA level during genetic crosses (Butow, Perlman, and Grossman 1985
; Wenzlau and Perlman 1990
). Interestingly, G+C-rich clusters occur in several Saccharomyces species (deZamaroczy and Bernardi 1986; Wenzlau and Perlman 1990
) but are absent from the mtDNA of the yeast Candida (Torulopsis) glabrata (Clark-Walker, McArthur, and Sriprakash 1985
), hence reinforcing the view that G+C-rich clusters are most likely mobile elements. In plant mitochondria, two different types of structural elements have been identified. Members of one family, termed palindromic repeat sequences (PRSs), are highly conserved at the primary sequence level and are believed to be mobile because of their variable occurrence in closely related plant species (Nakazono et al. 1994
). Elements in the second group are also characterized by stem-and-loop structures but are less conserved at the primary sequence level than are PRS elements and are apparently involved in RNA processing (Schuster et al. 1986
; Dombrowski, Brennicke, and Binder 1997
). Finally, 11 palindromic sequences (up to 65 nt long) displaying conserved primary sequence have been identified in the mtDNA of the green alga Chlamydomonas reinhardtii. The distribution of these sequences within the genome suggests a role in gene expression (Boer and Gray 1991
).
All of the above-mentioned sequence elements are confined to groups of closely related species, and much of their distribution can be explained by direct exchange of genetic material following sexual crosses. We identified a novel type of structural element that is different from all of the previously described elements: it is widespread in fungi and folds into a characteristic double-hairpin structure (also referred to as a double-hairpin element [DHE]). DHEs were first recognized in the 57.5-kb-long mtDNA of the chytridiomycete Allomyces macrogynus (Paquin and Lang 1996
). These elements are spread throughout intergenic spacers and introns (five of the DHEs inserted in introns introduce frameshifts of intronic ORFs), and some are inserted in variable domains of the rRNA-coding regions. DHEs are also found in the mtDNA of the closely related species Allomyces arbusculus, as well as in those of distantly related fungal groups such as Monoblepharidales, Spizellomycetales (Paquin et al. 1997
), Zygomycota (unpublished results), and Ascomycota. In this paper, we present a detailed analysis of the DHE structural features and describe the distribution patterns of DHEs in various mtDNAs. We discuss evidence that DHEs are active mobile elements and that they are transferred across species boundaries.
|
Materials and Methods |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResults and DiscussionAcknowledgementsliterature cited |
|---|
Culture Conditions, Preparation of mtDNA from A. macrogynus and A. arbusculus, and Cloning and Sequencing Strategy
Maintenance of cultures, purification of mtDNA by cesium chloride/bisbenzimide density gradient centrifugation from total cellular DNA of A. macrogynus his1 3–35 (35°C) (ATCC 46923) and A. arbusculus (ATCC 10983), and cloning and sequencing procedures have previously been described (Paquin et al. 1995
). Further information can be obtained at URL http://megasun.bch.umontreal.ca/People/lang/FMGP/.
Sequence Analysis
The complete sequence of the A. macrogynus mtDNA (Paquin and Lang 1996
; accession number U41288) and part of the A. arbusculus mtDNA (accession number AF281324) were analyzed using programs supplied in the FASTA package (Pearson and Lipman 1988
) and our collection of programs (http://megasun.bch.umontreal.ca/ogmp/ogmpid.html). DHEs were identified by visual examination following the criteria defined in the text.
cDNA Amplification
Total RNA was extracted according to Deeley et al. (1977)
, except that a 6 M guanidine-HCl solution was employed for cell lysis. One microgram of RNA was incubated with FPLC pure DNAse I (Pharmacia) at 37°C for 15 min. to eliminate DNA contaminants. The RNA was then extracted with phenol/chloroform and precipitated with ethanol. First-strand DNA synthesis was carried out with AMV reverse transcriptase (Boehringer Mannheim), as detailed by the manufacturer using the oligonucleotide 5'-AGATGGTAACCTAACTCTAC-3', a primer hybridizing downstream of DHE10 within the ORF of cobi6 (intron 6 of the apocytochrome b gene). PCR amplification was carried out after adding the primer 5'-AGCTCCTCCGAGACTACATG-3' and Vent DNA polymerase (New England Biolabs), to yield a fragment of about 800 bp covering the region in which DHE9 and DHE10 are inserted. Control experiments without first-strand cDNA synthesis were performed, showing that the amplified DNA had been amplified from reverse-transcribed RNA and not from contaminating genomic DNA.
Southern Hybridization
The PCR-amplified DNAs were separated by electrophoresis on a 0.8% agarose gel. Only one major band of the same size was observed, both for the cDNA and the genomic DNA. To ensure the detection of weaker bands indicative of partial DHE removal, the DNA was transferred on a nylon membrane (Hybond-N, Amersham) according to the manufacturer's instructions and hybridized with the gel-purified PCR fragment.
|
Results and Discussion |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResults and DiscussionAcknowledgementsliterature cited |
|---|
Distribution and Features of the DHEs
The mtDNA of A. macrogynus has a low A+T content (60%) compared with other fungal mtDNAs. This is due to the presence of numerous G+C-rich polynucleotide runs that can be folded into two adjacent, highly stable hairpin-loop structures (Paquin and Lang 1996
). We identified 81 of these DHEs in the mtDNA of A. macrogynus. DHEs are distributed throughout this genome; 40 are found in intergenic regions, 35 in introns, and 6 in variable domains of ribosomal RNA (rRNA) genes (table 1
). Among the 35 DHEs found in introns, five are inserted in intronic ORFs and introduce frameshifts.
|
DHEs range in size from 26 to 79 nt. The canonical DHE has two adjacent hairpins, contains up to two mismatches located near the central region of the DHE in one or both hairpins, generally has 3–5-nt loops, and shows extensive G-C pairings in at least one stem (fig. 1 ). Sixty-one of the 81 identified DHEs conform to this structural definition (see fig. 2a for a typical example). Fifteen of the noncanonical DHEs have larger loops (up to 8 nt) and/or do not contain at least four consecutive G-C base pairs in one of the two stems. In a further group of three DHEs, the two stems are distanced by two unpaired nucleotides. One of the noncanonical DHEs (DHE41, fig. 2b ) is inserted in a variable region of the rns gene (coding for the ribosomal RNA of the small subunit). Its deletion (on paper) makes the surrounding rRNA sequence conform almost perfectly to the Escherichia coli secondary-structure model (similar to the other five DHEs inserted in rRNA coding genes; see Paquin and Lang 1996
). Because DHEs are rich in G+C and folded, sequencing them was extremely difficult, and the precise sequence of the remaining two DHEs (DHE3 and DHE13; for location, see table 1
) could not be determined. In addition to regular DHE structures, a number of single G+C-rich hairpins are present in intergenic and intronic regions of this genome. Because they also have high G+C contents and few or no mismatches in long base-paired regions and small loops, these single hairpins are most probably derived from DHEs.
|
6 bp long
|
Primary Sequence and Secondary-Structure Conservation
The overall primary sequence similarity of DHEs spans a wide range, from little similarity (G or C polynucleotide runs in one or both of the helices) to complete identity. In performing sequence comparisons, we observed that stretches of similarity between two DHEs were sometimes interrupted by an insertion whose sequence itself folds into a typical DHE. Indeed, we found nine DHEs embedded within other DHEs, reminiscent in organization of the "twintrons" in Euglena chloroplast DNA (Copertino and Hallick 1991
). For example, in figure 3a,
four similar DHEs are shown, two of which contain an insertion of a second DHE of almost identical sequence, resulting in twin DHEs (fig. 3b
). In addition, DHE37 of the twin DHE36/37 comprises yet a further insertion, DHE38, resulting in a triple, consecutively interlocked, insertion (fig. 3b
). Interestingly, the triplet DHE36/37/38 was in an inverted orientation compared to the three other elements, indicating that the insertion of an element can occur in both orientations of transcription, whereas all identified genes are transcribed from only one strand of the mtDNA.
|
We identified 14 subgroups of two to four DHEs that were highly similar at the primary sequence level (>90% identity) and even identical in exceptional cases (table 1 ). Within these groups, the sequences of several DHEs had to be reverse-complemented in order to be aligned, supporting the concept that DHEs can be inserted in both orientations. The alignment of these similar DHEs revealed a selective pressure for maintaining a double-hairpin secondary structure. Compensatory base changes were found that maintain the base pairing, the relevance of which was further underlined by an overall higher sequence conservation in the stem versus loop regions of the elements (fig. 4 , but see also figs. 3 and 6 ). This is in contrast to some other structured RNAs, such as group I and group II introns (Michel, Umesono, and Ozeki 1989
; Michel and Westhoff 1990
), in which the primary sequences of loops tend to be more conserved than the helical regions. In some instances, this is due to conservation of tetraloop structures; in other cases, it is because of tertiary interactions that are important for the three-dimensional RNA architecture. The lack of sequence conservation in the loops of DHEs suggests that they have little structural importance and that they are not likely involved in tertiary interactions.
|
We also noted frequent (about 15% of the DHEs) alternative pairings involving flanking sequences and the central parts of a DHE. The possible pairing of the flanking sequence would elongate one of the hairpins while unfolding the other, resulting in long single hairpins or a DHE-like structure with two hairpins of unequal lengths (e.g., fig. 5a ). In other cases, the flanking sequences are implicated in alternative stem-and-loop structures (fig. 5b ). Interestingly, the alternative pairing of DHE44 includes nucleotide positions 1–8 of tRNAThr (boxed nucleotides in fig. 5b ). A similar alternative folding of DHE33 includes the tRNAArg (UCU) sequence (nucleotide positions 1–11). The effect of these strong alternative pairings is likely a reduced efficiency of maturation of tRNAs from their respective precursor RNAs.
|
Palindromic sequences in mtDNAs of other organisms, like the PstI palindromes of N. crassa (Yin, Heckman, and RajBhandary 1981
) and the PRSs of higher plants (Nakazono et al. 1994
) and of C. reinhardtii (Boer and Gray 1991
) share strong primary sequence similarity within a given species. The G+C-rich clusters of yeast have been subdivided into eight families according to their sequence similarities (de Zamaroczy and Bernardi 1986
). None of these elements have secondary-structure motifs characteristic of DHEs.
Are DHEs Spliced from Precursor RNAs?
Eleven DHEs are inserted in coding regions: six in the rRNA genes and five in intronic ORFs. The latter introduce frameshift in four ORFs, potentially inhibiting their expression. Apart from these DHE insertions, there are no further nonsense mutations in the intronic ORFs, suggesting either that insertions occurred only recently or that they are spliced out from precursor RNAs and do not interfere with the expression of the intronic ORFs. We experimentally tested the latter possibility.
We chose the ORF of cob intron 6 (cobi6), which contains two DHEs (DHE9 and DHE10), and as detailed in the methods section, we generated the cDNA encoding a portion of the intronic ORF and amplified it by PCR. After electrophoretic separation of the products in a 0.8% agarose gel, we observed a single cDNA band of the same size as PCR-amplified genomic DNA (data not shown). To further test the possibility that some spliced RNA was present at a low concentration, we transferred the amplified DNAs to a nylon membrane and hybridized with the radio-labeled PCR fragment. Again, only a single band was detected (data not shown). Finally, the PCR fragment obtained from the cDNA was cloned, and 10 independent clones were sequenced. The resulting sequences were all identical to the genomic sequence. This result implies that DHE9 and DHE10 are not spliced from this precursor RNA, at least not within the detection limits of the experiment performed.
The finding that DHE insertions are not removed from the cobi6 transcript is consistent with the observation that they never occur in structurally important portions of genes, e.g., protein-coding genes, tRNAs, highly conserved domains of rRNA structures, or the conserved core structures of group I and group II introns. Our results also parallel conclusions for G+C-rich clusters in yeast mitochondria, which are not removed or edited at the RNA level either in the var1 ORF or in rRNAs (Sor and Fukuhara 1982, 1983
; Zinn et al. 1988
).
DHEs Are Widespread in mtDNAs of Lower Fungi
In order to test the presence and distribution of DHEs in other Allomyces species, we sequenced a 4-kb fragment of the A. arbusculus mtDNA comprising the 3' region of nad5, atp6, and the 5' portion of cox1. Within this and other fragments (unpublished results), the sequence of A. arbusculus mtDNA is highly similar to that of A. macrogynus (>95%), both in coding and in intergenic regions. Nine DHEs were detected in A. arbusculus, and eight of these were 90%–100% identical to DHEs in A. macrogynus mtDNA. Five of these eight DHEs were inserted at the same position as in A. macrogynus, while three others appeared in different genome locations in the two species (table 1
). For example, DHE16 is located in the intergenic spacer between nad5 and atp6 of A. macrogynus. The corresponding region of A. arbusculus contains an identical DHE insertion (DHEa1; fig. 6a
). However, it has an insertion of a twin DHE of 62 nt (DHEa2; fig. 6b
), whereas DHE16 is uninterrupted. An almost identical copy of the DHEa2 sequence was also found in intron 1 of cox1 (DHEa3) of A. arbusculus. In addition, DHE14 (inserted in the nad5 intron 3 of A. macrogynus) is identical in sequence to DHEa2 (fig. 6b
). These results indicate that not only are DHEs present in A. arbusculus mtDNA, but they also seem to show similar patterns of distribution and organization within both Allomyces mtDNAs.
|
DHEs have also been identified in other chytridiomycete mtDNAs, as well as in zygomycete and ascomycete mtDNAs, namely, in three members of the Monoblepharidales (Monoblepharella sp., Harpochytrium #105, and Harpochytrium #94), in the Spizellomycetales (Spizellomyces punctatus), in the zygomycetes Rhizopus stolonifer and Mucor mucedo, and in the ascomycete Schizosaccharomyces octosporus (Paquin et al. 1997
; unpublished data). However, other lower fungal mtDNAs, such as those of Rhizophydium sp. (Chytridiales) and Mortierella verticillata (Zygomycota, Mortierellales) seem to be devoid of DHEs. The number of DHEs in these genomes is not always as high as that in Allomyces mtDNAs. Although this wide distribution of DHEs may reflect acquisition by lateral transfer, we cannot exclude the possibility that DHEs are ancient elements and that they were vertically inherited and occasionally lost in certain evolutionary lineages.
Do DHEs Have a Function in Mitochondrial Recombination?
Because of their sequence similarity and their structure, DHEs could be used as preferential recombination sites, similar to GC clusters in yeast mitochondria (Dieckmann and Gandy 1987
; Clark-Walker 1989
; Weiller, Schueller, and Schweyen 1989
; Weiller et al. 1991
). When comparing A. macrogynus and A. arbusculus sequences, we found three macrodeletions within three genomic fragments of approximately 4 kb each (this study and unpublished data). One, a 300-bp deletion in A. macrogynus mtDNA, occurred in the intergenic region between nad4l and atp9 (coding for subunits of the NADH-ubiquinone dehydrogenase and of the ATP synthetase complex, respectively). This region contains three DHEs in A. macrogynus (table 1
), and, most interestingly, the deletion is mapped within one of them (DHE59). Instead of the 300-bp fragment present in A. arbusculus, DHE59 in A. macrogynus contains a twin DHE (DHE81) not present in the former. In the other two cases (a 1-kb deletion that includes an unidentified ORF in A. arbusculus and a 600-bp deletion that includes an intronic ORF in A. macrogynus), the deletions were not mapped within DHEs, although we identified several of them near the deletion boundaries. These results provide evidence that DHEs actively contribute to the plasticity of mtDNAs.
Are DHEs Mobile?
The distribution pattern of DHEs is reminiscent of mobile elements. They are widely dispersed throughout A. macrogynus and A. arbusculus mtDNAs. Five of the nine DHEs identified in A. arbusculus are highly similar to and located at the same positions as their A. macrogynus counterparts, suggesting that DHEs were present in the mtDNA of the common ancestor of the two species. The difference in location of three other similar DHEs most likely reflects transposition events that occurred only recently, after the divergence of the two closely related Allomyces species, suggesting that DHEs are still active. Their scattered distribution in mtDNAs of lower fungi also favors the hypothesis that DHEs are mobile. Some mtDNAs, like that of Monoblepharella sp., contain numerous DHEs, whereas that of close relatives like Harpochytrium sp. contain relatively few. Similarly, the mtDNA of S. octosporus contains few DHEs, whereas that of its close relative Schizosaccharomyces pombe contains none (unpublished data). We believe that such a sporadic, uneven distribution is due to lateral acquisition of DHEs and their ongoing propagation.
This is not the first claim that small palindromic sequences could be mobile. PRSs are variably inserted into the mtDNA of rice species and are believed to be mobile (Nakazono et al. 1994
). In some yeast strains, two optional G+C-rich clusters called a and cc are inserted into the coding region of the mitochondrial var1 gene. During genetic crosses between a-cc- and a+cc+, nonparental genotypes were observed at a high frequency. Since there was no coconversion of flanking markers, these results were explained by G+C cluster mobility rather than by regular, homologous recombination (Butow, Perlman, and Grossman 1985
; Wenzlau and Perlman 1990
). There is compelling evidence that the transposition of the yeast mitochondrial elements occurs at the DNA level (Wenzlau and Perlman 1990
), probably following a "cut and paste" model (reviewed in Grindley and Reed 1985
). This is supported by the observation of in vivo double-strand cuts near G+C-rich clusters (Zinn et al. 1988
) and the duplication of two nucleotides flanking the mobile G+C-rich clusters.
The existence of twin DHEs in which the insertion was limited to the double-hairpin structure without disrupting that of the surrounding DHE (figs. 3 and 6 ) indicates that mobility of DHEs does not result in the coconversion of flanking markers. However, the mechanism of transposition of DHEs is likely to be different from that of G+C-rich clusters, since duplications of nucleotides are not consistently observed in the flanking sequences of DHEs. In addition, the evolutionary pressure to maintain the double-hairpin structure of DHEs includes the option that they transpose via an RNA intermediate and that the secondary structure is essential for mobility.
|
|
Acknowledgements |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResults and DiscussionAcknowledgementsliterature cited |
|---|
We thank Drs. G. Burger, C. Bullerwell, and I. Debie for comments on the manuscript and C. Bullerwell for sharing unpublished information on the presence of DHEs in S. octosporus. This work was supported by an operating grant (MT-14028) of the Medical Research Council (Canada) and by scholarships (B.P.) from the Natural Sciences and Engineering Research Council (Canada) and the Formation de Chercheurs et l'Aide à la Recherche funds (FCAR, Québec). Generous donations of equipment from Sun Microsystems Inc. are gratefully acknowledged, as is salary (B.F.L.) and interaction support from the Canadian Institute for Advanced Research.
|
Footnotes |
|---|
Geoffrey McFadden, Reviewing Editor
1 Present address: Galileo Genomics Inc., Montreal, Quebec, Canada. 
1 Keywords: double hairpins
repetitive sequences
mobile elements
fungi
comparative RNA modeling
2 Address for correspondence and reprints: B. Franz Lang, Département de Biochimie, Université de Montréal, CP 6128 succ. Centre-Ville, Montreal, Quebec, Canada H3C 3J7. E-mail: franz.lang{at}umontreal.ca
|
literature cited |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResults and DiscussionAcknowledgementsliterature cited |
|---|
Boer, P. H., and M. W. Gray. 1991. Short dispersed repeats localized in spacer regions of Chlamydomonas reinhardtii mitochondrial DNA. Curr. Genet. 19:309–312.[Web of Science][Medline]
Burger, G., D. Saint-Louis, M. W. Gray, and B. F. Lang. 1999. Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea: cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 11:1–22.
Butow, R., P. Perlman, and L. Grossman. 1985. The unusual varl gene of yeast mitochondrial DNA. Science 228:1496–1501.
Clark-Walker, G. D., C. R. McArthur, and K. S. Sriprakash. 1985. Location of transcriptional control signals and transfer RNA sequences in Torulopsis glabrata mitochondrial DNA. EMBO J. 4:465–473.[Web of Science][Medline]
Clark-Walker, G. D. 1989. In vivo rearrangement of mitochondrial DNA in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 86:8847–8851.
Copertino, D. W., and R. B. Hallick. 1991. Group II twintron: an intron within an intron in a chloroplast cytochrome b-559 gene. EMBO J. 10:433–442.[Web of Science][Medline]
de Zamaroczy, M., and G. Bernardi. 1986. The GC clusters of the mitochondrial genome of yeast and their evolutionary origin. Gene 41:1–22.
Deeley, R. G., J. I. Gordon, A. T. H. Burns, K. P. Mullinix, M. Binastein, and R. F. Goldberg. 1977. Primary activation of the vitellogenin gene in the rooster. J. Biol. Chem. 252:8310–8319.
Dieckmann, C. L., and B. Gandy. 1987. Preferential recombination between GC clusters in yeast mitochondrial DNA. EMBO J. 6:4197–4203.[Web of Science][Medline]
Dombrowski, S., A. Brennicke, and S. Binder. 1997. 3'-Inverted repeats in plant mitochondrial mRNAs are processing signals rather than transcription terminators. EMBO J. 16:5069–5076.[Web of Science][Medline]
Gray, M. W., B. F. Lang, R. Cedergren et al. (15 co-authors). 1998. Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res. 26:865–878.
Grindley, N. D. F., and R. R. Reed. 1985. Transpositional recombination in prokaryotes. Annu. Rev. Biochem. 54:863–896.[Web of Science][Medline]
Koll, F., J. Boulay, L. Belcour, and Y. d'Aubenton-Carafa. 1996. Contribution of ultra-short invasive elements to the evolution of the mitochondrial genome in the genus Podospora. Nucleic Acids Res. 24:1734–1741.
Lang, B. F., C. J. O'Kelly, and G. Burger. 1998. Mitochondrial genomics in protists, an approach to probing eukaryotic evolution. Protist 149:313–322.
Michel F., K. Umesono, and H. Ozeki. 1989. Comparative and functional anatomy of group II catalytic introns—a review. Gene 82:5–30.
Michel, F., and E. Westhoff. 1990. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J. Mol. Biol. 216:585–610.[Web of Science][Medline]
Muhich, M. L., N. Neckelmann, and L. Simpson. 1985. The divergent region of the Leishmania tarentolae kinetoplast maxicircle DNA contains a diverse set of repetitive sequences. Nucleic Acids Res. 13:3241–3260.
Nakazono, M., A. Kanno, N. Tsutsumi, and A. Hirai. 1994. Palindromic repeated sequences (PRSs) in the mitochondrial genome of rice: evidence for their insertion after divergence of the genus Oryza from the other Gramineae. Plant Mol. Biol. 24:273–281.
Nedelcu, A. M., and R. W. Lee. 1998. Short repetitive sequences in green algal mitochondrial genomes: potential roles in mitochondrial genome evolution. Mol. Biol. Evol. 15:690–701.[Abstract]
Paquin, B., L. Forget, I. Roewer, and B. F. Lang. 1995. Molecular phylogeny of Allomyces macrogynus: congruency between nuclear ribosomal RNA- and mitochondrial protein-based trees. J. Mol. Evol. 41:657–665.[Web of Science][Medline]
Paquin, B., M.-J. Laforest, L. Forget, I. Roewer, Z. Wang, J. Longcore, and B. F. Lang. 1997. The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression. Curr. Genet. 31:380–395.[Web of Science][Medline]
Paquin, B., and B. F. Lang. 1996. The mitochondrial DNA of Allomyces macrogynus: the complete genomic sequence from an ancestral fungus. J. Mol. Biol. 255:688–701.[Web of Science][Medline]
Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444–2448.
Schuster, W., R. Hiesel, P. G. Isaac, C. J. Leaver, and A. Brennicke. 1986. Transcript termini of messenger RNAs in higher plant mitochondria. Nucleic Acids Res. 14:5943–5954.
Simpson, L., N. Neckelmann, V. F. de la Cruz, A. M. Simpson, J. E. Feagin, D. P. Jasmer, and K. Stuart. 1987. Comparison of the maxicircle (mitochondrial) genomes of Leishmania tarentolae and Trypanosoma brucei at the level of nucleotide sequence. J. Biol. Chem. 262:6182–6196.
Sor, F., and H. Fukuhara. 1982. Nature of an inserted sequence in the mitochondrial gene coding for the 15S ribosomal RNA of yeast. Nucleic Acids Res. 10:1625–1633.
———. 1983. Complete DNA sequence coding for the large ribosomal RNA of yeast mitochondria. Nucleic Acids Res. 11:339–348.
Turmel, M., C. Lemieux, G. Burger, B. F. Lang, C. Otis, I. Plante, and M. W. Gray. 1999. The complete mitochondrial DNA sequence of Nephroselmis olivacea and Pedinomonas minor: two radically different evolutionary patterns within green algae. Plant Cell 11:1717–1730.
Weiller, G., H. Bruckner, S. H. Kim, E. Pratje, and R. F. Schweyen. 1991. A GC cluster repeat is a hotspot for mit- macro-deletions in yeast mitochondrial DNA. Mol. Gen. Genet. 226:233–240.[Web of Science][Medline]
Weiller, G., C. M. E. Schueller, and R. F. Schweyen. 1989. Putative target sites for mobile G+C rich clusters in yeast mitochondrial DNA: single elements and tandem arrays. Mol. Gen. Genet. 218:272–283.[Web of Science][Medline]
Wenzlau, J. M., and P. S. Perlman. 1990. Mobility of two optional G+C-rich clusters of the var1 gene of yeast mitochondrial DNA. Genetics 126:53–62.
Wolff, G., I. Plante, B. F. Lang, U. Kück, and G. Burger. 1994. Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. J. Mol. Biol. 237:75–86.
Yin, S., J. Heckman, and U. L. RajBhandary. 1981. Highly conserved GC-rich palindromic DNA sequences flank tRNA genes in Neurospora crassa mitochondria. Cell 26:325–332.
Zinn, A. R., J. K. Pohlman, P. S. Perlman, and R. A. Butow. 1988. In vivo double-strand breaks occur at recombinogenic G+C-rich sequences in the yeast mitochondrial genome. Proc. Natl. Acad. Sci. USA 85:2686–2690.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  Q. Meng, Y. Zhang, and X.-Q. Liu Rare Group I Intron with Insertion Sequence Element in a Bacterial Ribonucleotide Reductase Gene J. Bacteriol., March 1, 2007; 189(5): 2150 - 2154. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Seif, J. Leigh, Y. Liu, I. Roewer, L. Forget, and B. F. Lang Comparative mitochondrial genomics in zygomycetes: bacteria-like RNase P RNAs, mobile elements and a close source of the group I intron invasion in angiosperms Nucleic Acids Res., February 2, 2005; 33(2): 734 - 744. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. B. Moore, K. M. Ferguson, W. K. W. Loh, O. Hoegh-Guldberg, and D. A. Carter Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium Int J Syst Evol Microbiol, November 1, 2003; 53(6): 1725 - 1734. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. E. Bullerwell, L. Forget, and B. F. Lang Evolution of monoblepharidalean fungi based on complete mitochondrial genome sequences Nucleic Acids Res., March 15, 2003; 31(6): 1614 - 1623. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. E. Bullerwell, J. Leigh, L. Forget, and B. F. Lang A comparison of three fission yeast mitochondrial genomes Nucleic Acids Res., January 15, 2003; 31(2): 759 - 768. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Forget, J. Ustinova, Z. Wang, V. A. R. Huss, and B. Franz Lang Hyaloraphidium curvatum: A Linear Mitochondrial Genome, tRNA Editing, and an Evolutionary Link to Lower Fungi Mol. Biol. Evol., March 1, 2002; 19(3): 310 - 319. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||