Mitochondrial Plasmids
| Fungal mitochondrial plasmids | Plant mitochondrial plasmids |
| Partially or completely sequenced fungal mitochondrial plasmids | Neurospora crassa Plasmids |
In addition to mobile genetic elements associated with mtDNA, such as mobile introns and certain repetitive elements, extragenomic DNA molecules are frequently detected in fungal mitochondria. These elements can be divided into two groups; those that are derived from the mitochondrial genome via intra- or inter-molecular recombination and true plasmids that are autonomously-replicating genetic elements having little or no homology with the host genome. The former group has been intensely studied in the filamentous fungus Podospora anserina where it has been demonstrated that they are associated with a cell death phenomenon, called senescence. Called senDNAs (among other names), the closed circular, multimeric DNA molecules are derived from one of several regions of the mtDNA (reviewed by Griffiths 1992). Other well-studied examples of the formation of circular DNAs derived from mtDNA occur in Neurospora crassa (Bertrand et al. 1980; de Vries et al. 1986) and Aspergillus nidulans (Lazarus et al. 1980). Called “stoppers” or “ragged,” respectively, these DNAs are found in certain growth-defective mutants and show similarities to some of the senDNAs.
True plasmids are DNAs (or RNAs) that have little or no homology to mtDNA and replicate separately from the mitochondrial genome. Most mt plasmids encode polymerases that are involved in their replication. Initially discovered by chance, surveys of various genera indicate that they are widespread, especially among filamentous fungi. They have been studied most thoroughly in Neurospora spp., and it is estimated that more than half of all natural isolates contain one or more plasmid type (Arganoza et al. 1994; Griffiths 1995). The finding of highly similar plasmids in distantly related fungi infers that these elements are horizontally transmitted, and is further supported by laboratory studies that demonstrate plasmids can readily be transmitted via anastomosis.
A list of all reported fungal mitochondrial plasmids is in Table A and those plasmids that have been completely sequenced are shown in the Table B and those found in Neurospora crassa are in Table C.
In general, mitochondrial plasmids fall into specific groups based on their replication cycle which is dictated by the polymerase(s) they encode. The most common are DNA plasmids (encoding a DNA polymerase), which can be further divided by their structure, being either linear or circular. Linear plasmids have similar features: they usually encode an RNA polymerase in addition to the DNA polymerase and contain terminal inverted repeats having 5’-linked terminal proteins. Circular types generally only have a single ORF encoding the DNA polymerase. Another group of fungal mt plasmids encode a reverse transcriptase (RT), and are classified as retroplasmids. Although similar in size and shape to the DNA plasmids, the replication cycle of the retroplasmids is quite distinct (Kennell et al. 1994). Based on some unique characteristics of the mechanism of replication, it has been proposed that these elements represent a type of “molecular fossil,” which is defined as a contemporary genetic element that is ancient in origin (Maizels and Weiner 1993), and thereby can provide information about the evolutionary history of other retroelements, including telomerase (Wang and Lambowitz 1993; Walther and Kennell 1999).
In most cases, mitochondrial plasmids have little or no effect on their fungal host. Although there is a report that at high temperatures they may provide a small benefit to their host (Bok and Griffiths 2000) that could help explain their prevalence, it is generally assumed that plasmids are parasites and represent a type of selfish DNA. In some cases, certain plasmids can be quite detrimental and cause senescence. Two well-studied senescent plasmid groups are linear DNA plasmids of the Kalilo group, and retroplasmids of the Mauriceville group. When strains containing these natural plasmids are subjected to repeated transfer, cultures frequently senescence, a process that is associated with the integration of the plasmid or plasmid-derivatives into the mtDNA and additional recombinations that lead to large deletions or rearrangement in the mtDNA (Griffiths 1992). Other studies show that certain plasmids are also capable of causing mitochondrial dysfunction without integration, by over-replicating and interfering with mitochondrial translation (Stevenson et al. 2000). Although senescence has rarely been observed in nature, these studies indicate that, under certain circumstances, mitochondrial plasmids harm their fungal host. Correspondingly, a mitochondrial plasmid harbored by certain strains of the chestnut-blight fungus Cryphonectria parasitica is associated with the attenuation of virulence (reviewed by Bertrand 2000).
References
| Arganoza MT, Min J, Hu Z and Akins RA (1994). Distribution of seven homology groups of mitochondrial plasmids in Neurospora: evidence for widespread mobility between species in nature. Curr Genet 26: 62-73. |
| Bertrand H (2000). Role of mitochondrial DNA in the senescence and hypovirulence of fungi and potential for plant disease control. Annu Rev Phytopathol 38: 397-422. |
| Bertrand H, Collins RA, Stohl LL, Goewert RR and Lambowitz AM (1980). Deletion mutants of Neurospora crassa mitochondrial DNA and their relationship to the "stop-start" growth phenotype. Proc Natl Acad Sci USA 77: 6032-6036. |
| Bok JW and Griffiths AJ (2000). Possible benefits of kalilo plasmids to their Neurospora hosts. Plasmid 43: 176-180. |
| de Vries H, Schrage C and de Jonge JC (1986). The mitochondrial DNA of Neurospora crassa: deletion by intramolecular recombination and the expression of mitochondrial genes. Basic Life Sci 40: 57-65. |
| Griffiths AJ (1992). Fungal senescence. Annu Rev Genet 26: 351-372. |
| Griffiths AJ (1995). Natural plasmids of filamentous fungi. Microbiol Rev 59: 673-685. |
| Kennell JC, Wang H and Lambowitz AM (1994). The Mauriceville plasmid of Neurospora spp. uses novel mechanisms for initiating reverse transcription in vivo. Mol Cell Biol 14: 3094-3107. |
| Maizels N and Weiner AM (1993). The genomic tag hypothesis: modern viruses as molecular fossils of ancient strategies for genomic replication. In: RF Gesteland and JA Atkins, eds. The RNA World. 1st ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp 577-602. |
| Stevenson CB, Fox AN and Kennell JC (2000). Senescence associated with the over-replication of a mitochondrial retroplasmid in Neurospora crassa. Mol Gen Genet 263: 433-444. |
| Walther TC and Kennell JC (1999). Linear mitochondrial plasmids of F. oxysporum are novel, telomere-like retroelements. Mol Cell 4: 229-238. |
| Wang H and Lambowitz AM (1993). The Mauriceville plasmid reverse transcriptase can initiate cDNA synthesis de novo and may be related to reverse transcriptase and DNA polymerase progenitor. Cell 75 1071-1081. |
