Abstract
Among eukaryotes, plasmids have been found in fungi and plants but not in animals. Most plasmids are mitochondrial. In filamentous fungi, plasmids are commonly encountered in isolates from natural populations. Individual populations may show a predominance of one type, but some plasmids have a global distribution, often crossing species boundaries. Surveys have shown that strains can contain more than one type of plasmid and that different types appear to be distributed independently. In crosses, plasmids are generally inherited maternally. Horizontal transmission is by cell contact. Circular plasmids are common only in Neurospora spp., but linear plasmids have been found in many fungi. Circular plasmids have one open reading frame (ORF) coding for a DNA polymerase or a reverse transcriptase. Linear plasmids generally have two ORFs, coding for presumptive DNA and RNA polymerases with amino acid motifs showing homology to viral polymerases. Plasmids often attain a high copy number, in excess of that of mitochondrial DNA. Linear plasmids have a protein attached to their 5' end, and this is presumed to act as a replication primer. Most plasmids are neutral passengers, but several linear plasmids integrate into mitochondrial DNA, causing death of the host culture. Inferred amino acid sequences of linear plasmid ORFs have been used to plot phylogenetic trees, which show a fair concordance with conventional trees. The circular Neurospora plasmids have replication systems that seem to be evolutionary intermediates between the RNA and the DNA worlds.
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- Akins R. A., Grant D. M., Stohl L. L., Bottorff D. A., Nargang F. E., Lambowitz A. M. Nucleotide sequence of the Varkud mitochondrial plasmid of Neurospora and synthesis of a hybrid transcript with a 5' leader derived from mitochondrial RNA. J Mol Biol. 1988 Nov 5;204(1):1–25. doi: 10.1016/0022-2836(88)90594-3. [DOI] [PubMed] [Google Scholar]
- Akins R. A., Kelley R. L., Lambowitz A. M. Characterization of mutant mitochondrial plasmids of Neurospora spp. that have incorporated tRNAs by reverse transcription. Mol Cell Biol. 1989 Feb;9(2):678–691. doi: 10.1128/mcb.9.2.678. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Akins R. A., Kelley R. L., Lambowitz A. M. Mitochondrial plasmids of Neurospora: integration into mitochondrial DNA and evidence for reverse transcription in mitochondria. Cell. 1986 Nov 21;47(4):505–516. doi: 10.1016/0092-8674(86)90615-x. [DOI] [PubMed] [Google Scholar]
- Akins R. A., Lambowitz A. M. Analysis of large deletions in the Mauriceville and Varkud mitochondrial plasmids of Neurospora. Curr Genet. 1990 Nov;18(4):365–369. doi: 10.1007/BF00318218. [DOI] [PubMed] [Google Scholar]
- Almasan A., Mishra N. C. Recombination by sequence repeats with formation of suppressive or residual mitochondrial DNA in Neurospora. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7684–7688. doi: 10.1073/pnas.88.17.7684. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arganoza M. T., Min J., Hu Z., Akins R. A. Distribution of seven homology groups of mitochondrial plasmids in Neurospora: evidence for widespread mobility between species in nature. Curr Genet. 1994 Jul;26(1):62–73. doi: 10.1007/BF00326306. [DOI] [PubMed] [Google Scholar]
- Bertrand H., Chan B. S., Griffiths A. J. Insertion of a foreign nucleotide sequence into mitochondrial DNA causes senescence in Neurospora intermedia. Cell. 1985 Jul;41(3):877–884. doi: 10.1016/s0092-8674(85)80068-4. [DOI] [PubMed] [Google Scholar]
- Bertrand H., Collins R. A., Stohl L. L., Goewert R. R., Lambowitz A. M. Deletion mutants of Neurospora crassa mitochondrial DNA and their relationship to the "stop-start" growth phenotype. Proc Natl Acad Sci U S A. 1980 Oct;77(10):6032–6036. doi: 10.1073/pnas.77.10.6032. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bertrand H., Griffiths A. J., Court D. A., Cheng C. K. An extrachromosomal plasmid is the etiological precursor of kalDNA insertion sequences in the mitochondrial chromosome of senescent neurospora. Cell. 1986 Dec 5;47(5):829–837. doi: 10.1016/0092-8674(86)90525-8. [DOI] [PubMed] [Google Scholar]
- Birky C. W., Jr Relaxed cellular controls and organelle heredity. Science. 1983 Nov 4;222(4623):468–475. doi: 10.1126/science.6353578. [DOI] [PubMed] [Google Scholar]
- Caten C. E. Vegetative incompatibility and cytoplasmic infection in fungi. J Gen Microbiol. 1972 Sep;72(2):221–229. doi: 10.1099/00221287-72-2-221. [DOI] [PubMed] [Google Scholar]
- Chan B. S., Court D. A., Vierula P. J., Bertrand H. The kalilo linear senescence-inducing plasmid of Neurospora is an invertron and encodes DNA and RNA polymerases. Curr Genet. 1991 Aug;20(3):225–237. doi: 10.1007/BF00326237. [DOI] [PubMed] [Google Scholar]
- Chiang C. C., Kennell J. C., Wanner L. A., Lambowitz A. M. A mitochondrial retroplasmid integrates into mitochondrial DNA by a novel mechanism involving the synthesis of a hybrid cDNA and homologous recombination. Mol Cell Biol. 1994 Oct;14(10):6419–6432. doi: 10.1128/mcb.14.10.6419. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins R. A., Saville B. J. Independent transfer of mitochondrial chromosomes and plasmids during unstable vegetative fusion in Neurospora. Nature. 1990 May 10;345(6271):177–179. doi: 10.1038/345177a0. [DOI] [PubMed] [Google Scholar]
- Collins R. A., Stohl L. L., Cole M. D., Lambowitz A. M. Characterization of a novel plasmid DNA found in mitochondria of N. crassa. Cell. 1981 May;24(2):443–452. doi: 10.1016/0092-8674(81)90335-4. [DOI] [PubMed] [Google Scholar]
- Court D. A., Bertrand H. Expression of the open reading frames of a senescence-inducing, linear mitochondrial plasmid of Neurospora crassa. Plasmid. 1993 Jul;30(1):51–66. doi: 10.1006/plas.1993.1033. [DOI] [PubMed] [Google Scholar]
- Court D. A., Bertrand H. Genetic organization and structural features of maranhar, a senescence-inducing linear mitochondrial plasmid of Neurospora crassa. Curr Genet. 1992 Nov;22(5):385–397. doi: 10.1007/BF00352440. [DOI] [PubMed] [Google Scholar]
- Court D. A., Griffiths A. J., Kraus S. R., Russell P. J., Bertrand H. A new senescence-inducing mitochondrial linear plasmid in field-isolated Neurospora crassa strains from India. Curr Genet. 1991 Feb;19(2):129–137. doi: 10.1007/BF00326294. [DOI] [PubMed] [Google Scholar]
- Debets F., Yang X., Griffiths A. J. Vegetative incompatibility in Neurospora: its effect on horizontal transfer of mitochondrial plasmids and senescence in natural populations. Curr Genet. 1994 Aug;26(2):113–119. doi: 10.1007/BF00313797. [DOI] [PubMed] [Google Scholar]
- Düvell A., Hessberg-Stutzke H., Oeser B., Rogmann-Backwinkel P., Tudzynski P. Structural and functional analysis of mitochondrial plasmids in Claviceps purpurea. Mol Gen Genet. 1988 Sep;214(1):128–134. doi: 10.1007/BF00340190. [DOI] [PubMed] [Google Scholar]
- Gessner-Ulrich K., Tudzynski P. Transcripts and translation products of a mitochondrial plasmid of Claviceps purpurea. Curr Genet. 1992 Mar;21(3):249–254. doi: 10.1007/BF00336849. [DOI] [PubMed] [Google Scholar]
- Griffiths A. J. Fungal senescence. Annu Rev Genet. 1992;26:351–372. doi: 10.1146/annurev.ge.26.120192.002031. [DOI] [PubMed] [Google Scholar]
- Griffiths A. J., Xiao Y., Barton R., Myers C. Suppression of cytoplasmic senescence in Neurospora. Curr Genet. 1992 May;21(6):479–484. doi: 10.1007/BF00351658. [DOI] [PubMed] [Google Scholar]
- Gross S. R., Hsieh T. S., Levine P. H. Intramolecular recombination as a source of mitochondrial chromosome heteromorphism in Neurospora. Cell. 1984 Aug;38(1):233–239. doi: 10.1016/0092-8674(84)90545-2. [DOI] [PubMed] [Google Scholar]
- Gunge N., Tamaru A., Ozawa F., Sakaguchi K. Isolation and characterization of linear deoxyribonucleic acid plasmids from Kluyveromyces lactis and the plasmid-associated killer character. J Bacteriol. 1981 Jan;145(1):382–390. doi: 10.1128/jb.145.1.382-390.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hermanns J., Asseburg A., Osiewacz H. D. Evidence for a life span-prolonging effect of a linear plasmid in a longevity mutant of Podospora anserina. Mol Gen Genet. 1994 May 10;243(3):297–307. doi: 10.1007/BF00301065. [DOI] [PubMed] [Google Scholar]
- Hermanns J., Osiewacz H. D. The linear mitochondrial plasmid pAL2-1 of a long-lived Podospora anserina mutant is an invertron encoding a DNA and RNA polymerase. Curr Genet. 1992 Dec;22(6):491–500. doi: 10.1007/BF00326415. [DOI] [PubMed] [Google Scholar]
- Hermanns J., Osiewacz H. D. Three mitochondrial unassigned open reading frames of Podospora anserina represent remnants of a viral-type RNA polymerase gene. Curr Genet. 1994 Feb;25(2):150–157. doi: 10.1007/BF00309541. [DOI] [PubMed] [Google Scholar]
- Hongo M., Miyasaka A., Suzuki F., Hashiba T. Expression of the linear DNA plasmid pRS64 in the plant pathogenic fungus Rhizoctonia solani. Mol Gen Genet. 1994 Nov 1;245(3):265–271. doi: 10.1007/BF00290105. [DOI] [PubMed] [Google Scholar]
- Hänfler J., Teepe H., Weigel C., Kruft V., Lurz R., Wöstemeyer J. Circular extrachromosomal DNA codes for a surface protein in the (+) mating type of the zygomycete Absidia glauca. Curr Genet. 1992 Oct;22(4):319–325. doi: 10.1007/BF00317929. [DOI] [PubMed] [Google Scholar]
- Jabaji-Hare S. H., Burger G., Forget L., Lang B. F. Extrachromosomal plasmids in the plant pathogenic fungus Rhizoctonia solani. Curr Genet. 1994 May;25(5):423–431. doi: 10.1007/BF00351781. [DOI] [PubMed] [Google Scholar]
- Kempken F., Hermanns J., Osiewacz H. D. Evolution of linear plasmids. J Mol Evol. 1992 Dec;35(6):502–513. doi: 10.1007/BF00160211. [DOI] [PubMed] [Google Scholar]
- Kempken F., Meinhardt F., Esser K. In organello replication and viral affinity of linear, extrachromosomal DNA of the ascomycete Ascobolus immersus. Mol Gen Genet. 1989 Sep;218(3):523–530. doi: 10.1007/BF00332419. [DOI] [PubMed] [Google Scholar]
- Kennell J. C., Saville B. J., Mohr S., Kuiper M. T., Sabourin J. R., Collins R. A., Lambowitz A. M. The VS catalytic RNA replicates by reverse transcription as a satellite of a retroplasmid. Genes Dev. 1995 Feb 1;9(3):294–303. doi: 10.1101/gad.9.3.294. [DOI] [PubMed] [Google Scholar]
- Kennell J. C., Wang H., Lambowitz A. M. The Mauriceville plasmid of Neurospora spp. uses novel mechanisms for initiating reverse transcription in vivo. Mol Cell Biol. 1994 May;14(5):3094–3107. doi: 10.1128/mcb.14.5.3094. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuiper M. T., Lambowitz A. M. A novel reverse transcriptase activity associated with mitochondrial plasmids of Neurospora. Cell. 1988 Nov 18;55(4):693–704. doi: 10.1016/0092-8674(88)90228-0. [DOI] [PubMed] [Google Scholar]
- Kuiper M. T., Sabourin J. R., Lambowitz A. M. Identification of the reverse transcriptase encoded by the Mauriceville and Varkud mitochondrial plasmids of Neurospora. J Biol Chem. 1990 Apr 25;265(12):6936–6943. [PubMed] [Google Scholar]
- Lambowitz A. M. Infectious introns. Cell. 1989 Feb 10;56(3):323–326. doi: 10.1016/0092-8674(89)90232-8. [DOI] [PubMed] [Google Scholar]
- Li Q., Nargang F. E. Two Neurospora mitochondrial plasmids encode DNA polymerases containing motifs characteristic of family B DNA polymerases but lack the sequence Asp-Thr-Asp. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4299–4303. doi: 10.1073/pnas.90.9.4299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lim L., Howlett B. J. Linear plasmids, pLm9 and pLm10, can be isolated from the phytopathogenic ascomycete Leptosphaeria maculans by pulsed-field gel electrophoresis. Curr Genet. 1994 Sep;26(3):276–280. doi: 10.1007/BF00309560. [DOI] [PubMed] [Google Scholar]
- Maleszka R. Electrophoretic profiles of mitochondrial plasmids in Neurospora suggest they replicate by a rolling circle mechanism. Biochem Biophys Res Commun. 1992 Aug 14;186(3):1669–1673. doi: 10.1016/s0006-291x(05)81600-6. [DOI] [PubMed] [Google Scholar]
- Marcinko-Kuehn M., Yang X., Debets F., Jacobson D. J., Griffiths A. J. A kalilo-like linear plasmid in Louisiana field isolates of the pseudohomothallic fungus Neurospora tetrasperma. Curr Genet. 1994 Oct;26(4):336–343. doi: 10.1007/BF00310498. [DOI] [PubMed] [Google Scholar]
- Martin F. N. Characterization of circular mitochondrial plasmids in three Pythium species. Curr Genet. 1991 Jul;20(1-2):91–97. doi: 10.1007/BF00312771. [DOI] [PubMed] [Google Scholar]
- May G., Taylor J. W. Independent transfer of mitochondrial plasmids in Neurospora crassa. Nature. 1989 May 25;339(6222):320–322. doi: 10.1038/339320a0. [DOI] [PubMed] [Google Scholar]
- Meinhardt F., Kempken F., Kämper J., Esser K. Linear plasmids among eukaryotes: fundamentals and application. Curr Genet. 1990 Feb;17(2):89–95. doi: 10.1007/BF00312851. [DOI] [PubMed] [Google Scholar]
- Meyer R. J. Mitochondrial DNAs and plasmids as taxonomic characteristics in Trichoderma viride. Appl Environ Microbiol. 1991 Aug;57(8):2269–2276. doi: 10.1128/aem.57.8.2269-2276.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Michel F., Lang B. F. Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses. Nature. 1985 Aug 15;316(6029):641–643. doi: 10.1038/316641a0. [DOI] [PubMed] [Google Scholar]
- Miyashita S., Hirochika H., Ikeda J. E., Hashiba T. Linear plasmid DNAs of the plant pathogenic fungus Rhizoctonia solani with unique terminal structures. Mol Gen Genet. 1990 Jan;220(2):165–171. doi: 10.1007/BF00260476. [DOI] [PubMed] [Google Scholar]
- Mogen K. L., Siegel M. R., Schardl C. L. Linear DNA plasmids of the perennial ryegrass choke pathogen, Epichloë typhina (Clavicipitaceae). Curr Genet. 1991 Dec;20(6):519–526. doi: 10.1007/BF00334781. [DOI] [PubMed] [Google Scholar]
- Myers C. J., Griffiths A. J., Bertrand H. Linear kalilo DNA is a Neurospora mitochondrial plasmid that integrates into the mitochondrial DNA. Mol Gen Genet. 1989 Dec;220(1):113–120. doi: 10.1007/BF00260864. [DOI] [PubMed] [Google Scholar]
- Nargang F. E., Bell J. B., Stohl L. L., Lambowitz A. M. The DNA sequence and genetic organization of a Neurospora mitochondrial plasmid suggest a relationship to introns and mobile elements. Cell. 1984 Sep;38(2):441–453. doi: 10.1016/0092-8674(84)90499-9. [DOI] [PubMed] [Google Scholar]
- Nargang F. E., Pande S., Kennell J. C., Akins R. A., Lambowitz A. M. Evidence that a 1.6 kilobase region of Neurospora mtDNA was derived by insertion of part of the LaBelle mitochondrial plasmid. Nucleic Acids Res. 1992 Mar 11;20(5):1101–1108. doi: 10.1093/nar/20.5.1101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Natvig D. O., May G., Taylor J. W. Distribution and evolutionary significance of mitochondrial plasmids in Neurospora spp. J Bacteriol. 1984 Jul;159(1):288–293. doi: 10.1128/jb.159.1.288-293.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oeser B., Rogmann-Backwinkel P., Tudzynski P. Interaction between mitochondrial DNA and mitochondrial plasmids in Claviceps purpurea: analysis of plasmid-homologous sequences upstream of the lrRNA-gene. Curr Genet. 1993;23(4):315–322. doi: 10.1007/BF00310892. [DOI] [PubMed] [Google Scholar]
- Oeser B., Tudzynski P. The linear mitochondrial plasmid pClK1 of the phytopathogenic fungus Claviceps purpurea may code for a DNA polymerase and an RNA polymerase. Mol Gen Genet. 1989 May;217(1):132–140. doi: 10.1007/BF00330952. [DOI] [PubMed] [Google Scholar]
- Pande S., Lemire E. G., Nargang F. E. The mitochondrial plasmid from Neurospora intermedia strain Labelle-1b contains a long open reading frame with blocks of amino acids characteristic of reverse transcriptases and related proteins. Nucleic Acids Res. 1989 Mar 11;17(5):2023–2042. doi: 10.1093/nar/17.5.2023. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Qin H., Welker D. L., Youssef N. N. Isolation and characterization of a linear plasmid from the entomopathogenic fungus Ascosphaera apis. Plasmid. 1993 Jan;29(1):19–30. doi: 10.1006/plas.1993.1003. [DOI] [PubMed] [Google Scholar]
- Robison M. M., Royer J. C., Horgen P. A. Homology between mitochondrial DNA of Agaricus bisporus and an internal portion of a linear mitochondrial plasmid of Agaricus bitorquis. Curr Genet. 1991 Jun;19(6):495–502. doi: 10.1007/BF00312742. [DOI] [PubMed] [Google Scholar]
- Rohe M., Schrage K., Meinhardt F. The linear plasmid pMC3-2 from Morchella conica is structurally related to adenoviruses. Curr Genet. 1991 Dec;20(6):527–533. doi: 10.1007/BF00334782. [DOI] [PubMed] [Google Scholar]
- Rohe M., Schründer J., Tudzynski P., Meinhardt F. Phylogenetic relationships of linear, protein-primed replicating genomes. Curr Genet. 1992 Feb;21(2):173–176. doi: 10.1007/BF00318478. [DOI] [PubMed] [Google Scholar]
- Sakaguchi K. Invertrons, a class of structurally and functionally related genetic elements that includes linear DNA plasmids, transposable elements, and genomes of adeno-type viruses. Microbiol Rev. 1990 Mar;54(1):66–74. doi: 10.1128/mr.54.1.66-74.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salas M. Initiation of DNA replication by primer proteins: bacteriophage phi 29 and its relatives. Curr Top Microbiol Immunol. 1988;136:71–88. doi: 10.1007/978-3-642-73115-0_4. [DOI] [PubMed] [Google Scholar]
- Samac D. A., Leong S. A. Two linear plasmids in mitochondria of Fusarium solani f. sp. cucurbitae. Plasmid. 1988 Jan;19(1):57–67. doi: 10.1016/0147-619x(88)90063-7. [DOI] [PubMed] [Google Scholar]
- Saville B. J., Collins R. A. A site-specific self-cleavage reaction performed by a novel RNA in Neurospora mitochondria. Cell. 1990 May 18;61(4):685–696. doi: 10.1016/0092-8674(90)90480-3. [DOI] [PubMed] [Google Scholar]
- Saville B. J., Collins R. A. RNA-mediated ligation of self-cleavage products of a Neurospora mitochondrial plasmid transcript. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8826–8830. doi: 10.1073/pnas.88.19.8826. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schulte U., Lambowitz A. M. The LaBelle mitochondrial plasmid of Neurospora intermedia encodes a novel DNA polymerase that may be derived from a reverse transcriptase. Mol Cell Biol. 1991 Mar;11(3):1696–1706. doi: 10.1128/mcb.11.3.1696. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shepherd H. S. Linear, non-mitochondrial plasmids of Alternaria alternata. Curr Genet. 1992 Feb;21(2):169–172. doi: 10.1007/BF00318477. [DOI] [PubMed] [Google Scholar]
- Stahl U., Lemke P. A., Tudzynski P., Kück U., Esser K. Evidence for plasmid like DNA in a filamentous fungus, the ascomycete Podospora anserina. Mol Gen Genet. 1978 Jul 4;162(3):341–343. doi: 10.1007/BF00268860. [DOI] [PubMed] [Google Scholar]
- Stohl L. L., Collins R. A., Cole M. D., Lambowitz A. M. Characterization of two new plasmid DNAs found in mitochondria of wild-type Neurospora intermedia strains. Nucleic Acids Res. 1982 Mar 11;10(5):1439–1458. doi: 10.1093/nar/10.5.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stohl L. L., Lambowitz A. M. Construction of a shuttle vector for the filamentous fungus Neurospora crassa. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1058–1062. doi: 10.1073/pnas.80.4.1058. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taylor J. W., Smolich B. D., May G. An evolutionary comparison of homologous mitochondrial plasmid DNAs from three Neurospora species. Mol Gen Genet. 1985;201(2):161–167. doi: 10.1007/BF00425654. [DOI] [PubMed] [Google Scholar]
- Vickery D. B., Griffiths A. J. Transcription of the kalilo linear senescence plasmid from Neurospora intermedia. Plasmid. 1993 May;29(3):180–192. doi: 10.1006/plas.1993.1021. [DOI] [PubMed] [Google Scholar]
- Vierula P. J., Bertrand H. A deletion derivative of the kalilo senescence plasmid forms hairpin and duplex DNA structures in the mitochondria of Neurospora. Mol Gen Genet. 1992 Sep;234(3):361–368. doi: 10.1007/BF00538695. [DOI] [PubMed] [Google Scholar]
- Wang H., Kennell J. C., Kuiper M. T., Sabourin J. R., Saldanha R., Lambowitz A. M. The Mauriceville plasmid of Neurospora crassa: characterization of a novel reverse transcriptase that begins cDNA synthesis at the 3' end of template RNA. Mol Cell Biol. 1992 Nov;12(11):5131–5144. doi: 10.1128/mcb.12.11.5131. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang H., Lambowitz A. M. Reverse transcription of the Mauriceville plasmid of Neurospora. Lack of ribonuclease H activity associated with the reverse transcriptase and possible use of mitochondrial ribonuclease H. J Biol Chem. 1993 Sep 5;268(25):18951–18959. [PubMed] [Google Scholar]
- Wang H., Lambowitz A. M. The Mauriceville plasmid reverse transcriptase can initiate cDNA synthesis de novo and may be related to reverse transcriptase and DNA polymerase progenitor. Cell. 1993 Dec 17;75(6):1071–1081. doi: 10.1016/0092-8674(93)90317-j. [DOI] [PubMed] [Google Scholar]
- Yang X., Griffiths A. J. Male transmission of linear plasmids and mitochondrial DNA in the fungus Neurospora. Genetics. 1993 Aug;134(4):1055–1062. doi: 10.1093/genetics/134.4.1055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang X., Griffiths A. J. Plasmid diversity in senescent and nonsenescent strains of Neurospora. Mol Gen Genet. 1993 Feb;237(1-2):177–186. doi: 10.1007/BF00282799. [DOI] [PubMed] [Google Scholar]
- Yang X., Griffiths A. J. Plasmid suppressors active in the sexual cycle of Neurospora intermedia. Genetics. 1993 Dec;135(4):993–1002. doi: 10.1093/genetics/135.4.993. [DOI] [PMC free article] [PubMed] [Google Scholar]