Abstract
Plant mitochondrial genomes share several unique structural features that distinguish them from both mammalian and fungal mitochondrial genomes. The size of plant mitochondrial genomes is highly variable and quite large, ranging in size from approximately 208 kilobases (kb) to over 2200 kb (Palmer & Herbon 1987; Ward et al. 1981). In contrast, the circular genomes of animal and fungal mitochondria range in size from 15–75 kb (Kessler & Avise 1985; Clark-Walker 1985). Perhaps the most unique structural feature of plant mitochondrial DNAs (mtDNAs) is the presence of large repeated sequences, many of which appear to be involved in intra- and inter-molecular recombination. Multicircular mitochondrial genomes are predicted to result from these recombination events. In addition to recombination involving large repeats, recombination between short homologous sequences occasionally occurs within the plant mitochondrion. These rare recombinational events play an important role in the continual evolution of the mitochondrial genome, creating chimeric genes, pseudogenes, duplications, deletions and new copies of the large recombination repeats.
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References
Abbott AG & Fauron CM-R (1986) Structural alterations in a transcribed region of the T type cytoplasmic male sterile maize mitochondrial genome. Curr Genet 10: 777–783.
Bailey-Serres J, Hanson DK, Fox TD & Leaver CJ (1986) Mitochondrial genome rearrangement leads to extension and relocation of the cytochrome c oxidase subunit I gene in sorghum. Cell 47: 567–576.
Belliard G, Vedel F & Pelletier G (1979) Mitochondrial recombination in cytoplasmic hybrids of Nicotiana tabacum by protoplast fusion. Nature 281: 401–403.
Bendich AJ (1985) Plant mitochondrial DNA: unusual variation on a common theme. In: Hohn B & Dennis ES (eds) Genetic Flux in Plants (pp 111–138). Springer Verlag, New York.
Bendich AJ & Smith SB (1990) Moving pictures and pulsed-field gel electrophoresis show linear DNA molecules from chloroplasts and mitochondria. Curr Genet 17: 421–425.
Bland MM, Levings CSIII & Matzinger DF (1987) The ATPase subunit 6 gene of tobacco mitochondria contains an unusual sequence. Curr Genet 12: 475–481.
Boeshore ML, Hanson MR, Lifshitz I, & Izhar S (1983) Novel composition of mitochondrial genomes in Petunia somatic hybrids derived from cytoplasmic male sterile and fertile plants. Mol Gen Genet 190: 459–467.
Bonen L & Bird S (1988) Sequence analysis of the wheat mitochondrial atp6 gene reveals a fused upstream reading frame and markedly divergent N termini among plant ATP6 proteins. Gene 73: 47–56.
Brears T & Lonsdale DM (1988) The sugar beet mitochondrial genome: a complex organization generated by homologous recombination. Mol Gen Genet 214: 514–522.
Brennicke A & Blanz P (1982) Circular mitochondrial DNA species from Oenothera with unique sequences. Mol Gen Genet 187: 461–466.
Cerutti H, Osman M, Grandoni P & Jagendorf AT (1992) A homolog of Escherichia coli recA protein in plastids of higher plants. Proc Natl Acad Sci USA 89: 8068–8072.
Chen H-C, Wintz H, Weil J-H & Pillay DTN (1989) Three mitochondrial transfer RNA genes from Arabidopsis thaliana: evidence for the conversion of a phenylalanine transfer RNA gene into a tyrosine transfer RNA gene. Nucleic Acids Res 17: 2613–2621.
Chetrit P, Mathieu C, Muller JP & Vedel F (1984) Physical and gene mapping of cauliflower (Brassica oleracea) mitochondrial DNA. Curr Genet 8: 413–421.
Clark-Walker GD (1985) Basis of diversity in mitochondrial DNAs. In: Cavalier-Smith T (ed) The Evolution of Genome Size (pp 277–297). John Wiley and Sons, New York.
Conklin PL & Hanson MR (1993) A truncated recombination repeat in the mitochondrial genome of a Petunia CMS line. Curr Genet 23: 477–482.
Cox MM & Lehman IR (1987) Enzymes of general recombination. Annu Rev Biochem 56: 229–262.
Dewey RE, Levings CS III and Timothy DH (1985) Nucleotide sequence of ATPase subunit 6 gene of maize mitochondria. Plant Physiol 79: 914–919.
Dewey RE, Levings CSIII & Timothy DH (1986) Novel recombinations on the maize mitochondrial genome produce a unique transcription unit in the Texas male-sterile cytoplasm (cms-T). Cell 44: 439–449.
Dewey RE, Timothy DH & Levings CS III (1991) Chimeric mitochondrial genes expressed in the C male-sterile cytoplasm of maize. Curr Genet 20: 475–482.
Dixon LK & Leaver CJ (1982) Mitochondrial gene expression and cytoplasmic male sterility in sorghum. Plant Mol Biol 1: 89–102.
Dykstra CC, Kitada K, Clark AB, Hamatake RK & Sugino A (1991) Cloning and characterization of DST2, the gene for DNA strand transfer protein B from Saccharomyces cerevisiae. Mol Cell Biol 11: 2583–2592.
Eisen A & Camerini-Otero RD (1988) A recombinase from Drosophila melanogaster embryos. Proc Natl Acad Sci USA 85: 7481–7485.
Falconet D, Delorme S, Lejeune B, Sevignac M, Delcher E, Bazetoux S & Quetier F (1985) Wheat mitochondrial 26S ribosomal RNA gene has no intron and is present in multiple copies arising by recombination. Curr Genet 9: 169–174.
Falconet DMS & Quetier F (1988) Nucleotide sequence and determination of extremities of the 26S ribosomal RNA gene in wheat mitochondria: evidence for sequence rearrangements in the ribosomal genes of higher plants. Curr Genet 13: 75–82.
Fauron CM-R & Havlik M (1988) The BamHI, XhoI, SmaI restriction enzyme maps of the normal maize mitochondrial genome B37. Nucleic Acids Res 16: 10395–10396.
Fauron CM-R, Abbott AG, Brettell R & Gesteland R (1987) Maize mitochondrial DNA rearrangements between the normal type, the Texas male sterile cytoplasm and a fertile revertant cms-T regenerated plant. Curr Genet 11: 339–346.
Fauron CM-R, Havlik M, Lonsdale D & Nichols L (1989) Mitochondrial genome organization of the maize cytoplasmic male sterile type T. Mol Gen Genet 216: 395–401.
Fauron CM-R, Havlik M & Brettell RIS (1990a) The mitochondrial genome organization of a maize fertile cmsT revertant line is generated through recombination between two sets of repeats. Genetics 124: 423–428.
Fauron CM-R, Havlik M, Hafezi S, Brettell RIS & Albertsen M (1990b) Study of two different recombination events in maize cmsT-regenerated plants during reversion to fertility. Theor Appl Genet 79: 593–599.
Fauron CM-R, Casper M, Gesteland R, & Albertsen M (1992) A multi-recombination model for the mtDNA rearrangements seen in maize cmsT regenerated plants. Plant J 2: 949–958.
Folkerts O & Hanson MR (1989) Three copies of a single recombination repeat occur on the 443 kb mastercircle of the Petunia hybrida 3704 mitochondrial genome. Nucleic Acids Res 17: 7345–7357.
Folkerts O & Hanson MR (1991) The male sterility-associated pcf gene and the normal atp9-1 gene in Petunia are located on different mitochondrial DNA molecules. Genetics 129: 885–895.
Fragoso LL, Nichols SE & Levings CS III (1989) Rearrangements in maize mitochondrial genes. Genome 31: 160–168.
Grabau E, Hablik M & Gesteland R (1988) Chimeric organization of two genes for the soybean mitochondrial ATPase subunit 6. Curr Genet 13: 83–89.
Gross SR, Hsieh T-S & Levine PH (1984) Intramolecular recombination as a source of mitochondrial chromosome heteromorphism in Neurospora. Cell 38: 233–239.
Hattori K, Tanaka M, Sugiyama S, Obayashi T, Ito T, Satake T, Hanaki Y, Asai J, Nagano M & Ozawa T (1991) Age-dependent increase in deleted mitochondrial DNA in the human heart; possible contributory factor to presbycardia. Am Heart J 121: 1735–1742.
Hiesel R, Schobel W, Schuster W & Brennicke A (1987) The cytochrome oxidase subunit I and III genes in Oenothera mitochondria are transcribed from identical promoter sequences. EMBO J 6: 29–34.
Houchins JP, Ginsburg H, Rohrbaugh M, Dale RMK, Schardl CL, Hodge TP & Lonsdale DM (1986) DNA sequence analysis of a 5.27 kb direct repeat occuring adjacent to the regions of S-episome homology in maize mitochondria. EMBO J 5: 2781–2788.
Hsieh P, Meyn MS & Camerini-Otero RD (1986) Partial purification and characterization of a recombinase from human cells. Cell 44: 885–894.
Hunt MD & Newton KJ (1991) The NCS3 mutation: genetic evidence for the expression of ribosomal protein genes in Zea mays mitochondria. EMBO J 10: 1045–1052.
Johns C, Lu M, Lyznik A & Mackenzie S (1992) A mitochondrial DNA sequence is associated with abnormal pollen development in cytoplasmid male sterile bean plants. Plant Cell 4: 435–449.
Kadowaki K, Takeshi S & Kazama S (1990) A chimeric gene containing the 5′ portion of atp6 is associated with cytoplasmic male sterility in rice. Mol Gen Genet 224: 10–16.
Kemble RJ & Thompson RD (1982) S1 and S2, the linear mitochondrial DNAs present in a male sterile line of maize, possess terminally attached proteins. Nucleic Acids Res 10: 8181–8190.
Kemble RJ, Mans RJ, Gabay-Laughnan S & Laughnan JR (1983) Sequences homologous to episomal mitochondrial DNAs in the maize nuclear genome. Nature 304: 744–747.
Kessler LG & Avise JC (1985) A comparative description of mitochondrial DNA differentiation in selected avian and other vertebrate genera. Mol Bio Evol 2: 109–115.
Kmiec EB & Holloman WK (1983) Heteroduplex formation and polarity during strand transfer promoted by Ustilago Rec1 protein. Cell 33: 857–864.
Kohler RH, Horn R, Lossl A & Zetsche K (1991) Cytoplasmic male sterility in sunflower is correlated with the co-transcription of a new open reading frame with the atpA gene. Mol Gen Genet 227: 369–376.
Lauer MC, Knudsen C, Newton KJ, Gabay-Laughnan S & Laughnan JR (1990) A partially deleted mitochondrial cytochrome oxidase gene in the NCS6 abnormal growth mutant of maize. New Biol 2: 179–186.
Leaver CJ & Gray MW (1982) Mitochondrial genome organization and expression in higher plants. Ann Rev Plant Physiol 33: 373–402.
Lejeune B, Delorme S, Delcher E, Quetier, F (1987) Recombination in wheat mitochondrial DNA: occurrence of nine different genomic contexts for the 18S-5S genes. Plant Physiol Biochem 25: 227–233.
Levings CSIII & Sederoff RR (1983) Nucleotide sequence of the S-2 mitochondrial DNA from the S cytoplasm of maize. Proc Natl Acad Sci USA 80: 4055–4059.
Levy AA, Andre CP & Walbot V (1991) Analysis of a 120-kilobase mitochondrial chromosome in maize. Genetics 128: 417–424.
Lindahl KF (1991) His and hers recombinational hotspots. Trends Genet 7: 273–276.
Lonsdale DM (1985) Movement of genetic material between the chloroplast and mitochondrial genome of higher plants. In: Hohn B and Dennis ES (eds) Plant Gene Research. Genetic Flux in Plants (pp 51–60). Springer-Verlag, New York.
Lonsdale DM, Hodge TP & Fauron CM-F (1984) The physical map and organisation of the mitochondrial genome from the fertile cytoplasm of maize. Nucleic Acids Res 12: 9249–9261.
Lonsdale DM, Brears T, Hodge TP, Melville SE & Rottmann WH (1988) The plant mitochondrial genome: homologous recombination as a mechanism for generating heterogeneity. Phil Trans R Soc Lond B 319: 149–163.
Mackensie, S & Bassett M (1987) Genetics of restoration in cytoplasmic male sterile Phaseolus vulgaris L. Theor Appl Genet 74: 642–645.
Makaroff CA & Palmer JD (1988) Mitochondrial DNA rearrangements and transcriptional alterations in the male-sterile cytoplasm of Ogura radish. Mol Cell Biol 8: 1474–1480.
Makaroff CA, Apel IJ & Palmer JD (1989) The atp6 coding region has been disrupted and a novel reading frame generated in the mitochondrial genome of cytoplasmic male-sterile radish. J Biol Chem 264: 11706–11713.
Manna E & Brennicke A (1986) Site-specific circularisation at an intragenic sequence in Oenothera. Mol Gen Genet 203: 377–381.
Martinez-Zapater JM, Gil P, Capei J & Somerville CR (1992) Mutations at the Arabidopsis CHM locus promote rearrangements of the mitochondrial genome. Plant Cell 4: 889–899.
Miller RV & Kokjohn TA (1990) General microbiology of recA: environmental and evolutionary significance. Annu Rev Microbiol 44: 365–394.
Morgan A & Maliga P (1987) Rapid chloroplast segregation and recombination of mitochondrial DNA in Brassica cybrids. Mol Gen Genet 209: 240–246.
Morikami A & Nakamura K (1987) Structure and expression of pea mitochondrial F1ATPase a-subunit gene and its pseudogene involved in homologous recombination. J Biochem 101: 967–976.
Nagy F, Lazar G, Menczel L & Maliga P (1983) A heteroplasmic state induced by protoplast fusion is a necessary condition for detecting rearrangements in Nicotiana mitochondrial DNA. Theor Appl Genet 66: 203–207.
Newton KJ, Knudsen C, Gabay-Laughnan S & Laughnan JR (1990) An abnormal growth mutant in maize has a defective mitochondrial cytochrome oxidase gene. Plant Cell 2: 107–113.
Nugent JM & Palmer JD (1991) RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell 66: 473–481.
Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T & Ohyama K (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. J Mol Biol 223: 1–7.
Paillard M, Sederoff RR & Levings CS III (1985) Nucleotide sequence of the S-l mitochondrial DNA from the S cytoplasm of maize. EMBO J 4: 1125–1128.
Palmer JD (1988) Intraspecific variation and multicircularity in Brassica mitochondrial DNAs. Genetics 118: 341–351.
Palmer JD & Herbon LA (1986) Tricircular mitochondrial genomes of Brassica and Raphanus: reversal of repeat configurations by inversion. Nucleic Acids Res 14: 9755–9764.
Palmer JD & Herbon LA (1987) Unicircular structure of the Brassica hirta mitochondrial genome. Curr Genet 11: 565–570.
Palmer JD & Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 28: 87–97.
Palmer JD & Shields CR (1984) Tripartite structure of the Brassica campestris mitochondrial genome. Nature 307: 437–440.
Palmer JD, Shields CR, Cohen DB & Orton TJ (1983) An unusual mitochondrial DNA plasmid in the genus Brassica. Nature 301: 725–728.
Petes TD & Hill CW (1988) Recombination between repeated genes in microorganisms. Annu Rev Genet 22: 147–168.
Pring DR, Levings CS III, Hu WWL & Timothy DH (1977) Unique DNA associated with mitochondria in the “S”-type cytoplasm of male-sterile maize. Proc Natl Acad Sci USA 74: 2904–2908.
Pruitt KD & Hanson MR (1989) Cytochrome oxidase subunit II sequences in Petunia mitochondria: two intron-containing genes and an intron-less pseudogene associated with cytoplasmic male sterility. Curr Genet 16: 281–291.
Rothenberg M & Hanson MR (1987) Recombination between parental mitochondrial DNA following protoplast fusion can occur in a region which normally does not undergo intragenomic recombination in parental plants. Curr Genet 12: 235–240.
Rothenberg M & Hanson MR (1988) A functional mitochondrial ATP synthase proteolipid gene produced by recombination of parental genes in a Petunia somatic hybrid. Genetics 118: 155–161.
Rottmann WH, Brears T, Hodge TP & Lonsdale DM (1987) A mitochondrial gene is lost via homologous recombination during reversion of CMS T maize to fertility. EMBO J 6: 1541–1546.
Sander M, Lowenhaupt K, Lane WS & Rich A (1991) Cloning and characterization of Rrp1, the gene encoding Drosophila strand transferase: carboxy-terminal homology to DNA repair endo/exonucleases. Nucleic Acids Res 19: 4523–4529.
Schardl CL, Londale DM, Pring DR & Rose KR (1984) Linearization of maize mitochondrial chromosomes by recombination with linear episomes. Nature 310: 292–296.
Schon EA, Rizzuto R, Morases CT, Nakase H, Zeviani M & DiMauro S (1989) A direct repeat is a hotspot for large-scale deletion of human mitochondrial DNA. Science 244: 346–349.
Schuster W & Brennicke A (1986) Pseudocopies of the ATPase a-subunit gene in Oenothera mitochondria are present on different circular molecules. Mol Gen Genet 204: 29–35.
Schuster W & Brennicke A (1987) Plastid DNA in the mitochondrial genome of Oenothera: Intra- and interorganellar rearrangements involving part of the plastid ribosomal cistron. Mol Gen Genet 210: 44–51.
Schuster W, Hiesel R, Manna E, Schobel W, Wissinger B & Brennicke A (1987) Molecular analysis of the mitochondrial genome in Oenothera berteriana. Plant Physiol Biochem 25: 259–264.
Senda M, Harada T, Mikami T, Sugiura M & Kinoshita T (1991) Genomic organization and sequence analysis of the cytochrome oxidase subunit II gene from normal and male-sterile mitochondria in sugar beet. Curr Genet 19: 175–181.
Shirzadegan M, Palmer JD, Christey M & Earle ED (1991) Patterns of mitochondrial DNA instability in Brassica campestris cultured cells. Plant Mol Biol 16: 21–37.
Siculella L & Palmer JD (1988) Physical and gene organization of mitochondrial DNA in fertile and male sterile sunflower. CMS-associated alterations in structure and transcription of the atpA gene. Nucleic Acids Res 16: 3787–3799.
Small I, Suffolk R & Leaver CJ (1989) Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58: 69–76.
Small ID, Isaac PG & Leaver CJ (1987) Stoichiometric differences in DNA molecules containing the atpA gene suggest mechanisms for the generation of mitochondrial genome diversity in maize. EMBO J 6: 865–869.
Stern DB & Palmer JD (1984) Extensive and widespread homologies between mitochondrial DNA and chloroplast DNA in plants. Proc Natl Acad Sci USA 81: 1946–1950.
Stern DB & Palmer JD (1986) Tripartite mitochondrial genome of spinach: physical structure, mitochondrial gene mapping, and locations of transposed chloroplast DNA sequences. Nucleic Acids Res 14: 5651–5666.
Sutton CA, Conklin PL, Pruitt KD, Calfee AJ, Cobb AG & Hanson MR (1993) Editing of rps3/rpl16 transcripts creates a premature truncation of the rpl16 reading frame. Curr Genet 23: 472–476.
Tishkoff DX, Johnson AW & Kolodner RD (1991) Molecular and genetic analysis of the gene encoding Saccharomyces cervisiae strand exchange protein Sepl. Mol Cell Biol 11: 2593–2608.
Umbeck PE & Gengenbach BG (1983) Reversion of male-sterile T cytoplasm maize to male fertility in tissue culture. Crop Sci 23: 584–588.
Ward BL, Anderson RS & Bendich AJ (1981) The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae). Cell 25: 793–803.
Young EG & Hanson MR (1987) A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 50: 41–49.
Young EG, Hanson MR & Dierks PM (1986) Sequence and transcriptional analysis of the Petunia mitochondrial gene for the ATPase synthase proteolipid subunit. Nucleic Acids Res 14: 7995–8006.
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Conklin, P.L., Hanson, M.R. (1994). Recombination of Plant Mitochondrial Genomes. In: Paszkowski, J. (eds) Homologous Recombination and Gene Silencing in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-1094-5_4
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