Abstract
A fundamental paradox motivates the study of plant mitochondrial genomics: the mutation rate is very low (lower than in the nucleus) but the rearrangement rate is high. A landmark paper published in Journal of Molecular Evolution in 1988 established these facts and revealed the paradox. Jeffrey Palmer and Laura Herbon did a prodigious amount of work in the pre-genome sequencing era to identify both the high frequency of rearrangements between closely related species, and the low frequency of mutations, observations that have now been confirmed many times by sequencing. This paper was also the first to use molecular data on rearrangements as a phylogenetic trait to build a parsimonious tree. The work was a technical tour-de-force, its findings are still at the heart of plant mitochondrial genomics, and the underlying molecular mechanisms that produce this paradox are still not completely understood.
References
Bader DA, Moret BME, Yan M (2001) A linear-time algorithm for computing inversion distance between signed permutations with an experimental study. J ComputBiol 8:483
Bendich AJ (1993) Reaching for the ring: the study of mitochondrial genome structure. Curr Genet 24:279
Bendich A (1996) Structural analysis of mitochondrial DNA molecules from fungi and plants using moving pictures and pulsed field gel electrophoresis. J MolBiol 255:564
Bendich AJ (2007) The size and form of chromosomes are constant in the nucleus, but highly variable in bacteria, mitochondria and chloroplasts. BioEssays 29:474
Bendich AJ (2013) DNA abandonment and the mechanisms of uniparental inheritance of mitochondria and chloroplasts. Chromosome Res 21:287
Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197
Blanchette M, Kunisawa T, Sankoff D (1999) Gene order breakpoint evidence in animal mitochondrial phylogeny. J MolEvol 49:193
Boore JL, Brown WM (1998) Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. CurrOpin Genet Dev 8:668
Brown WM, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. ProcNatlAcadSci USA 76:1967
Cai G, Yang Q, Yi B, Fan C, Edwards D, Batley J, Zhou Y (2014) A complex recombination pattern in the genome of allotetraploidBrassica napus as revealed by a high-density genetic map. PLoS ONE 9:e109910
Chang S, Yang T, Du T, Huang Y, Chen J, Yan J, He J, Guan R (2011) Mitochondrial genome sequencing helps show the evolutionary mechanism of mitochondrial genome formation in Brassica. BMC Genomics 12:497
Christensen AC (2013) Plant mitochondrial genome evolution can be explained by DNA repair mechanisms. Genome BiolEvol 5:1079
Christensen AC (2014) Genes and junk in plant mitochondria—repair mechanisms and selection. Genome BiolEvol 6:1448
Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J MolEvol 22:252
Clary DO, Goddard JM, Martin SC, Fauron CM, Wolstenholme DR (1982) Drosophila mitochondrial DNA: a novel gene order. Nucleic Acids Res 10:6619
Cole LW, Guo W, Mower JP, Palmer JD (2018) High and variable rates of repeat-mediated mitochondrial genome rearrangement in a genus of plants. MolBiolEvol 35:2773
Darracq A, Varre JS, Touzet P (2010) A scenario of mitochondrial genome evolution in maize based on rearrangement events. BMC Genomics 11:233
Dobzhansky T, Sturtevant AH (1938) Inversions in the chromosomes of Drosophila pseudoobscura. Genetics 23:28
Graur D, Zheng Y, Azevedo RBR (2015) An evolutionary classification of genomic function. Genome BiolEvol 7(3):642–645
Grewe F, Edger PP, Keren I, Sultan L, Pires JC, Ostersetzer-Biran O, Mower JP (2014) Comparative analysis of 11 Brassicales mitochondrial genomes and the mitochondrial transcriptome of Brassica oleracea. Mitochondrion 19(Part B):135
Gualberto JM, Newton KJ (2017) Plant mitochondrial genomes: dynamics and mechanisms of mutation. Annu Rev Plant Biol 68:225–252
Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31:5907
Kumar RA, Oldenburg DJ, Bendich AJ (2015) Molecular integrity of chloroplast DNA and mitochondrial DNA in mesophyll and bundle sheath cells of maize. Planta 241:1221
Makaroff CA, Palmer JD (1987) Extensive mitochondrial specific transcription of the Brassica campestris mitochondrial genome. Nucleic Acids Res 15:5141
Makaroff CA, Palmer JD (1988) Mitochondrial DNA rearrangements and transcriptional alterations in the male-sterile cytoplasm of Ogura radish. Mol Cell Biol 8:1474
Mower JP, Stefanović S, Hao W, Gummow JS, Jain K, Ahmed D, Palmer JD (2010) Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol 8:150
Oldenburg DJ, Kumar RA, Bendich AJ (2013) The amount and integrity of mtDNA in maize decline with development. Planta 237:603
Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J MolEvol 28:87
Palmer JD, Shields CR (1984) Tripartite structure of the Brassica campestris mitochondrial genome. Nature 307:437
Palmer JD, Shields CR, Cohen DB, Orton TJ (1983) Chloroplast DNA evolution and the origin of amphidiploid Brassica species. TheorAppl Genet 65:181
Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV, Munzinger J, Barry K, Boore JL, Zhang Y, dePamphilis CW, Knox EB, Palmer JD (2013) Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 342:1468
Richardson AO, Palmer JD (2007) Horizontal gene transfer in plants. J Exp Bot 58:1
Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. ProcNatlAcadSci USA 74:5463
Sankoff D, Leduc G, Antoine N, Paquin B, Lang BF, Cedergren R (1992) Gene order comparisons for phylogenetic inference: evolution of the mitochondrial genome. ProcNatlAcadSci USA 89:6575
Sloan DB, Taylor DR (2010) Testing for selection on synonymous sites in plant mitochondrial DNA: the role of codon bias and RNA editing. J MolEvol 70:479
Smith MJ, Arndt A, Gorski S, Fajber E (1993) The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J MolEvol 36:545
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J MolBiol 98:503
Stent GS (1968) That was the molecular biology that was. Science 160:390
Sturtevant AH, Dobzhansky T (1936) Inversions in the third chromosome of wild races of Drosophila pseudoobscura, and their use in the study of the history of the species. ProcNatlAcadSci USA 22:448
Tesler G (2002) GRIMM: genome rearrangements web server. Bioinformatics 18:492
U N (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7:389
Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57
Ward BL, Anderson RS, Bendich AJ (1981) The mitochondrial genome is large and variable in a family of plants (cucurbitaceae). Cell 25:793
Wolfe K, Li W, Sharp P (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast and nuclear DNAs. ProcNatlAcadSci USA 84:9054
Wu Z, Waneka G, Broz AK, King CR, Sloan DB (2020) MSH1 is required for maintenance of the low mutation rates in plant mitochondrial and plastid genomes. ProcNatlAcadSci USA 117:16448
Wynn EL, Christensen AC (2015) Are synonymous substitutions in flowering plant mitochondria neutral? J MolEvol 81:131
Wynn EL, Christensen AC (2019) Repeats of unusual size in plant mitochondrial genomes: identification, incidence and evolution. G3 9:549
Wynn E, Purfeerst E, Christensen A (2020) Mitochondrial DNA repair in an Arabidopsis thaliana uracil N-glycosylase mutant. Plants (Basel) 9:261
Acknowledgements
Apologies to Sir Winston Churchill for the title. The author is grateful to Beth Rowan, Emily Wynn, Wayne Riekhof, and members of his lab for helpful comments on the manuscript, and to Jeff Mower for discussions about rearrangements as a phylogenetic trait. This work in his lab is supported by a Grant from the National Science Foundation (MCB-1933590).
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Christensen, A.C. Plant Mitochondria are a Riddle Wrapped in a Mystery Inside an Enigma. J Mol Evol 89, 151–156 (2021). https://doi.org/10.1007/s00239-020-09980-y
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DOI: https://doi.org/10.1007/s00239-020-09980-y