Mutation rates in plastid genomes: They are lower than you might think

Genome Biology and Evolution

Volumn 7, Issue 5, 2015, Pages 1227-1234

  Smith, David Roy ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Chloroplast genome; Mitochondrial DNA; Mutation rate; Plastid DNA; Synonymous substitution

Indexed keywords

MITOCHONDRIAL DNA;

CHEMISTRY; GENETICS; GREEN ALGA; MITOCHONDRIAL GENOME; MUTATION RATE; PLANT; PLASTID GENOME; RED ALGA;

CHLOROPHYTA; DNA, MITOCHONDRIAL; GENOME, MITOCHONDRIAL; GENOME, PLASTID; MUTATION RATE; PLANTS; RHODOPHYTA;

EID: 84941003465     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evv069     Document Type: Article

References (53)

1. Arrigo KR, et al. 1999. Phytoplankton community structure and the drawdown of nutrients and CO2 in the Southern Ocean. Science 283:365-367.
2. Barnard-Kubow KB, Sloan DB, Galloway LF. 2014. Correlation between sequence divergence and polymorphism reveals similar evolutionary mechanisms acting across multiple timescales in a rapidly evolving plastid genome. BMC Evol Biol. 14:1.
3. Baurain D, et al. 2010. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol. 27:1698-1709.
4. Bendif EM, et al. 2014. Genetic delineation between and within the widespread coccolithophore morpho-species Emiliania huxleyi and Gephyrocapsa oceanica (Haptophyta). J Phycol. 50:140-148.
5. Brown WM, George M, Wilson AC. 1979. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA. 76:1967-1971.
6. Budowle B, Allard MW, Wilson MR, Chakraborty R. 2003. Forensics and mitochondrial DNA: applications, debates, and foundations. Annu Rev Genomics Hum Genet. 4:119-141.
7. Cannarozzi GM, Schneider A. 2012. Codon evolution: mechanisms and models. New York: Oxford University Press.
8. Carrie C, Giraud E, Whelan J. 2009. Protein transport in organelles: dual targeting of proteins to mitochondria and chloroplasts. FEBS J. 276:1187-1195.
9. Cattolico RA, et al. 2008. Chloroplast genome sequencing analysis of Heterosigma akashiwo CCMP452 (West Atlantic) and NIES293 (West Pacific) strains. BMC Genomics 9:211.
10. Chong J, Jackson C, Kim JI, Yoon HS, Reyes-Prieto A. 2014. Molecular markers from different genomic compartments reveal cryptic diversity within glaucophyte species. Mol Phylogenet Evol. 76:181-188.
11. Christensen AC. 2013. Plant mitochondrial genome evolution can be explained by DNA repair mechanisms. Genome Biol Evol. 5:1079-1086.
12. Dahl EL, Rosenthal PJ. 2008. Apicoplast translation, transcription and genome replication: targets for antimalarial antibiotics. Trends Parasitol. 24:279-284.
13. Davila JI, et al. 2011. Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol. 9:64.
14. Del Vasto M, et al. 2015. Massive and widespread organelle genomic expansion in the green algal genus Dunaliella. Genome Biol Evol. 7:656-663.
15. Drouin G, Daoud H, Xia J. 2008. Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol. 49:827-831.
16. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
17. Goldman N, Yang ZA. 1994. Codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 11:725-736.
18. Hannon M, Gimpel J, Tran M, Rasala B, Mayfield S. 2010. Biofuels from algae: challenges and potential. Biofuels 1:763-784.
19. Hua J, Smith DR, Borza T, Lee RW. 2012. Similar relative mutation rates in the three genetic compartments of Mesostigma and Chlamydomonas. Protist 163:105-115.
20. Keeling PJ. 2010. The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B Biol Sci. 365:729-748.
21. Keeling PJ, et al. 2014. The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 12:e1001889.
22. Kimura M. 1983. The neutral theory of molecular evolution. Cambridge (England): Cambridge University Press.
23. Li WH, Wu CI, Luo CC. 1985. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol. 2:150-174.
24. Lynch M, Koskella B, Schaack S. 2006. Mutation pressure and the evolution of organelle genomic architecture. Science 311:1727-1730.
25. Mower JP, Touzet P, Gummow JS, Delph LF, Palmer JD. 2007. Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants. BMC Evol Biol. 7:135.
26. Muse SV. 1996. Estimating synonymous and nonsynonymous substitution rates. Mol Biol Evol. 13:105-114.
27. Oliveira DCSG, Raychoudhury R, Lavrov DV, Werren JH. 2008. Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Mol Biol Evol. 25:2167-2180.
28. Orlando L. 2014. A 400, 000-year-old mitochondrial genome questions phylogenetic relationships amongst archaic hominins. BioEssays 36:598-605.
29. Pochon X, Putnam HM, Gates RD. 2014. Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution. PeerJ. 2:e394.
30. Popescu CE, Lee RW. 2007. Mitochondrial genome sequence evolution in Chlamydomonas. Genetics 175:819-826.
31. Preston MD, et al. 2014. A barcode of organellar genome polymorphisms identifies the geographic origin of Plasmodium falciparum strains. Nat Commun. 5:4052.
32. Richardson AO, Rice DW, Young GJ, Alverson AJ, Palmer JD. 2013. The "fossilized" mitochondrial genome of Liriodendron tulipifera: ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate. BMC Biol. 11:29.
33. Riisberg I, Edvardsen B. 2014. Genetic variation in bloom-forming ichthyotoxic Pseudochattonella species (Dictyochophyceae, Heterokonta) using nuclear, mitochondrial and plastid DNA sequence data. Eur J Phycol. 43:413-422.
34. Sloan DB, Alverson, Chuckalovcak, et al. 2012. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 10:e1001241.
35. Sloan DB, Alverson AJ, Wu M, Palmer JD, Taylor DR. 2012. Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol Evol. 4:294-306.
36. Sloan DB, Taylor DR. 2012. Evolutionary rate variation in organelle genomes: the role of mutational processes. In: Bullerwell C, editor. Organelle genetics. Berlin (Germany): Springer. p. 123-146.
37. Smith DR. 2012. Not seeing the genomes for the DNA. Brief Funct Genomics. 11:289-290.
38. Smith DR. 2013. RNA-Seq data: a goldmine for organelle research. Brief Funct Genomics. 12:454.
39. Smith DR, Arrigo KR, Alderkamp AC, Allen AE. 2014. Massive difference in synonymous substitution rates among mitochondrial, plastid, and nuclear genes of Phaeocystis algae. Mol Phylogenet Evol. 71:36-40.
40. Smith DR, Hua J, Lee RW, Keeling PJ. 2012. Relative rates of evolution among the three genetic compartments of the red alga Porphyra differ from those of green plants and do not correlate with genome architecture. Mol Phylogenet Evol. 65:339-344.
41. Smith DR, Jackson CJ, Reyes-Prieto A. 2014. Nucleotide substitution rate analyses of the glaucophyte Cyanophora suggest an ancestrally lower mutation rate in plastid vs mitochondrial DNA for the Archaeplastida. Mol Phylogenet Evol. 79:380-384.
42. Smith DR, Keeling PJ. 2012. Twenty-fold difference in evolutionary rates between the mitochondrial and plastid genomes of species with secondary red plastids. J Eukaryotic Microbiol. 59:181-184.
43. Smith DR, Keeling PJ. Forthcoming 2015. Mitochondrial and plastid genome architecture: reoccurring themes, but significant differences at the extremes. Proc Natl Acad Sci USA., doi: 10.1073/pnas.1422049112.
44. Starkenburg SR, et al. 2014. A pangenomic analysis of Nannochloropsis organellar genomes reveals novel genetic variations in key metabolic genes. BMC Genomics 15:212.
45. Wicke S, Schäferhoff B, Müller KF. 2014. Disproportional plastome-wide increase of substitution rates and relaxed purifying selection in genes of carnivorous lentibulariaceae. Mol Biol Evol. 31:529-545.
46. Wicke S, Schneeweiss GM, De Pamphilis CW, Müller KF, Quandt D. 2011. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol. 76:273-297.
47. Willerslev E, et al. 2014. Fifty thousand years of Arctic vegetation and megafaunal diet. Nature 506:47-51.
48. Williams TA, Foster PG, Cox CJ, Embley TM. 2013. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231-236.
49. Wolfe KH, Li WH, Sharp PM. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA. 84:9054-9058.
50. Worden AZ, et al. 2009. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268-272.
51. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
52. Yang Z, Nielsen R. 2000. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol. 1:32-43.
53. Zhu A, Guo W, Jain K, Mower JP. 2014. Unprecedented heterogeneity in the synonymous substitution rate within a plant genome. Mol Biol Evol. 31:1228-1236.