On the adaptive value of cytoplasmic genomes in plants

Molecular Ecology

Volumn 23, Issue 20, 2014, Pages 4899-4911

  Bock, Dan G ^a   Andrew, Rose L ^a,b   Rieseberg, Loren H ^a,c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF NEW ENGLAND   (Australia)

^c INDIANA UNIVERSITY   (United States)

Author keywords

chloroplast DNA; mitochondrial DNA; neutrality tests; plant local adaptation; positive Darwinian selection; selective neutrality

Indexed keywords

PLANT DNA;

ADAPTATION; CHLOROPLAST GENOME; CYTOPLASM; EVOLUTION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; MITOCHONDRIAL GENOME; MUTATION RATE; PLANT; PLANT GENOME;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; CYTOPLASM; DNA, PLANT; GENETIC VARIATION; GENOME, CHLOROPLAST; GENOME, MITOCHONDRIAL; GENOME, PLANT; MUTATION RATE; PLANTS; SELECTION, GENETIC;

EID: 84907900767     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12920     Document Type: Review

References (107)

1. Acosta MC, Premoli AC, (2010) Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae). Molecular Phylogenetics and Evolution, 54, 235-242.
2. Atkin OK, Macherel D, (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Annals of Botany, 103, 581-597.
3. Avise JC, Giblin-Davidson C, Laerm J, Patton JC, Lansman RA, (1979) Mitochondrial DNA clones and matriarchal phylogeny within and among geographic populations of the pocket gopher, Geomys pinetis. Proceedings of the National Academy of Sciences USA, 76, 6694-6698.
4. Bakker FT, Breman F, Merckx V, (2006) DNA sequence evolution in fast evolving mitochondrial DNA nad1 exons in Geraniaceae and Plantaginaceae. Taxon, 55, 887-896.
5. Ballard JWO, Melvin RG, (2010) Linking the mitochondrial genotype to the organismal phenotype. Molecular Ecology, 19, 1523-1539.
6. Ballard JWO, Whitlock MC, (2004) The incomplete natural history of mitochondria. Molecular Ecology, 13, 729-744.
7. Balloux F, (2010) The worm in the fruit of the mitochondrial DNA tree. Heredity, 104, 419-420.
8. Barr CM, Keller SR, Ingvarsson PK, Sloan DB, Taylor DR, (2007) Variation in mutation rate and polymorphism among mitochondrial genes in Silene vulgaris. Molecular Biology and Evolution, 24, 1783-1791.
9. Bashalkhanov S, Eckert AJ, Rajora OP, (2013) Genetic signatures of natural selection in response to air pollution in red spruce (Picea rubens, Pinaceae). Molecular Ecology, 22, 5877-5889.
10. Bazin E, Glémin S, Galtier N, (2006) Population size does not influence mitochondrial genetic diversity in animals. Science, 312, 570-571.
11. Beaumont MA, (2005) Adaptation and speciation: what can Fst tell us? Trends in Ecology & Evolution, 20, 435-440.
12. Beaumont MA, Balding DJ, (2004) Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology, 13, 969-980.
13. Betancourt AJ, Welch JJ, Charlesworth B, (2009) Reduced effectiveness of selection caused by a lack of recombination. Current Biology, 19, 655-660.
14. Birky CW Jr, Maruyama T, Fuerst P, (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics, 103, 513-527.
15. Bock DG, Kane NC, Ebert DP, Rieseberg LH, (2014) Genome skimming reveals the origin of the Jerusalem Artichoke tuber crop species: neither from Jerusalem nor an artichoke. New Phytologist, 201, 1021-1030.
16. Bromham L, Cowman PF, Lanfear R, (2013) Parasitic plants have increased rates of molecular evolution across all three genomes. BMC Evolutionary Biology, 13, 126.
17. Brown WM, George M Jr, Wilson AC, (1979) Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences USA, 76, 1967-1971.
18. Budar F, Roux F, (2011) The role of organelle genomes in plant adaptation. Plant Signaling & Behavior, 6, 635-639.
19. Burton RS, Pereira RJ, Barreto FS, (2013) Cytonuclear genomic interactions and hybrid breakdown. Annual Review of Ecology, Evolution, and Systematics, 44, 281-302.
20. Campbell DR, Waser NM, Aldridge G, Wu CA, (2008) Lifetime fitness in two generations of Ipomopsis hybrids. Evolution, 62, 2616-2627.
21. Chaves MM, Flexas J, Pinheiro C, (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany, 103, 551-560.
22. Cho Y, Mower JP, Qiu YL, Palmer JD, (2004) Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. Proceedings of the National Academy of Sciences USA, 101, 17741-17746.
23. Christin PA, Salamin N, Muasya AM, et al,. (2008) Evolutionary switch and genetic convergence on rbcL following the evolution of C4 photosynthesis. Molecular Biology and Evolution, 25, 2361-2368.
24. Chung S-M, Gordon VS, Staub JE, (2007) Sequencing cucumber (Cucumis sativus L.) chloroplast genomes identifies differences between chilling-tolerant and -susceptible cucumber lines. Genome, 50, 215-225.
25. Comes HP, Abbott RJ, (2001) Molecular phylogeography, reticulation, and lineage sorting in Mediterranean Senecio sect. Senecio (Asteraceae). Evolution, 55, 1943-1962.
26. Coop G, Witonsky D, Di Rienzo A, Pritchard JK, (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics, 185, 1411-1423.
27. Cutter AD, Payseur BA, (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nature Reviews Genetics, 14, 262-274.
28. Dowling DK, Friberg U, Lindell J, (2008) Evolutionary implications of non-neutral mitochondrial genetic variation. Trends in Ecology & Evolution, 23, 546-554.
29. Drouin G, Daoud H, Xia J, (2008) Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Molecular Phylogenetics and Evolution, 49, 827-831.
30. Dumolin-Lapegue S, Demesure B, Fineschi S, Come VL, Petit RJ, (1997) Phylogeographic structure of white oaks throughout the European continent. Genetics, 146, 1475-1487.
31. Erixon P, Oxelman B, (2008) Whole-gene positive selection, elevated synonymous substitution rates, duplication, and indel evolution of the chloroplast clpP1 gene. PLoS One, 3, e1386.
32. da Fonseca RR, Johnson WE, O'Brien SJ, Ramos MJ, Antunes A, (2008) The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics, 9, 119.
33. Fuentes I, Stegemann S, Golczyk H, Karcher D, Bock R, (2014) Horizontal genome transfer as an asexual path to the formation of new species. Nature, 511, 232-235.
34. Galmes J, Andralojc PJ, Kapralov MV, et al,. (2014) Environmentally driven evolution of Rubisco and improved photosynthesis and growth within the C3 genus Limonium (Plumbaginaceae). New Phytologist, 203, 989-999.
35. Galtier N, Nabholz B, Glemin S, Hurst GD, (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology, 18, 4541-4550.
36. Gordon VS, Staub JE, (2011) Comparative analysis of chilling response in cucumber through plastidic and nuclear genetic effects component analysis. Journal of the American Society for Horticultural Science, 136, 256-264.
37. Greiner S, (2012) Plastome mutants of higher plants. In: Genomics of Chloroplasts and Mitochondria (eds, Bock R, Knoop V,), pp. 237-266. Springer, Dordrecht, Heidelberg, New York, London, the Netherlands.
38. Greiner S, Bock R, (2013) Tuning a ménage à trois: co-evolution and co-adaptation of nuclear and organelle genomes in plants. BioEssays, 35, 354-365.
39. Guisinger MM, Kuehl JV, Boore JL, Jansen RK, (2008) Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proceedings of the National Academy of Sciences USA, 105, 18424-18429.
40. Haag-Liautard C, Coffey N, Houle D, et al,. (2008) Direct estimation of the mitochondrial DNA mutation rate in Drosophila melanogaster. PLoS Biology, 6, e204.
41. Hansen AK, Escobar LK, Gilbert LE, Jansen RK, (2007) Paternal, maternal, and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies. American Journal of Botany, 94, 42-46.
42. Hao DC, Chen SL, Xiao PG, (2010) Molecular evolution and positive Darwinian selection of the chloroplast maturase matK. Journal of Plant Research, 123, 241-247.
43. Hill WG, Robertson A, (1966) The effect of linkage on limits to artificial selection. Genetical Research, 8, 269-294.
44. Hill JH, Chen Z, Xu H, (2014) Selective propagation of functional mitochondrial DNA during oogenesis restricts the transmission of a deleterious mitochondrial variant. Nature Genetics, 46, 389-392.
45. Hough J, Hollister JD, Wang W, Barrett SCH, Wright SI, (2014) Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus. Proceedings of the National Academy of Sciences USA, 111, 7713-7718.
46. Iida S, Miyagi A, Aoki S, et al,. (2009) Molecular adaptation of rbcL in the heterophyllous aquatic plant Potamogeton. PLoS One, 4, e4633.
47. Irwin DE, (2012) Local adaptation along smooth ecological gradients causes phylogeographic breaks and phenotypic clustering. The American Naturalist, 180, 35-49.
48. Jaramillo-Correa JP, Bousquet J, (2005) Mitochondrial genome recombination in the zone of contact between two hybridizing conifers. Genetics, 171, 1951-1962.
49. Kapralov MV, Filatov DA, (2006) Molecular adaptation during adaptive radiation in the Hawaiian endemic genus Schiedea. PLoS One, 1, e8.
50. Kapralov MV, Filatov DA, (2007) Widespread positive selection in the photosynthetic Rubisco enzyme. BMC Evolutionary Biology, 7, 73.
51. Kapralov MV, Kubien DS, Andersson I, Filatov DA, (2011) Changes in Rubisco kinetics during the evolution of C4 photosynthesis in Flaveria (Asteraceae) are associated with positive selection on genes encoding the enzyme. Molecular Biology and Evolution, 28, 1491-1503.
52. Kapralov MV, Smith JAC, Filatov DA, (2012) Rubisco evolution in C4 eudicots: an analysis of Amaranthaceae sensu lato. PLoS One, 7, e52974.
53. Khakhlova O, Bock R, (2006) Elimination of deleterious mutations in plastid genomes by gene conversion. The Plant Journal, 46, 85-94.
54. Kimball S, Campbell DR, Lessin C, (2008) Differential performance of reciprocal hybrids in multiple environments. Journal of Ecology, 96, 1306-1318.
55. Kimura M, (1983) The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge.
56. Krause K, (2012) Plastid genomes of parasitic plants: a trail of reductions and losses. In: Organelle Genetics (ed., Bullerwell C,). Springer, Berlin.
57. Leinonen PH, Remington DL, Savolainen O, (2011) Local adaptation, phenotypic differentiation and hybrid fitness in diverged natural populations of Arabidopsis lyrata. Evolution, 65, 90-107.
58. Leinonen P, Remington DL, Leppala J, Savolainen O, (2013) Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata. Molecular Ecology, 22, 709-723.
59. Lin Z, Kong H, Nei M, Ma H, (2006) Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. Proceedings of the National Academy of Sciences USA, 103, 10328-10333.
60. Llopart A, Herrig D, Brud E, Stecklein Z, (2014) Sequential adaptive introgression of the mitochondrial genome in Drosophila yakuba and Drosophila santomea. Molecular Ecology, 23, 1124-1236.
61. Maheshwari S, Barbash DA, (2011) The genetics of hybrid incompatibilities. Annual Review of Genetics, 45, 331-355.
62. Maréchal A, Brisson N, (2010) Recombination and the maintenance of plant organelle genome stability. New Phytologist, 186, 299-317.
63. Mariac C, Scarcelli N, Pouzadou J, et al,. (2014) Cost-effective enrichment hybridization capture of chloroplast genomes at deep multiplexing levels for population genetics and phylogeography studies. Molecular Ecology Resources, 14, 1109-1113.
64. McCauley DE, (2013) Paternal leakage, heteroplasmy, and the evolution of plant mitochondrial genomes. New Phytologist, 200, 966-977.
65. McKinnon GE, Vaillancourt RE, Steane DA, Potts BM, (2004) The rare silver gum, Eucalyptus cordata, is leaving its trace in the organellar gene pool of Eucalyptus globulus. Molecular Ecology, 13, 3751-3762.
66. Mower JP, Touzet P, Gummow JS, Delph LF, Palmer JD, (2007) Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants. BMC Evolutionary Biology, 7, 135.
67. Muir G, Filatov D, (2007) A selective sweep in the chloroplast DNA of dioecious Silene (section Elisanthe). Genetics, 177, 1239-1247.
68. Nachman MW, (1998) Deleterious mutations in animal mitochondrial DNA. Genetica, 102-103, 61-69.
69. Neale DB, Wheeler NC, Allard RW, (1986) Paternal inheritance of chloroplast DNA in Douglas-fir. Canadian Journal of Forest Research, 16, 1152-1154.
70. Neiva J, Pearson G, Valero M, Serrão E, (2010) Surfing the wave on a borrowed board: range expansion and spread of introgressed organellar genomes in the seaweed Fucus ceranoides L. Molecular Ecology, 19, 4812-4822.
71. Nielsen R, (2001) Statistical tests of selective neutrality in the age of genomics. Heredity, 86, 641-647.
72. Osada N, Akashi H, (2012) Mitochondrial-nuclear interactions and accelerated compensatory evolution: evidence from the primate cytochrome c oxidase complex. Molecular Biology and Evolution, 29, 337-346.
73. Palme A, Su Q, Palsson S, Lascoux M, (2004) Extensive sharing of chloroplast haplotypes among European birches indicates hybridization among Betula pendula, B. pubescens and B. nana. Molecular Ecology, 13, 167-178.
74. Parkinson CL, Mower JP, Qiu YL, et al,. (2005) Multiple major increases and decreases in mitochondrial substitution rates in the plant family Geraniaceae. BMC Evolutionary Biology, 5, 73.
75. Parks M, Cronn R, Liston A, (2009) Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes. BMC Biology, 7, 84.
76. Petit RJ, Pineau E, Demesure B, Bacilieri R, Ducousso A, Kremer A, (1997) Chloroplast DNA footprints of postglacial recolonization by oaks. Proceedings of the National Academy of Sciences USA, 94, 9996-10001.
77. Petit RJ, Csaikl UM, Bordacs S, et al,. (2002a) Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations. Forest Ecology and Management, 156, 5-26.
78. Petit RJ, Latouche-Hallé C, Pemonge M-H, Kremer A, (2002b) Chloroplast DNA variation of oaks in France and the influence of forest fragmentation on genetic diversity. Forest Ecology and Management, 156, 115-130.
79. Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer A, (2004) Hybridization as a mechanism of invasion in oaks. New Phytologist, 161, 151-164.
80. Petit RJ, Duminil J, Fineschi S, et al,. (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology, 14, 689-701.
81. Powles SB, Yu Q, (2010) Evolution in action: plants resistant to herbicides. Annual Review of Plant Biology, 61, 317-347.
82. Rand DM, Kann LM, (1998) Mutation and selection at silent and replacement sites in the evolution of animal mitochondrial DNA. Genetica, 102-103, 393-407.
83. Rieseberg LH, Soltis DE, (1991) Phylogenetic consequences of cytoplasmic gene flow in plants. Evolutionary Trends in Plants, 5, 65-84.
84. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC, (2004) Effects of purifying and adaptive selection on regional variation in human mtDNA. Science, 303, 223-226.
85. Sambatti JBM, Ortiz-Barrientos D, Baack EJ, Rieseberg LH, (2008) Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecology Letters, 11, 1082-1091.
86. Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA, (1998) Phylogeographic studies in plants: problems and prospects. Molecular Ecology, 7, 465-474.
87. Schmitz-Linneweber C, Kushnir S, Babiychuk E, et al,. (2005) Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase alpha-subunit mRNA. Plant Cell, 17, 1815-1828.
88. Scowcroft WR, (1979) Nucleotide polymorphism in chloroplast DNA of Nicotiana debneyi. Theoretical and Applied Genetics, 55, 133-137.
89. Sen L, Fares M, Liang B, et al,. (2011) Molecular evolution of rbcL in three gymnosperm families: identifying adaptive and coevolutionary patterns. Biology Direct, 6, 29.
90. Sloan DB, Taylor DR, (2012) Evolutionary rate variation in organelle genomes: the role of mutational processes. In: Organelle Genetics: Evolution of Organelle Genomes and Gene Expression (ed., Bullerwell CE,), pp. 123-146. Springer-Verlag, Berlin.
91. 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 Biology and Evolution, 4, 294-306.
92. Sloan DB, Triant DA, Forrester NJ, et al,. (2014a) A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae). Molecular Phylogenetics and Evolution, 72, 82-89.
93. Sloan DB, Triant DA, Wu M, Taylor DR, (2014b) Cytonuclear interactions and relaxed selection accelerate sequence evolution in organelle ribosomes. Molecular Biology and Evolution, 31, 673-682.
94. Stegemann S, Keuthe M, Greiner S, Bock R, (2012) Horizontal transfer of chloroplast genomes between plant species. Proceedings of the National Academy of Sciences USA, 109, 2434-2438.
95. Stewart JB, Freyer C, Elson JL, et al,. (2008) Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biology, 6, e10.
96. Straub SC, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A, (2012) Navigating the tip of the genomic iceberg: next generation sequencing for plant systematics. American Journal of Botany, 99, 349-364.
97. Timmis JN, Ayliffe MA, Huang CY, Martin W, (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Reviews Genetics, 5, 123-135.
98. Toews DPL, Brelsford A, (2012) The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21, 3907-3930.
99. Toews DPL, Mandic M, Richards JG, Irwin DE, (2013) Migration, mitochondria and the yellow-rumped warbler. Evolution, 68, 241-255.
100. Tsitrone A, Kirkpatrick M, Levin DA, (2003) A model for chloroplast capture. Evolution, 57, 1776-1782.
101. Wallace DC, (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annual Review of Genetics, 39, 359-407.
102. Weng ML, Ruhlman TA, Gibby M, Jansen RK, (2012) Phylogeny, rate variation, and genome size evolution in Pelargonium (Geraniaceae). Molecular Phylogenetics and Evolution, 64, 654-670.
103. Weng ML, Blazier JC, Govindu M, Jansen RK, (2014) Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. Molecular Biology and Evolution, 31, 645-659.
104. Wolfe KH, Li W-H, Sharp PM, (1987) Rates of nucleotide substitutions vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences USA, 84, 9054-9058.
105. Wright SI, Nano N, Foxe JP, Dar VN, (2008) Effective population size and tests of neutrality at cytoplasmic genes in Arabidopsis. Genetics Research, 90, 119-128.
106. Zhong B, Yonezawa T, Zhong Y, Hasegawa M, (2009) Episodic evolution and adaptation of chloroplast genomes in ancestral grasses. PLoS One, 4, e5297.
107. Zhu A, Guo W, Jain K, Mower JP, (2014) Unprecedented heterogeneity in the synonymous substitution rate within a plant genome. Molecular Biology and Evolution, 31, 1228-1236.