Paternal leakage, heteroplasmy, and the evolution of plant mitochondrial genomes

New Phytologist

Volumn 200, Issue 4, 2013, Pages 966-977

  Mccauley, David E ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Gynodioecy; Heteroplasmy; Mitochondrial genome; Paternal leakage; Recombination; Silene

Indexed keywords

CYTOPLASM; EVOLUTIONARY BIOLOGY; GENE FLOW; GENOME; GYNODIOECY; HERITABILITY; MITOCHONDRION; PATERNAL EFFECT; PLANT COMMUNITY;

GENE FLOW; GENETICS; GYNODIOECY; HETEROPLASMY; INHERITANCE; MITOCHONDRIAL GENOME; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATERNAL LEAKAGE; PLANT GENOME; PLANT INFERTILITY; RECOMBINATION; REVIEW; SILENE;

GYNODIOECY; HETEROPLASMY; MITOCHONDRIAL GENOME; PATERNAL LEAKAGE; RECOMBINATION; SILENE;

BASE SEQUENCE; EVOLUTION, MOLECULAR; GENE FLOW; GENOME, MITOCHONDRIAL; GENOME, PLANT; INHERITANCE PATTERNS; MOLECULAR SEQUENCE DATA; PLANT INFERTILITY;

EID: 84887032675     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12431     Document Type: Review

References (85)

1. Akeyonova E, Sinyavskaya M, Danilenko N, Pershina L, Nakamura C, Davydenko O. 2005. Heteroplasmy and paternally oriented shift of the organellar DNA composition in barley-wheat hybrids during backcrosses with wheat parents. Genome 48: 761-769.
2. Apitz J, Weihe A, Pohlheim F. 2012. Biparental inheritance of organelles in Pelargonium: evidence for intergenomic recombination of mitochondrial DNA. Planta 237: 509-515.
3. Arimura S, Yamamoto J, Aida GP, Nakazono M, Tsutsumi N. 2004. Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proceedings of the National Academy of Sciences, USA 101: 7805-7808.
4. Bailey MF, Delph LF. 2007. A field guide to models of sex-ratio evolution in gynodioecious species. Oikos 116: 1609-1617.
5. Barr CM, Keller SR, Ingvarsson PK, Sloan DB, Taylor DR. 2007. Variation in mutation rate and polymorphism among mitochondrial genes of Silene vulgaris. Molecular Biology and Evolution 24: 1783-1791.
6. Barr CM, Neiman M, Taylor DR. 2005. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytologist 168: 39-50.
7. Bentley KE, Mandel JR, McCauley DE. 2010. Paternal leakage and heteroplasmy of mitochondrial genomes in Silene vulgaris: evidence from experimental crosses. Genetics 185: 961-968.
8. Birky CW. 1995. Uniparental inheritance of mitochondrial and chloroplast genes -mechanisms and evolution. Proceedings of the National Academy of Sciences, USA 92: 11331-11338.
9. Birky CW. 2001. The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annual Review of Genetics 35: 125-148.
10. Birky CW, 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.
11. Burt A, Trivers R. 2006. Genes in conflict. Cambridge, MA, USA: Harvard University Press.
12. Charlesworth D, Morgan MT, Charlesworth B. 1993. Mutation accumulation in finite populations. Journal of Heredity 84: 321-325.
13. Cho Y, Mower JP, Qiu JL, 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.
14. Cosmides LM, Tooby J. 1981. Cytoplasmic inheritance and intragenomic conflict. Journal of Theoretical Biology 89: 83-129.
15. Dufay M, Billard E. 2012. How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioeciois species. Annals of Botany 109: 505-519.
16. Felsenstein J. 1974. The evolutionary advantage of recombination. Genetics 78: 737-756.
17. Fontaine KM, Cooley JR, Simon CM. 2007. Evidence for paternal leakage in hybrid periodical cicadas (Hemiptera: Magicicada spp.). PLoS ONE 9: e892.
18. Frank SA. 1989. The evolutionary dynamics of cytoplasmic male sterility. American Naturalist 133: 345-376.
19. Gabriel W, Lynch M, Burger R. 1993. Muller's Ratchet and mutational meltdowns. Evolution 47: 1744-1757.
20. Galtier N, Nabholz B, Glemin S, Hurst GDD. 2009. Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology 18: 4541-4550.
21. Halkett F, Simon J-C, Balloux F. 2005. Tackling the population genetics of clonal and partially clonal organisms. Trends in Ecology and Evolution 20: 194-201.
22. Havey MJ. 1997. Predominant paternal inheritance of the mitochondrial genome in cucumber. Journal of Heredity 88: 232-235.
23. Hedrick PW. 2011. Genetics of populations, 4th edn. Sudbury, MA, USA: Jones and Bartlett.
24. Hoarau G, Coyer JA, Olsen J. 2009. Paternal leakage of mitochondrial DNA in a Fucus (Phaeophyceae) hybrid zone. Journal of Phycology 45: 621-624.
25. Hoekstra RF. 2000. Evolutionary origin and consequences of uniparental mitochondrial inheritance. Human Reproduction 15(suppl. 2): 102-111.
26. Houliston GJ, Olson MS. 2006. Nonneutral evolution of organelle genes in Silene vulgaris. Genetics 174: 1983-1994.
27. Hudson RR, Kaplan NL. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111: 147-164.
28. Jaramillo-Correa JP, Bousquet J. 2005. Mitochondrial genome recombination in the zone of contact between two hybridizing conifers. Genetics 171: 1951-1962.
29. Keller SR, Taylor DR. 2010. Genomic admixture increases fitness during a biological invasion. Journal of Evolutionary Biology 23: 1720-1731.
30. Kmiec B, Woloszynska M, Janska H. 2006. Heteroplasmy as a common state of mitochondrial genetic information in plants and animals. Current Genetics 50: 149-159.
31. Kühn K, Gualberto JM. 2012. Recombination in the stability, repair and evolution of the mitochondrial genome. Advances in Botanical Research 63: 215-252.
32. Lenski RE. 1993. Assessing the genetic structure of microbial populations. Proceedings of the National Academy of Sciences, USA 90: 4334-4336.
33. Loewe L. 2006. Quantifying the genomic decay paradox due to Muller's ratchet in human mitochondrial DNA. Genetical Research 87: 133-159.
34. Lynch M, Blanchard JL. 1998. Deleterious mutation accumulation in organelle genomes. Genetics 103: 29-39.
35. Mackenzie S, McIntosh I. 1999. Higher plant mitochondria. Plant Cell 11: 571-585.
36. Mandel JR, McAssey EV, Roland KM, McCauley DE. 2012. Mitochondrial gene diversity associated with the atp9 stop codon in natural population of wild carrot (Daucus carota ssp. carota). Journal of Heredity 103: 418-425.
37. 2+-dependent exonuclease degrades organelle DNA during Arabidopsis pollen development. Plant Cell 23: 1608-1624.
38. Maynard Smith J, Smith NH, O'Rourke M, Spratt BG. 1993. How clonal are bacteria? Proceedings of the National Academy of Sciences, USA 90: 4384-4388.
39. McCauley DE. 1998. The genetic structure of a gynodioecious plant: nuclear and cytoplasmic genes. Evolution 52: 255-260.
40. McCauley DE, Bailey MF. 2009. Recent advances in the study of gynodioecy: the interface of theory and empiricism. Annals of Botany 104: 611-620.
41. McCauley DE, Bailey MF, Sherman NA, Darnell MZ. 2005. Evidence for paternal transmission and heteroplasmy in the mitochondrial genome of Silene vulgaris, a gynodioecious plant. Heredity 95: 50-58.
42. McCauley DE, Ellis JR. 2008. Recombination and linkage disequilibrium among mitochondrial genes in structured populations of the gynodioecious plant Silene vulgaris. Evolution 62: 823-832.
43. McCauley DE, Olson MS. 2008. Do recent findings in plant mitochondrial and population genetics have implications for the study of gynodioecy and cytonuclear conflict? Evolution 62: 1013-1025.
44. McVean GAT. 2001. What do patterns of genetic variability reveal about mitochondrial recombination? Heredity 87: 613-620.
45. Milligan BG. 1992. Is organelle DNA strictly maternally inherited? Power analysis of a binomial distribution. American Journal of Botany 79: 1325-1328.
46. Mogensen HL. 1996. The hows and whys of cytoplasmic inheritance in seed plants. American Journal of Botany 83: 383-404.
47. Muller HJ. 1964. The relation of recombination to mutational load. Mutation Research 1: 2-9.
48. Nagata N. 2010. Mechanisms for independent cytoplasmic inheritance of mitochondria and plastids in angiosperms. Journal of Plant Research 123: 193-199.
49. Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T. 1999. The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209: 53-65.
50. Neale DB, Marshall KA, Sederoff RR. 1989. Chloroplast and mitochondrial DNA are paternally inherited in Sequoia sempervirens D. Don Endl. Proceedings of the National Academy of Sciences, USA 86: 9347-9349.
51. Neiman M, Taylor DR. 2009. The causes of mutation accumulation in mitochondrial genomes. Proceedings of the Royal Society of London, B: Biological Sciences 276: 1201-1209.
52. Olson MS, McCauley DE. 2002. Mitochondrial DNA diversity, population structure, and gender association in the gynodioecious plant Silene vulgaris. Evolution 56: 253-262.
53. Ota M, Fukushima H, Kulski JK, Inoko H. 2007. Single nucleotide polymorphism detection by polymerase chain reaction-restriction length polymorphism. Nature Protocols 2: 2857-2864.
54. Palmer J, Herbon LA. 1988. Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. Journal of Molecular Evolution 28: 87-97.
55. Pearl SA, Welch ME, McCauley DE. 2009. Mitochondrial heteroplasmy and paternal leakage in natural populations of Silene vulgaris, a gynodioecious plant. Molecular Biology and Evolution 26: 537-545.
56. Petit RJ, Duminil J, Fineschi S, Hampte A, Salvini D, Vendramin GG. 2005. Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology 14: 689-701.
57. Petit RJ, Kremer A, Wagner DB. 1993. Finite island model for organelle and nuclear genes in plants. Heredity 71: 630-641.
58. Rokas A, Abbot P. 2009. Harnessing genomics for evolutionary insights. Trends in Ecology and Evolution 24: 192-200.
59. Rokas A, Ladoukakis E, Zouros E. 2003. Animal mitochondrial DNA recombination revisited. Trends in Ecology and Evolution 18: 411-417.
60. Schnable PS, Wise RP. 1998. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends in Plant Science 3: 175-180.
61. Sheahan MB, McCurdy DW, Rose RJ. 2005. Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion. Plant Journal 44: 744-755.
62. Shykoff JA, Kolokotronis S-O, Collin CL, Lopez-Villavicencio M. 2003. Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135: 1-9.
63. Sloan DB. 2013. One ring to rule them all? Genome sequencing provides new insights into the 'master circle' model of plant mitochondrial DNA structure. New Phytologist 200: 978-985.
64. Sloan DB, Alverson AJ, Chuckalovak JP, Wu M, McCauley DE, Palmer JD, Taylor DR. 2012a. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptional high mutation rates. PLoS Biology 10: e1001241.
65. Sloan DB, Barr CM, Olson MS, Keller SR, Taylor DR. 2008. Evolutionary rate variation at multiple levels of biological organization in plant mitochondrial DNA. Molecular Biology and Evolution 25: 243-246.
66. Sloan DB, Müller K, McCauley DE, Taylor DR, Štorchová H. 2012b. Intraspecific variation in mitochondrial genome sequence, structure, and gene content in Silene vulgaris, an angiosperm with pervasive cytoplasmic male sterility. New Phytologist 196: 1228-1239.
67. Sokal RR, Rohlf FJ. 2012. Biometry, 4th edn. New York, NY, USA: Freeman and Co.
68. Städler T, Delph LF. 2002. Ancient mitochondrial haplotypes and evidence for intragenic recombination in a gynodioecious plant. Proceedings of the National Academy of Sciences, USA 99: 11730-11735.
69. Svab Z, Maliga P. 2007. Exceptional transmission of plastids and mitochondria from the transplastonic pollen parent and its impact on transgenic containment. Proceedings of the National Academy of Sciences, USA 104: 7003-7008.
70. Takahata N, Maruyama T. 1981. A mathematical model of extranuclear genes and the genetic variability maintained in a finite population. Genetical Research 37: 291-302.
71. Tibayrence M, Ayala FJ. 2012. Reproductive clonality of pathogens: a perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa. Proceedings of the National Academy of Sciences, USA 109: E3305-E3313.
72. Touzet P. 2012. Mitochondrial genome evolution and gynodioecy. Advances in Botanical Research 63: 71-98.
73. Touzet P, Delph LF. 2009. The effect of breeding system on polymorphism in mitochondrial genes of Silene. Genetics 181: 631-644.
74. Trusty JL, Johnston KJ, Lockaby BG, Goertzen LR. 2007. Bi-parental cytoplasmic DNA inheritance in Wisteria (Fabaceae): evidence from a natural experiment. Plant Cell Physiology 48: 662-665.
75. Wade MJ, McCauley DE. 2005. Paternal leakage sustains the cytoplasmic polymorphism underlying gynodioecy but remains invasible by nuclear restorers. American Naturalist 166: 592-602.
76. Wagner DB, Dong J, Carlson MR, Yanchuk AD. 1991. Paternal leakage of mitochondrial DNA in Pinus. Theoretical and Applied Genetics 82: 510-514.
77. Wang D-Y, Zhang Q, Liu Y, Lin Z-F, Zhang S-X, Sun M-X. 2010. The levels of male gametic mitochondrial DNA are highly regulated in angiosperms with regard to mitochondrial inheritance. Plant Cell 22: 2402-2416.
78. Weihe A, Apitz J, Pohlheim F, Salinas-Hartwig A, Borner T. 2009. Biparental inheritance of plastidal and mitochondrial DNA and hybrid variegation in Pelargonium. Molecular Genetics and Genomics 282: 587-593.
79. Welch ME, Darnell MZ, McCauley DE. 2006. Variable populations within variable populations: quantifying mitochondrial heteroplasmy in natural populations of the gynodioecious plant Silene vulgaris. Genetics 174: 829-837.
80. White DJ, Wolff JK, Pierson M, Gemmell NJ. 2008. Revealing the hidden complexities of mtDNA inheritance. Molecular Ecology 17: 4925-4942.
81. Wolfe KH, Li WH, Sharp PM. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast and nuclear DNAs. Proceedings of the National Academy of Sciences, USA 84: 9054-9058.
82. Wolff JN, Nafisinia M, Sutovsky P, Ballard JWO. 2013. Paternal transmission of mitochondrial DNA as an integral part of mitochondrial inheritance in metapopulations of Drosophila simulans. Heredity 110: 57-62.
83. Wright S. 1978. Evolution and the genetics of population, volume 4: variability within and among natural populations. Chicago, IL, USA: University of Chicago Press.
84. Xu J. 2005. The inheritance of organelle genes and genomes: patterns and mechanisms. Genome 48: 951-958.
85. Zhang Q, Liu Y, Sodmergen. 2003. Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiology 44: 941-951.