Cytonuclear genomic interactions and hybrid breakdown

Annual Review of Ecology, Evolution, and Systematics

Volumn 44, Issue , 2013, Pages 281-302

  Burton, Ronald S ^a   Pereira, Ricardo J ^a   Barreto, Felipe S ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Coadaptation; Dobzhansky Muller incompatibilities; Intergenomic coevolution; Organellar genomes; Reproductive isolation

Indexed keywords

ADAPTATION; CHLOROPLAST; FITNESS; GENETIC ANALYSIS; GENOME; GENOMICS; HYBRID; HYBRIDIZATION; INTERPOPULATION VARIATION; MITOCHONDRION; POPULATION STRUCTURE; PROTEIN; REPRODUCTIVE ISOLATION;

BACTERIA (MICROORGANISMS);

EID: 84888611453     PISSN: 1543592X     EISSN: 15452069     Source Type: Book Series    
DOI: 10.1146/annurev-ecolsys-110512-135758     Document Type: Review

References (116)

1. Arnqvist G, Dowling DK, Eady P, Gay L, Tregenza T, et al. 2010. Genetic architecture of metabolic rate: environment specific epistasis between mitochondrial and nuclear genes in an insect. Evolution 64:3354-63
2. Azevedo L, Carneiro J, van Asch B, Moleirinho A, Pereira F, Amorim A. 2009. Epistatic interactions modulate the evolution of mammalian mitochondrial respiratory complex components. BMC Genomics 10:266
3. Ballard JWO, Melvin RG. 2010. Linking the mitochondrial genotype to the organismal phenotype. Mol. Ecol. 19:1523-39
4. Barr CM, Fishman L. 2010. The nuclear component of a cytonuclear hybrid incompatibility in Mimulus maps to a cluster of pentatricopeptide repeat genes. Genetics 184:455-65
5. Barreto FS, Burton RS. 2013. Evidence for compensatory evolution of ribosomal proteins in response to rapid divergence of mitochondrial r RNA. Mol. Biol. Evol. 30:310-14
6. Barton NH. 1979. The dynamics of hybrid zones. Heredity 43(34):1-359
7. Barton NH, Hewitt GM. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113-49
8. Bateson W. 1909. Heredity and variation in modern lights. In Darwin and Modern Science, ed. AC Seward, pp. 85-101. Cambridge, UK: Cambridge Univ. Press
9. Berthier P, Excoffier L, Ruedi M. 2006. Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species Myotis myotis and Myotis blythii. Proc. R. Soc. B 273:3101-9
10. Birky CW Jr. 2001. The inheritance of genes in mitochondria and chloroplasts: Laws, mechanisms, and models. Annu. Rev. Genet. 35:125-48
11. Blier PU, Dufresne F, Burton RS. 2001. Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet. 17:400-6
12. Bogdanova VS, Berdnikov VA. 2001. Observation of a phenomenon resembling hybrid dysgenesis, in a wild pea subspecies Pisum sativum ssp. elatius. Pisum Genet. 33:5-8
13. Bogdanova VS, Galieva ER, Kosterin OE. 2009. Genetic analysis of nuclear-cytoplasmic incompatibility in pea associated with cytoplasm of an accession of wild subspecies Pisum sativum subsp. elatius (Bieb.) Schmahl. Theor. Appl. Genet. 118:801-9
14. Bolnick DI, Turelli M, Lopez-Fernandez H, Wainwright PC, Near TJ. 2008. Accelerated mitochondrial evolution and "Darwin's corollary": Asymmetric viability of reciprocal F-1 hybrids in centrarchid fishes. Genetics 178:1037-48
15. Bruley C, Dupierris V, Salvi D, Rolland N, Ferro M. 2012. AT-CHLORO: a chloroplast protein database dedicated to sub-plastidial localization. Front. Plant Sci. 3:205
16. Budar F, Touzet P, De Paepe R. 2003. The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited. Genetica 117:3-16
17. Burke J, Arnold ML. 2001. Genetics and the fitness of hybrids. Annu. Rev. Genet. 35:31-52
18. Burton RS, Barreto FS. 2012. A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Mol. Ecol. 21:4942-57
19. Burton RS, Byrne RJ, Rawson PD. 2007. Three divergent mitochondrial genomes from California populations of the copepod Tigriopus californicus. Gene 403:53-59
20. 2 hybrids: Consequences of rapid mitochondrial DNA evolution in allopatric populations. Am. Nat. 168(Suppl. 6):S14-24
21. Calvo SE, Mootha VK. 2010. The mitochondrial proteome and human disease. Annu. Rev. Genomics Hum. Genet. 11:25-44
22. Carneiro M, Baird SJE, Afonso S, Ramirez E, Tarroso P, et al. 2013. Steep clines within a highly permeable genome across a hybrid zone between two subspecies of the European rabbit. Mol. Ecol. 22:2511-25
23. Carneiro M, Ferrand N, Nachman MW. 2009. Recombination and speciation: loci near centromeres are more differentiated than loci near telomeres between subspecies of the European rabbit (Oryctolagus cuniculus). Genetics 181:593-606
24. Case AL, Willis JH. 2008. Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically restricted mitochondrial rearrangement. Evolution 62:1026-39
25. Castellana S, Vicario S, Saccone C. 2011. Evolutionary patterns of the mitochondrial genome in metazoa: exploring the role of mutation and selection in mitochondrial protein-coding genes. Genome Biol. Evol. 3:1067-79
26. Chase CD. 2007. Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet. 23:81-90
27. Cho Y, Mower JP, Qiu Y-L, Palmer JD. 2004. Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. Proc. Natl. Acad. Sci. USA 101:17741-46
28. Chou J-Y, Hung Y-S, Lin K-H, Lee H-Y, Leu J-Y. 2010. Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biol. 8:e1000432
29. Chou J-Y, Leu J-Y. 2010. Speciation through cytonuclear incompatibility: Insights from yeast and implications for higher eukaryotes. BioEssays 32:401-11
30. Derr JN, Hedrick PW, Halbert ND, Plough L, Dobson LK, et al. 2012. Phenotypic effects of cattle mito-chondrial DNA in American bison. Conserv. Biol. 26:1130-36
31. Dietrich W, Wagner WL, Raven PH. 1997. Systematics of Oenothera section Oenothera subsection Oenothera (Onagraceae). In Systematic Botany Monographs, ed. C Anderson, 50:1-234. Laramie, WY: The Am. Soc. Plant Taxon.
32. Dobzhansky TH. 1937. Genetics and the Origin of Species. New York: Columbia Univ. Press
33. Doiron S, Bernatchez L, Blier PU. 2002. A comparative mitogenomic analysis of the potential adaptive value of arctic charr mtDNA introgression in brook charr populations (Salvelinus fontinalis Mitchill). Mol. Biol. Evol. 19:1902-9
34. Dowling DK, Frigerg U, Hailer F, Arnqvist G. 2007. Intergenomic epistasis for fitness: within-population interactions between cytoplasmic and nuclear genes in Drosophila melanogaster. Genetics 175:235-44
35. Duchene AM, Pujol C, Marechal-Drouard L. 2009. Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr. Genet. 55:1-18
36. Ellison CK, Burton RS. 2006. Disruption of mitochondrial function in interpopulation hybrids of Tigriopus californicus. Evolution 60:1382-91
37. Ellison CK, Burton RS. 2008a. Genotype-dependent variation of mitochondrial transcriptional profiles in interpopulation hybrids. Proc. Natl. Acad. Sci. USA 105:15831-36
38. Ellison CK, Burton RS. 2008b. Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 62:631-38
39. Ellison CK, Burton RS. 2010. Cytonuclear conflict in interpopulation hybrids: the role of RNA polymerase in mtDNA transcription and replication. J. Evol. Biol. 23:528-38
40. Ellison CK, Niehuis O, Gadau J. 2008. Hybrid breakdown and mitochondrial dysfunction in hybrids of Nasonia parasitoid wasps. J. Evol. Biol. 21(6):1844-51
41. Fishman L, Willis JH. 2006. A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 60(7):1372-81
42. Gagnaire P-A, Normandeau E, Bernatchez L. 2012. Comparative genomics reveals adaptive protein evolution and a possible cytonuclear incompatibility between European and American eels. Mol. Biol. Evol. 29:2909-19
43. Galtier N. 2011. The intriguing evolutionary dynamics of plant mitochondrial DNA. BMC Biol. 9:61
44. Gaspari M, Falkenberg M, Larsson NG, Gustafsson CM. 2004. The mitochondrial RNA polymerase contributes critically to promoter specificity in mammalian cells. EMBO J. 23:4606-14
45. Glick RE, Sears BB. 1994. Geneticallyprogrammed chloroplast dedifferentiationasaconsequenceofplastome-genome incompatibility in Oenothera. Plant Physiol. 106:367-73
46. Greiner S, Rauwolf U, Meurer J, Herrmann RG. 2011. The role of plastids in plant speciation. Mol. Ecol. 20:371-91
47. Greiner S, Wang X, Herrmann RG, Rauwolf U, Mayer K, et al. 2008a. The complete nucleotide sequences of the 5 genetically distinct plastid genomes of Oenothera, subsection Oenothera: II. A microevolutionary view using bioinformatics and formal genetic data. Mol. Biol. Evol. 25:2019-30
48. Greiner S, Wang X, Rauwolf U, Silber MV, Mayer K, et al. 2008b. The complete nucleotide sequences of the five genetically distinct plastid genomes of Oenothera, subsection Oenothera: I. Sequence evaluation and plastome evolution. Nucleic Acids Res. 36:2366-78
49. Hanson MR, Bentolila S. 2004. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154-69
50. Harrison RG. 1993. Hybrid Zones and the Evolutionary Process. New York: Oxford Univ. Press
51. He F, Zhang X, Hu JY, Turck F, Dong X, et al. 2012. Genome-wide analysis of cis-regulatory divergence between species in the Arabidopsis genus. Mol. Biol. Evol. 29(11): 3385-95
52. Hofman S, Pabijan M, Dziewulska-Szwajkowska D, Szymura JM. 2012. Mitochondrial genome organization and divergence in hybridizing central European waterfrogs of the Pelophylax esculentus complex (Anura, Ranidae). Gene 491:71-80
53. Johnson NA. 2010. Hybrid incompatibility genes: remnants of a genomic battlefield? Trends Genet. 26:317-25
54. Joyce PBM, Gray MW. 1989. Chloroplast-like transfer RNA genes expressed in wheat mitochondria. Nucleic Acid Res. 17:5461-76
55. King MP, Attardi G. 1989. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246:500-3
56. Kita K, Kurshige Y, Yukawa T, Nishimura S, Handa T. 2005. Plastid inheritance and plastome-genome incompatibility of intergeneric hybrids between Menziesia and Rhododendron. J. Jpn. Soc. Hortic. Sci. 74:318-23
57. Kubo T, Newton KJ. 2008. Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5-14
58. Lane N. 2011. Mitonuclear match: Optimizing fitness and fertility over generations drives ageing within generations. BioEssays 33:860-69
59. Lang BF, Gray MW, Burger G. 1999. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33:351-97
60. Lee HY, Chou JY, Cheong L, Chang NH, Yang SY, Leu JY. 2008. Incompatibility of nuclear and mitochon-drial genomes causes hybrid sterility between two yeast species. Cell 135:1065-73
61. Levin DA. 2003. The cytoplasmic factor in plant speciation. Syst. Bot. 28:5-11
62. Linke B, Borner T. 2005. Mitochondrial effects on flower and pollen development. Mitochondrion 5:389-402
63. Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, et al. 2004. Genome-wide analysis of Arabidopsis penta-tricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089-103
64. Maheshwari S, Barbash DA. 2011. The genetics of hybrid incompatibilities. Annu. Rev. Genet. 45:331-55
65. Maréchal-Drouard L, Weil JH, Guillemaut P. 1988. Import of several tRNAs from the cytoplasm into the mitochondria in bean Phaseolus vulgaris. Nucleic Acids Res. 16:4777-88
66. Matthews DE, Hessler RA, O'Brien TW. 1978. Rapid evolutionary divergence of proteins in mammalian mitochondrial ribosomes. FEBS Lett. 86:76-80
67. Meiklejohn CD, Holmbeck MA, Siddiq MA, Abt DN, Rand DM, Montooth KL. 2013. An incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genet. 9(1):e1003238
68. Metzlaff M, Pohlheim F, Börner T, Hagemann R. 1982. Hybrid variegation in the genus Pelargonium. Curr. Genet. 5:245-49
69. Michishita A, Ureshino K, Miyajima I. 2002. Plastome-genome incompatibility of Rhododendron serpylli-folium (A. Gray) Miq. to evergreen Azalea species belonging to series Kaempferia. J. Jpn. Soc. Hortic. Sci. 71:375-81
70. Millar AH, Heazlewood JL, Kristensen BK, Braun H-P, Møller IM. 2005. The plant mitochondrial proteome. Trends Plant Sci. 10:36-43
71. Moffett AA. 1965. Genetical studies in acacias. Heredity 20:609-20
72. Montooth KL, Meiklejohn CD, Abt DN, Rand DM. 2010. Mitochondrial-nuclear epistasis affects fitness within species but does not contribute to fixed incompatibilities between species of Drosophila. Evolution 64:3364-79
73. Moreno-Loshuertos R, Ferrín G, Acín-Pérez R, Gallardo ME, Viscomi C, et al. 2011. Evolution meets disease: penetrance and functional epistasis of mitochondrial tRNA mutations. PLoS Genet. 7:e1001379
74. Muller HJ. 1942. Isolating mechanisms, evolution, and temperature. Biol. Symp. 6:71-125
75. Nevado B, Fazalova V, Backeljau T, Hanssens M, Verheyen E. 2011. Repeated unidirectional introgression of nuclear and mitochondrial DNA between four congeneric Tanganyikan cichlids. Mol. Biol. Evol. 28:2253-67
76. Oliveira DCSG, Raychoudhury R, Lavrov DV, Werren JH. 2008. Rapidly evolvingmitochondrialgenome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Mol. Biol. Evol. 25:2167-80
77. Osada N, Akashi H. 2012. Mitochondrial-nuclear interactions and accelerated compensatory evolution: Evidence from the primate cytochrome c oxidase complex. Mol. Biol. Evol. 29:337-46
78. Palmer JD, Herbon LA. 1988. Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J. Mol. Evol. 28:87-97
79. Pante E, Rohfritsch A, Becquet V, Belkhir K, Bierne N, Garcia P. 2012. SNP detection from de novo transcriptome sequencing in the bivalve Macoma balthica: marker development for evolutionary studies. PLoS ONE 7:e52302
80. Presgraves DC. 2010. Darwin and the origin of interspecific genetic incompatibilities. Am. Nat. 176(Suppl. 1):S45-60
81. Procházka E, Franko F, Poláková S, Sulo P. 2012. A complete sequence of Saccharomyces paradoxus mitochon-drial genome that restores the respiration in S. cerevisiae. FEMS Yeast Res. 12:819-830
82. Rand DM, Haney RA, Fry AJ. 2004. Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19:645-53
83. Rawson PD, Burton RS. 2002. Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proc. Natl. Acad. Sci. USA 99:12955-58
84. Regneri J, Schartl M. 2012. Expression regulation triggers oncogenicity of xmrk alleles in the Xiphophorus melanoma system. Comp. Biochem. Physiol. C 155(Spec. Issue):71-80
85. Rieseberg LH. 2006. Hybrid speciation in wild sunflowers. Ann. Mo. Bot. Gard. 93(1):34-48
86. Rieseberg LH, Blackman BK. 2010. Speciation genes in plants. Ann. Bot. 106:439-55
87. Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, et al. 2003. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301(5637):1211-16
88. Sackton TB, Haney RA, Rand DM. 2003. Cytonuclear coadaptation in Drosophila: Disruption of cytochrome c oxidase activity in backcross genotypes. Evolution 57:2315-25
89. Sambatti JBM, Ortiz-Barrientos D, Baack EJ, Rieseberg LH. 2008. Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecol. Lett. 11:1082-91
90. Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S. 1999. Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res. 6(5):283-90
91. Scaglia F, Wong LJC. 2008. Human mitochondrial transfer RNAs: role of pathogenic mutation in disease. Muscle Nerve 37:150-71
92. Schmitz-Linneweber C, Kushnir S, Babiychuk E, Poltnigg P, Herrmann RG, Maier RM. 2005. Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase alpha-subunit m RNA. Plant Cell 17:1815-28
93. Schneider A. 2011. Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu. Rev. Biochem. 80:1033-53
94. Schuster W, Brennicke A. 1994. The plant mitochondrial genome: Physical structure, information content, RNA editing, and gene migration to the nucleus. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:61-78
95. Shearer TL, van Oppen MJH, Romanos SL, Wörheide G. 2002. Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol. Ecol. 11:2475-87
96. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, et al. 2003. The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. USA 100:13207-12
97. Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, et al. 2012. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 10:e1001241
98. Smith WK. 1954. Viability of interspecific hybrids in Melilotus. Genetics 39:266-69
99. Stebbins G. 1950. Variation and evolution in plants. In Columbia Biological Series, ed. LC Dunn, HT Clarke, SR Detwiler, T Dobzhansky, F Schrader, pp. 1-643. New York: Columbia Univ. Press
100. Strand AE, Williams LM, Oleksiak MF, Sotka EE. 2012. Can diversifying selection be distinguished from history in geographic clines? A population genomic study of killifish (Fundulus heteroclitus). PLoS ONE 7(9):e45138
101. Stubbe W. 1964. The role of the plastome in evolution of the genus Oenothera. Genetica 35:28-33
102. Stubbe W. 1989. Oenothera-An ideal system for studying the interactions of genome and plastome. Plant Mol. Biol. Rep. 7:245-57
103. Stubbe W, Steiner E. 1999. Inactivation of pollen and other effects of genome-plastome incompatibility in Oenothera. Plant Syst. Evol. 217:259-77
104. Sugiura M. 1989. The chloroplast chromosomes in land plants. Annu. Rev. Cell Biol. 5:51-70
105. Sweigart AL, Fishman L, Willis JH. 2006. A simple genetic incompatibility causes hybrid male sterility in Mimulus. Genetics 172:2465-79
106. Tiffin P, Olson MS, Moyle LC. 2001. Asymmetrical crossing barriers in angiosperms. Proc. R. Soc. Lond. 268:861-67
107. Toews DPL, Brelsford A. 2012. The biogeography of mitochondrial and nuclear discordance in animals. Mol. Ecol. 21(16):3907-30
108. Turelli M, Moyle LC. 2007. Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176:1059-88
109. van der Meer JP. 1974. Hybrid chlorosis in interspecific crosses of Oenothera: Polygenic inheritance of the nuclear component. Can. J. Genet. Cytol. 16:193-201
110. Vickery RK. 1978. Case studies in the evolution of species complexes in Mimulus. Evol. Biol. 11:405-507
111. Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK. 2010. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327:343-48
112. Wise RP, Pring DR. 2002. Nuclear-mediated mitochondrial gene regulation and male fertility in higher plants: light at the end of the tunnel? Proc. Natl. Acad. Sci. USA 99:10240-42
113. Wolfe KH, LiW-H, Sharp PM. 1987. Ratesofnucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 84:9054-58
114. Xu J. 2005. The inheritance of organelle genes and genomes: patterns and mechanisms. Genome 48:951-58
115. Yamagata Y, Yamamoto E, Aya K, Win KT, Doi K, et al. 2010. Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Proc. Natl. Acad. Sci. USA 107:1494-99
116. Yao J-L, Cohen D. 2000. Multiple gene control of plastome-genome incompatibility and plastid DNA inheritance in interspecific hybrids of Zantedeschia. Theor. Appl. Genet. 101:400-6