Cytoplasmic male sterility contributes to hybrid incompatibility between subspecies of arabidopsis lyrata

G3: Genes, Genomes, Genetics

Volumn 3, Issue 9, 2013, Pages 1727-1740

  Aalto, Esa A ^a   Koelewijn, Hans Peter ^b   Savolainen, Outi ^a  

^a UNIVERSITY OF OULU   (Finland)

^b Nunhems Netherlands   (Netherlands)

Author keywords

Arabidopsis; Cytoplasmic male sterility; Hybrid incompatibility; QTL mapping; Speciation

Indexed keywords

BINDING PROTEIN; MOLECULAR MARKER; PENTATRICOPEPTIDE REPEAT PROTEIN; UNCLASSIFIED DRUG;

ARABIDOPSIS LYRATA; ARTICLE; CHROMOSOME 2; CONTROLLED STUDY; CYTOPLASM; CYTOPLASMIC MALE STERILITY; GENE CLUSTER; GENE EXPRESSION; GENETIC VARIABILITY; GENOTYPE; HERMAPHRODITE; HYBRID; NONHUMAN; PLANT GENETICS; POLLEN; PROGENY; QUANTITATIVE TRAIT LOCUS MAPPING; SEED PRODUCTION; SELF-INCOMPATIBILITY (PLANT); SPECIES DIFFERENTIATION; SPECIES DIVERSITY; SUBSPECIES; GENETIC INCOMPATIBILITY; NUCLEOTIDE REPEAT; OUTCROSSING; PHENOTYPE; PLANT GENOME;

ARABIDOPSIS; ARABIDOPSIS LYRATA;

ARABIDOPSIS; CYTOPLASMIC MALE STERILITY; HYBRID INCOMPATIBILITY; QTL MAPPING; SPECIATION;

ARABIDOPSIS; CYTOPLASM; GENES, PLANT; GENETIC SPECIATION; INBREEDING; PLANT INFERTILITY; POLLEN; QUANTITATIVE TRAIT LOCI; SELF-INCOMPATIBILITY IN FLOWERING PLANTS;

EID: 84885756814     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.007815     Document Type: Article

References (79)

1. Balañá-Alcaide, D., S. E. Ramos-Onsins, Q. Boone, and M. Aguadé, 2006 Highly structured nucleotide variation within and among arabidopsis lyrata populations at the FAH1 and DFR gene regions. Mol. Ecol. 15: 2059-2068.
2. Barr, C. M., and L. Fishman, 2010 The nuclear component of a cytonuclear hybrid incompatibility in mimulus maps to a cluster of pentatricopeptide repeat genes. Genetics 184: 455-466.
3. Bateson, W., 1909 Heredity and variation in modern lights, pp. 85-101 in Darwin and Modern Science, edited by A. C. Seward Cambridge University Press, Cambridge.
4. Belhassen, E., B. Dommee, A. Atlan, P. Goyon, D. Pomente et al., 1991 Complex determination of male-sterility in thymus-vulgaris L - genetic and molecular analysis. Theor. Appl. Genet. 82: 137-143.
5. Bentolila, S., A. Alfonso, and M. Hanson, 2002 A pentatricopeptide repeatcontaining gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl. Acad. Sci. USA 99: 10887-10892.
6. Bomblies, K., and D. Weigel, 2007 Hybrid necrosis: Autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8: 382-393.
7. Bomblies, K., and D. Weigel, 2010 Arabidopsis and relatives as models for the study of genetic and genomic incompatibilities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365: 1815-1823.
8. Broman, K., H. Wu, S. Sen, and G. Churchill, 2003 R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889-890.
9. Case, A. L., and J. H. Willis, 2008 Hybrid male sterility in mimulus (phrymaceae) is associated with a geographically restricted mitochondrial rearrangement. Evolution 62: 1026-1039.
10. Charlesworth, B., and D. Charlesworth, 1978 Model for evolution of dioecy and gynodioecy rid F-3071-2011. Am. Nat. 112: 975-997.
11. Charlesworth, D., 1981 A further study of the problem of the maintenance of females in gynodioecious species. Heredity 46: 27-39.
12. Charlesworth, D., and F. Ganders, 1979 Population-genetics of gynodioecy with cytoplasmic-genic male-sterility rid F-3071-2011. Heredity 43: 213- 218.
13. Charlesworth, D., and V. Laporte, 1998 The male-sterility polymorphism of silene vulgaris: Analysis of genetic data from two populations and comparison with thymus vulgaris. Genetics 150: 1267-1282.
14. Chase, C. D., 2007 Cytoplasmic male sterility: A window to the world of plant mitochondrial-nuclear interactions. Trends Genet. 23: 81-90.
15. Cosmides, L., and J. Tooby, 1981 Cytoplasmic inheritance and intragenomic conflict. J. Theor. Biol. 89: 83-129.
16. Darwin, C., 1859 the Origin of Species by Means of Natural Selection.
17. DeHaan, A., and R. Luyten, T. Bakx-Schotman and J. VanDamme, 1997 The dynamics of gynodioecy in plantago lanceolata L. 1. frequencies of male-steriles and their cytoplasmic male sterility types. Heredity 79: 453-462.
18. Ding, J., Q. Lu, Y. Ouyang, H. Mao, P. Zhang et al., 2012 A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc. Natl. Acad. Sci. USA 109: 2654-2659.
19. Dobzhansky, T. H., 1936 Studies on hybrid sterility. 11. localization of sterility factors in drosophila pseudoobscura hybrids. Genetics 21: 113- 135.
20. Dufay, M., and E. Billard, 2012 How much better are females? the occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species. Ann. Bot. (Lond.) 109: 505-519.
21. Dufay, M., P. Touzet, S. Maurice, and J. Cuguen, 2007 Modelling the maintenance of male-fertile cytoplasm in a gynodioecious population. Heredity 99: 349-356.
22. Dufay, M., V. Vaudey, I. De Cauwer, P. Touzet, J. Cuguen et al., 2008 Variation in pollen production and pollen viability in natural populations of gynodioecious beta vulgaris ssp maritima: Evidence for a cost of restoration of male function? J. Evol. Biol. 21: 202-212.
23. Fishman, L., and J. H. Willis, 2001 Evidence for dobzhansky-muller incompatibilities contributing to the sterility of hybrids between mimulus guttatus and M. nasutus. Evolution 55: 1932-1942.
24. Fishman, L. A., and J. Willis, 2006 A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 60: 1372-1381.
25. Fishman, L., A. Kelly, E. Morgan, and J. Willis, 2001 A genetic map in the mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159: 1701- 1716.
26. Foxe, J. P., and S. I. Wright, 2009 Signature of diversifying selection on members of the pentatricopeptide repeat protein family in arabidopsis lyrata. Genetics 183: 663-672.
27. Frank, S., 1989 The evolutionary dynamics of cytoplasmic male-sterility. Am. Nat. 133: 345-376.
28. Fujii, S., C. S. Bond, and I. D. Small, 2011 Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc. Natl. Acad. Sci. USA 108: 1723- 1728.
29. Garraud, C., B. Brachi, M. Dufay, P. Touzet, and J. A. Shykoff, 2011 Genetic determination of male sterility in gynodioecious silene nutans. Heredity 106: 757-764.
30. Green, P., K. Falls, and S. Crook, 1990 Documentation for CRIMAP, Version 2.4, Washington University School of Medicine, St Louis.
31. Goyon, P., F. Vichot, and J. VanDamme, 1991 Nuclear-Cytoplasmic Male-Sterility - Single-Point Equilibria Versus Limit-Cycles. American Naturalist 137: 498-514.
32. Hall, M., and J. Willis, 2005 Transmission ratio distortion in intraspecific hybrids of mimulus guttatus: Implications for genomic divergence. Genetics 170: 375-386.
33. Hanson, M., and S. Bentolila, 2004 Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16: S154-S169.
34. Harushima, Y., M. Nakagahra, M. Yano, T. Sasaki, and N. Kurata, 2001 A genome-wide survey of reproductive barriers in an intraspecific hybrid. Genetics 159: 883-892.
35. Hu, T. T., P. Pattyn, E. G. Bakker, J. Cao, J. Cheng et al., 2011 The arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43: 476-483.
36. Kearns, C. A., and D. W. Inouye, 1993 Techniques for Pollination Biologists. University of Colorado Press, Niwot, CO.
37. Kheyr-Pour, A., 1981 Wide nucleo-cytoplasmic polymorphism for male sterility in origanum vulgare L. J. Hered. 72: 45-51.
38. Koelewijn, H., 2003 Variation in restorer genes and primary sexual investment in gynodioecious plantago coronopus: The trade-off between male and female function. Proc. Biol. Sci. 270: 1939-1945.
39. Koelewijn, H., and J. van Damme, 1995a Genetics of male-sterility in gynodioecious plantago-coronopus. 1. cytoplasmic variation. Genetics 139: 1749-1758.
40. Koelewijn, H., and J. van Damme, 1995b Genetics of male-sterility in gynodioecious plantago-coronopus. 2. nuclear genetic-variation. Genetics 139: 1759-1775.
41. Kuittinen, H., A. Da Haan, C. Vogl, S. Oikarinen, J. Leppala, M. Koch, T. Mitchell-Olds, C. Langley, and O. Savolainen, 2004 Comparing the linkage maps of the close relatives Arabidopsis lyrata and A-thaliana RID A-4924-2011. Genetics 168: 1575-1584.
42. Leinonen, P. H., D. L. Remington, and O. Savolainen, 2011 Local adaptation, phenotypic differentiation, and hybrid fitness in diverged natural populations of arabidopsis lyrata. Evolution 65: 90-107.
43. Leppälä, J., and O. Savolainen, 2011 Nuclear-cytoplasmic interactions reduce male fertility in hybrids of arabidopsis lyrata subspecies. Evolution 65: 2959-2972.
44. Leppälä, J., F. Bokma, and O. Savolainen, 2013 Investigating incipient speciation in Arabidopsis lyrata from patterns of transmission ratio distortion. Genetics 194:697-708.
45. Lexer, C., and A. Widmer, 2008 The genic view of plant speciation: Recent progress and emerging questions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363: 3023-3036.
46. Li, S., D. Yang, and Y. Zhu, 2007 Characterization and use of male sterility in hybrid rice breeding. J. Integr. Plant Biol. 49: 791-804.
47. Long, Y., L. Zhao, B. Niu, J. Su, H. Wu et al., 2008 Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc. Natl. Acad. Sci. USA 105: 18871-18876.
48. Lowry, D. B., J. L. Modliszewski, K. M. Wright, C. A. Wu, and J. H. Willis, 2008 The strength and genetic basis of reproductive isolating barriers in flowering plants. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363: 3009-3021.
49. Martin, N. H., and J. H. Willis, 2007 Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric mimulus species. Evolution 61: 68-82.
50. Martin, N. H., and J. H. Willis, 2010 Geographical variation in postzygotic isolation and its genetic basis within and between two mimulus species. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365: 2469-2478.
51. McCauley, D. E., and M. F. Bailey, 2009 Recent advances in the study of gynodioecy: The interface of theory and empiricism. Ann. Bot. (Lond.) 104: 611-620.
52. Mizuta, Y., Y. Harushima, and N. Kurata, 2010 Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc. Natl. Acad. Sci. USA 107: 20417-20422.
53. Moyle, L. C., and E. B. Graham, 2005 Genetics of hybrid incompatibility between lycopersicon esculentum and L. hirsutum. Genetics 169: 355- 373.
54. Muller, H. J., 1939 Reversibility in evolution considered from the standpoint of genetics. Biol. Rev. Camb. Philos. Soc. 14: 261-280.
55. Muller, M., J. Leppaelae, and O. Savolainen, 2008 Genome-wide effects of postglacial colonization in arabidopsis lyrata. Heredity 100: 47-58.
56. O'Kane, S., and I. Al-Shehbaz, 1997 A synopsis of arabidopsis (brassicaceae). Novon 7: 323-327.
57. Ossowski, S., K. Schneeberger, J. I. Lucas-Lledo, N. Warthmann, R. M. Clark et al., 2010 The rate and molecular spectrum of spontaneous mutations in arabidopsis thaliana. Science 327: 92-94.
58. Pannell, C., and B. Charlesworth, 2000 Effects of metapopulation processes on measures of genetic diversity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355: 1851-1864.
59. Phadnis, N., 2011 Genetic architecture of male sterility and segregation distortion in Drosophila pseudoobscura Bogota-USA Hybrids. Genetics 189: 1001-1009.
60. Phadnis, N., and H. A. Orr, 2009 A single gene causes both male sterility and segregation distortion in drosophila hybrids. Science 323: 376-379.
61. Presgraves, D. C., 2008 Sex chromosomes and speciation in drosophila. Trends Genet. 24: 336-343.
62. Pyhäjärvi, T., E. Aalto, and O. Savolainen, 2012 Time scales of divergence and speciation among natural populations and subspecies of arabidopsis lyrata (brassicaceae). Am. J. Bot. 99: 1314-1322.
63. R Development Core Team, 2010 R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria
64. Rieseberg, L. H., and J. H. Willis, 2007 Plant speciation. Science 317: 910- 914.
65. Rieseberg, L. H., and B. K. Blackman, 2010 Speciation genes in plants. Ann. Bot. (Lond.) 106: 439-455.
66. Ross-Ibarra, J., S. I. Wright, J. P. Foxe, A. Kawabe, L. DeRose-Wilson et al., 2008 Patterns of polymorphism and demographic history in natural populations of arabidopsis lyrata. PLoS ONE 3: e2411.
67. Roux, C., V. Castric, M. Pauwels, S. I. Wright, P. Saumitou-Laprade et al., 2011 Does speciation between arabidopsis halleri and arabidopsis lyrata coincide with major changes in a molecular target of adaptation? PLoS ONE 6: e26872.
68. Savolainen, O., and H. Kuittinen, 2011 Arabidopsis lyrata genetics, pp. 347-372 in Genetics and genomics of the Brassicaceae, edited by R. Schmidt and I. Bancroft. Plant Genetics and genomics: Crops and Models 9. Springer-Verlag, Berlin.
69. Shykoff, J., S. Kolokotronis, C. Collin, and M. Lopez-Villavicencio, 2003 Effects of male sterility on reproductive traits in gynodioecious plants: A meta-analysis. Oecologia 135: 1-9.
70. Sweigart, A., L. Fishman, and J. Willis, 2006 A simple genetic incompatibility causes hybrid male sterility in mimulus. Genetics 172: 2465-2479.
71. Tiffin, P., M. Olson, and L. Moyle, 2001 Asymmetrical crossing barriers in angiosperms. Proc. R. Soc. Lond. B Biol. Sci. 268: 861-867.
72. Turelli, M., and L. C. Moyle, 2007 Asymmetric postmating isolation: Darwin's corollary to haldane's rule. Genetics 176: 1059-1088.
73. van Damme, J., and W. van Delden, 1982 Gynodioecy in plantagolanceolata L. 1. polymorphism for plasmon type. Heredity 49: 303-318.
74. van Damme, J., M. Hundscheid, S. Ivanovic, and H. Koelewijn, 2004 Multiple CMS - restorer gene polymorphism in gynodioecious plantago coronopus. Heredity 93: 175-181.
75. Wang, Z., Y. Zou, X. Li, Q. Zhang, L. Chen et al., 2006 Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18: 676-687.
76. Widmer, A., C. Lexer, and S. Cozzolino, 2009 Evolution of reproductive isolation in plants. Heredity 102: 31-38.
77. Wise, M., j. V. Vu, and D. E. Carr, 2011 Potential ecological constraints on the evolution of gynodioecy in Mimulus guttatus: relative fecundity and pollinator behavior in a mixed-sex population. Int. J. Plant Sci. 172: 199- 210.
78. Yamagata, Y., E. Yamamoto, K. Aya, K. T. Win, K. Doi et al., 2010 Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Proc. Natl. Acad. Sci. USA 107: 1494-1499.
79. Yamamoto, M. P., H. Shinada, Y. Onodera, C. Komaki, T. Mikami et al., 2008 A male sterility-associated mitochondrial protein in wild beets causes pollen disruption in transgenic plants. Plant J. 54: 1027-1036.