Evidence of natural selection acting on a polymorphic hybrid incompatibility locus in mimulus

Genetics

Volumn 199, Issue 2, 2014, Pages 543-554

  Sweigart, Andrea L ^a   Flagel, Lex E ^b,c,d  

^a University of Georgia   (United States)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d MONSANTO COMPANY   (United States)

Author keywords

Hybrid incompatibilities; Mimulus; Monkeyflower; Postzygotic reproductive isolation; Speciation

Indexed keywords

ARTICLE; FLOWER; GENE; GENE FREQUENCY; GENE MAPPING; GENETIC CROSS; GENETIC INCOMPATIBILITY; HMS1 GENE; HMS2 GENE; HYBRID; MIMULUS; MIMULUS GUTTATUS; MIMULUS NASUTUS; NATURAL POPULATION; NATURAL SELECTION; NONHUMAN; PLANT GENOME; POLYMORPHIC LOCUS; PRIORITY JOURNAL; SPECIES DIFFERENTIATION; ALLELE; CHROMOSOMAL MAPPING; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETIC SELECTION; GENETICS; GENOMICS; HETEROZYGOTE; HYBRIDIZATION; PLANT GENE; POPULATION GENETICS; QUANTITATIVE TRAIT LOCUS;

MIMULUS (ANGIOSPERM); MIMULUS GUTTATUS; MIMULUS NASUTUS;

ALLELES; CHROMOSOME MAPPING; GENE FREQUENCY; GENES, PLANT; GENETICS, POPULATION; GENOME, PLANT; GENOMICS; HETEROZYGOTE; HYBRIDIZATION, GENETIC; MIMULUS; POLYMORPHISM, GENETIC; QUANTITATIVE TRAIT LOCI; RECOMBINATION, GENETIC; SELECTION, GENETIC;

EID: 84930085285     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.171819     Document Type: Article

References (77)

1. Alcázar, R., A. V. García, J. E. Parker, and M. Reymond, 2009 Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proc. Natl. Acad. Sci. USA 106: 334–339.
2. Bai, C., P. Sen, K. Hofmann, L. Ma, M. Goebl et al., 1996 SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86: 263–274.
3. Barbash, D. A., P. Awadalla, and A. M. Tarone, 2006 Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus. PLoS Biol. 2: e142.
4. Barkan, A., and I. Small, 2014 Pentatricopeptide repeat proteins in plants. Annu. Rev. Plant Biol. 65: 415–442.
5. 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: 455–465.
6. Bikard, D., D. Patel, C. L. Metté, V. Giorgi, C. Camilleri et al., 2009 Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323: 623–626.
7. Bomblies, K., and D. Weigel, 2007 Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8: 382–393.
8. Bomblies, K., J. Lempe, P. Epple, N. Warthmann, C. Lanz et al., 2007 Autoimmune response as a mechanism for a DobzhanskyMuller-type incompatibility syndrome in plants. PLoS Biol. 5: e236.
9. Brandvain, Y., A. M. Kenney, L. Flagel, G. Coop, and A. L. Sweigart, 2014 Speciation and introgression between Mimulus nasutus and Mimulus guttatus. PLoS Genet. 10: e1004410.
10. Brideau, N. J., H. A. Flores, J. Wang, S. Maheshwari, X. Wang et al., 2006 Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314: 1292–1295.
11. Broman, K. W., H. Wu, Ś. Sen, and G. A. Churchill, 2003 R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889– 890.
12. Canales, C., A. M. Bhatt, R. Scott, and H. Dickinson, 2002 EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr. Biol. 12: 1718–1727.
13. 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.
14. Charlesworth, D., and S. I. Wright, 2001 Breeding systems and genome evolution. Curr. Opin. Genet. Dev. 11: 685–690.
15. Chen, C., H. Chen, Y. S. Lin, J. B. Shen, J. X. Shan et al., 2014 A two-locus interaction causes interspecific hybrid weakness in rice. Nat. Commun. 5: 3357.
16. Cheung, W. Y., N. Hubert, and B. S. Landry, 1993 A simple and rapid DNA microextraction method for plant, animal, and insect suitable for RAPD and other PCR analyses. Genome Res. 3: 69–70.
17. Choi, Y., G. E. Sims, S. Murphy, J. R. Miller, and A. P. Chan, 2012 Predicting the functional effect of amino acid substitutions and indels. PLoS ONE 7: e46688.
18. Christie, P., and M. R. MacNair, 1987 The distribution of postmating reproductive isolating genes in populations of the yellow monkey flower, Mimulus guttatus. Evolution 41: 571–578.
19. Cutter, A. D., 2012 The polymorphic prelude to Bateson-Dobzhansky Muller incompatibilities. Trends Ecol.Evol. 27: 209–218.
20. J Darwin, C., 1859 On the Origin of Species by Means of Natural Selection. J. Murray, London.
21. DePristo, M. A., E. Banks, R. Poplin, K. V. Garimella, J. R. Maguire et al., 2011 A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 5: 491–498.
22. Devoto, A., M. Nieto-Rostro, D. Xie, C. Ellis, R. Harmston et al., 2002 COI1 links jasmonate signaling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J. 32: 457–466.
23. Dewitte, W., and J. A. Murray, 2003 The plant cell cycle. Annu. Rev. Plant Biol. 54: 235–264.
24. Diaz, A., and M. R. MacNair, 1999 Pollen tube competition as a mechanism of prezygotic reproductive isolation between Mimulus nasutus and its presumed progenitor M. guttatus. New Phytol. 144: 471–478.
25. Diévart, A., and S. E. Clark, 2004 LRR-containing receptors regulating plant development and defense. Development 131: 251– 261.
26. Dobzhansky, T. H., 1937 Genetics and the Origin of Species, Columbia University Press, New York.
27. Drakakaki, G., W. van de Ven, S. Pan, Y. Miao, J. Wang et al., 2012 Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res. 22: 413–424.
28. Fishman, L., and A. Saunders, 2008 Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322: 1559–1562.
29. Fishman, L., A. L. Sweigart, A. M. Kenney, and S. Campbell, 2014 Major quantitative trait loci control divergence in critical photoperiod for flowering between selfing and outcrossing species of monkeyflower (Mimulus). New Phytol. 201: 1498–1507.
30. Flagel, L. E., J. H. Willis, and T. J. Vision, 2014 The standing pool of genomic structural variation in a natural population of Mimulus guttatus. Genome Biol.Evol. 6: 53–64.
31. Frank, S. A., 1990 Divergence of meiotic drive-suppression systems as an explanation for sex-biased hybrid sterility and inviability. Evolution 45: 262–267.
32. Gusti, A., N. Baumberger, M. Nowack, S. Pusch, H. Eisler et al., 2009 The Arabidopsis thaliana F-box protein FBL17 is essential for progression through the second mitosis during pollen development. PLoS ONE 4: e4780.
33. Hellmann, H., and M. Estelle, 2002 Plant development: regulation by protein degradation. Science 297: 793–797.
34. Hurst, L. D., and A. Pomiankowski, 1991 Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane’s rule and related phenomena. Genetics 128: 841–858.
35. Iwakawa, H., A. Shinmyo, and M. Sekine, 2006 Arabidopsis CDKA; 1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J. 45: 819–831.
36. Jeuken, M. J. W., N. W. Zhang, L. K. McHale, K. Pelgrom, E. Den Boer et al., 2009 Rin4 causes hybrid necrosis and race-specific resistance in an interspecific lettuce hybrid. Plant Cell 21: 3368– 3378.
37. Kim, H. J., S. A. Oh, L. Brownfield, S. H. Hong, H. Ryu et al., 2008 Control of plant germline proliferation by SCFFBL17 degradation of cell cycle inhibitors. Nature 455: 1134–1137.
38. Kim, O. K., J. H. Jung, and C. M. Park, 2010 An Arabidopsis F-box protein regulates tapetum degeneration and pollen maturation during anther development. Planta 232: 353–366.
39. Kong, H., L. L. Landherr, M. W. Frohlich, J. Leebens-Mack, H. Ma et al., 2007 Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J. 50: 873–885.
40. Krüger, J., C. M. Thomas, C. Golstein, M. S. Dixon, M. Smoker et al., 2002 A tomato cysteine protease required for cf-2-dependent disease resistance and suppression of autonecrosis. Science 296: 744–747.
41. Li, H., and R. Durbin, 2010 Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589–595.
42. Liu, J., and L. J. Qu, 2008 Meiotic and mitotic cell cycle mutants involved in gametophyte development in Arabidopsis. Mol. Plant 1: 564–574.
43. 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.
44. Lynch, M., and A. Force, 2000 The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459–473.
45. Maheshwari, S., J. Wang, and D. A. Barbash, 2008 Recurrent positive selection of the Drosophila hybrid incompatibility gene Hmr. Mol. Biol. Evol. 25: 2421–2430.
46. Maheshwari, S., and D. Barbash, 2011 The genetics of hybrid incompatibilities. Annu. Rev. Genet. 45: 331–355.
47. 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.
48. 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.
49. Menges, M., S. M. De Jager, W. Gruissem, and J. A. Murray, 2005 Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J. 41: 546–566.
50. 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.
51. Muller, H. J., 1942 Isolating mechanisms, evolution, and temperature. Biol. Symp. 6: 71–125.
52. Nordborg, M., 2000 Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154: 923–929.
53. Nowack, M. K., P. E. Grini, M. J. Jakoby, M. Lafos, C. Koncz et al., 2005 A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat. Genet. 38: 63–67.
54. Oliver, P. L., L. Goodstadt, J. J. Bayes, Z. Birtle, K. C. Roach et al., 2009 Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet. 5: e1000753.
55. Phadnis, N., and H. A. Orr, 2009 A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323: 376–379.
56. Presgraves, D. C., 2010 The molecular evolutionary basis of species formation. Nat. Rev. Genet. 11: 175–180.
57. Presgraves, D. C., L. Balagopalan, S. M. Abmayr, and H. A. Orr, 2003 Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423: 715–719.
58. Saha, D., A. M. Prasad, and R. Srinivasan, 2007 Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol. Biochem. 45: 521–534.
59. Sweigart, A. L., and J. H. Willis, 2003 Patterns of nucleotide diversity in two species of Mimulus are affected by mating system and asymmetric introgression. Evolution 57: 2490–2506.
60. Sweigart, A. L., and J. H. Willis, 2012 Molecular evolution and genetics of postzygotic reproductive isolation in plants. F1000 Biol. Rep. 4: 23.
61. Sweigart, A. L., L. Fishman, and J. H. Willis, 2006 A simple genetic incompatibility causes hybrid male sterility in Mimulus. Genetics 172: 2465–2479.
62. Sweigart, A. L., A. R. Mason, and J. H. Willis, 2007 Natural variation for a hybrid incompatibility between two species of Mimulus. Evolution 61: 141–151.
63. Tang, S., and D. C. Presgraves, 2009 Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science 323: 779–782.
64. Tao, Y., D. L. Hartl, and C. C. Laurie, 2001 Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc. Natl. Acad. Sci. USA 98: 13183–13188.
65. Ting, C. T., S. C. Tsaur, M. L. Wu, and C. I. Wu, 1998 A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282: 1501–1504.
66. Van Ooijen, J. W., 2006 JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma B. V., Wageningen, The Netherlands.
67. Vickery, Jr., R. K., 1964 Barriers to gene exchange between members of the Mimulus guttatus complex Scrophulariaceae. Evolution 18: 52–69.
68. Vickery, Jr., R. K., 1978 Case studies in the evolution of species complexes in Mimulus. Evol. Biol. 11: 405–507.
69. Voight, B. F., S. Kudaravalli, X. Wen, and J. K. Pritchard, 2006 A map of recent positive selection in the human genome. PLoS Biol. 4: e72.
70. Wright, K. M., D. Lloyd, D. B. Lowry, M. R. MacNair, and J. H. Willis, 2013 Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus. PLoS Biol. 11: 1001497.
71. Xie, D. X., B. F. Feys, S. James, M. Nieto-Rostro, and J. G. Turner, 1998 COI1: an Arabidopsis gene required for jasmonateregulated defense and fertility. Science 280: 1091–1094.
72. Yamagata, Y., E. Yamamoto, K. Aya, K. T. Win, and K. Doi et al. 2010 Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Proc. Natl. Acad. Sci. USA 107: 1494–1499.
73. Yamamoto, E., T. Takashi, Y. Morinaka, S. Lin, J. Wu et al., 2010 Gain of deleterious function causes an autoimmune response and Bateson-Dobzhansky-Muller incompatibility in rice. Mol. Genet. Genomics 283: 305–315.
74. Yang, M., Y. Hu, M. Lodhi, W. R. McCombie, and H. Ma, 1999 The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proc. Natl. Acad. Sci. USA 96: 11416–11421.
75. Yang, J., X. Zhao, K. Cheng, H. Du, Y. Ouyang et al., 2012 A killerprotector system regulates both hybrid sterility and segregation distortion in rice. Science 337: 1336–1340.
76. Zhao, D. Z., G. F. Wang, B. Speal, and H. Ma, 2002 The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16: 2021– 2031.
77. Zhao, Z. G., S. S. Zhu, Y. H. Zhang, X. F. Bian, Y. Wang et al., 2010 Molecular analysis of an additional case of hybrid sterility in rice (Oryza sativa L.). Planta 233: 485–494.