Hybrids between flowering plant species often exhibit reduced fitness, including sterility and inviability. Such hybrid incompatibilities create barriers to genetic exchange that can promote reproductive isolation between diverging populations and, ultimately, speciation. Additionally, hybrid breakdown opens a window into hidden molecular and evolutionary processes occurring within species. Here, we review recent work on the mechanisms and origins of hybrid incompatibility in flowering plants, including both diverse genic interactions and chromosomal incompatibilities. Conflict and coevolution among and within plant genomes contributes to the evolution of some well-characterized genic incompatibilities, but duplication and drift also play important roles. Inversions, while contributing to speciation by suppressing recombination, rarely cause underdominant sterility. Translocations cause severe F sterility by disrupting meiosis in heterozygotes, making their fixation in outcrossing sister species a paradox. Evolutionary genomic analyses of both genic and chromosomal incompatibilities, in the context of population genetic theory, can explicitly test alternative scenarios for their origins.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Alcázar R, Reth von M, Bautor J, Chae E, Weigel D. 1.  et al. 2014. Analysis of a plant complex resistance gene locus underlying immune-related hybrid incompatibility and its occurrence in nature. PLOS Genet 10:e1004848 [Google Scholar]
  2. Arunkumar R, Josephs EB, Williamson RJ, Wright SI. 2.  2013. Pollen-specific, but not sperm-specific, genes show stronger purifying selection and higher rates of positive selection than sporophytic genes in Capsellagrandiflora. Mol. Biol. Evol 30:2475–86 [Google Scholar]
  3. Baack E, Melo MC, Rieseberg LH. 3.  2015. The origins of reproductive isolation in plants. New Phytol 207:968–84Provides a thorough review of current research on mechanisms of plant speciation. [Google Scholar]
  4. Barnard Kubow KB, McCoy MA, Galloway LF. 4.  2017. Biparental chloroplast inheritance leads to rescue from cytonuclear incompatibility. New Phytol 213:1466–76 [Google Scholar]
  5. Barnard Kubow KB, Sloan DB, Galloway LF. 5.  2014. Correlation between sequence divergence and polymorphism reveals similar evolutionary mechanisms acting across multiple timescales in a rapidly evolving plastid genome. BMC Evol. Biol. 14:268 [Google Scholar]
  6. Barnard Kubow KB, So N, Galloway LF. 6.  2016. Cytonuclear incompatibility contributes to the early stages of speciation. Evolution 70:2752–66 [Google Scholar]
  7. Barr CM, Fishman L. 7.  2010. The nuclear component of a cytonuclear hybrid incompatibility in Mimulus maps to a cluster of pentatricopeptide repeat genes. Genetics 184:455–65 [Google Scholar]
  8. Barr CM, Fishman L. 8.  2011. Cytoplasmic male sterility in Mimulus hybrids has pleiotropic effects on corolla and pistil traits. Heredity 106:886–93 [Google Scholar]
  9. Bateson W.9.  1909. Heredity and Variation in Modern Lights Oxford, UK: Cambridge Univ. Press [Google Scholar]
  10. Bikard D, Patel D, Le Metté C, Giorgi V, Camilleri C. 10.  et al. 2009. Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323:623–26 [Google Scholar]
  11. Blevins T, Wang J, Pflieger D, Pontvianne F, Pikaard CS. 11.  2017. Hybrid incompatibility caused by an epiallele. PNAS 114:3702–7 [Google Scholar]
  12. Bock DG, Andrew RL, Rieseberg LH. 12.  2014. On the adaptive value of cytoplasmic genomes in plants. Mol. Ecol. 23:4899–911 [Google Scholar]
  13. Bogdanova VS, Galieva ER, Yadrikhinskiy AK, Kosterin OE. 13.  2012. Inheritance and genetic mapping of two nuclear genes involved in nuclear-cytoplasmic incompatibility in peas (Pisumsativum L.). Theor. Appl. Genet. 124:1503–12 [Google Scholar]
  14. Bomblies K.14.  2010. Doomed lovers: mechanisms of isolation and incompatibility in plants. Annu. Rev. Plant Biol. 61:109–24 [Google Scholar]
  15. Brandvain Y, Haig D. 15.  2005. Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants. Am. Nat. 166:330–38Discusses the importance of mating systems in shaping the evolution of hybrid incompatibilities. [Google Scholar]
  16. Brink RA, Cooper DC. 16.  1947. The endosperm in seed development (concluded). Bot. Rev. 13:479–541 [Google Scholar]
  17. Buerkle CA, Morris RJ, Asmussen MA, Rieseberg LH. 17.  2000. The likelihood of homoploid hybrid speciation. Heredity 84:441–51 [Google Scholar]
  18. Burkart-Waco D, Ngo K, Lieberman M, Comai L. 18.  2015. Perturbation of parentally biased gene expression during interspecific hybridization. PLOS ONE 10:e0117293 [Google Scholar]
  19. Burke JM, Lai Z, Salmaso M, Nakazato T, Tang S. 19.  et al. 2004. Comparative mapping and rapid karyotypic evolution in the genus Helianthus. Genetics 167:449–57 [Google Scholar]
  20. Burt A, Trivers R. 20.  1998. Selfish DNA and breeding system in flowering plants. Proc. R. Soc. B 265:141–46 [Google Scholar]
  21. Burt A, Trivers R. 21.  2006. Genes in Conflict Cambridge, MA: Belknap Press [Google Scholar]
  22. Burton RS, Pereira RJ, Barreto FS. 22.  2013. Cytonuclear genomic interactions and hybrid breakdown. Annu. Rev. Ecol. Evol. Syst. 44:281–302 [Google Scholar]
  23. Cameron DR, Moav RM. 23.  1957. Inheritance in Nicotianatabacum XXVII. Pollen killer, an alien genetic locus inducing abortion of microspores not carrying it. Genetics 42:326–35 [Google Scholar]
  24. Caruso CM, Case AL, Bailey MF. 24.  2012. The evolutionary ecology of cytonuclear interactions in angiosperms. Trends Plant Sci 17:638–43 [Google Scholar]
  25. Case AL, Finseth FR, Barr CM, Fishman L. 25.  2016. Selfish evolution of cytonuclear hybrid incompatibility in Mimulus. Proc. R. Soc. B 283:20161493Provides direct population genetic evidence of cryptic CMS-Rf coevolution as the cause of cytonuclear hybrid incompatibility. [Google Scholar]
  26. Case AL, Willis JH. 26.  2008. Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically restricted mitochondrial rearrangement. Evolution 62:1026–39 [Google Scholar]
  27. Chae E, Bomblies K, Kim S-T, Karelina D, Zaidem M. 27.  et al. 2014. Species-wide genetic incompatibility analysis identifies immune genes as hot spots of deleterious epistasis. Cell 159:1341–51 [Google Scholar]
  28. Chae E, Tran DTN, Weigel D. 28.  2016. Cooperation and conflict in the plant immune system. PLOS Pathog 12:e1005452 [Google Scholar]
  29. Charlesworth D, Ganders FR. 29.  1979. The population genetics of gynodioecy with cytoplasmic-genic male-sterility. Heredity 43:213–18 [Google Scholar]
  30. Chase CD.30.  2007. Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23:81–90 [Google Scholar]
  31. Chen C, Chen H, Lin Y-S, Shen J-B, Shan J-X. 31.  et al. 2014. A two-locus interaction causes interspecific hybrid weakness in rice. Nat. Comm. 5:1–11 [Google Scholar]
  32. Chen C, E Z, Lin H-X. 32.  2016. Evolution and molecular control of hybrid incompatibility in plants. Front. Plant Sci. 7:e1004848 [Google Scholar]
  33. Chen H, Zhao Z, Liu L, Kong W, Lin Y. 33.  et al. 2017. Genetic analysis of a hybrid sterility gene that causes both pollen and embryo sac sterility in hybrids between Oryzasativa L. and Oryza longistaminata. Heredity 119:166–73 [Google Scholar]
  34. Chen L, Liu Y-G. 34.  2014. Male sterility and fertility restoration in crops. Annu. Rev. Plant Biol. 65:579–606Reviews the molecular mechanisms of numerous well-characterized CMS-Rf systems. [Google Scholar]
  35. Chen Z, Zhao N, Li S, Grover CE, Nie H. 35.  et al. 2017. Plant mitochondrial genome evolution and cytoplasmic male sterility. Crit. Rev. Plant Sci. 36:55–69 [Google Scholar]
  36. Coyne JA, Orr HA. 36.  2004. Speciation Sunderland, MA: Sinauer. , 1st ed.. [Google Scholar]
  37. Dahan J, Mireau H. 37.  2013. The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes. RNA Biol 10:1469–76 [Google Scholar]
  38. Darracq A, Varré JS, Maréchal-Drouard L, Courseaux A, Castric V. 38.  et al. 2011. Structural and content diversity of mitochondrial genome in beet: a comparative genomic analysis. Genome Biol. Evol. 3:723–36 [Google Scholar]
  39. Darwin CR.39.  1859. The Origin of Species London: John Murray [Google Scholar]
  40. Diggle PK, Di Stilio VS, Gschwend AR, Golenberg EM, Moore RC. 40.  et al. 2011. Multiple developmental processes underlie sex differentiation in angiosperms. Trends Genet 27:368–76 [Google Scholar]
  41. Dilkes BP, Comai L. 41.  2004. A differential dosage hypothesis for parental effects in seed development. Plant Cell 16:3174–80 [Google Scholar]
  42. Dobzhansky TG.42.  1937. Genetics and the Origin of Species New York: Columbia Univ. Press [Google Scholar]
  43. Durand S, Bouché N, Perez Strand E, Loudet O, Camilleri C. 43.  2012. Rapid establishment of genetic incompatibility through natural epigenetic variation. Curr. Biol. 22:326–31 [Google Scholar]
  44. Erilova A, Brownfield L, Exner V, Rosa M, Twell D. 44.  et al. 2009. Imprinting of the Polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLOS Genet 5:e1000663 [Google Scholar]
  45. Fishman L, Saunders A. 45.  2008. Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322:1559–62 [Google Scholar]
  46. Fishman L, Stathos A, Beardsley P, Williams CF, Hill JP. 46.  2013. Chromosomal rearrangements and the genetics of reproductive barriers in Mimulus (monkeyflowers). Evolution 67:2547–60 [Google Scholar]
  47. Fishman L, Willis JH. 47.  2006. A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 60:1372–81 [Google Scholar]
  48. Flood PJ, van Heerwaarden J, Becker F, de Snoo CB, Harbinson J, Aarts MGM. 48.  2016. Whole-genome hitchhiking on an organelle mutation. Curr. Biol. 26:1306–11 [Google Scholar]
  49. Florez-Rueda AM, Paris M, Schmidt A, Widmer A, Grossniklaus U, Städler T. 49.  2016. Genomic imprinting in the endosperm is systematically perturbed in abortive hybrid tomato seeds. Mol. Biol. Evol. 33:2935–46 [Google Scholar]
  50. Frank SA.50.  1989. The evolutionary dynamics of cytoplasmic male sterility. Am. Nat. 133:345–76 [Google Scholar]
  51. Fujii S, Bond CS, Small ID. 51.  2011. Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. PNAS 108:1723–28 [Google Scholar]
  52. Gaborieau L, Brown GG, Mireau H. 52.  2016. The propensity of pentatricopeptide repeat genes to evolve into restorers of cytoplasmic male sterility. Front. Plant Sci. 7:e1002910 [Google Scholar]
  53. Gao Z-P, Yu Q-B, Zhao T-T, Ma Q, Chen G-X, Yang Z-N. 53.  2011. A functional component of the transcriptionally active chromosome complex, Arabidopsis PTAC14, interacts with pTAC12/HEMERA and regulates plastid gene expression. Plant Physiol 157:1733–45 [Google Scholar]
  54. Garner AG, Kenney AM, Fishman L, Sweigart AL. 54.  2016. Genetic loci with parent-of-origin effects cause hybrid seed lethality in crosses between Mimulus species. New Phytol 211:319–31 [Google Scholar]
  55. Garraud C, Brachi B, Dufaÿ M, Touzet P, Shykoff JA. 55.  2011. Genetic determination of male sterility in gynodioecious Silenenutans. Heredity 106:757–64 [Google Scholar]
  56. Geddy R, Brown GG. 56.  2007. Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection. BMC Genom 8:130 [Google Scholar]
  57. Gehring M, Bubb KL Henikoff S. 57.  2009. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324:1447–51 [Google Scholar]
  58. Gehring M, Satyaki PR. 58.  2017. Endosperm and imprinting, inextricably linked. Plant Physiol 173:143–54 [Google Scholar]
  59. Gossmann TI, Schmid MW, Grossniklaus U, Schmid KJ. 59.  2013. Selection-driven evolution of sex-biased genes is consistent with sexual selection in Arabidopsis thaliana. Mol. Biol. Evol 31:574–83 [Google Scholar]
  60. Grant V.60.  1971. Plant Speciation New York: Columbia Univ. Press [Google Scholar]
  61. Greiner S, Bock R. 61.  2013. Tuning a ménage à trois: co-evolution and co-adaptation of nuclear and organellar genomes in plants. BioEssays 35:354–65 [Google Scholar]
  62. Greiner S, Rauwolf U, Meurer J, Herrmann RG. 62.  2011. The role of plastids in plant speciation. Mol. Ecol. 20:671–91 [Google Scholar]
  63. Guerrero RF, Muir CD, Josway S, Moyle LC. 63.  2017. Pervasive antagonistic interactions among hybrid incompatibility loci. PLOS Genet 13:e1006817Uses a powerful co-introgression approach to show that male sterility loci interact less-than-additively in tomato hybrids. [Google Scholar]
  64. Guisinger MM, Kuehl JV, Boore JL, Jansen RK. 64.  2008. Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. PNAS 105:18424–29 [Google Scholar]
  65. Gutierrez-Marcos JF, Pennington PD, Costa LM, Dickinson HG. 65.  2003. Imprinting in the endosperm: a possible role in preventing wide hybridization. Philos. Trans. R. Soc. B 358:1105–11 [Google Scholar]
  66. Haig D, Westoby M. 66.  1989. Parent-specific gene expression and the triploid endosperm. Am. Nat. 134:147–55 [Google Scholar]
  67. Haig D, Westboy M. 67.  1991. Genomic imprinting in endosperm: its effect on seed development in crosses between species, and its implications for the evolution of apomixis. Philos. Trans. R. Soc. B 333:1–13 [Google Scholar]
  68. Hanson MR, Bentolila S. 68.  2004. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–69 [Google Scholar]
  69. Hatorangan MR, Laenen B, Steige KA, Slotte T, Köhler C. 69.  2016. Rapid evolution of genomic imprinting in two species of the Brassicaceae. Plant Cell 28:1815–27 [Google Scholar]
  70. Hoffmann AA, Rieseberg LH. 70.  2008. Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation?. Annu. Rev. Ecol. Evol. Syst. 39:21–42Reviews classic and newer models about the diverse roles of inversions in speciation. [Google Scholar]
  71. Honys D, Twell D. 71.  2004. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85 [Google Scholar]
  72. Hopkins R.72.  2013. Reinforcement in plants. New Phytol 197:1095–103 [Google Scholar]
  73. Ishikawa R, Ohnishi T, Kinoshita Y, Eiguchi M, Kurata N, Kinoshita T. 73.  2011. Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. Plant J 65:798–806 [Google Scholar]
  74. Itabashi E, Iwata N, Fujii S, Kazama T, Toriyama K. 74.  2011. The fertility restorer gene, Rf2, for Lead Rice-type cytoplasmic male sterility of rice encodes a mitochondrial glycine-rich protein. Plant J 65:359–67 [Google Scholar]
  75. Jacob F, Vernaldi S, Maekawa T. 75.  2013. Evolution and conservation of plant NLR functions. Front. Immunol. 4:297 [Google Scholar]
  76. Jeuken MJ, Zhang NW, McHale LK, Pelgrom K, Den Boer E. 76.  et al. 2009. Rin4 causes hybrid necrosis and race-specific resistance in an interspecific lettuce hybrid. Plant Cell 21:3368–78 [Google Scholar]
  77. Johnston SA, Nijs den TP, Peloquin SJ, Hanneman RE. 77.  1980. The significance of genic balance to endosperm development in interspecific crosses. Theor. Appl. Genet. 57:5–9 [Google Scholar]
  78. Josefsson C, Dilkes B, Comai L. 78.  2006. Parent-dependent loss of gene silencing during interspecies hybridization. Curr. Biol. 16:1322–28 [Google Scholar]
  79. Jullien PE, Berger F. 79.  2010. Parental genome dosage imbalance deregulates imprinting in Arabidopsis. PLOS Genet 6:e1000885 [Google Scholar]
  80. Karasov TL, Horton MW, Bergelson J. 80.  2014. Genomic variability as a driver of plant-pathogen coevolution?. Curr. Opin. Plant. Biol. 18:24–30 [Google Scholar]
  81. Kerwin R, Sweigart AL. 81.  Mechanisms of transmission ratio distortion at hybrid sterility loci within and between Mimulus species. Genes Genomes Genet 7:3719–30 [Google Scholar]
  82. Kirkbride RC, Yu HH, Nah G, Zhang C, Shi X, Chen ZJ. 82.  2015. An epigenetic role for disrupted paternal gene expression in postzygotic seed abortion in Arabidopsis interspecific hybrids. Mol. Plant 8:1766–75 [Google Scholar]
  83. Kirkpatrick M, Barton NH. 83.  2006. Chromosome inversions, local adaptation and speciation. Genetics 173:419–34 [Google Scholar]
  84. Knox EB.84.  2014. The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms. PNAS 111:11097–102 [Google Scholar]
  85. Köhler C, Wolff P, Spillane C. 85.  2012. Epigenetic mechanisms underlying genomic imprinting in plants. Annu. Rev. Plant Biol. 63:331–52 [Google Scholar]
  86. Kradolfer D, Wolff P, Jiang H, Siretskiy A, Köhler C. 86.  2013. An imprinted gene underlies postzygotic reproductive isolation in Arabidopsis thaliana. Dev. Cell 26:525–35 [Google Scholar]
  87. Kubo T.87.  2013. Genetic mechanisms of postzygotic reproductive isolation: an epistatic network in rice. Breed. Sci. 63:359–66 [Google Scholar]
  88. Kubo T, Takashi T, Ashikari M, Yoshimura A, Kurata N. 88.  2016. Two tightly linked genes at the Hsa1 locus cause both F1 and F2 hybrid sterility in rice. Mol. Plant 9:221–32 [Google Scholar]
  89. Kubo T, Yoshimura A, Kurata N. 89.  2016. Pollen killer gene S35 function requires interaction with an activator that maps close to S24, another pollen killer gene in rice. Genes Genomes Genet 6:1459–68 [Google Scholar]
  90. Kubo T, Yoshimura A, Kurata N, Paterson AH. 90.  2011. Hybrid male sterility in rice is due to epistatic interactions with a pollen killer locus. Genetics 189:1083–92 [Google Scholar]
  91. Lafon Placette C, Johannessen IM, Hornslien KS, Ali MF, Bjerkan KN. 91.  et al. 2017. Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsislyrata and Arabidopsisarenosa in Central Europe. PNAS 114:E1027–35 [Google Scholar]
  92. Lafon Placette C, Köhler C. 92.  2016. Endosperm-based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers. Mol. Ecol. 25:2620–29 [Google Scholar]
  93. Lai Z, Nakazato T, Salmaso M, Burke JM, Tang S. 93.  et al. 2005. Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171:291–303 [Google Scholar]
  94. Lee C-R, Wang B, Mojica JP, Mandáková T, Prasad KVSK. 94.  et al. 2017. Young inversion with multiple linked QTLs under selection in a hybrid zone. Nat. Ecol. Evol. 1:0119 [Google Scholar]
  95. Lee YW, Fishman L, Kelly JK, Willis JH. 95.  2016. A segregating inversion generates fitness variation in yellow monkeyflower (Mimulusguttatus). Genetics 202:1473–84 [Google Scholar]
  96. Leppälä J, Savolainen O. 96.  2011. Nuclear-cytoplasmic interactions reduce male fertility in hybrids of Arabidopsislyrata subspecies. Evolution 65:2959–72 [Google Scholar]
  97. Levin DA.97.  2002. The Role of Chromosomal Change in Plant Evolution New York: Oxford Univ. Press [Google Scholar]
  98. Levin DA.98.  2003. The cytoplasmic factor in plant speciation. Syst. Bot. 28:5–11 [Google Scholar]
  99. Liu F, Cui X, Horner HT, Weiner H, Schnable PS. 99.  2001. Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell 13:1063–78 [Google Scholar]
  100. Loegering WQ, Sears ER. 100.  1963. Distorted inheritance of stem-rust resistance of Timstein wheat caused by a pollen-killing gene. Can. J. Genet. Cytol. 5:65–72 [Google Scholar]
  101. Long Y, Zhao L, Niu B, Su J, Wu H. 101.  et al. 2008. Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. PNAS 105:18871–76 [Google Scholar]
  102. Lowry DB, Willis JH. 102.  2010. A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLOS Biol 8:e1000500 [Google Scholar]
  103. Luo D, Xu H, Liu Z, Guo J, Li H. 103.  et al. 2013. A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat. Genet. 45:573–77 [Google Scholar]
  104. Lynch M, Force AG. 104.  2000. The origin of interspecific genomic incompatibility via gene duplication. Am. Nat. 156:590–605 [Google Scholar]
  105. Martin H, Touzet P, Dufay M, Godé C, Schmitt E. 105.  et al. 2017. Lineages of Silenenutans developed rapid, strong, asymmetric postzygotic reproductive isolation in allopatry. Evolution 71:1519–31 [Google Scholar]
  106. Martin NH, Willis JH. 106.  2007. Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61:68–82 [Google Scholar]
  107. Mizuta Y, Harushima Y, Kurata N, Weigel D. 107.  2010. Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. PNAS 107:20417–22 [Google Scholar]
  108. Mower JP, Case AL, Floro ER, Willis JH. 108.  2012. Evidence against equimolarity of large repeat arrangements and a predominant master circle structure of the mitochondrial genome from a monkeyflower (Mimulusguttatus) lineage with cryptic CMS. Genome Biol. Evol. 4:670–86 [Google Scholar]
  109. Moyle LC, Nakazato T. 109.  2008. Comparative genetics of hybrid incompatibility: sterility in two Solanum species crosses. Genetics 179:1437–53 [Google Scholar]
  110. Muller HJ.110.  1942. Isolating mechanisms, evolution and temperature. Biol. Symp. 6:71–125 [Google Scholar]
  111. Nei M, Maruyama T, Wu CI. 111.  1983. Models of the evolution of reproductive isolation. Genetics 103:557–79 [Google Scholar]
  112. Nguyen GN, Yamagata Y, Shigematsu Y, Watanabe M, Miyazaki Y. 112.  et al. 2017. Duplication and loss of function of genes encoding RNA polymerase III subunit C4 causes hybrid incompatibility in rice. Genes Genomics Genet 7:2565–75 [Google Scholar]
  113. Noor MAF, Grams KL, Bertucci LA, Reiland J. 113.  2001. Chromosomal inversions and the reproductive isolation of species. PNAS 98:12084–88 [Google Scholar]
  114. Oka H.114.  1974. Analysis of genes controlling F1 sterility in rice by the use of isogenic lines. Genetics 77:521–34 [Google Scholar]
  115. Oneal E, Willis JH, Franks RG. 115.  2016. Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulusguttatus and Mimulusnudatus. New Phytol 210:1107–20 [Google Scholar]
  116. Ouyang Y, Li G, Mi J, Xu C, Du H. 116.  et al. 2016. Origination and establishment of a trigenic reproductive isolation system in rice. Mol. Plant 9:1542–45 [Google Scholar]
  117. Ouyang Y, Zhang Q. 117.  2013. Understanding reproductive isolation based on the rice model. Annu. Rev. Plant Biol. 64:111–35 [Google Scholar]
  118. Palmer ME, Feldman MW. 118.  2009. Dynamics of hybrid incompatibility in gene networks in a constant environment. Evolution 63:418–31 [Google Scholar]
  119. Pardo-Manuel de Villena F, Sapienza C. 119.  2001. Female meiosis drives karyotypic evolution in mammals. Genetics 159:1179–89 [Google Scholar]
  120. Pardo-Manuel de Villena F, Sapienza C. 120.  2001. Nonrandom segregation during meiosis: the unfairness of females. Mamm. Genome 12:331–39 [Google Scholar]
  121. Pignatta D, Erdmann RM, Scheer E, Picard CL, Bell GW, Gehring M. 121.  2014. Natural epigenetic polymorphisms lead to intraspecific variation in Arabidopsis gene imprinting. eLife 3:6919–24 [Google Scholar]
  122. Pyhäjärvi T, Hufford MB, Mezmouk S, Ross-Ibarra J. 122.  2013. Complex patterns of local adaptation in teosinte. Genome Biol. Evol. 5:1594–609 [Google Scholar]
  123. Ramsey J, Jr. Bradshaw HD, Schemske DW. 123.  2003. Components of reproductive isolation between the monkeyflowers Mimuluslewisii and M.cardinalis (Phrymaceae). Evolution 57:1520–34 [Google Scholar]
  124. Rand DM, Haney RA, Fry AJ. 124.  2004. Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19:645–53 [Google Scholar]
  125. Rebernig CA, Lafon Placette C, Hatorangan MR, Slotte T, Köhler C. 125.  2015. Non-reciprocal interspecies hybridization barriers in the Capsella genus are established in the endosperm. PLOS Genet 11:e1005295 [Google Scholar]
  126. Rick CM.126.  1966. Abortion of male and female gametes in the tomato determined by allelic interaction. Genetics 53:85–96 [Google Scholar]
  127. Rieseberg LH.127.  2001. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16:351–58 [Google Scholar]
  128. Rieseberg LH, Blackman BK. 128.  2010. Speciation genes in plants. Ann. Bot. 106:439–55 [Google Scholar]
  129. Rockenbach K, Havird JC, Monroe JG, Triant DA, Taylor DR, Sloan DB. 129.  2016. Positive selection in rapidly evolving plastid-nuclear enzyme complexes. Genetics 204:1507–22 [Google Scholar]
  130. Roussell DL, Thompson DL, Pallardy SG, Miles D, Newton KJ. 130.  1991. Chloroplast structure and function is altered in the NCS2 maize mitochondrial mutant. Plant Physiol 96:232–38 [Google Scholar]
  131. Sambatti JBM, Ortiz-Barrientos D, Baack EJ, Rieseberg LH. 131.  2008. Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecol. Lett. 11:1082–91 [Google Scholar]
  132. Sano Y.132.  1990. The genic nature of gamete eliminator in rice. Genetics 125:183–91 [Google Scholar]
  133. Saur Jacobs MS, Wade MJ. 133.  2003. A synthetic review of the theory of gynodioecy. Am. Nat. 161:837–51 [Google Scholar]
  134. Schmitz-Linneweber C, Kushnir S, Babiychuk E, Poltnigg P, Herrmann RG, Maier RM. 134.  2005. Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase α-subunit mRNA. Plant Cell 17:1815–28 [Google Scholar]
  135. Schnable PS, Wise RP. 135.  1994. Recovery of heritable, transposon-induced, mutant alleles of the rf2 nuclear restorer of T-cytoplasm maize. Genetics 136:1171–85 [Google Scholar]
  136. Sekine D, Ohnishi T, Furuumi H, Ono A, Yamada T. 136.  et al. 2013. Dissection of two major components of the post-zygotic hybridization barrier in rice endosperm. Plant J 76:792–99 [Google Scholar]
  137. Sicard A, Kappel C, Josephs EB, Lee YW, Marona C. 137.  et al. 2015. Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella. Nat. Comm 6:7960Demonstrates a novel evolutionary route to hybrid lethality via balancing selection and divergent lineage-sorting into selfing species. [Google Scholar]
  138. Simon M, Durand S, Pluta N, Gobron N, Botran L. 138.  et al. 2016. Genomic conflicts that cause pollen mortality and raise reproductive barriers in Arabidopsis thaliana. Genetics 203:1353–67 [Google Scholar]
  139. Sloan DB.139.  2015. Using plants to elucidate the mechanisms of cytonuclear co-evolution. New Phytol 205:1040–46 [Google Scholar]
  140. Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE. 140.  et al. 2012. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLOS Biol 10:e1001241 [Google Scholar]
  141. Sloan DB, Havird JC, Sharbrough J. 141.  2017. The on-again, off-again relationship between mitochondrial genomes and species boundaries. Mol. Ecol. 26:2212–36 [Google Scholar]
  142. Sloan DB, Müller K, McCauley DE, Taylor DR, Štorchová H. 142.  2012. Intraspecific variation in mitochondrial genome sequence, structure, and gene content in Silenevulgaris, an angiosperm with pervasive cytoplasmic male sterility. New Phytol 196:1228–39 [Google Scholar]
  143. Spencer HG, Clark AG. 143.  2014. Non-conflict theories for the evolution of genomic imprinting. Heredity 113:112–18 [Google Scholar]
  144. Stathos A, Fishman L. 144.  2014. Chromosomal rearrangements directly cause underdominant F1 pollen sterility in MimuluslewisiiMimuluscardinalis hybrids. Evolution 68:3109–19Uses experimental chromosome-doubling to show that translocations, but not inversions, cause hybrid sterility in a classic model system. [Google Scholar]
  145. Stebbins GL.145.  1950. Variation and Evolution in Plants New York: Columbia Univ. Press [Google Scholar]
  146. Stebbins GL.146.  1958. The inviability, weakness, and sterility of interspecific hybrids. Adv. Genet. 9:147–215 [Google Scholar]
  147. Sweigart AL, Fishman L, Willis JH. 147.  2006. A simple genetic incompatibility causes hybrid male sterility in Mimulus. Genetics 172:2465–79 [Google Scholar]
  148. Sweigart AL, Flagel LE. 148.  2015. Evidence of natural selection acting on a polymorphic hybrid incompatibility locus in Mimulus. Genetics 199:543–54 [Google Scholar]
  149. Sweigart AL, Mason AR, Willis JH. 149.  2007. Natural variation for a hybrid incompatibility between two species of Mimulus. Evolution 61:141–51 [Google Scholar]
  150. Sweigart AL, Willis JH. 150.  2012. Molecular evolution and genetics of postzygotic reproductive isolation in plants. F1000 Biol. Rep. 4:23 [Google Scholar]
  151. Thompson WP.151.  1930. Causes of difference in success of reciprocal interspecific crosses. Am. Nat. 64:407–21 [Google Scholar]
  152. Todesco M, Kim S-T, Chae E, Bomblies K, Zaidem M. 152.  et al. 2014. Activation of the Arabidopsis thaliana immune system by combinations of common ACD6 alleles. PLOS Genet 10:e1004459 [Google Scholar]
  153. Turelli M, Moyle LC. 153.  2007. Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176:1059–88 [Google Scholar]
  154. Valentine DH, Woodell SRJ. 154.  1963. Studies in British primulas. X. Seed incompatibility in intraspecific and interspecific crosses at diploid and tetraploid levels. New Phytol 62:125–43 [Google Scholar]
  155. Walsh JB.155.  1982. Rate of accumulation of reproductive isolation by chromosome rearrangements. Am. Nat. 120:510–32 [Google Scholar]
  156. Wang Z, Zou Y, Li X, Zhang Q, Chen L. 156.  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 18:676–87 [Google Scholar]
  157. Wang ZW, Zhang YJ, Xiang CP, Mei SY, Zhou Y. 157.  et al. 2008. A new fertility restorer locus linked closely to the Rfo locus for cytoplasmic male sterility in radish. Theor. Appl. Genet. 117:313–20 [Google Scholar]
  158. Waters AJ, Bilinski P, Eichten SR, Vaughn MW, Ross-Ibarra J. 158.  et al. 2013. Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species. PNAS 110:19639–44 [Google Scholar]
  159. Werth CR, Windham MD. 159.  1991. A model for divergent, allopatric speciation of polyploid pteridophytes resulting from silencing of duplicate gene expression. Am. Nat. 137:515–26 [Google Scholar]
  160. Willis JH.160.  1992. Genetic analysis of inbreeding depression caused by chlorophyll-deficient lethals in Mimulusguttatus. Heredity 69:562–72 [Google Scholar]
  161. Wolf JB, Hager R. 161.  2006. A maternal-offspring coadaptation theory for the evolution of genomic imprinting. PLOS Biol 4:e380–86 [Google Scholar]
  162. Wolff P, Jiang H, Wang G, Santos-González J, Köhler C. 162.  2015. Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana. eLife 4:e1000605 [Google Scholar]
  163. Wright KM, Lloyd D, Lowry DB, Macnair MR, Willis JH. 163.  2013. Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulusguttatus. PLOS Biol 11:e1001497 [Google Scholar]
  164. Wu F, Tanksley SD. 164.  2010. Chromosomal evolution in the plant family Solanaceae. BMC Genom 11:182 [Google Scholar]
  165. Xie Y, Xu P, Huang J, Ma S, Xie X. 165.  et al. 2017. Interspecific hybrid sterility in rice is mediated by OgTPR1 at the S1 locus encoding a peptidase-like protein. Mol. Plant 10:1137–40 [Google Scholar]
  166. Yamagata Y, Yamamoto E, Aya K, Win KT, Doi K. 166.  et al. 2010. Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. PNAS 107:1494–99 [Google Scholar]
  167. Yang J, Zhao X, Cheng K, Du H, Ouyang Y. 167.  et al. 2012. A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337:1336–40 [Google Scholar]
  168. Yu Y, Zhao Z, Shi Y, Tian H, Liu L. 168.  et al. 2016. Hybrid sterility in rice (Oryzasativa L.) involves the tetratricopeptide repeat domain containing protein. Genetics 203:1439–51 [Google Scholar]
  169. Zhang J, Ruhlman TA, Sabir J, Blazier JC, Jansen RK. 169.  2015. Coordinated rates of evolution between interacting plastid and nuclear genes in Geraniaceae. Plant Cell 27:563–73 [Google Scholar]
  170. Zuellig MP, Sweigart AL. 170.  2018. Gene duplicates cause hybrid lethality between species of sympatric Mimulus. PLOS Genet In press Identifies, for the first time, the genes underlying hybrid lethality in naturally hybridizing plant species. [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error