Review Article

Non-self- and self-recognition models in plant self-incompatibility

  • Nature Plants 2, Article number: 16130 (2016)
  • doi:10.1038/nplants.2016.130
  • Download Citation
Received:
Accepted:
Published online:

Abstract

The mechanisms by which flowering plants choose their mating partners have interested researchers for a long time. Recent findings on the molecular mechanisms of non-self-recognition in some plant species have provided new insights into self-incompatibility (SI), the trait used by a wide range of plant species to avoid self-fertilization and promote outcrossing. In this Review, we compare the known SI systems, which can be largely classified into non-self- or self-recognition systems with respect to their molecular mechanisms, their evolutionary histories and their modes of evolution. We review previous controversies on haplotype evolution in the gametophytic SI system of Solanaceae species in light of a recently elucidated non-self-recognition model. In non-self-recognition SI systems, the transition from self-compatibility (SC) to SI may be more common than previously thought. Reversible transition between SI and SC in plants may have contributed to their adaptation to diverse and fluctuating environments.

  • Subscribe to Nature Plants for full access:

    $62

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    , & Loss of self-incompatibility and its evolutionary consequences. Int. J. Plant Sci. 169, 93–104 (2008).

  2. 2.

    & Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am. J. Bot. 88, 1143–1150 (2001).

  3. 3.

    The evolution of plant reproductive systems: how often are transitions irreversible?. Proc. R. Soc. 280, 20130913 (2013).

  4. 4.

    , & Evolutionary consequences of self-fertilization in plants. Proc. Biol. Sci. 280, 20130133 (2013).

  5. 5.

    & Self-incompatibility in plants. Annu. Rev. Plant Biol. 56, 467–489 (2005).

  6. 6.

    & Self/non-self discrimination in angiosperm self-incompatibility. Curr. Opin. Plant Biol. 15, 78–83 (2012).

  7. 7.

    , , , & Pollenpistil interactions and self-incompatibility in the Asteraceae: new insights from studies of Senecio squalidus (Oxford ragwort). Ann. Bot. 108, 687–698 (2011).

  8. 8.

    et al. Expression of stigma- and anther-specific genes located in the S locus region of Ipomoea trifida. Sex. Plant Reprod. 20, 73–85 (2007).

  9. 9.

    et al. Molecular and genetic characterization of the S locus in Hordeum bulbosum L., a wild self-incompatible species related to cultivated barley. Mol. Genet. Genomics 280, 509–519 (2008).

  10. 10.

    et al. The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl Acad. Sci. USA. 97, 1920–1925 (2000).

  11. 11.

    , & The male determinant of self-incompatibility in Brassica. Science 286, 1697–1700 (1999).

  12. 12.

    et al. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403, 913–916 (2000).

  13. 13.

    et al. Characterization of the SP11/SCR high-affinity binding site involved in self/nonself recognition in Brassica self-incompatibility. Plant Cell 19, 107–117 (2007).

  14. 14.

    et al. Direct ligand–receptor complex interaction controls Brassica self-incompatibility. Nature 413, 534–538 (2001).

  15. 15.

    , , & Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 293, 1824–1826 (2001).

  16. 16.

    et al. A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 303, 1516–1519 (2004).

  17. 17.

    , & A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 286, 1729–1731 (1999).

  18. 18.

    , , , & Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc. Natl Acad. Sci. USA. 95, 382–387 (1998).

  19. 19.

    et al. Calcium signalling mediates self-incompatibility response in the Brassicaceae. Nat. Plants 1, 15128 (2015).

  20. 20.

    et al. Identification of the pollen self-incompatibility determinant in Papaver rhoeas. Nature 459, 992–995 (2009).

  21. 21.

    et al. Self-incompatibility in Papaver targets soluble inorganic pyrophosphatases in pollen. Nature 444, 490–493 (2006).

  22. 22.

    & Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429, 305–309 (2004).

  23. 23.

    et al. Self-incompatibility-induced programmed cell death in field poppy pollen involves dramatic acidification of the incompatible pollen tube cytosol. Plant Physiol. 167, 766–779 (2015).

  24. 24.

    , & The pollen S-determinant in Papaver: comparisons with known plant receptors and protein ligand partners. J. Exp. Bot. 61, 2015–2025 (2010).

  25. 25.

    , & S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367, 560–563 (1994).

  26. 26.

    , , , & S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367, 563–566 (1994).

  27. 27.

    , , & Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347, 757–760 (1990).

  28. 28.

    et al. Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342, 955–957 (1989).

  29. 29.

    et al. Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429, 302–305 (2004).

  30. 30.

    et al. Collaborative non-self recognition system in S-RNase-based self-incompatibility. Science 330, 796–799 (2010).

  31. 31.

    , , & Identification of the self-incompatibility locus F-box protein-containing complex in Petunia inflata. Plant Reprod. 27, 31–45 (2014).

  32. 32.

    et al. Ubiquitin-proteasome-mediated degradation of S-RNase in a Solanaceous cross-compatibility reaction. Plant J. 78, 1014–1021 (2014).

  33. 33.

    , & Compatibility and incompatibility in S-RNase-based systems. Ann. Bot. 108, 647–658 (2011).

  34. 34.

    et al. Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439, 805–810 (2006).

  35. 35.

    , & An S-RNase-based gametophytic self-incompatibility system evolved only once in eudicots. J. Mol. Evol. 67, 179–190 (2008).

  36. 36.

    & Evolutionary relationships among self-incompatibility RNases. Proc. Natl Acad. Sci. USA. 98, 13167–13171 (2001).

  37. 37.

    & S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. Mol. Biol. Evol. 19, 825–829 (2002).

  38. 38.

    et al. Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia. Nat. Plants 1, 14005 (2015).

  39. 39.

    , & Molecular mechanisms of self-incompatibility in flowering plants and fungi. Different means to the same end. Trends Cell Biol. 6, 421–428 (1996).

  40. 40.

    & in Self-Incompatibility Flowering Plants (ed. Franklin-Tong, V. E.) 3–32 (Springer, 2008).

  41. 41.

    , , & Transcriptome analysis reveals the same 17 S-Locus F-Box genes in two haplotypes of the self-incompatibility locus of Petunia inflata. Plant Cell 26, 2873–2888 (2014).

  42. 42.

    et al. Four previously identified Petunia inflata S-locus F-box genes are involved in pollen specificity in self-incompatibility. Mol. Plant 7, 567–569 (2014).

  43. 43.

    et al. Species selection maintains self-incompatibility. Science 330, 493–495 (2010).

  44. 44.

    et al. Patterns of evolution at the gametophytic self-incompatibility Sorbus aucuparia (Pyrinae) S pollen genes support the non-self recognition by multiple factors model. J. Exp. Bot. 64, 2423–2434 (2013).

  45. 45.

    et al. Sequence divergence and loss-of-function phenotypes of S locus F-box brothers genes are consistent with non-self recognition by multiple pollen determinants in self-incompatibility of Japanese pear (Pyrus pyrifolia). Plant J. 68, 1028–1038 (2011).

  46. 46.

    et al. Apple S locus region represents a large cluster of related, polymorphic and pollen-specific F-box genes. Plant Mol. Biol. 74, 143–154 (2010).

  47. 47.

    & Genetical studies in pears—III. Incompatibility and sterility. J. Genet. 43, 31–43 (1942).

  48. 48.

    et al. Characteristics of fruiting and pollen tube growth of apple autotetraploid cultivars showing self-compatibility. J. Japanese Soc. Hortic. Sci. 78, 402–409 (2009).

  49. 49.

    & Genetical studies in pears—IV. Pollen-tube growth and incompatibility. J. Genet. 43, 211–222 (1942).

  50. 50.

    et al. Deletion of a 236 kb region around S4-RNase in a stylar-part mutant S4sm-haplotype of Japanese pear. Plant Mol. Biol. 66, 389–400 (2008).

  51. 51.

    et al. Coevolution of the S-locus genes SRK, SLG and SP11/SCR in Brassica oleracea and B. rapa. Genetics 162, 931–940 (2002).

  52. 52.

    et al. Effects of recombination on hitchhiking diversity in the Brassica self-incompatibility locus complex. Genetics 177, 949–958 (2007).

  53. 53.

    , & RNase-based self-incompatibility: puzzled by pollen S. Plant Cell 20, 2286–2292 (2008).

  54. 54.

    , , & Different positively selected sites at the gametophytic self-incompatibility pistil S-RNase gene in the Solanaceae and Rosaceae (Prunus, Pyrus, and Malus). J. Mol. Evol. 65, 175–185 (2007).

  55. 55.

    , , , & Studies of self-incompatibility in wild tomatoes: I. S-allele diversity in Solanum chilense (Dun.) Reiche [corrected] (Solanaceae). Heredity 99, 553–561 (2007).

  56. 56.

    , , & Reply: establishing a paradigm for the generation of new S alleles. Plant Cell 12, 313–315 (2000).

  57. 57.

    & Evolutionary dynamics of dual-specificity self-incompatibility alleles. Plant Cell 12, 310–312 (2000).

  58. 58.

    How can two-gene models of self-incompatibility generate new specificities? Plant Cell 12, 309–310 (2000).

  59. 59.

    , , On the origin of self-incompatibility haplotypes: transition through self-compatible intermediates. Genetics 157, 1805–1817 (2001).

  60. 60.

    , , & Primary structural features of the self-incompatibility protein in Solanaceae. Sex. Plant Reprod. 4, 81–87 (1991).

  61. 61.

    et al. Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9, 1757–1766 (1997).

  62. 62.

    et al. Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles. Plant Cell 11, 2087–2097 (1999).

  63. 63.

    & in Petunia: Evolutionary, Developmental and Physiological Genetics (eds Gerats, T. & Strommer, J.) 85–106 (Springer, 2009).

  64. 64.

    , & Molecular bases and evolutionary dynamics of self-incompatibility in the Pyrinae (Rosaceae). J. Exp. Bot. 63, 4015–4032 (2012).

  65. 65.

    , The evolution of self-incompatibility when mates are limiting. Trends Plant Sci. 13, 128–136 (2008).

  66. 66.

    , Effects of pollen availability and the mutation bias on the fixation of mutations disabling the male specificity of self-incompatibility. J. Evol. Biol. 26, 2221–2232 (2013).

  67. 67.

    et al. Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature 464, 1342–1346 (2010).

  68. 68.

    , & Ancient polymorphism reveals unidirectional breeding system shifts. Proc. Natl Acad. Sci. USA. 103, 1359–1363 (2006).

  69. 69.

    , Evolution of selfing: recurrent patterns in molecular adaptation. Annu. Rev. Ecol. Evol. Syst. 46, 593–622 (2015).

  70. 70.

    et al. Self-compatible peach (Prunus persica) has mutant versions of the S haplotypes found in self-incompatible Prunus species. Plant Mol. Biol. 63, 109–123 (2007).

  71. 71.

    , , , & Self-(in)compatibility of the almonds P. dulcis and P. webbii: detection and cloning of ‘wild-type Sf’ and new self-compatibility alleles encoding inactive S-RNases. Mol. Genet. Genomics 278, 665–676 (2007).

  72. 72.

    & Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of Solanum species. Proc. Natl Acad. Sci. USA. 112, 4417–4422 (2015).

  73. 73.

    et al. Insights into the evolution of self-compatibility in Lycopersicon from a study of stylar factors. Plant J. 30, 143–153 (2002).

  74. 74.

    , , , & Duplication of the S-locus F-box gene is associated with breakdown of pollen function in an S-haplotype identified in a natural population of self-incompatible Petunia axillaris. Plant Mol. Biol. 57, 141–153 (2005).

  75. 75.

    , , A tale of two continents: Baker's rule and the maintenance of self-incompatibility in Lycium (Solanaceae). Evolution 62, 1052–1065 (2008).

  76. 76.

    , Differential strengths of selection on S-RNases from Physalis and Solanum (Solanaceae). BMC Evol. Biol. 11, 243 (2011).

  77. 77.

    et al. Comparative analysis of the self-incompatibility (S-) locus region of Prunus mume: identification of a pollen-expressed F-box gene with allelic diversity. Genes Cells 8, 203–213 (2003).

  78. 78.

    et al. Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-box gene with haplotype-specific polymorphism. Plant Cell 15, 771–81 (2003).

  79. 79.

    , , & Accumulation of nonfunctional S-haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus. Genetics 172, 1191–1198 (2006).

  80. 80.

    , , , , Molecular and genetic analyses of four nonfunctional S haplotype variants derived from a common ancestral S haplotype identified in sour cherry (Prunus cerasus L.). Genetics 184, 411–27 (2010).

  81. 81.

    , , & Loss of pollen-S function in two self-compatible selections of Prunus avium is associated with deletion/mutation of an S haplotype-specific F-box gene. Plant Cell 17, 37–51 (2005).

  82. 82.

    et al. The S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume. Plant J. 39, 573–586 (2004).

  83. 83.

    , , & Insights into the Prunus-specific S-RNase-based self-incompatibility system from a genome-wide analysis of the evolutionary radiation of S locus-related F-box genes. Plant Cell Physiol. 57, 1281–1294 (2016).

  84. 84.

    et al. Convergent evolution at the gametophytic self-incompatibility system in Malus and Prunus. PLoS One 10, e0126138 (2015).

  85. 85.

    , , Evolutionary analysis of genes for S-RNase-based self-incompatibility reveals S locus duplications in the ancestral Rosaceae. Hortic. J. 84, 233–242 (2015).

  86. 86.

    & Recognition of a wide-range of S-RNases by S locus F-box like 2, a general-inhibitor candidate in the Prunus-specific S-RNase-based self-incompatibility system. Plant Mol. Biol. 91, 459–469 (2016).

  87. 87.

    , , , & Insight into S-RNase-based self-incompatibility in Petunia: recent findings and future directions. Front. Plant Sci. 6, 1–6 (2015).

  88. 88.

    et al. Inheritance of hetero-diploid pollen S-haplotype in self-compatible tetraploid Chinese cherry (Prunus pseudocerasus Lindl). PLoS One 8, e61219 (2013).

  89. 89.

    , , , , Variability patterns and positively selected sites at the gametophytic self-incompatibility pollen SFB gene in a wild self-incompatible Prunus spinosa (Rosaceae) population. New Phytol. 172, 577–587 (2006).

  90. 90.

    & Unilateral interspecific incompatibility in flowering plants. Heredity 12, 233–256 (1958).

  91. 91.

    et al. S RNase and interspecific pollen rejection in the genus Nicotiana: multiple pollen-rejection pathways contribute to unilateral incompatibility between self-incompatible and self-compatible species. Plant Cell 8, 943–958 (1996).

  92. 92.

    & A pollen factor linking inter- and intraspecific pollen rejection in tomato. Science 330, 1827–1830 (2010).

  93. 93.

    et al. Multiple features that distinguish unilateral incongruity and self-incompatibility in the tomato clade. Plant J. 64, 367–378 (2010).

  94. 94.

    et al. A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol. 125, 2095–2103 (2001).

  95. 95.

    et al. The dominance of alleles controlling self-incompatibility in Brassica pollen is regulated at the RNA level. Plant Cell 14, 491–504 (2002).

  96. 96.

    et al. Dominance relationships between self-incompatibility alleles controlled by DNA methylation. Nat. Genet. 38, 297–299 (2006).

  97. 97.

    et al. Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature 466, 983–986 (2010).

  98. 98.

    & Evidence for Fisher's dominance theory: how many ‘special cases’? Trends Genet. 27, 441–5 (2011).

  99. 99.

    et al. Dominance hierarchy arising from the evolution of a complex small RNA regulatory network. Science 346, 1200–1205 (2014).

  100. 100.

    , & A general model to explore complex dominance patterns in plant sporophytic self-incompatibility systems. Genetics 175, 1351–1369 (2007).

  101. 101.

    et al. Progress towards elucidating the mechanisms of self-incompatibility in the grasses: further insights from studies in Lolium. Ann. Bot. 108, 677–685 (2011).

  102. 102.

    S locus-linked F-box genes expressed in anthers of Hordeum bulbosum. Plant Cell Rep. 28, 1453–1460 (2009).

  103. 103.

    , , & Expression and trans-specific polymorphism of self-incompatibility RNases in Coffea (Rubiaceae). PLoS One 6, e21019 (2011).

  104. 104.

    Angiosperm Phylogeny Group. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161, 105–121 (2009).

  105. 105.

    , , , & MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).

Download references

Acknowledgements

This work was supported in part by Grants-in-Aid for Scientific Research on Innovative Areas (23113002, 16H06467, 16H06464 to S.T.; 16H01467 to S.F.), and Grants-in-Aid for Scientific Research (21248014, 25252021, 16H06380 to S.T.) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT).

Author information

Affiliations

  1. Graduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma 630-0192, Japan.

    • Sota Fujii
    • , Ken-ichi Kubo
    •  & Seiji Takayama

Authors

  1. Search for Sota Fujii in:

  2. Search for Ken-ichi Kubo in:

  3. Search for Seiji Takayama in:

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Seiji Takayama.