Skip to main content
SpringerLink
Log in

Evolutionary genetics of self-incompatibility in the Solanaceae

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The self-incompatibility (S) gene in flowering plants has long been appreciated as an example of extreme allelic polymorphism maintained by frequency-dependent selection. Recent studies of population samples of S-allele sequences obtained by RT-PCR from five species of Solanaceae now reveal a picture of conspicuous inter-specific variation in both S-allele number and age. Explanations for this variation are examined with reference to current theory. We propose that changes in species' effective population size, particularly those associated with the evolution of different life histories, best account for interspecific differences in both the number and average age of S alleles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Anderson MA, McFadden GI, Bernatzky R, Atkinson A, Orpin T, Dedman H, Tregear G, Fernley R, Clarke AE: Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. Plant Cell 1: 483–491 (1989).

    Google Scholar 

  2. Broothaerts W, Janssens GA, Proost P, Broekaert WF: cDNA cloning and molecular analysis of two self-incompatibility alleles from apple. Plant Mol Biol 27: 499–511 (1995).

    Google Scholar 

  3. Clark AG, Kao T-h: Excess nonsynonymous substitution at shared polymorphic sites among self-incompatibility alleles of Solanaceae. Proc Natl Acad Sci USA 88: 9823–9827 (1991).

    Google Scholar 

  4. Clarke AE, Newbigin E: Molecular aspects of selfincompatibility in flowering plants. Annu Rev Genet 27: 257–279 (1993).

    Google Scholar 

  5. Coleman CE, Kao T-h: The flanking regions of two Petunia inflata S-alleles are heterogeneous and contain repetitive sequences. Plant Mol Biol 18: 725–737 (1992).

    Google Scholar 

  6. Emerson S: A preliminary survey of the Oenothera organensis population. Evolution 24: 524–537 (1939).

    Google Scholar 

  7. Felsenstein J: PHYLIP (Phylogeny Inference Package). Distributed by the author. Department of Genetics, University of Washington, Seattle, WA (1996).

    Google Scholar 

  8. Franklin FCH, Franklin-Tong VE, Thorlby GJ, Howell EC, Atwal K, Lawrence MJ: Molecular basis of the incompatibility mechanism in Papaver rhoeas L. Plant Growth Regul 11: 5–12 (1992).

    Google Scholar 

  9. Hinata K, Watanabe M, Yamakawa S, Satta Y, Isogai A: Evolutionary aspects of the S-related genes of the Brassica selfincompatibility system: synonymous and nonsynonymous base substitutions. Genetics 140: 1099–1104 (1995).

    Google Scholar 

  10. Ioerger TR, Gohlke JR, Xu B, Kao T-h: Primary structural features of the self-incompatibility protein in Solanaceae. Sex Plant Reprod 4: 81–87 (1991).

    Google Scholar 

  11. Klein J, Satta Y, Takahata N, O'hUigin C: Trans-specific Mhc polymorphism and the origin of species in primates. J Med Primatol 22: 57–64 (1993).

    Google Scholar 

  12. Lawrence MJ, Lane MD, O'Donnell S, Franklin-Tong VE: The population genetics of the self-incompatibility polymorphism in Papaver rhoeas. V. Cross-classification of the Salleles of samples from three natural populations. Heredity 71: 581–590 (1993).

    Google Scholar 

  13. Lee HS, Huang SS, Kao T-H: S-proteins control rejection of self-incompatible pollen in Petunia inflata. Nature 367: 560–563 (1994).

    Google Scholar 

  14. Mantel N: Approaches to a health research occupancy problem. Biometrics 30: 355–362 (1974).

    Google Scholar 

  15. Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M: Hypervariable domains of self-incompatibility RNases mediated allele-specific pollen recognition. Plant Cell 9: 1757–1766 (1997).

    Google Scholar 

  16. McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE: Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 21: 955–957 (1989).

    Google Scholar 

  17. O'Donnell S, Lane MD, Lawrence MJ: The population genetics of the self-incompatibility polymorphism in Papaver rhoeas.VI. Estimation of the overlap between the allelic complements of a pair of populations. Heredity 71: 591–595 (1993).

    Google Scholar 

  18. O'Donnell S, Lawrence MJ: The population genetics of the self-incompatibility polymorphism in Papaver rhoeas. IV. The estimation of the number of alleles in a population. Heredity 53: 495–507 (1984).

    Google Scholar 

  19. Olmstead RG, Sweere JA: Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Syst Biol 43: 467–481 (1994).

    Google Scholar 

  20. Parry S, Newbigin E, Craik D, Nakamura KT, Bacic A, Oxley D: Structural analysis and molecular model of a selfincompatibility RNase from wild tomato. Plant Physiol 116: 463–469 (1998).

    Google Scholar 

  21. Paxman GJ: The maximum likelihood estimation of the number of self-sterility alleles in a population. Genetics 48: 1029–1032 (1963).

    Google Scholar 

  22. Richman AD, Kao T-h, Schaeffer SW, Uyenoyama MK: Sallele sequence diversity in natural populations of Solanum carolinense Horsenettle. Heredity 75: 405–415 (1995).

    Google Scholar 

  23. Richman AD, Kohn JR: Learning from rejection: the evolutionary biology of single-locus incompatibility. Trends Ecol Evol 11: 497–502 (1996).

    Google Scholar 

  24. Richman AD, Kohn JR: Self-incompatibility alleles in Physalis: implications for historical inference from balanced polymorphisms. Proc Natl Acad Sci USA 96: 168–172 (1999).

    Google Scholar 

  25. Richman AD: S-allele diversity in Lycium andersonii: implications for inter-specific variation in S-allele age in the Solanaceae. Ann Bot (in press).

  26. Richman AD, Kohn JR: Significant differences in S-allele diversification in taxa arising after a bottleneck event. Heredity (submitted).

  27. Richman AD, Uyenoyama MK, Kohn J: S-allele diversity in a natural population of ground cherry Physalis crassifolia (Solanaceae) assessed by RT-PCR. Heredity 76: 497–505 (1996).

    Google Scholar 

  28. Richman AD, Uyenoyama MK, Kohn JR: Allelic diversity and gene genealogy at the self-incompatibility locus in the Solanaceae. Science 273: 1212–1216 (1996).

    Google Scholar 

  29. Saba-El-Leil MK, Rivard S, Morse D, Cappadocia M: The S11 and S13 self-incompatibility alleles in Solanum chacoense Bitt. are remarkably similar. Plant Mol Biol 24: 571–583 (1994).

    Google Scholar 

  30. Schierup M: The number of self-incompatibility alleles in a finite, subdivided population. Genetics 149: 1153–1162 (1998).

    Google Scholar 

  31. Singh A, Kao T-h: Gametophytic self-incompatibility: biochemical, molecular genetic, and evolutionary aspects. Int Rev Cytol 140: 449–483 (1992).

    Google Scholar 

  32. Swofford DL: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, MA (1998).

    Google Scholar 

  33. Takahata N: A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proc Natl Acad Sci USA 87: 2419–2423 (1990).

    Google Scholar 

  34. Takahata N: Allelic genealogy and human evolution. Mol Biol Evol 10: 2–22 (1993).

    Google Scholar 

  35. Takahata N: Evolutionary genetics of human paleopopulations. In: Takahata, N, Clarke AG (eds), Mechanisms of Molecular Evolution, pp. 1–21. Sinauer Associates, Sunderland MA (1993).

    Google Scholar 

  36. Takahata N, Nei M: Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124: 967–978 (1990).

    Google Scholar 

  37. Takezaki N, Rzhetsky A, Nei M: Phylogenetic test of themolecular clock and linearized trees. Mol Biol Evol 12: 823–833 (1995).

    Google Scholar 

  38. Thompson RD, Kirsch H-H: The S locus of flowering plants: when self-rejection is self-interest. Trends Genet 8: 381–387 (1992).

    Google Scholar 

  39. Uyenoyama MK: Genealogical structure among alleles regulating self-incompatibility in natural populations of flowering plants. Genetics 147: 1389–1400 (1997).

    Google Scholar 

  40. Vekemans X, Slatkin M: Gene and allelic genealogies at a gametophytic self-incompatibility locus. Genetics 137: 1157–1165 (1994).

    Google Scholar 

  41. Wright S: On the number of self-incompatibility alleles maintained in equilibrium by a given mutation rate in the population of a given size: a re-examination. Biometrics 16: 61–85 (1960).

    Google Scholar 

  42. Wright S: The distribution of self-incompatibility alleles in populations. Evolution 18: 609–619 (1965).

    Google Scholar 

  43. Wu J, Saupe SJ, Glass NL: Evidence for balancing selection operating at the het-c heterokaryon incompatibility locus in filamentous fungi. Proc Natl Acad Sci USA 95: 12398–12403 (1998).

    Google Scholar 

  44. Xue Y, Carpenter R, Dickinson HG, Coen ES: Origin of allelic diversity in Antirrhinum S locus RNases. Plant Cell 8: 805–814 (1996).

    Google Scholar 

  45. Yokoyama S, Hetherington LE: The expected number of selfincompatibility alleles in finite plant populations. Heredity 48: 299–303 (1982).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant Sciences Department, Montana State University, Bozeman, MT, 59717-0346, USA

    Adam D. Richman

  2. Biology Department, University of California San Diego, 9500 Gilman Dr., La Jolla, CA , 92093-0116, USA

    Joshua R. Kohn

Authors
  1. Adam D. Richman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joshua R. Kohn
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Richman, A.D., Kohn, J.R. Evolutionary genetics of self-incompatibility in the Solanaceae. Plant Mol Biol 42, 169–179 (2000). https://doi.org/10.1023/A:1006336206637

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006336206637

Search

Navigation