Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1999 Nov;11(11):2087–2097. doi: 10.1105/tpc.11.11.2087

Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles.

D P Matton 1, D T Luu 1, Q Xike 1, G Laublin 1, M O'Brien 1, O Maes 1, D Morse 1, M Cappadocia 1
PMCID: PMC144125  PMID: 10559436

Abstract

Gametophytic self-incompatibility in plants involves rejection of pollen when pistil and pollen share the same allele at the S locus. This locus is highly multiallelic, but the mechanism by which new functional S alleles are generated in nature has not been determined and remains one of the most intriguing conceptual barriers to a full understanding of self-incompatibility. The S(11) and S(13) RNases of Solanum chacoense differ by only 10 amino acids, but they are phenotypically distinct (i.e., they reject either S(11) or S(13) pollen, respectively). These RNases are thus ideally suited for a dissection of the elements involved in recognition specificity. We have previously found that the modification of four amino acid residues in the S(11) RNase to match those in the S(13) RNase was sufficient to completely replace the S(11) phenotype with the S(13) phenotype. We now show that an S(11) RNase in which only three amino acid residues were modified to match those in the S(13) RNase displays the unprecedented property of dual specificity (i.e., the simultaneous rejection of both S(11) and S(13) pollen). Thus, S(12)S(14) plants expressing this hybrid S RNase rejected S(11), S(12), S(13), and S(14) pollen yet allowed S(15) pollen to pass freely. Surprisingly, only a single base pair differs between the dual-specific S allele and a monospecific S(13) allele. Dual-specific S RNases represent a previously unsuspected category of S alleles. We propose that dual-specific alleles play a critical role in establishing novel S alleles, because the plants harboring them could maintain their old recognition phenotype while acquiring a new one.

Full Text

The Full Text of this article is available as a PDF (639.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Cappadocia M., Heizmann P., Dumas C. Tissue printing and its applications in self-incompatibility studies. Plant Mol Biol. 1993 Dec;23(5):1079–1085. doi: 10.1007/BF00021823. [DOI] [PubMed] [Google Scholar]
  2. Clark A. G., Kao T. H. Excess nonsynonymous substitution of shared polymorphic sites among self-incompatibility alleles of Solanaceae. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9823–9827. doi: 10.1073/pnas.88.21.9823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Coleman C. E., Kao T. The flanking regions of two Petunia inflata S alleles are heterogeneous and contain repetitive sequences. Plant Mol Biol. 1992 Feb;18(4):725–737. doi: 10.1007/BF00020014. [DOI] [PubMed] [Google Scholar]
  4. Ebert P. R., Anderson M. A., Bernatzky R., Altschuler M., Clarke A. E. Genetic polymorphism of self-incompatibility in flowering plants. Cell. 1989 Jan 27;56(2):255–262. doi: 10.1016/0092-8674(89)90899-4. [DOI] [PubMed] [Google Scholar]
  5. FISHER R. A model for the generation of self-sterility alleles. J Theor Biol. 1961 Oct;1:411–414. [PubMed] [Google Scholar]
  6. Grant M. R., Godiard L., Straube E., Ashfield T., Lewald J., Sattler A., Innes R. W., Dangl J. L. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science. 1995 Aug 11;269(5225):843–846. doi: 10.1126/science.7638602. [DOI] [PubMed] [Google Scholar]
  7. Harikrishna K., Jampates-Beale R., Milligan S. B., Gasser C. S. An endochitinase gene expressed at high levels in the stylar transmitting tissue of tomatoes. Plant Mol Biol. 1996 Mar;30(5):899–911. doi: 10.1007/BF00020802. [DOI] [PubMed] [Google Scholar]
  8. Huang S., Lee H. S., Karunanandaa B., Kao T. H. Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self-pollen. Plant Cell. 1994 Jul;6(7):1021–1028. doi: 10.1105/tpc.6.7.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ishimizu T., Shinkawa T., Sakiyama F., Norioka S. Primary structural features of rosaceous S-RNases associated with gametophytic self-incompatibility. Plant Mol Biol. 1998 Aug;37(6):931–941. doi: 10.1023/a:1006078500664. [DOI] [PubMed] [Google Scholar]
  10. Jones J. D., Dunsmuir P., Bedbrook J. High level expression of introduced chimaeric genes in regenerated transformed plants. EMBO J. 1985 Oct;4(10):2411–2418. doi: 10.1002/j.1460-2075.1985.tb03949.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kronstad J. W., Leong S. A. The b mating-type locus of Ustilago maydis contains variable and constant regions. Genes Dev. 1990 Aug;4(8):1384–1395. doi: 10.1101/gad.4.8.1384. [DOI] [PubMed] [Google Scholar]
  12. Kusaba M., Nishio T., Satta Y., Hinata K., Ockendon D. Striking sequence similarity in inter- and intra-specific comparisons of class I SLG alleles from Brassica oleracea and Brassica campestris: implications for the evolution and recognition mechanism. Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7673–7678. doi: 10.1073/pnas.94.14.7673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Leckie F., Mattei B., Capodicasa C., Hemmings A., Nuss L., Aracri B., De Lorenzo G., Cervone F. The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed beta-strand/beta-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J. 1999 May 4;18(9):2352–2363. doi: 10.1093/emboj/18.9.2352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lee H. S., Huang S., Kao T. S proteins control rejection of incompatible pollen in Petunia inflata. Nature. 1994 Feb 10;367(6463):560–563. doi: 10.1038/367560a0. [DOI] [PubMed] [Google Scholar]
  15. MARTIN F. W. Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol. 1959 May;34(3):125–128. doi: 10.3109/10520295909114663. [DOI] [PubMed] [Google Scholar]
  16. Matton D. P., Maes O., Laublin G., Xike Q., Bertrand C., Morse D., Cappadocia M. Hypervariable Domains of Self-Incompatibility RNases Mediate Allele-Specific Pollen Recognition. Plant Cell. 1997 Oct;9(10):1757–1766. doi: 10.1105/tpc.9.10.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Matton D. P., Mau S. L., Okamoto S., Clarke A. E., Newbigin E. The S-locus of Nicotiana alata: genomic organization and sequence analysis of two S-RNase alleles. Plant Mol Biol. 1995 Aug;28(5):847–858. doi: 10.1007/BF00042070. [DOI] [PubMed] [Google Scholar]
  18. McClure B. A., Haring V., Ebert P. R., Anderson M. A., Simpson R. J., Sakiyama F., Clarke A. E. Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature. 1989 Dec 21;342(6252):955–957. doi: 10.1038/342955a0. [DOI] [PubMed] [Google Scholar]
  19. Murfett J., Atherton T. L., Mou B., Gasser C. S., McClure B. A. S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature. 1994 Feb 10;367(6463):563–566. doi: 10.1038/367563a0. [DOI] [PubMed] [Google Scholar]
  20. Nasrallah J. B. Evolution of the Brassica self-incompatibility locus: a look into S-locus gene polymorphisms. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9516–9519. doi: 10.1073/pnas.94.18.9516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pandey K. K. New self-incompatibility alleles produced through inbreeding. Nature. 1970 Aug 15;227(5259):689–690. doi: 10.1038/227689a0. [DOI] [PubMed] [Google Scholar]
  22. Parry S., Newbigin E., Craik D., Nakamura K. T., Bacic A., Oxley D. Structural analysis and molecular model of a self-incompatibility RNase from wild tomato. Plant Physiol. 1998 Feb;116(2):463–469. doi: 10.1104/pp.116.2.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Reiter R. S., Williams J. G., Feldmann K. A., Rafalski J. A., Tingey S. V., Scolnik P. A. Global and local genome mapping in Arabidopsis thaliana by using recombinant inbred lines and random amplified polymorphic DNAs. Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1477–1481. doi: 10.1073/pnas.89.4.1477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Saba-el-Leil M. K., Rivard S., Morse D., Cappadocia M. The S11 and S13 self incompatibility alleles in Solanum chacoense Bitt. are remarkably similar. Plant Mol Biol. 1994 Feb;24(4):571–583. doi: 10.1007/BF00023555. [DOI] [PubMed] [Google Scholar]
  25. Yen Y., Green P. J. Identification and Properties of the Major Ribonucleases of Arabidopsis thaliana. Plant Physiol. 1991 Dec;97(4):1487–1493. doi: 10.1104/pp.97.4.1487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Zurek D. M., Mou B., Beecher B., McClure B. Exchanging sequence domains between S-RNases from Nicotiana alata disrupts pollen recognition. Plant J. 1997 Apr;11(4):797–808. doi: 10.1046/j.1365-313x.1997.11040797.x. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES