Skip to main content
NCBI home page
The Plant Cell logoLink to The Plant Cell
. 1997 Oct;9(10):1757–1766. doi: 10.1105/tpc.9.10.1757

Hypervariable Domains of Self-Incompatibility RNases Mediate Allele-Specific Pollen Recognition.

D P Matton 1, O Maes 1, G Laublin 1, Q Xike 1, C Bertrand 1, D Morse 1, M Cappadocia 1
PMCID: PMC157019  PMID: 12237346

Abstract

Self-incompatibility (SI) in angiosperms is a genetic mechanism that promotes outcrossing through rejection of self-pollen. In the Solanaceae, SI is determined by a multiallelic S locus whose only known product is an S RNase. S RNases show a characteristic pattern of five conserved and two hypervariable regions. These are thought to be involved in the catalytic function and in allelic specificity, respectively. When the Solanum chacoense S12S14 genotype is transformed with an S11 RNase, the styles of plants expressing significant levels of the transgene reject S11 pollen. A previously characterized S RNase, S13, differs from the S11 RNase by only 10 amino acids, four of which are located in the hypervariable regions. When S12S14 plants were transformed with a chimeric S11 gene in which these four residues were substituted with those present in the S13 RNase, the transgenic plants acquired the S13 phenotype. This result demonstrates that the S RNase hypervariable regions control allelic specificity.

Full Text

The Full Text of this article is available as a PDF (2.5 MB).

Selected References

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

  1. A simple and general method for transferring genes into plants. Science. 1985 Mar 8;227(4691):1229–1231. doi: 10.1126/science.227.4691.1229. [DOI] [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Clarke A. E., Newbigin E. Molecular aspects of self-incompatibility in flowering plants. Annu Rev Genet. 1993;27:257–279. doi: 10.1146/annurev.ge.27.120193.001353. [DOI] [PubMed] [Google Scholar]
  5. Dodds P. N., Clarke A. E., Newbigin E. A molecular perspective on pollination in flowering plants. Cell. 1996 Apr 19;85(2):141–144. doi: 10.1016/s0092-8674(00)81090-9. [DOI] [PubMed] [Google Scholar]
  6. 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]
  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. 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]
  10. Kao T. H., McCubbin A. G. How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12059–12065. doi: 10.1073/pnas.93.22.12059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Karunanandaa B., Huang S., Kao T. Carbohydrate moiety of the Petunia inflata S3 protein is not required for self-incompatibility interactions between pollen and pistil. Plant Cell. 1994 Dec;6(12):1933–1940. doi: 10.1105/tpc.6.12.1933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kurihara H., Mitsui Y., Ohgi K., Irie M., Mizuno H., Nakamura K. T. Crystal and molecular structure of RNase Rh, a new class of microbial ribonuclease from Rhizopus niveus. FEBS Lett. 1992 Jul 20;306(2-3):189–192. doi: 10.1016/0014-5793(92)80997-u. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Matton D. P., Nass N., Clarke A. E., Newbigin E. Self-incompatibility: how plants avoid illegitimate offspring. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):1992–1997. doi: 10.1073/pnas.91.6.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Murfett J., Ebert P. R., Haring V., Clarke A. E. An S-RNase promoter from Nicotiana alata functions in transgenic N. alata plants but not Nicotiana tabacum. Plant Mol Biol. 1995 Aug;28(5):957–963. doi: 10.1007/BF00042080. [DOI] [PubMed] [Google Scholar]
  18. Nasrallah J. B., Stein J. C., Kandasamy M. K., Nasrallah M. E. Signaling the arrest of pollen tube development in self-incompatible plants. Science. 1994 Dec 2;266(5190):1505–1508. doi: 10.1126/science.266.5190.1505. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Rivers B. A., Bernatzky R., Robinson S. J., Jahnen-Dechent W. Molecular diversity at the self-incompatibility locus is a salient feature in natural populations of wild tomato (Lycopersicon peruvianum). Mol Gen Genet. 1993 Apr;238(3):419–427. doi: 10.1007/BF00292001. [DOI] [PubMed] [Google Scholar]
  21. Royo J., Kowyama Y., Clarke A. E. Cloning and nucleotide sequence of two S-RNases from Lycopersicon peruvianum (L.) Mill. Plant Physiol. 1994 Jun;105(2):751–752. doi: 10.1104/pp.105.2.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Sassa H., Hirano H., Ikehashi H. Identification and characterization of stylar glycoproteins associated with self-incompatibility genes of Japanese pear, Pyrus serotina Rehd. Mol Gen Genet. 1993 Oct;241(1-2):17–25. doi: 10.1007/BF00280196. [DOI] [PubMed] [Google Scholar]
  24. Singh A., Kao T. H. Gametophytic self-incompatibility: biochemical, molecular genetic, and evolutionary aspects. Int Rev Cytol. 1992;140:449–483. doi: 10.1016/s0074-7696(08)61106-7. [DOI] [PubMed] [Google Scholar]
  25. Wemmer T., Kaufmann H., Kirch H. H., Schneider K., Lottspeich F., Thompson R. D. The most abundant soluble basic protein of the stylar transmitting tract in potato (Solanum tuberosum L.) is an endochitinase. Planta. 1994;194(2):264–273. [PubMed] [Google Scholar]
  26. Yee A. R., Kronstad J. W. Construction of chimeric alleles with altered specificity at the b incompatibility locus of Ustilago maydis. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):664–668. doi: 10.1073/pnas.90.2.664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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