Abstract
Many flowering plants avoid inbreeding through a genetic mechanism termed self-incompatibility. An extremely polymorphic S-locus1 controls the gametophytic self-incompatibility system that causes pollen rejection (that is, active arrest of pollen tube growth inside the style) when an S-allele carried by haploid pollen matches one of the S-alleles present in the diploid style. The only known product of the S-locus is an S-RNase expressed in the mature style2. The pollen component to this cell–cell recognition system is unknown and current models3,4 propose that it either acts as a gatekeeper allowing only its cognate S-RNase to enter the pollen tube, or as an inhibitor of non-cognate S-RNases. In the latter case, all S-RNases are presumed to enter pollen tubes; thus, the two models make diametrically opposed predictions concerning the entry of S-RNases into compatible pollen. Here we use immunocytochemical labelling of pollen tubes growing in styles to show accumulation of an S-RNase in the cytoplasm of all pollen-tube haplotypes, thus providing experimental support for the inhibitor model.
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References
de Nettancourt, D. Incompatibility in Angiosperms (Springer, New York, 1977).
McClure, B. et al. Style self-incompatibility products of Nicotiana alata are ribonucleases. Nature 32, 955– 957 (1989).
Kao, T.-H. & McCubbin, A. How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc. Natl Acad. Sci. USA 93, 12059–12065 (1996).
Dodds, P., Clarke, A. & Newbigin, E. A molecular perspective on pollination in flowering plants. Cell 85, 141–144 (1996).
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 6, 1021–1028 (1994).
McClure, B., Gray, J., Anderson, M. & Clarke, A. Self-incompatibility in Nicotiana alata involves degradation of pollen RNA. Nature 347, 757–760 ( 1990).
Matton, D. P. et al. Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9, 1757–1766 (1997).
Matton, D. P. et al. The 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).
Cheung, A. The pollen tube growth pathway: its molecular and biochemical contributions and responses to pollination. Sex. Plant Reprod. 9, 330–336 (1996).
de Nettancourt, D. et al. Ultrastructural aspects of the self-incompatibility mechanism in Lycopersicum peruvianum Mill. J. Cell Sci. 12, 403–419 (1973).
Steer, M. W. & Steer, J. M. Pollen tube tip growth. New Phytol. 111, 323–358 (1989).
Anderson, M. et al. Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Nature 321, 38–44 ( 1986).
Certal, A. et al. S-RNases in apple are expressed in the pistil along the pollen tube growth path. Sex. Plant Reprod. 12, 94–98 (1999).
Gray, J., McClure, B., Bönig, I., Anderson, M. & Clarke, A. Action of the style product of the self-incompatibility gene of Nicotiana alata (S-RNase) on in vitro grown pollen tubes. Plant Cell 3, 271 –283 (1991).
Jahnen, W., Lush, W. & Clarke, A. Inhibition of in vitro pollen tube growth by isolated S-glycoproteins of Nicotiana alata. Plant Cell 1, 501–510 (1989).
Hess, D., Gresshoff, P., Fielitz, U. & Gleiss, D. Uptake of protein and bacteriophage into swelling and germinating pollen of Petunia hybrida. Z. Pflanzenphysiol. 74, 371–376 (1974).
Golz, J., Clarke, A. E. & Newbegin, E. Mutational approaches to the study of self-incompatibility: revisiting the pollen-part mutants. Ann. Botany 85, 95–103 (2000).
Lewis, D. Chromosome fragments and mutation of the incompatibility gene. Nature 190, 990–991 ( 1961).
Pandey, K. Elements of the S-gene complex. II. Mutations and complementation at the SI locus in Nicotiana alata. Heredity 22, 255–284 (1967).
Saba-El-Leil, M., 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).
Despres, C., Saba-El-Leil, M., Rivard, S., Morse, D. & Cappadocia, M. Molecular cloning of two Solanum chacoense S-alleles and a hypothesis concerning their evolution. Sex. Plant Reprod. 7, 169– 176 (1994).
Van Sint Jan, V., Laublin, G., Birhman, R. & Cappadocia, M. Genetic analysis of leaf explant regenerability in Solanum chacoense. Plant Cell Tissue Org. Cult. 47, 9–13 (1996).
Veronneau, H., Lavoie, G. & Cappadocia, M. Genetic analysis of anther and leaf disk culture in two clones of Solanum chacoense Bitt and their reciprocal hybrids. Plant Cell Tissue Org. Cult. 30, 199– 209 (1992).
Rivard, S., Saba-El-Leil, M., Landry, B. & Cappadocia, M. RFLP analyses and segregation of molecular markers in plants produced by in vitro anther culture, selfing, and reciprocal crosses of two lines of self-incompatible Solanum chacoense. Genome 37, 775–783 (1994).
Vandenbosch, K. in Electron Microscopy of Plant Cells (eds Hall, J. & Hawes, C.) 181–218 (Academic, New York, 1991).
Martin, F. Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol. 34, 125– 128 (1959).
McFadden, G. in Electron Microscopy of Plant Cells (eds Hall, J. & Hawes, C.) 220–255 (Academic, New York, 1991).
Acknowledgements
We thank L. Pelletier and N. Nassoury for technical assistance, G. Teodorescu for plant care, and S. McCormick, A. Cheung, T.-H. Kao and V. de Luca for helpful discussions. The work was supported by a fellowship from Programme Québecois de Bourses d'Excellence, Québec (D.-T.L.) and by grants from NSERC (M.C.) and Fonds pour la Formation de Chercheurs et l’Aide à la Recherche (D.M., M.C.).
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Luu, DT., Qin, X., Morse, D. et al. S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility . Nature 407, 649–651 (2000). https://doi.org/10.1038/35036623
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DOI: https://doi.org/10.1038/35036623
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