A mutant S3 RNase of Petunia inflata lacking RNase activity has an allele-specific dominant negative effect on self-incompatibility interactions

Plant Cell

Volumn 9, Issue 1, 1997, Pages 85-95

  McCubbin, Andrew G ^a   Chung, Yong Yoon ^a   Kao, Teh Hui ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAGNOLIOPHYTA; PETUNIA; PETUNIA INTEGRIFOLIA SUBSP. INFLATA; SOLANACEAE;

EID: 0030906082     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.9.1.85     Document Type: Article

References (35)

1. Ai, Y., Singh, A., Coleman, C.E., loerger, T.R., Kheyr-Pour, A., and Kao, T.-h. (1990). Self-incompatibility in Petunia inflata: Isolation and characterization of cDNAs encoding three S-allele-associated proteins. Sex. Plant Reprod. 3, 130-138.
2. Anderson, M.A., Cornish, E.C., Mau, S.-L., Williams, E.G., Hoggart, R.M., Atkinson, R.J., Roche, P., Haley, J., Penschow, J., Niall, H., Tregear, G., Coghlan, J., Crawford, R., and Clarke, A.E. (1986). Molecular cloning of a cDNA clone of a stylar glycoprotein associated with the expression of self-incompatibility in Nicotiana alata Link and Otto. Nature 321, 38-44.
3. Anderson, M.A., McFadden, G.I., Bernatzky, R., Atkinson, A., Orpin, T., Dedman, H., Tregear, G., Fernley, R., and Clarke, A.E. (1989). Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. Plant Cell 1, 483-491.
4. Bell, P.R. (1995). Incompatibility in flowering plants: Adaptation of an ancient response. Plant Cell 7, 5-16.
5. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
6. Brown, P.H., and Ho, T.-h.D. (1986). Barley aleurone layers secrete a nuclease in response to gibberellic acid. Plant Physiol. 82, 801-806.
7. Clark, K.R., Okuley, J.J., Collins, P.D., and Sims, T.L. (1990). Sequence variability and developmental expression of S-alleles in self-incompatible and pseudo-self-compatible petunia. Plant Cell 2, 815-826.
8. de Nettancourt, D. (1977). Incompatibility in angiosperms. In Monographs on Theoretical and Applied Genetics, R. Frankel, G.A.E. Gall, and H.F. Linskens, eds (Berlin: Springer-Verlag), pp. 28-57.
9. Huang, S., Lee, H.-S., Karunanandaa, B., and Kao, T.-h. (1994). Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self-pollen. Plant Cell 6, 1021-1028.
10. Ioerger, T.R., Gohlke, J.R., Xu, B., and Kao, T.-h. (1991). Primary structural features of the self-incompatibility proteins in the Solanaceae. Sex. Plant Reprod. 4, 81-87.
11. Kao, T.-h., and McCubbin, A.G. (1996). How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc. Natl. Acad. Sci. USA 93, 12059-12065.
12. Kaufmann, H., Salamini, F., and Thompson, R.D. (1991). Sequence variability and gene structure at the self-incompatibility locus of Solanum tuberosum. Mol. Gen. Genet. 226, 457-466.
13. Kawata, Y., Sakiyama, F., Hayashi, F., and Kyogoku, Y. (1990). Identification of two essential histidine residues of ribonuclease T2 from Aspergillus oryzae. Eur. J. Biochem. 187, 255-262.
14. Kheyr-Pour, A., Bintrim, S.B., Ioerger, T.R., Remy, R., Hammond, S.A., and Kao. T.-h. (1990). Sequence diversity of pistil S-proteins associated with gametophytic self-incompatibility in Nicotiana alata. Sex. Plant Reprod. 3, 88-97.
15. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
16. Lee, H.-S., Singh, A., and Kao, T.-h. (1992). RNase X2, a pistilspecific ribonuclease from Petunia inflata, shares sequence similarity with solanaceous S proteins. Plant Mol. Biol. 20, 1131-1141.
17. Lee, H.-S., Huang, S., and Kao, T.-h. (1994). S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367, 560-563.
18. Lewis, D. (1949). Structure of the incompatibility gene. II. Induced mutation rate. Heredity 3, 339-355.
19. Lewis, D. (1960). Genetic control of specificity and activity of the S antigen in plants. Proc. R. Soc. Lond. Ser. B Biol. Sci. 151, 468-477.
20. McClure, B.A., Haring, V., Ebert, P.R., Anderson, M.A., Simpson, R.J., Sakiyama, F., and Clarke, A.E. (1989). Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342, 955-957.
21. Murfett, J., Atherton, T.L., Mou, B., Gasser, C.S., and McClure, B.A. (1994). S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367, 563-566.
22. Napoli, C., Lemieux, C., and Jorgensen, R. (1990). Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2, 279-289.
23. Ohgi, K., Horiuchi, H., Watanabe, H., Iwama, M., Takagi, M., and Masachika, I. (1992). Evidence that three histidine residues of a base non-specific and adenylic acid preferential ribonuclease from Rhizopus niveus are involved in the catalytic function. J. Biochem. 112, 132-138.
24. Richman, A.D., Kao, T.-h., Schaeffer, S.W., and Uyenoyama, M.K. (1995). S-allele sequence diversity in natural populations of Solanum carolinense (horsenettle). Heredity 75, 405-415.
25. Rogers, S.O., and Bendich, A.J. (1988). Extraction of DNA from plant tissue. In Plant Molecular Biology Manual, S.B. Gelvin and R.A. Schilperoort, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. A6:1-10.
26. Royo, J., Kowayama, K., and Clarke, A.E. (1994a). Cloning and nucleotide sequence of two S-RNases from Lycopersicon peruvianum (L.) Mill. Plant Physiol. 105, 751-752.
27. Royo, J., Kunz, C., Kowayama, Y., Anderson, M., and Clarke, A.E. (1994b). Loss of a histidine residue at the active site of S-locus ribonuclease is associated with self-compatibility in Lycopersicon peruvianum. Proc. Natl. Acad. Sci. USA 91, 6511-6514.
28. 13 self-incompatibility alleles in Solanum chacoense Bitt. are remarkably similar. Plant Mol. Biol. 24, 571-583.
29. Smith, D.E., and Fisher, P.A. (1984). Identification, developmental regulation, and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryos: Application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots. J. Cell Biol. 99, 20-28.
30. Stebbins, G.L. (1950). Variation and Evolution in Plants. (New York: Columbia University Press).
31. Thompson, R.D., and Kircn, H.-H. (1992). The S locus of flowering plants: When self-rejection is self-interest. Trends Genet. 8, 381-387.
32. Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354.
33. Tsai, D.-S., Lee, H.-S., Post, L.C., Kreiling, K.M., and Kao, T.-h. (1992). Sequence of an S protein of Lycopersicon peruvianum and comparison with other solanaceous S proteins. Sex. Plant Reprod. 5, 256-263.
34. Whitehouse, K.L.K. (1950). Multiple-allelomorph incompatibility of pollen and style in the evolution of the angiosperms. Ann. Bot. New Ser. 54, 199-216.
35. Xu, B., Mu, J., Nevins, D.L., Grun, P., and Kao, T.-h. (1990). Cloning and sequencing of cDNAs encoding two self-incompatibility associated proteins in Solanum chacoense. Mol. Gen. Genet. 224, 341-346.