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Genotype-dependent differences in S12-RNase expression lead to sporadic self-compatibility

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Abstract

Sporadic self-compatibility, the occasional fruit formation after otherwise incompatible pollinations, has been observed in some S 12-containing genotypes of Solanum chacoense but not in others. We have sequenced this S 12 allele and analyzed its expression in four different genotypes. The S12-RNase levels were generally less abundant than those of other S-RNases present in the same plants. In addition, two-fold and five-fold differences in the amount of S12-RNase and S 12 RNA, respectively, were observed among the genotypes analyzed. A comparison with the genetic data showed that genotypes with the highest levels were fully and permanently self-incompatible, whereas those with the lowest levels were those in which sporadic self-compatibility had been observed. The mature protein contains four potential glycosylation sites and genotype-specific differences in the pattern of glycosylation are also observed. Our results suggest the presence of modifier genes which affect, in a genotype-dependent manner, the level of expression and the post-translational modification of the S12-RNase.

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References

  • Ai, Y., Kron, E. and Kao, T. 1991. S-alleles are retained and expressed in a self-compatible cultivar of Petunia hybrida.Mol. Gen. Genet. 230: 353–358.

    Google Scholar 

  • Altschul, S.F., Gish, W., Miller, E.W. and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410.

    Google Scholar 

  • Amit, A., Mariuzaa, R., Phillips, S. and Poljak, R. 1986. Three dimensional structure of an antigen antibody complex at 2.8 Å resolution. Science 233: 747–753

    Google Scholar 

  • Anderson, M. et al. 1989. Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. Plant Cell 1: 483–491.

    Google Scholar 

  • Birhman, R., Laublin, G. and Cappadocia, M. 1994. Genetic control of in vitro shoot regeneration from leaf explants in S. chacoense Bitt. Theor. Appl. Genet. 88: 535–540.

    Google Scholar 

  • Charlesworth, D., Morgan, M. and Charlesworth, B. 1990. Inbreeding depression with heterozygote advantage and its effect on selection for modifiers changing the outcrossing rate. Evolution 44: 870–888.

    Google Scholar 

  • Cipar, M., Peloquin, S. and Hougas, R. 1964. Variability in the expression of self-incompatibility in tuber-bearing diploid Solanum species. Am. Potato J. 41: 155–162.

    Google Scholar 

  • Clark, K., Okuley, J., Collins, P. and Sims, T. 1990. Sequence variability and developmental expression of S-alleles in self-incompatible and pseudo-self-compatible Petunia. Plant Cell 2: 815–826.

    Google Scholar 

  • de Nettancourt, D. 1977. Incompatibility in Angiosperms. Springer-Verlag, New York.

    Google Scholar 

  • de Nettancourt, D. 1997. Incompatibility in angiosperms. Sex. Plant Reprod. 10: 185–199.

    Google Scholar 

  • Gaude, T., Rougier, M., Heizmann, P., Ockendon, D. and Dumas, C. 1995. Expression level of the SLG gene is not correlated with the self-incompatibility phenotype in the class II S haplotypes of Brassica oleracea. Plant Mol. Biol. 27: 1003–1014.

    Google Scholar 

  • Golz, J., Clarke, A., Newbigin, E. and Anderson, M. 1998. A relic S-RNase is expressed in the styles of self-compatible Nicotiana sylvestris. Plant J. 16: 591–599.

    Google Scholar 

  • Golz, J., Su, V., Clarke, A. and Newbegin, E. 1999. A molecular description of mutations affecting the pollen component of the Nicotiana alata S locus. Genetics 152: 1123–1135.

    Google Scholar 

  • Hiratsuka, S., Nakashima, M., Kamasaki, K., Kubo, T. and Kawai, Y. 1999. Comparison of an S-protein expression between self-compatible and-incompatible Japanese pear cultivars. Sex. Plant Reprod. 12: 88–93.

    Google Scholar 

  • Hosaka, K. and Hanneman, R. 1998a. Genetics of self-compatibility in a self-incompatible wild diploid potato species Solanum chacoense. 2. Localization of an S-locus inhibitor (Sli) gene on the potato genome using DNA markers. Euphytica 103: 265–271.

    Google Scholar 

  • Hosaka, K. and Hanneman, R.J. 1998b. Genetics of self-compatibility in self-incompatible wild diploid species. I. Detection of an S-locus inhibitor (Sli) gene. Euphytica 99: 191–197.

    Google Scholar 

  • 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.

    Google Scholar 

  • Jones, J., Dunsmuir, P. and Bedbrook, J. 1985. High level expression of introduced chimeric genes in regenerated transformed plants. EMBO J. 4: 2411–2418.

    Google Scholar 

  • Kao, T.-H. and McCubbin, A. 1996. How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc. Natl. Acad Sci. USA 93: 12059–12065.

    Google Scholar 

  • Kowyama, Y. et al. 1994. Self-compatibility in Lycopersicon peruvianum variant (LA2157) is associated with a lack of style S-RNase activity. Theor. Appl. Genet. 88: 859–864.

    Google Scholar 

  • Leckie, F. et al. 1999. The specificity of polygalacturonase-inhibiting proteins (PGIP): a single amino-acid substitution in the solvent-exposed β-strand/β-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J. 18: 2352–2363.

    Google Scholar 

  • Matton, D.P. et al. 1997. Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9: 1757–1766.

    Google Scholar 

  • Matton, D.P. et al. 1999. 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.

    Google Scholar 

  • McClure, B., Mou, B., Canevascini, S. and Bernatzky, R. 1999. A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc. Natl. Acad. Sci. USA 96: 13548–13553.

    Google Scholar 

  • McCubbin, A. and Kao, T.-H. 1999. The emerging complexity of the self-incompatibility (itS) loci. Sex. Plant Reprod. 12: 1–5.

    Google Scholar 

  • McCubbin, A., Chung, Y. and Kao, T. 1997. A mutant S3 RNase of Petunia inflata lacking RNase activity has an allele-specific dominant negative effect on self-incompatibility.

  • Murfett, J. et al. 1996. S RNase and interspecific pollen rejection in the genus Nicotiana multiple pollen-rejection pathways contribute to unilateral incompatibility between self-incompatible and self-compatible species. Plant Cell 8: 943–958.

    Google Scholar 

  • Nasrallah, M., Kandasamy, M. and Nasrallah, J. 1992. A genetically defined trans-acting locus regulate S-locus function in Brassica. Plant J. 2: 497–506.

    Google Scholar 

  • Oxley, D., Munro, S., Craik, D. and Bacic, A. 1996. Structure of N-glycans on the S 3 and S 6-allele stylar self-incompatability ribonucleases of Nicotiana alata. Glycobiology 6: 611–618.

    Google Scholar 

  • Parry, S. et al. 1998. Structural analysis and molecular of a self-incompatibility RNase from wild tomato. Plant Physiol. 116: 463–469.

    Google Scholar 

  • Pushkarnath. 1942. Studies on sterility in potatoes. 1. The genetics of self-and cross-incompatibilities. Indian J. Genet. Plant Breed. 2: 11–36.

    Google Scholar 

  • Rivard, S.R., Cappadocia, M., Vincent, G., Brisson, N. and Landry, B.S. 1989. Restriction fragment length polymorphism (RFLP) analyses of plants produced by in vitro anther culture of Solanum chacoense Bitt. Theor. Appl. Genet. 78: 49–56.

    Google Scholar 

  • Rivard, S., Saba-El-Leil, M., Landry, B. and Cappadocia, M. 1994. 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.

    Google Scholar 

  • Royo, J., Kowyama, Y. and Clarke, A. 1994. Cloning and nucleotide sequence of two S-RNases from Lycopersico peruvianum (L.) Mill. Plant Physiol. 105: 751–752.

    Google Scholar 

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

    Google Scholar 

  • Sambrook, J., Fritsch, E. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.

    Google Scholar 

  • Sassa, H., Hirano, H. Nishio, T. and Koba, T. 1998. Style-specific self-compatible mutation caused by deletion of the S-RNase gene in Japanese pear (Pyrus serotina). Plant J. 12: 223–227.

    Google Scholar 

  • Schopfer, C., Nasrallah, M. and Nasrallah, J. 1999. The male determinant of self-incompatibility in Brassica. Science 286: 1697–1700.

    Google Scholar 

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

    Google Scholar 

  • Takayama S. et al. 2000. The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl. Acad. Sci. USA 97: 1920–1925.

    Google Scholar 

  • Thompson, R., Uhrig, H., Hermsen, J., Salamini, F. and Kauf-mann, H. 1991. Investigation of a self-compatible mutation in Solanum tuberosum clones inhibiting S-allele activity in pollen differentially. Mol. Gen. Genet. 226: 283–288

    Google Scholar 

  • Tsukamoto, T. et al. 1999. Breakdown of self-incompatibility in a natural population of Petunia axillaris (Solanaceae) in Uruguay containing self-incompatible and self-compatible plants. Sex. Plant Reprod. 12: 6–13.

    Google Scholar 

  • Van Sint Jan, V., Laublin, G., Birhman, R. and Cappadocia, M. 1996. Genetic analysis of leaf explant regenerability in Solanum chacoense. Plant Cell Tissue Org. Cult. 47: 9–13.

    Google Scholar 

  • Woodward, J., Bacic, A., Jahnen, W. and Clarke, A. 1989. N-linked glycan chains on S-allele-associated glycoproteins from Nicotiana alata. Plant Cell 1: 511–514.

    Google Scholar 

  • Xu, B., Grun, P., Kheir-Pour, A. and Kao, T. 1990. Identification of pistil-specific proteins associated with three self-incompatibility alleles in Solanum chacoense. Sex. Plant Reprod. 3: 54–60.

    Google Scholar 

  • Yee, A. and Kronstad, J. 1993. Constructions of chimeric alleles with altered specificity at the b incompatibility locus of Ustilago maydis. Proc. Natl. Acad. Sci. USA 90: 664–668.

    Google Scholar 

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Qin, X., Luu, D., Yang, Q. et al. Genotype-dependent differences in S12-RNase expression lead to sporadic self-compatibility. Plant Mol Biol 45, 295–305 (2001). https://doi.org/10.1023/A:1006445120648

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