Summary
We present a sequence comparison of 12 S-allele-associated proteins from three solanaceous species with gametophytic self-incompatibility: Nicotiana alata, Petunia inflata, and Solanum chacoense. The allelic variants of the S-protein exhibit a very high degree of sequence diversity consistent with their function as recognition molecules. We identify 41 perfectly conserved residues, 18 of which are also conserved in two fungal ribonucleases, RNase T2 and RNase Rh. The residues conserved in both the S-proteins and the ribonucleases include two histidines essential for catalysis, four cysteines involved in disulfide bridges, and hydrophobic residues probably involved in the core structure of the proteins. This conservation between the two ribonucleases and the 12 divergent S-proteins confirms the previously recognized similarity between 3 more closely related N. alata S-proteins and these ribonucleases, and argues strongly for the functional importance of the ribonuclease activity of the S-protein in self-incompatibility. We also identify the 19 most variable residues, which are the prime candidates for the S-allele-specificity determinant. Twelve of these nineteen residues are clustered in two regions of hypervariability, designated HVa and HVb, which are also the most prominent hydrophilic regions of the S-protein. We suggest that these two regions might form parts of the putative pollen recognition site. Identification of these structural features forms a foundation for the study of the molecular basis of self-recognition and the biochemical mechanism of inhibition of self-pollen tube growth.
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Ai Y, Singh A, Coleman CE, Ioerger TR, Kheyr-Pour A, 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
Anderson MA, Cornish EC, Mau S-L, Williams EG, Hoggart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penschow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE (1986) Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompativility in Nicotiana alata. Nature 321:38–44
Anderson MA, McFadden GI, Bernatzky R, Atkinson A, Orpin T, Dedman H, Tregear G, Fernley R, Clarke AE (1989) Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. Plant Cell 1:483–491
Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC (1987) The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329:512–518
Bredemeijer GM, Blass J (1981) S-specific proteins in styles of self-incompatible Nicotiana alata. Theor Appl Genet 59:185–190
Broothaerts WJ, van Laere A, Witters R, Preaux G, Decock B, van Damme J, Vendrig JC (1989) Purification and N-terminal sequencing of style glycoproteins associated with self-incompatibility in Petunia hybrida. Plant Mol Biol 14:93–102
Clark KR, Okuley JJ, Collins PD, Sims TL (1990) Sequence variability and developmental expression of S-alleles in self-incompatible and pseudo-self-compatible petunia. Plant Cell 2:815–826
Dayhoff MO, Schwartz RM, Orcutt BC (1979) A model of evolutionary change in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure vol 5 [Suppl 3] National Biomedical Research Foundation, Washington D.C., pp 345–352
de Nettancourt D (1977) Incompatibility in angiosperms. Springer, Berlin Heidelberg New York
Ebert PR, Anderson MA, Bernatzky R, Altschuler M, Clarke AE (1989) Genetic polymorphism of self-incompatibility in flowering plants. Cell 56:255–262
Gleich GJ, Loegering DA, Bell MP, Checkel JL, Ackerrnan SJ, McKean DJ (1986) Biochemical and functional similarities between human eosinophil-derived neurotoxin and eosinophil cationic protein: Homology with ribonuclease. Proc Natl Acad Sci USA 83:3146–3150
Haring V, Gray JE, McClure BA, Anderson MA, Clarke AE (1990) Self-incompatibility as a model of cell-cell recognition in plants. Science 250:937–941
Horiuchi H, Yanai K, Takagi M, Yano K, Wakabayashi E, Sanda A, Mine S, Ohgi K, Irie M (1988) Primary structure of a base non-specific ribonuclease from Rhizopus niveus. J Biochem 103:408–418
Ioerger TR, Clark AG, Kao T-H (1990) Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Natl Acad Sci USA 87:9732–9735
Jahnen W, Batterham MP, Clarke AE, Moritz RL, Simpson RJ (1989) Identification, isolation, and N-terminal sequencing of style glycoproteins associated with self-incompatibility in Nicotiana alata. Plant Cell 1:493–499
Kamboj RK, Jackson JF (1986) Self-incompatibility alleles control a low molecular weight, basic protein in pistils of Petunia hybrida. Theor Appl Genet 71:815–819
Kawata Y, Sakiyama F, Tamaoki H (1988) Amino-acid sequence of ribonuclease T2 from Aspergillus oryzae. Eur J Biochem 176:683–697
Kheyr-Pour A, Bintrim SB, Ioerger TR, Remy R, Hammond SA. Kao T-H (1990) Sequence diversity of pistil S-proteins associated with gametophytic self-incompatibility in Nicotiana alata. Sex Plant Reprod 3:88–97
Kirch HH, Uhrig H, Lottspeich F, Salamini F, Thompson RD (1989) Characterization of proteins associated with self-incompatibility in Solanum tuberosum. Theor Appl Genet 78:581–588
Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132
Lewis MT, Hunt LT, Barker WC (1989) Striking sequence similarity among sialic acid-binding lectin, pancreatic ribonucleases, and angiogenin: possible structural and functional relationships. Protein Seq Data Anal 2:101–105
Mau S-L, Raff JW, Clarke AE (1982) Isolation and partial characterization of components of Prunus avium L. styles, including an antigenic glycoprotein associated with a self-incompatibility genotype. Planta 156:505–516
Mau S-L, Williams EG, Atkinson A, Anderson MA, Cornish EC, Grego B, Simpson RJ, Kheyr-Pour A, Clarke AE (1986) Style proteins of a wild tomato (Lycopersicon peruvianum) associated with expression of self-incompatibility. Planta 169:184–191
McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342:955–957
Nemethy G, Scheraga HA (1979) A possible folding pathway of bovine pancreatic RNase. Proc Natl Acad Sci USA 76:6050–6054
Shapiro R, Riordan JF, Vallee BL (1986) Characteristic ribonucleolytic activity of human angiogenin. Biochemistry 25:3527–3532
Wright S (1939) The distribution of self-sterility alleles in a population. Genetica 24:538–552
Xu B (1990) Molecular genetics of self-incompatibility in Solanum chacoense. Ph.D. thesis. Pennsylvania State University, University Park, Pa
Xu B, Grun P, Kheyr-Pour A, Kao T-H (1990a) Identification of pistil-specific proteins associated with three self-incompatibility alleles in Solanum chacoense. Sex Plant Reprod 3:54–60
Xu B, Mu J, Nevins DL, Grun P, Kao T-H (1990b) Cloning and sequencing of cDNAs encoding two self-incompatibility associated proteins in Solanum chacoense. Mol Gen Genet 224:341–346
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On sabbatical leave from Biotechnology Center, General Foods USA, Tarrytown, NY 10591, USA
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Ioerger, T.R., Gohlke, J.R., Xu, B. et al. Primary structural features of the self-incompatibility protein in solanaceae. Sexual Plant Reprod 4, 81–87 (1991). https://doi.org/10.1007/BF00196492
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DOI: https://doi.org/10.1007/BF00196492