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. 2004 Mar 9;16(Suppl):S72–S83. doi: 10.1105/tpc.016154

The molecular and genetic bases of S-RNase-based self-incompatibility.

Teh-hui Kao 1, Tatsuya Tsukamoto 1
PMCID: PMC2643390  PMID: 15010517

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Selected References

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

  1. Ai Y. J., Kron E., Kao T. H. S-alleles are retained and expressed in a self-compatible cultivar of Petunia hybrida. Mol Gen Genet. 1991 Dec;230(3):353–358. doi: 10.1007/BF00280291. [DOI] [PubMed] [Google Scholar]
  2. Bai C., Sen P., Hofmann K., Ma L., Goebl M., Harper J. W., Elledge S. J. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell. 1996 Jul 26;86(2):263–274. doi: 10.1016/s0092-8674(00)80098-7. [DOI] [PubMed] [Google Scholar]
  3. Bernatzky R., Glaven R. H., Rivers B. A. S-related protein can be recombined with self-compatibility in interspecific derivatives of Lycopersicon. Biochem Genet. 1995 Aug;33(7-8):215–225. [PubMed] [Google Scholar]
  4. Cenciarelli C., Chiaur D. S., Guardavaccaro D., Parks W., Vidal M., Pagano M. Identification of a family of human F-box proteins. Curr Biol. 1999 Oct 21;9(20):1177–1179. doi: 10.1016/S0960-9822(00)80020-2. [DOI] [PubMed] [Google Scholar]
  5. Cheung A. Y., May B., Kawata E. E., Gu Q., Wu H. M. Characterization of cDNAs for stylar transmitting tissue-specific proline-rich proteins in tobacco. Plant J. 1993 Jan;3(1):151–160. [PubMed] [Google Scholar]
  6. Clark K. R., Okuley J. J., Collins P. D., Sims T. L. Sequence variability and developmental expression of S-alleles in self-incompatible and pseudo-self-compatible petunia. Plant Cell. 1990 Aug;2(8):815–826. doi: 10.1105/tpc.2.8.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cruz-Garcia Felipe, Hancock C. Nathan, McClure Bruce. S-RNase complexes and pollen rejection. J Exp Bot. 2003 Jan;54(380):123–130. doi: 10.1093/jxb/erg045. [DOI] [PubMed] [Google Scholar]
  8. East E. M., Mangelsdorf A. J. A New Interpretation of the Hereditary Behavior of Self-Sterile Plants. Proc Natl Acad Sci U S A. 1925 Feb;11(2):166–171. doi: 10.1073/pnas.11.2.166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Entani Tetsuyuki, Iwano Megumi, Shiba Hiroshi, Che Fang-Sik, Isogai Akira, Takayama Seiji. Comparative analysis of the self-incompatibility (S-) locus region of Prunus mume: identification of a pollen-expressed F-box gene with allelic diversity. Genes Cells. 2003 Mar;8(3):203–213. doi: 10.1046/j.1365-2443.2003.00626.x. [DOI] [PubMed] [Google Scholar]
  10. Golz J. F., Clarke A. E., Newbigin E., Anderson M. A relic S-RNase is expressed in the styles of self-compatible Nicotiana sylvestris. Plant J. 1998 Dec;16(5):591–599. doi: 10.1046/j.1365-313x.1998.00331.x. [DOI] [PubMed] [Google Scholar]
  11. Golz J. F., Oh H. Y., Su V., Kusaba M., Newbigin E. Genetic analysis of Nicotiana pollen-part mutants is consistent with the presence of an S-ribonuclease inhibitor at the S locus. Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15372–15376. doi: 10.1073/pnas.261571598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Golz J. F., Su V., Clarke A. E., Newbigin E. A molecular description of mutations affecting the pollen component of the Nicotiana alata S locus. Genetics. 1999 Jul;152(3):1123–1135. doi: 10.1093/genetics/152.3.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Ida K., Norioka S., Yamamoto M., Kumasaka T., Yamashita E., Newbigin E., Clarke A. E., Sakiyama F., Sato M. The 1.55 A resolution structure of Nicotiana alata S(F11)-RNase associated with gametophytic self-incompatibility. J Mol Biol. 2001 Nov 16;314(1):103–112. doi: 10.1006/jmbi.2001.5127. [DOI] [PubMed] [Google Scholar]
  15. Igic B., Kohn J. R. Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci U S A. 2001 Nov 6;98(23):13167–13171. doi: 10.1073/pnas.231386798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ishimizu T., Endo T., Yamaguchi-Kabata Y., Nakamura K. T., Sakiyama F., Norioka S. Identification of regions in which positive selection may operate in S-RNase of Rosaceae: implication for S-allele-specific recognition sites in S-RNase. FEBS Lett. 1998 Dec 4;440(3):337–342. doi: 10.1016/s0014-5793(98)01470-7. [DOI] [PubMed] [Google Scholar]
  17. Ishimizu T., Sato Y., Saito T., Yoshimura Y., Norioka S., Nakanishi T., Sakiyama F. Identification and partial amino acid sequences of seven S-RNases associated with self-incompatibility of Japanese pear, Pyrus pyrifolia Nakai. J Biochem. 1996 Aug;120(2):326–334. doi: 10.1093/oxfordjournals.jbchem.a021417. [DOI] [PubMed] [Google Scholar]
  18. Kachroo Aardra, Nasrallah Mikhail E., Nasrallah June B. Self-incompatibility in the Brassicaceae: receptor-ligand signaling and cell-to-cell communication. Plant Cell. 2002;14 (Suppl):S227–S238. doi: 10.1105/tpc.010440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Kawata Y., Sakiyama F., Tamaoki H. Amino-acid sequence of ribonuclease T2 from Aspergillus oryzae. Eur J Biochem. 1988 Oct 1;176(3):683–697. doi: 10.1111/j.1432-1033.1988.tb14331.x. [DOI] [PubMed] [Google Scholar]
  22. Kondo Katsuhiko, Yamamoto Mayu, Matton Daniel P., Sato Takanori, Hirai Masashi, Norioka Shigemi, Hattori Tsukaho, Kowyama Yasuo. Cultivated tomato has defects in both S-RNase and HT genes required for stylar function of self-incompatibility. Plant J. 2002 Mar;29(5):627–636. doi: 10.1046/j.0960-7412.2001.01245.x. [DOI] [PubMed] [Google Scholar]
  23. Lai Zhao, Ma Wenshi, Han Bin, Liang Lizhi, Zhang Yansheng, Hong Guofan, Xue Yongbiao. An F-box gene linked to the self-incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol Biol. 2002 Sep;50(1):29–42. doi: 10.1023/a:1016050018779. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Luu D. T., Qin X., Laublin G., Yang Q., Morse D., Cappadocia M. Rejection of S-heteroallelic pollen by a dual-specific s-RNase in Solanum chacoense predicts a multimeric SI pollen component. Genetics. 2001 Sep;159(1):329–335. doi: 10.1093/genetics/159.1.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Luu D. T., Qin X., Morse D., Cappadocia M. S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature. 2000 Oct 5;407(6804):649–651. doi: 10.1038/35036623. [DOI] [PubMed] [Google Scholar]
  27. Martin F W. The Inheritance of Self-Incompatibility in Hybrids of Lycopersicon Esculentum Mill. x L. Chilense Dun. Genetics. 1961 Nov;46(11):1443–1454. doi: 10.1093/genetics/46.11.1443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Matsuura T., Sakai H., Unno M., Ida K., Sato M., Sakiyama F., Norioka S. Crystal structure at 1.5-A resolution of Pyrus pyrifolia pistil ribonuclease responsible for gametophytic self-incompatibility. J Biol Chem. 2001 Sep 27;276(48):45261–45269. doi: 10.1074/jbc.M107617200. [DOI] [PubMed] [Google Scholar]
  29. Matton D. P., Luu D. T., Xike Q., Laublin G., O'Brien M., Maes O., Morse D., Cappadocia M. Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles. Plant Cell. 1999 Nov;11(11):2087–2097. doi: 10.1105/tpc.11.11.2087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Matton D. P., Maes O., Laublin G., Xike Q., Bertrand C., Morse D., Cappadocia M. Hypervariable Domains of Self-Incompatibility RNases Mediate Allele-Specific Pollen Recognition. Plant Cell. 1997 Oct;9(10):1757–1766. doi: 10.1105/tpc.9.10.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. McClure B., Mou B., Canevascini S., Bernatzky R. A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13548–13553. doi: 10.1073/pnas.96.23.13548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. McCubbin A. G., Wang X., Kao T. H. Identification of self-incompatibility (S-) locus linked pollen cDNA markers in Petunia inflata. Genome. 2000 Aug;43(4):619–627. [PubMed] [Google Scholar]
  34. 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]
  35. Murfett J., Strabala T. J., Zurek D. M., Mou B., Beecher B., McClure B. A. 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. 1996 Jun;8(6):943–958. doi: 10.1105/tpc.8.6.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. O'Brien M., Kapfer C., Major G., Laurin M., Bertrand C., Kondo K., Kowyama Y., Matton D. P. Molecular analysis of the stylar-expressed Solanum chacoense small asparagine-rich protein family related to the HT modifier of gametophytic self-incompatibility in Nicotiana. Plant J. 2002 Dec;32(6):985–996. doi: 10.1046/j.1365-313x.2002.01486.x. [DOI] [PubMed] [Google Scholar]
  37. Richman A. D., Kao T. H., Schaeffer S. W., Uyenoyama M. K. S-allele sequence diversity in natural populations of Solanum carolinense (Horsenettle). Heredity (Edinb) 1995 Oct;75(Pt 4):405–415. doi: 10.1038/hdy.1995.153. [DOI] [PubMed] [Google Scholar]
  38. Royo J., Kunz C., Kowyama Y., Anderson M., Clarke A. E., Newbigin E. 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 U S A. 1994 Jul 5;91(14):6511–6514. doi: 10.1073/pnas.91.14.6511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Sims T. L., Ordanic M. Identification of a S-ribonuclease-binding protein in Petunia hybrida. Plant Mol Biol. 2001 Dec;47(6):771–783. doi: 10.1023/a:1013639528858. [DOI] [PubMed] [Google Scholar]
  41. Singh A., Ai Y., Kao T. H. Characterization of Ribonuclease Activity of Three S-Allele-Associated Proteins of Petunia inflata. Plant Physiol. 1991 May;96(1):61–68. doi: 10.1104/pp.96.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Takebayashi Naoki, Brewer Philip B., Newbigin Ed, Uyenoyama Marcy K. Patterns of variation within self-incompatibility loci. Mol Biol Evol. 2003 Jul 28;20(11):1778–1794. doi: 10.1093/molbev/msg209. [DOI] [PubMed] [Google Scholar]
  43. Thomas Steve, Osman Kim, de Graaf Barend H. J., Shevchenko Galina, Wheeler Mike, Franklin Chris, Franklin-Tong Noni. Investigating mechanisms involved in the self-incompatibility response in Papaver rhoeas. Philos Trans R Soc Lond B Biol Sci. 2003 Jun 29;358(1434):1033–1036. doi: 10.1098/rstb.2003.1288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Thompson R. D., Kirch H. H. The S locus of flowering plants: when self-rejection is self-interest. Trends Genet. 1992 Nov;8(11):381–387. doi: 10.1016/0168-9525(92)90299-j. [DOI] [PubMed] [Google Scholar]
  45. Tyers M., Jorgensen P. Proteolysis and the cell cycle: with this RING I do thee destroy. Curr Opin Genet Dev. 2000 Feb;10(1):54–64. doi: 10.1016/s0959-437x(99)00049-0. [DOI] [PubMed] [Google Scholar]
  46. Ushijima K., Sassa H., Tamura M., Kusaba M., Tao R., Gradziel T. M., Dandekar A. M., Hirano H. Characterization of the S-locus region of almond (Prunus dulcis): analysis of a somaclonal mutant and a cosmid contig for an S haplotype. Genetics. 2001 May;158(1):379–386. doi: 10.1093/genetics/158.1.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Ushijima K., Sassa H., Tao R., Yamane H., Dandekar A. M., Gradziel T. M., Hirano H. Cloning and characterization of cDNAs encoding S-RNases from almond (Prunus dulcis): primary structural features and sequence diversity of the S-RNases in Rosaceae. Mol Gen Genet. 1998 Nov;260(2-3):261–268. doi: 10.1007/s004380050894. [DOI] [PubMed] [Google Scholar]
  48. Ushijima Koichiro, Sassa Hidenori, Dandekar Abhaya M., Gradziel Thomas M., Tao Ryutaro, Hirano Hisashi. Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-box gene with haplotype-specific polymorphism. Plant Cell. 2003 Mar;15(3):771–781. doi: 10.1105/tpc.009290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Verica J. A., McCubbin A. G., Kao T. Are the hypervariable regions of S RNases sufficient for allele-specific recognition of pollen? Plant Cell. 1998 Mar;10(3):314–317. [PMC free article] [PubMed] [Google Scholar]
  50. Wang X., Hughes A. L., Tsukamoto T., Ando T., Kao T. Evidence that intragenic recombination contributes to allelic diversity of the S-RNase gene at the self-incompatibility (S) locus in Petunia inflata. Plant Physiol. 2001 Feb;125(2):1012–1022. doi: 10.1104/pp.125.2.1012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Wu H. M., Wang H., Cheung A. Y. A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell. 1995 Aug 11;82(3):395–403. doi: 10.1016/0092-8674(95)90428-x. [DOI] [PubMed] [Google Scholar]
  52. Xue Y., Carpenter R., Dickinson H. G., Coen E. S. Origin of allelic diversity in antirrhinum S locus RNases. Plant Cell. 1996 May;8(5):805–814. doi: 10.1105/tpc.8.5.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Yamane Hisayo, Ikeda Kazuo, Ushijima Koichiro, Sassa Hidenori, Tao Ryutaro. A pollen-expressed gene for a novel protein with an F-box motif that is very tightly linked to a gene for S-RNase in two species of cherry, Prunus cerasus and P. avium. Plant Cell Physiol. 2003 Jul;44(7):764–769. doi: 10.1093/pcp/pcg088. [DOI] [PubMed] [Google Scholar]
  54. 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]
  55. de Graaf B. H. J., Knuiman B. A., Derksen J., Mariani C. Characterization and localization of the transmitting tissue-specific PELPIII proteins of Nicotiana tabacum. J Exp Bot. 2003 Jan;54(380):55–63. doi: 10.1093/jxb/erg002. [DOI] [PubMed] [Google Scholar]

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