Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2003 Jun 29;358(1434):1025–1032. doi: 10.1098/rstb.2003.1287

The different mechanisms of gametophytic self-incompatibility.

Vernonica E Franklin-Tong 1, F C H Franklin 1
PMCID: PMC1693207  PMID: 12831468

Abstract

Self-incompatibility (SI) involves the recognition and rejection of self or genetically identical pollen. Gametophytic SI is probably the most widespread of the SI systems and, so far, two completely different SI mechanisms, which appear to have evolved separately, have been identified. One mechanism is the RNase system, which is found in the Solanaceae, Rosaceae and Scrophulariaceae. The other is a complex system, so far found only in the Papaveraceae, which involves the triggering of signal transduction cascade(s) that result in rapid pollen tube inhibition and cell death. Here, we present an overview of what is currently known about the mechanisms involved in controlling pollen tube inhibition in these two systems.

Full Text

The Full Text of this article is available as a PDF (211.2 KB).

Selected References

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

  1. Anderson M. A., McFadden G. I., Bernatzky R., Atkinson A., Orpin T., Dedman H., Tregear G., Fernley R., Clarke A. E. Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. Plant Cell. 1989 May;1(5):483–491. doi: 10.1105/tpc.1.5.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Cooperman B. S., Baykov A. A., Lahti R. Evolutionary conservation of the active site of soluble inorganic pyrophosphatase. Trends Biochem Sci. 1992 Jul;17(7):262–266. doi: 10.1016/0968-0004(92)90406-y. [DOI] [PubMed] [Google Scholar]
  4. Craig K. L., Tyers M. The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol. 1999;72(3):299–328. doi: 10.1016/s0079-6107(99)00010-3. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. D'Silva I., Poirier G. G., Heath M. C. Activation of cysteine proteases in cowpea plants during the hypersensitive response--a form of programmed cell death. Exp Cell Res. 1998 Dec 15;245(2):389–399. doi: 10.1006/excr.1998.4256. [DOI] [PubMed] [Google Scholar]
  7. Foote H. C., Ride J. P., Franklin-Tong V. E., Walker E. A., Lawrence M. J., Franklin F. C. Cloning and expression of a distinctive class of self-incompatibility (S) gene from Papaver rhoeas L. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2265–2269. doi: 10.1073/pnas.91.6.2265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Franklin-Tong V. E., Drobak B. K., Allan A. C., Watkins PAC., Trewavas A. J. Growth of Pollen Tubes of Papaver rhoeas Is Regulated by a Slow-Moving Calcium Wave Propagated by Inositol 1,4,5-Trisphosphate. Plant Cell. 1996 Aug;8(8):1305–1321. doi: 10.1105/tpc.8.8.1305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Franklin-Tong Vernonica E., Holdaway-Clarke Terena L., Straatman Kornelis R., Kunkel Joseph G., Hepler Peter K. Involvement of extracellular calcium influx in the self-incompatibility response of Papaver rhoeas. Plant J. 2002 Feb;29(3):333–345. doi: 10.1046/j.1365-313x.2002.01219.x. [DOI] [PubMed] [Google Scholar]
  10. Frye C. A., Tang D., Innes R. W. Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci U S A. 2001 Jan 2;98(1):373–378. doi: 10.1073/pnas.98.1.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Geitmann A., Snowman B. N., Emons A. M., Franklin-Tong V. E. Alterations in the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas. Plant Cell. 2000 Jul;12(7):1239–1251. doi: 10.1105/tpc.12.7.1239. [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. Gray J. E., McClure B. A., Bonig I., Anderson M. A., Clarke A. E. Action of the Style Product of the Self-Incompatibility Gene of Nicotiana alata (S-RNase) on in Vitro-Grown Pollen Tubes. Plant Cell. 1991 Mar;3(3):271–283. doi: 10.1105/tpc.3.3.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Greenberg J. T., Guo A., Klessig D. F., Ausubel F. M. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell. 1994 May 20;77(4):551–563. doi: 10.1016/0092-8674(94)90217-8. [DOI] [PubMed] [Google Scholar]
  15. Innes R. W. Mapping out the roles of MAP kinases in plant defense. Trends Plant Sci. 2001 Sep;6(9):392–394. doi: 10.1016/s1360-1385(01)02058-1. [DOI] [PubMed] [Google Scholar]
  16. Ioerger T. R., Clark A. G., Kao T. H. Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9732–9735. doi: 10.1073/pnas.87.24.9732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ishimizu T., Miyagi M., Norioka S., Liu Y. H., Clarke A. E., Sakiyama F. Identification of histidine 31 and cysteine 95 in the active site of self-incompatibility associated S6-RNase in Nicotiana alata. J Biochem. 1995 Nov;118(5):1007–1013. doi: 10.1093/jb/118.5.1007. [DOI] [PubMed] [Google Scholar]
  18. Janmey P. A. The cytoskeleton and cell signaling: component localization and mechanical coupling. Physiol Rev. 1998 Jul;78(3):763–781. doi: 10.1152/physrev.1998.78.3.763. [DOI] [PubMed] [Google Scholar]
  19. Joazeiro C. A., Weissman A. M. RING finger proteins: mediators of ubiquitin ligase activity. Cell. 2000 Sep 1;102(5):549–552. doi: 10.1016/s0092-8674(00)00077-5. [DOI] [PubMed] [Google Scholar]
  20. Jordan N. D., Franklin F. C., Franklin-Tong V. E. Evidence for DNA fragmentation triggered in the self-incompatibility response in pollen of Papaver rhoeas. Plant J. 2000 Aug;23(4):471–479. doi: 10.1046/j.1365-313x.2000.00811.x. [DOI] [PubMed] [Google Scholar]
  21. Jordan N. D., Kakeda K., Conner A., Ride J. P., Franklin-Tong V. E., Franklin F. C. S-protein mutants indicate a functional role for SBP in the self-incompatibility reaction of Papaver rhoeas. Plant J. 1999 Oct;20(1):119–125. doi: 10.1046/j.1365-313x.1999.00585.x. [DOI] [PubMed] [Google Scholar]
  22. Kakeda K., Jordan N. D., Conner A., Ride J. P., Franklin-Tong V. E., Franklin F. C. Identification of residues in a hydrophilic loop of the Papaver rhoeas S protein that play a crucial role in recognition of incompatible pollen. Plant Cell. 1998 Oct;10(10):1723–1732. doi: 10.1105/tpc.10.10.1723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kondo Katsuhiko, Yamamoto Mayu, Itahashi Ryoko, Sato Takanori, Egashira Hiroaki, Hattori Tsukaho, Kowyama Yasuo. Insights into the evolution of self-compatibility in Lycopersicon from a study of stylar factors. Plant J. 2002 Apr;30(2):143–153. doi: 10.1046/j.1365-313x.2002.01275.x. [DOI] [PubMed] [Google Scholar]
  24. Korichneva I., Hämmerling U. F-actin as a functional target for retro-retinoids: a potential role in anhydroretinol-triggered cell death. J Cell Sci. 1999 Aug;112(Pt 15):2521–2528. doi: 10.1242/jcs.112.15.2521. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Lam E., Kato N., Lawton M. Programmed cell death, mitochondria and the plant hypersensitive response. Nature. 2001 Jun 14;411(6839):848–853. doi: 10.1038/35081184. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Levine A., Pennell R. I., Alvarez M. E., Palmer R., Lamb C. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol. 1996 Apr 1;6(4):427–437. doi: 10.1016/s0960-9822(02)00510-9. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
  32. 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]
  33. McCubbin A. G., Kao T. Molecular recognition and response in pollen and pistil interactions. Annu Rev Cell Dev Biol. 2000;16:333–364. doi: 10.1146/annurev.cellbio.16.1.333. [DOI] [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. Pennell R. I., Lamb C. Programmed Cell Death in Plants. Plant Cell. 1997 Jul;9(7):1157–1168. doi: 10.1105/tpc.9.7.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rao J. Y., Jin Y. S., Zheng Q., Cheng J., Tai J., Hemstreet G. P., 3rd Alterations of the actin polymerization status as an apoptotic morphological effector in HL-60 cells. J Cell Biochem. 1999 Dec 15;75(4):686–697. [PubMed] [Google Scholar]
  38. Ride J. P., Davies E. M., Franklin F. C., Marshall D. F. Analysis of Arabidopsis genome sequence reveals a large new gene family in plants. Plant Mol Biol. 1999 Mar;39(5):927–932. doi: 10.1023/a:1006178511787. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Rudd J. J., Franklin FCH., Lord J. M., Franklin-Tong V. E. Increased Phosphorylation of a 26-kD Pollen Protein Is Induced by the Self-Incompatibility Response in Papaver rhoeas. Plant Cell. 1996 Apr;8(4):713–724. doi: 10.1105/tpc.8.4.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rudd Jason J., Franklin-Tong Vernonica E. Signals and targets of the self-incompatibility response in pollen of Papaver rhoeas. J Exp Bot. 2003 Jan;54(380):141–148. doi: 10.1093/jxb/erg001. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. 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]
  44. 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]
  45. Snowman Benjamin N., Kovar David R., Shevchenko Galina, Franklin-Tong Vernonica E., Staiger Christopher J. Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. Plant Cell. 2002 Oct;14(10):2613–2626. doi: 10.1105/tpc.002998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Staiger Chris J. SIGNALING TO THE ACTIN CYTOSKELETON IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51(NaN):257–288. doi: 10.1146/annurev.arplant.51.1.257. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. 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]
  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. Walker E. A., Ride J. P., Kurup S., Franklin-Tong V. E., Lawrence M. J., Franklin F. C. Molecular analysis of two functional homologues of the S3 allele of the Papaver rhoeas self-incompatibility gene isolated from different populations. Plant Mol Biol. 1996 Mar;30(5):983–994. doi: 10.1007/BF00020809. [DOI] [PubMed] [Google Scholar]
  51. 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]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES