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. 1996 May;8(5):805–814. doi: 10.1105/tpc.8.5.805

Origin of allelic diversity in antirrhinum S locus RNases.

Y Xue 1, R Carpenter 1, H G Dickinson 1, E S Coen 1
PMCID: PMC161139  PMID: 8672882

Abstract

In many plant species, self-incompatibility (SI) is genetically controlled by a single multiallelic S locus. Previous analysis of S alleles in the Solanaceae, in which S locus ribonucleases (S RNases) are responsible for stylar expression of SI, has demonstrated that allelic diversity predated speciation within this family. To understand how allelic diversity has evolved, we investigated the molecular basis of gametophytic SI in Antirrhinum, a member of the Scrophulariaceae, which is closely related to the Solanaceae. We have characterized three Antirrhinum cDNAs encoding polypeptides homologous to S RNases and shown that they are encoded by genes at the S locus. RNA in situ hybridization revealed that the Antirrhinum S RNase are primarily expressed in the stylar transmitting tissue. This expression is consistent with their proposed role in arresting the growth of self-pollen tubes. S alleles from the Scrophulariaceae form a separate group from those of the Solanaceae, indicating that new S alleles have been generated since these families separated (approximately 40 million years). We propose that the recruitment of an ancestral RNase gene into SI occurred during an early stage of angiosperm evolution and that, since that time, new alleles subsequently have arisen at a low rate.

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Selected References

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  1. Ai Y., Tsai D. S., Kao T. H. Cloning and sequencing of cDNAs encoding two S proteins of a self-compatible cultivar of Petunia hybrida. Plant Mol Biol. 1992 Jun;19(3):523–528. doi: 10.1007/BF00023404. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Aranda A., Toro M. J., Usera F., Pascual A. Regulation by butyrate of the cAMP response to cholera toxin and forskolin in pituitary GH1 cells. Eur J Biochem. 1990 Feb 14;187(3):683–689. doi: 10.1111/j.1432-1033.1990.tb15354.x. [DOI] [PubMed] [Google Scholar]
  4. Baldwin T. C., Coen E. S., Dickinson H. G. The ptl1 gene expressed in the transmitting tissue of Antirrhinum encodes an extensin-like protein. Plant J. 1992 Sep;2(5):733–739. doi: 10.1046/j.1365-313x.1992.t01-14-00999.x. [DOI] [PubMed] [Google Scholar]
  5. Bariola P. A., Howard C. J., Taylor C. B., Verburg M. T., Jaglan V. D., Green P. J. The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J. 1994 Nov;6(5):673–685. doi: 10.1046/j.1365-313x.1994.6050673.x. [DOI] [PubMed] [Google Scholar]
  6. Broothaerts W., Janssens G. A., Proost P., Broekaert W. F. cDNA cloning and molecular analysis of two self-incompatibility alleles from apple. Plant Mol Biol. 1995 Feb;27(3):499–511. doi: 10.1007/BF00019317. [DOI] [PubMed] [Google Scholar]
  7. Chung I. K., Ito T., Tanaka H., Ohta A., Nan H. G., Takagi M. Molecular diversity of three S-allele cDNAs associated with gametophytic self-incompatibility in Lycopersicon peruvianum. Plant Mol Biol. 1994 Oct;26(2):757–762. doi: 10.1007/BF00013760. [DOI] [PubMed] [Google Scholar]
  8. Clark A. G., Kao T. H. Excess nonsynonymous substitution of shared polymorphic sites among self-incompatibility alleles of Solanaceae. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9823–9827. doi: 10.1073/pnas.88.21.9823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Coen E. S., Carpenter R., Martin C. Transposable elements generate novel spatial patterns of gene expression in Antirrhinum majus. Cell. 1986 Oct 24;47(2):285–296. doi: 10.1016/0092-8674(86)90451-4. [DOI] [PubMed] [Google Scholar]
  11. Coen E. S., Romero J. M., Doyle S., Elliott R., Murphy G., Carpenter R. floricaula: a homeotic gene required for flower development in antirrhinum majus. Cell. 1990 Dec 21;63(6):1311–1322. doi: 10.1016/0092-8674(90)90426-f. [DOI] [PubMed] [Google Scholar]
  12. Hinata K., Watanabe M., Yamakawa S., Satta Y., Isogai A. Evolutionary aspects of the S-related genes of the Brassica self-incompatibility system: synonymous and nonsynonymous base substitutions. Genetics. 1995 Jul;140(3):1099–1104. doi: 10.1093/genetics/140.3.1099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Horiuchi H., Yanai K., Takagi M., Yano K., Wakabayashi E., Sanda A., Mine S., Ohgi K., Irie M. Primary structure of a base non-specific ribonuclease from Rhizopus niveus. J Biochem. 1988 Mar;103(3):408–418. doi: 10.1093/oxfordjournals.jbchem.a122284. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Ide H., Kimura M., Arai M., Funatsu G. The complete amino acid sequence of ribonuclease from the seeds of bitter gourd (Momordica charantia). FEBS Lett. 1991 Jun 24;284(2):161–164. doi: 10.1016/0014-5793(91)80675-s. [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. Jost W., Bak H., Glund K., Terpstra P., Beintema J. J. Amino acid sequence of an extracellular, phosphate-starvation-induced ribonuclease from cultured tomato (Lycopersicon esculentum) cells. Eur J Biochem. 1991 May 23;198(1):1–6. doi: 10.1111/j.1432-1033.1991.tb15978.x. [DOI] [PubMed] [Google Scholar]
  18. Kandasamy M. K., Dwyer K. G., Paolillo D. J., Doney R. C., Nasrallah J. B., Nasrallah M. E. Brassica S-Proteins Accumulate in the Intercellular Matrix along the Path of Pollen Tubes in Transgenic Tobacco Pistils. Plant Cell. 1990 Jan;2(1):39–49. doi: 10.1105/tpc.2.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kaufmann H., Salamini F., Thompson R. D. Sequence variability and gene structure at the self-incompatibility locus of Solanum tuberosum. Mol Gen Genet. 1991 May;226(3):457–466. doi: 10.1007/BF00260659. [DOI] [PubMed] [Google Scholar]
  20. LEWIS D. Structure of the incompatibility gene; induced mutation rate. Heredity (Edinb) 1949 Dec;3(3):339–355. doi: 10.1038/hdy.1949.25. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Lee H. S., Singh A., Kao T. RNase X2, a pistil-specific ribonuclease from Petunia inflata, shares sequence similarity with solanaceous S proteins. Plant Mol Biol. 1992 Dec;20(6):1131–1141. doi: 10.1007/BF00028899. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Moore H. M., Nasrallah J. B. A Brassica Self-Incompatibility Gene Is Expressed in the Stylar Transmitting Tissue of Transgenic Tobacco. Plant Cell. 1990 Jan;2(1):29–38. doi: 10.1105/tpc.2.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Nasrallah J. B., Stein J. C., Kandasamy M. K., Nasrallah M. E. Signaling the arrest of pollen tube development in self-incompatible plants. Science. 1994 Dec 2;266(5190):1505–1508. doi: 10.1126/science.266.5190.1505. [DOI] [PubMed] [Google Scholar]
  27. Rivers B. A., Bernatzky R., Robinson S. J., Jahnen-Dechent W. Molecular diversity at the self-incompatibility locus is a salient feature in natural populations of wild tomato (Lycopersicon peruvianum). Mol Gen Genet. 1993 Apr;238(3):419–427. doi: 10.1007/BF00292001. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Saba-el-Leil M. K., Rivard S., Morse D., Cappadocia M. The S11 and S13 self incompatibility alleles in Solanum chacoense Bitt. are remarkably similar. Plant Mol Biol. 1994 Feb;24(4):571–583. doi: 10.1007/BF00023555. [DOI] [PubMed] [Google Scholar]
  30. Stein J. C., Howlett B., Boyes D. C., Nasrallah M. E., Nasrallah J. B. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8816–8820. doi: 10.1073/pnas.88.19.8816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Taylor C. B., Bariola P. A., delCardayré S. B., Raines R. T., Green P. J. RNS2: a senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5118–5122. doi: 10.1073/pnas.90.11.5118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Uyenoyama M. K. A generalized least-squares estimate for the origin of sporophytic self-incompatibility. Genetics. 1995 Feb;139(2):975–992. doi: 10.1093/genetics/139.2.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Watanabe H., Naitoh A., Suyama Y., Inokuchi N., Shimada H., Koyama T., Ohgi K., Irie M. Primary structure of a base non-specific and adenylic acid preferential ribonuclease from Aspergillus saitoi. J Biochem. 1990 Aug;108(2):303–310. doi: 10.1093/oxfordjournals.jbchem.a123198. [DOI] [PubMed] [Google Scholar]
  34. Waye M. M., Verhoeyen M. E., Jones P. T., Winter G. EcoK selection vectors for shotgun cloning into M13 and deletion mutagenesis. Nucleic Acids Res. 1985 Dec 9;13(23):8561–8571. doi: 10.1093/nar/13.23.8561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wright S. The Distribution of Self-Sterility Alleles in Populations. Genetics. 1939 Jun;24(4):538–552. doi: 10.1093/genetics/24.4.538. [DOI] [PMC free article] [PubMed] [Google Scholar]

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