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. 2001 Oct;159(2):811–822. doi: 10.1093/genetics/159.2.811

Intrahaplotype polymorphism at the Brassica S locus.

C Miege 1, V Ruffio-Châble 1, M H Schierup 1, D Cabrillac 1, C Dumas 1, T Gaude 1, J M Cock 1
PMCID: PMC1461823  PMID: 11606555

Abstract

The S locus receptor kinase and the S locus glycoproteins are encoded by genes located at the S locus, which controls the self-incompatibility response in Brassica. In class II self-incompatibility haplotypes, S locus glycoproteins can be encoded by two different genes, SLGA and SLGB. In this study, we analyzed the sequences of these genes in several independently isolated plants, all of which carry the same S haplotype (S(2)). Two groups of S(2) haplotypes could be distinguished depending on whether SRK was associated with SLGA or SLGB. Surprisingly, SRK alleles from the two groups could be distinguished at the sequence level, suggesting that recombination rarely occurs between haplotypes of the two groups. An analysis of the distribution of polymorphisms along the S domain of SRK showed that hypervariable domains I and II tend to be conserved within haplotypes but to be highly variable between haplotypes. This is consistent with these domains playing a role in the determination of haplotype specificity.

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Selected References

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  1. Awadalla P., Charlesworth D. Recombination and selection at Brassica self-incompatibility loci. Genetics. 1999 May;152(1):413–425. doi: 10.1093/genetics/152.1.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boyes D. C., Nasrallah J. B. An anther-specific gene encoded by an S locus haplotype of Brassica produces complementary and differentially regulated transcripts. Plant Cell. 1995 Aug;7(8):1283–1294. doi: 10.1105/tpc.7.8.1283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boyes D. C., Nasrallah J. B. Physical linkage of the SLG and SRK genes at the self-incompatibility locus of Brassica oleracea. Mol Gen Genet. 1993 Jan;236(2-3):369–373. doi: 10.1007/BF00277135. [DOI] [PubMed] [Google Scholar]
  4. Cabrillac D., Delorme V., Garin J., Ruffio-Châble V., Giranton J. L., Dumas C., Gaude T., Cock J. M. The S15 self-incompatibility haplotype in Brassica oleracea includes three S gene family members expressed in stigmas. Plant Cell. 1999 May;11(5):971–986. doi: 10.1105/tpc.11.5.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Delorme V., Giranton J. L., Hatzfeld Y., Friry A., Heizmann P., Ariza M. J., Dumas C., Gaude T., Cock J. M. Characterization of the S locus genes, SLG and SRK, of the Brassica S3 haplotype: identification of a membrane-localized protein encoded by the S locus receptor kinase gene. Plant J. 1995 Mar;7(3):429–440. doi: 10.1046/j.1365-313x.1995.7030429.x. [DOI] [PubMed] [Google Scholar]
  7. Dixit R., Nasrallah M. E., Nasrallah J. B. Post-transcriptional maturation of the S receptor kinase of Brassica correlates with co-expression of the S-locus glycoprotein in the stigmas of two Brassica strains and in transgenic tobacco plants. Plant Physiol. 2000 Sep;124(1):297–311. doi: 10.1104/pp.124.1.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Doughty J., Dixon S., Hiscock S. J., Willis A. C., Parkin I. A., Dickinson H. G. PCP-A1, a defensin-like Brassica pollen coat protein that binds the S locus glycoprotein, is the product of gametophytic gene expression. Plant Cell. 1998 Aug;10(8):1333–1347. doi: 10.1105/tpc.10.8.1333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dwyer K. G., Balent M. A., Nasrallah J. B., Nasrallah M. E. DNA sequences of self-incompatibility genes from Brassica campestris and B. oleracea: polymorphism predating speciation. Plant Mol Biol. 1991 Mar;16(3):481–486. doi: 10.1007/BF00024000. [DOI] [PubMed] [Google Scholar]
  10. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gaude T., Denoroy L., Dumas C. Use of a fast protein electrophoretic purification procedure for N-terminal sequence analysis to identify S-locus related proteins in stigmas of Brassica oleracea. Electrophoresis. 1991 Sep;12(9):646–653. doi: 10.1002/elps.1150120909. [DOI] [PubMed] [Google Scholar]
  12. Gaude T., Friry A., Heizmann P., Mariac C., Rougier M., Fobis I., Dumas C. Expression of a self-incompatibility gene in a self-compatible line of Brassica oleracea. Plant Cell. 1993 Jan;5(1):75–86. doi: 10.1105/tpc.5.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gaude T., Rougier M., Heizmann P., Ockendon D. J., Dumas C. 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. 1995 Mar;27(5):1003–1014. doi: 10.1007/BF00037027. [DOI] [PubMed] [Google Scholar]
  14. Giranton J. L., Ariza M. J., Dumas C., Cock J. M., Gaude T. The S locus receptor kinase gene encodes a soluble glycoprotein corresponding to the SKR extracellular domain in Brassica oleracea. Plant J. 1995 Dec;8(6):827–834. doi: 10.1046/j.1365-313x.1995.8060827.x. [DOI] [PubMed] [Google Scholar]
  15. Goring D. R., Glavin T. L., Schafer U., Rothstein S. J. An S receptor kinase gene in self-compatible Brassica napus has a 1-bp deletion. Plant Cell. 1993 May;5(5):531–539. doi: 10.1105/tpc.5.5.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hatakeyama K., Takasaki T., Watanabe M., Hinata K. Molecular characterization of S locus genes, SLG and SRK, in a pollen-recessive self-incompatibility haplotype of Brassica rapa L. Genetics. 1998 Jul;149(3):1587–1597. doi: 10.1093/genetics/149.3.1587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hudson R. R., Kreitman M., Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. doi: 10.1093/genetics/116.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Kusaba M., Matsushita M., Okazaki K., Satta Y., Nishio T. Sequence and structural diversity of the S locus genes from different lines with the same self-recognition specificities in Brassica oleracea. Genetics. 2000 Jan;154(1):413–420. doi: 10.1093/genetics/154.1.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kusaba M., Nishio T., Satta Y., Hinata K., Ockendon D. Striking sequence similarity in inter- and intra-specific comparisons of class I SLG alleles from Brassica oleracea and Brassica campestris: implications for the evolution and recognition mechanism. Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7673–7678. doi: 10.1073/pnas.94.14.7673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Luu D. T., Heizmann P., Dumas C. Pollen-Stigma Adhesion in Kale Is Not Dependent on the Self-(In)Compatibility Genotype. Plant Physiol. 1997 Nov;115(3):1221–1230. doi: 10.1104/pp.115.3.1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Luu D. T., Marty-Mazars D., Trick M., Dumas C., Heizmann P. Pollen-stigma adhesion in Brassica spp involves SLG and SLR1 glycoproteins. Plant Cell. 1999 Feb;11(2):251–262. doi: 10.1105/tpc.11.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Nasrallah J. B. Cell-cell signaling in the self-incompatibility response. Curr Opin Plant Biol. 2000 Oct;3(5):368–373. doi: 10.1016/s1369-5266(00)00098-4. [DOI] [PubMed] [Google Scholar]
  25. Parniske M., Jones J. D. Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family. Proc Natl Acad Sci U S A. 1999 May 11;96(10):5850–5855. doi: 10.1073/pnas.96.10.5850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pastuglia M., Roby D., Dumas C., Cock J. M. Rapid induction by wounding and bacterial infection of an S gene family receptor-like kinase gene in Brassica oleracea. Plant Cell. 1997 Jan;9(1):49–60. doi: 10.1105/tpc.9.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. doi: 10.1093/bioinformatics/15.2.174. [DOI] [PubMed] [Google Scholar]
  28. Sakamoto K., Kusaba M., Nishio T. Polymorphism of the S-locus glycoprotein gene (SLG) and the S-locus related gene (SLR1) in Raphanus sativus L. and self-incompatible ornamental plants in the Brassicaceae. Mol Gen Genet. 1998 May;258(4):397–403. doi: 10.1007/s004380050747. [DOI] [PubMed] [Google Scholar]
  29. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schopfer C. R., Nasrallah M. E., Nasrallah J. B. The male determinant of self-incompatibility in Brassica. Science. 1999 Nov 26;286(5445):1697–1700. doi: 10.1126/science.286.5445.1697. [DOI] [PubMed] [Google Scholar]
  31. Scutt C. P., Croy R. R. An S5 self-incompatibility allele-specific cDNA sequence from Brassica oleracea shows high homology to the SLR2 gene. Mol Gen Genet. 1992 Mar;232(2):240–246. doi: 10.1007/BF00280002. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Suzuki G., Kai N., Hirose T., Fukui K., Nishio T., Takayama S., Isogai A., Watanabe M., Hinata K. Genomic organization of the S locus: Identification and characterization of genes in SLG/SRK region of S(9) haplotype of Brassica campestris (syn. rapa). Genetics. 1999 Sep;153(1):391–400. doi: 10.1093/genetics/153.1.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Suzuki G., Watanabe M., Isogai A., Hinata K. Highly conserved 5'-flanking regions of two self-incompatibility genes, SLG9 and SRK9. Gene. 1997 May 20;191(1):123–126. doi: 10.1016/s0378-1119(97)00043-7. [DOI] [PubMed] [Google Scholar]
  35. Takasaki T., Hatakeyama K., Suzuki G., Watanabe M., Isogai A., Hinata K. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature. 2000 Feb 24;403(6772):913–916. doi: 10.1038/35002628. [DOI] [PubMed] [Google Scholar]
  36. Takayama S., Shiba H., Iwano M., Shimosato H., Che F. S., Kai N., Watanabe M., Suzuki G., Hinata K., Isogai A. The pollen determinant of self-incompatibility in Brassica campestris. Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1920–1925. doi: 10.1073/pnas.040556397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tantikanjana T., Nasrallah M. E., Stein J. C., Chen C. H., Nasrallah J. B. An alternative transcript of the S locus glycoprotein gene in a class II pollen-recessive self-incompatibility haplotype of Brassica oleracea encodes a membrane-anchored protein. Plant Cell. 1993 Jun;5(6):657–666. doi: 10.1105/tpc.5.6.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Toriyama K., Thorsness M. K., Nasrallah J. B., Nasrallah M. E. A Brassica S locus gene promoter directs sporophytic expression in the anther tapetum of transgenic Arabidopsis. Dev Biol. 1991 Feb;143(2):427–431. doi: 10.1016/0012-1606(91)90094-j. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Watanabe M., Takasaki T., Toriyama K., Yamakawa S., Isogai A., Suzuki A., Hinata K. A high degree of homology exists between the protein encoded by SLG and the S receptor domain encoded by SRK in self-incompatible Brassica campestris L. Plant Cell Physiol. 1994 Dec;35(8):1221–1229. doi: 10.1093/oxfordjournals.pcp.a078716. [DOI] [PubMed] [Google Scholar]
  41. 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]

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