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. 1999 May;11(5):971–986. doi: 10.1105/tpc.11.5.971

The S15 self-incompatibility haplotype in Brassica oleracea includes three S gene family members expressed in stigmas.

D Cabrillac 1, V Delorme 1, J Garin 1, V Ruffio-Châble 1, J L Giranton 1, C Dumas 1, T Gaude 1, J M Cock 1
PMCID: PMC144233  PMID: 10330480

Abstract

Self-incompatibility in Brassica is controlled by a single, highly polymorphic locus that extends over several hundred kilobases and includes several expressed genes. Two stigma proteins, the S locus receptor kinase (SRK) and the S locus glycoprotein (SLG), are encoded by genes located at the S locus and are thought to be involved in the recognition of self-pollen by the stigma. We report here that two different SLG genes, SLGA and SLGB, are located at the S locus in the class II, pollen-recessive S15 haplotype. Both genes are interrupted by a single intron; however, SLGA encodes both soluble and membrane-anchored forms of SLG, whereas SLGB encodes only soluble SLG proteins. Thus, including SRK, the S locus in the S15 haplotype contains at least three members of the S gene family. The protein products of these three genes have been characterized, and each SLG glycoform was assigned to an SLG gene. Evidence is presented that the S2 and S5 haplotypes carry only one or the other of the SLG genes, indicating either that they are redundant or that they are not required for the self-incompatibility response.

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Selected References

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  1. Boyes D. C., Chen C. H., Tantikanjana T., Esch J. J., Nasrallah J. B. Isolation of a second S-locus-related cDNA from Brassica oleracea: genetic relationships between the S locus and two related loci. Genetics. 1991 Jan;127(1):221–228. doi: 10.1093/genetics/127.1.221. [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 M. E., Vrebalov J., Nasrallah J. B. The self-incompatibility (S) haplotypes of Brassica contain highly divergent and rearranged sequences of ancient origin. Plant Cell. 1997 Feb;9(2):237–247. doi: 10.1105/tpc.9.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Charlesworth D., Awadalla P. Flowering plant self-incompatibility: the molecular population genetics of Brassica S-loci. Heredity (Edinb) 1998 Jul;81(Pt 1):1–9. doi: 10.1038/sj.hdy.6884000. [DOI] [PubMed] [Google Scholar]
  5. Chen C. H., Nasrallah J. B. A new class of S sequences defined by a pollen recessive self-incompatibility allele of Brassica oleracea. Mol Gen Genet. 1990 Jul;222(2-3):241–248. doi: 10.1007/BF00633824. [DOI] [PubMed] [Google Scholar]
  6. Cock J. M., Swarup R., Dumas C. Natural antisense transcripts of the S locus receptor kinase gene and related sequences in Brassica oleracea. Mol Gen Genet. 1997 Aug;255(5):514–524. doi: 10.1007/s004380050524. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Fernandez J., DeMott M., Atherton D., Mische S. M. Internal protein sequence analysis: enzymatic digestion for less than 10 micrograms of protein bound to polyvinylidene difluoride or nitrocellulose membranes. Anal Biochem. 1992 Mar;201(2):255–264. doi: 10.1016/0003-2697(92)90336-6. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Gangloff S., Zou H., Rothstein R. Gene conversion plays the major role in controlling the stability of large tandem repeats in yeast. EMBO J. 1996 Apr 1;15(7):1715–1725. [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. 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]
  15. 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]
  16. 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]
  17. 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]
  18. Liao D., Pavelitz T., Kidd J. R., Kidd K. K., Weiner A. M. Concerted evolution of the tandemly repeated genes encoding human U2 snRNA (the RNU2 locus) involves rapid intrachromosomal homogenization and rare interchromosomal gene conversion. EMBO J. 1997 Feb 3;16(3):588–598. doi: 10.1093/emboj/16.3.588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Matsui N. M., Smith D. M., Clauser K. R., Fichmann J., Andrews L. E., Sullivan C. M., Burlingame A. L., Epstein L. B. Immobilized pH gradient two-dimensional gel electrophoresis and mass spectrometric identification of cytokine-regulated proteins in ME-180 cervical carcinoma cells. Electrophoresis. 1997 Mar-Apr;18(3-4):409–417. doi: 10.1002/elps.1150180315. [DOI] [PubMed] [Google Scholar]
  20. McCormick S. Self-incompatibility and other pollen-pistil interactions. Curr Opin Plant Biol. 1998 Feb;1(1):18–25. doi: 10.1016/s1369-5266(98)80122-2. [DOI] [PubMed] [Google Scholar]
  21. Morsomme P., de Kerchove d'Exaerde A., De Meester S., Thinès D., Goffeau A., Boutry M. Single point mutations in various domains of a plant plasma membrane H(+)-ATPase expressed in Saccharomyces cerevisiae increase H(+)-pumping and permit yeast growth at low pH. EMBO J. 1996 Oct 15;15(20):5513–5526. [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Parniske M., Hammond-Kosack K. E., Golstein C., Thomas C. M., Jones D. A., Harrison K., Wulff B. B., Jones J. D. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell. 1997 Dec 12;91(6):821–832. doi: 10.1016/s0092-8674(00)80470-5. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Pastuglia M., Ruffio-Châble V., Delorme V., Gaude T., Dumas C., Cock J. M. A functional S locus anther gene is not required for the self-incompatibility response in Brassica oleracea. Plant Cell. 1997 Nov;9(11):2065–2076. doi: 10.1105/tpc.9.11.2065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sato T., Thorsness M. K., Kandasamy M. K., Nishio T., Hirai M., Nasrallah J. B., Nasrallah M. E. Activity of an S Locus Gene Promoter in Pistils and Anthers of Transgenic Brassica. Plant Cell. 1991 Sep;3(9):867–876. doi: 10.1105/tpc.3.9.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem. 1996 Mar 1;68(5):850–858. doi: 10.1021/ac950914h. [DOI] [PubMed] [Google Scholar]
  29. Stahl RJ, Arnoldo M, Glavin TL, Goring DR, Rothstein SJ. The self-incompatibility phenotype in brassica is altered by the transformation of a mutant S locus receptor kinase . Plant Cell. 1998 Feb;10(2):209–218. doi: 10.1105/tpc.10.2.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stein J. C., Dixit R., Nasrallah M. E., Nasrallah J. B. SRK, the stigma-specific S locus receptor kinase of Brassica, is targeted to the plasma membrane in transgenic tobacco. Plant Cell. 1996 Mar;8(3):429–445. doi: 10.1105/tpc.8.3.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. Suzuki G., Watanabe M., Kai N., Matsuda N., Toriyama K., Takayama S., Isogai A., Hinata K. Three members of the S multigene family are linked to the S locus of Brassica. Mol Gen Genet. 1997 Oct;256(3):257–264. doi: 10.1007/s004380050568. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Vallejos C. E., Sakiyama N. S., Chase C. D. A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics. 1992 Jul;131(3):733–740. doi: 10.1093/genetics/131.3.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Walsh J. B. Sequence-dependent gene conversion: can duplicated genes diverge fast enough to escape conversion? Genetics. 1987 Nov;117(3):543–557. doi: 10.1093/genetics/117.3.543. [DOI] [PMC free article] [PubMed] [Google Scholar]

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