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Isolation of S-RNase binding proteins from Solanum chacoense: identification of an SBP1 (RING finger protein) orthologue

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Abstract

Currently, the most attractive working model of gametophytic self-incompatibility (SI) involving S-RNases postulates the presence of an inhibitor protein or complex expressed in pollen tubes that would counteract the cytotoxic effect of the ribonuclease activity of the S-RNase. Since it has been previously shown that allele-specific recognition is mediated through the hypervariable domain sequence of the S-RNase, we have targeted this region to isolate pollen-expressed interacting proteins in the yeast two-hybrid system. One of the isolated proteins corresponds to a RING finger protein highly similar to the previously isolated SBP1 protein from Petunia hybrida. This protein is postulated to be part of the RING finger E3 ligase family. The ScSBP1 gene is expressed in almost all tissues tested, suggesting a more general role than only being involved in SI. Although the ScSBP1 gene is polymorphic, linkage analysis showed that it was unlinked to the S-locus. The isolation of this S-RNase-binding protein in two different species and with four different S-RNase sequences as bait, strengthens its putative involvement in the SI response. Furthermore, comparison of the bait sequences used suggests that the SBP1 protein interacts with conserved sequences located between the HVa and HVb domains.

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References

  • Bachmair A, Novatchkova M, Potuschak T, Eisenhaber F (2001) Ubiquitylation in plants: a post-genomic look at a post-translational modification. Trends Plant Sci 6:463–470

    Article  CAS  PubMed  Google Scholar 

  • Bernatzky R, Glaven RH, Rivers BA (1995) S-Related protein can be recombined with self-compatibility in interspecific derivatives of Lycopersicon. Biochem Genet 33:215–225

    CAS  PubMed  Google Scholar 

  • Entani T, Iwano M, Shiba H, Che FS, Isogai A, Takayama S (2003) 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 8:203–213

    Article  CAS  PubMed  Google Scholar 

  • Freemont PS (2000) RING for destruction? Curr Biol 10:R84–R87

    CAS  PubMed  Google Scholar 

  • Gietz RD, Woods RA (2002) Screening for protein-protein interactions in the yeast two-hybrid system. Methods Mol Biol 185:471–486

    CAS  PubMed  Google Scholar 

  • Golz JF, Oh HY, Su V, Kusaba M, Newbigin E (2001) 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 USA 98:15372–15376

    Article  CAS  PubMed  Google Scholar 

  • Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, Crosby WL, Yang M, Ma H, Estelle M (1999) Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev 13:1678–1691

    CAS  PubMed  Google Scholar 

  • Hellmann H, Estelle M (2002) Plant development: regulation by protein degradation. Science 297:793–797

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Lee H-S, Karunanandaa B, Kao T-h (1994) Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self pollen. Plant Cell 6:1021–1028

    CAS  PubMed  Google Scholar 

  • Ida K, Norioka S, Yamamoto M, Kumasaka T, Yamashita E, Newbigin E, Clarke AE, Sakiyama F, Sato M (2001) The 1.55 Å resolution structure of Nicotiana alata S (F11)-RNase associated with gametophytic self incompatibility. J Mol Biol 314:103–112

    Article  CAS  PubMed  Google Scholar 

  • Jones J, Dunsmuir P, Bedbrook J (1985) High level expression of introduced chimeric genes in regenerated transformed plants. EMBO J 4:2411–2418

    CAS  Google Scholar 

  • Joshi CP, Zhou H, Huang X, Chiang VL (1997) Context sequences of translation initiation codon in plants. Plant Mol Biol 35:993–1001

    CAS  PubMed  Google Scholar 

  • Kipreos ET, Pagano M (2000) The F-box protein family. Genome Biol 1:reviews3002.1–3002.7

    Article  CAS  PubMed  Google Scholar 

  • Kondo K, Yamamoto M, Matton DP, Sato T, Hirai M, Norioka S, Hattori T, Kowyama Y (2002) Cultivated tomato has defects in both S-RNase and HT genes required for stylar function of self incompatibility. Plant J 29:627–636

    Article  CAS  PubMed  Google Scholar 

  • Kunz C, Chang A, Faure J-D, Clarke AE, Polya GM (1996) Phosphorylation of the style S-RNases by Ca2+-dependent protein kinases from pollen tubes. Sex Plant Reprod 9:25–34

    Google Scholar 

  • Lai Z, Ma W, Han B, Liang L, Zhang Y, Hong G, Xue Y (2002) An F-box gene linked to the self incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol Biol 50:29–42

    Article  CAS  PubMed  Google Scholar 

  • Lukaszewicz M, Feuermann M, Jerouville B, Stas A, Boutry M (2000) In vivo evaluation of the context sequence of the translation initiation codon in plants. Plant Sci 154:89–98

    Article  CAS  PubMed  Google Scholar 

  • Luu DT, Qin X, Morse D, Cappadocia M (2000) S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature 407:649–651

    Article  CAS  PubMed  Google Scholar 

  • Luu DT, Qin X, Laublin G, Yang Q, Morse D, Cappadocia M (2001) Rejection of S-heteroallelic pollen by a dual-specific S-RNase in Solanum chacoense predicts a multimeric SI pollen component. Genetics 159:329–335

    CAS  PubMed  Google Scholar 

  • Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M (1997) Hypervariable domains of self-incompatibility Rnases mediate allele-specific pollen recognition. Plant Cell 9:1757–1766

    CAS  Google Scholar 

  • Matton DP, Luu DT, Xike Q, Laublin G, O’Brien M, Maes O, Morse D, Cappadocia M (1999) Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles. Plant Cell 11:2087–2097

    CAS  PubMed  Google Scholar 

  • Matton DP, Luu DT, Morse D, Cappadocia M (2000) Reply. Establishing a paradigm for the generation of new S alleles. Plant Cell 12:313–316

    Article  CAS  PubMed  Google Scholar 

  • McClure B, Haring V, Ebert P, Anderson M, Simpson R, Sakiyama F, Clarke A (1989) Style self incompatibility products of Nicotiana alata are ribonucleases. Nature 32:955–957

    Article  Google Scholar 

  • McClure B, Mou B, Canevascini S, Bernatzky R (1999) A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc Natl Acad Sci USA 96:13548–13553

    CAS  PubMed  Google Scholar 

  • Murfett J, Atherton TL, Mou B, Gasser CS, McClure BA (1994) S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367:563–566

    CAS  PubMed  Google Scholar 

  • Murfett J, Strabala TJ, Zurek DM, Mou B, Beecher B, McClure BA (1996) 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 8:943–958

    Google Scholar 

  • Nettancourt D de (1997) Incompatibility in angiosperms. Sex Plant Reprod 10:185–199

    Article  Google Scholar 

  • Noureddine MA, Donaldson TD, Thacker SA, Duronio RJ (2002) Drosophila Roc1a encodes a RING-H2 protein with a unique function in processing the Hh signal transducer Ci by the SCF E3 ubiquitin ligase. Dev Cell 2:757–770

    Article  CAS  PubMed  Google Scholar 

  • O’Brien M, Kapfer C, Major G, Laurin M, Bertrand C, Kondo K, Kowyama Y, Matton DP (2002) 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 32:985–996

    Article  CAS  PubMed  Google Scholar 

  • Parry S, Newbigin E, Craik D, Nakamura KT, Bacic A, Oxley D (1998) Structural analysis and molecular model of a self-incompatibility RNase from wild tomato. Plant Physiol 116:463–469

    Article  CAS  PubMed  Google Scholar 

  • Pozo JC del, Estelle M (2000) F-box proteins and protein degradation: an emerging theme in cellular regulation. Plant Mol Biol 44:123–128

    Article  PubMed  Google Scholar 

  • Qiao H, Wang H, Zhao L, Zhou J, Huang J, Zhang Y, Xue Y (2004) The F-box protein AhSLF-S2 physically interacts with S-RNases that may be inhibited by the ubiquitin/26S proteasome pathway of protein degradation during compatible pollination in Antirrhinum. Plant Cell 16:582–595

    Article  CAS  PubMed  Google Scholar 

  • Reiter RS, Young RM, Scolnik PA (1992) Genetic linkage of the Arabidopsis genome: methods for mapping with recombinant inbreds and Random Amplified Polymorphic DNAs (RAPDs). In: Koncz C, Chua N-H, Schell J (eds) Methods in Arabidopsis research. World Scientific, Singapore, pp 170–190

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Sims TL, Ordanic M (2001) Identification of a S-ribonuclease-binding protein in Petunia hybrida. Plant Mol Biol 47:771–783

    Article  CAS  PubMed  Google Scholar 

  • Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hirano H (2003) 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 15:771–781

    Google Scholar 

  • Yamane H, Ikeda K, Ushijima K, Sassa H, Tao R (2003) 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 44:764–769

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Wang F, Ma W, Zhang Y, Han B, Xue Y (2003) Structural and transcriptional analysis of S-locus F-box genes in Antirrhinum. Sex Plant Reprod 16:165–177

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Gabriel Téodorescu for plant care and maintenance. This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC, Canada) and by Le Fond pour la Formation et l’Aide à la Recherche (FCAR-FQRNT, Québec).

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Correspondence to Daniel P. Matton.

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Genbank accession numbers: ScSBP1, AY545464

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O’Brien, M., Major, G., Chantha, SC. et al. Isolation of S-RNase binding proteins from Solanum chacoense: identification of an SBP1 (RING finger protein) orthologue. Sex Plant Reprod 17, 81–87 (2004). https://doi.org/10.1007/s00497-004-0218-8

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  • DOI: https://doi.org/10.1007/s00497-004-0218-8

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