Skip to main content
SpringerLink
Log in

Structural and transcriptional analysis of S-locus F-box genes in Antirrhinum

  • Original Article
  • Published:
Sexual Plant Reproduction Aims and scope Submit manuscript

Abstract

A class of ribonucleases termed S-RNases, which control the pistil expression of self-incompatibility, represents the only known functional products encoded by the S locus in species from the Solanaceae, Scrophulariaceae and Rosaceae. Previously, we identified a pollen-specific F-box gene, AhSLF (S locus F-box)-S 2, very similar to S 2 -RNase in Antirrhinum, a member of the Scrophulariaceae. In addition, AhSLF-S 2 also detected the presence of its homologous DNA fragments. To identify these fragments, we constructed two genomic DNA libraries from Antirrhinum self-incompatible lines carrying alleles S 1 S 5 and S 2 S 4, respectively, using a transformation-competent artificial chromosome (TAC) vector. With AhSLF-S 2-specific primers, TAC clones containing both AhSLF-S 2 and its homologs were subsequently identified (S 2 TAC, S 5 TACa, S 4 TAC, and S 1 TACa). DNA blot hybridization, sequencing and segregation analyses revealed that they are organized as single allelic copies (AhSLF-S 2, -S 1, -S 4 and -S 5) tightly linked to the S-RNases. Furthermore, clusters of F-box genes similar to AhSLF-S 2 were identified. In total, three F-box genes (AhSLF-S 2, -S 2 A and -S 2 C) in S 2 TAC (51 kb), three (AhSLF-S 4, -S 4 A and -S 4 D) in S 4 TAC (75 kb), two (AhSLF-S 5 and -S 5 A) in S 5 TACa (55 kb), and two (AhSLF-S 1 and -S 1 E) in S 1 TACa (71 kb), respectively, were identified. Paralogous copies of these genes show 38–54% identity, with allelic copies sharing 90% amino acid identity. Among these genes, three (AhSLF-S 2 C, -S 4 D and -S 1 E) were specifically expressed in pollen, similar to AhSLF-S 2, implying that they likely play important roles in pollen, whereas three AhSLF-SA alleles showed no detectable expression. In addition, several types of retroelements and transposons were identified in the sequenced regions, revealing some detailed information on the structural diversity of the S locus region. Taken together, these results indicate that both single allelic and tandemly duplicated genes are associated with the S locus in Antirrhinum. The implications of these findings in evolution and possible roles of allelic AhSLF-S genes in the self-incompatible reaction are discussed in species like Antirrhinum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2A, B.
Fig. 3.
Fig. 4A–D.
Fig. 5.
Fig. 6A–D.
Fig. 7.

Similar content being viewed by others

References

  • Ai Y, Singh A, Coleman CE, Ioerger TR, Kheyr-Pour A (1990) Self-incompatibility in Petunia inflata: isolation and characterization of cDNA encoding S-allele-associated proteins. Sex Plant Reprod 3:130–138

    Google Scholar 

  • Anderson MA, Cornish EC, Mau SL, Williams EG, Hoggart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penshow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE (1986) Cloning of a cDNA for a style glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Nature 321:38–44

    CAS  Google Scholar 

  • Broothaerts W, Janssens GA, Proost P, Broekaert W (1995) cDNA cloning and molecular analysis of two self-incompatibility alleles from apple. Plant Mol Biol 27:499–511

    CAS  PubMed  Google Scholar 

  • Cheng Z, Dong F, Langdon T, Ouyang S, Buell CR (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14:1691–1704

    Article  CAS  PubMed  Google Scholar 

  • Coleman CE, Kao TH (1992) The flanking region of two Petunia inflate S alleles are heterogenous and contain repetitive sequences. Plant Mol Biol 18:725–737

    CAS  PubMed  Google Scholar 

  • Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S (1999) Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286:2468–2474

    Google Scholar 

  • Duret L, Marais G, Biemont C (2000) Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans. Genetics 156:1661–1669

    CAS  PubMed  Google Scholar 

  • Ellis J, Dodds P, Pryor T (2000a) The generation of plant disease resistance gene specificities. Trends Plant Sci 5:373–379

    CAS  PubMed  Google Scholar 

  • Ellis J, Dodds P, Pryor T (2000b) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284

    CAS  PubMed  Google Scholar 

  • Emerson S (1939) A preliminary survey of the Oenothera organensis population. Evolution 24:524–537

    Google Scholar 

  • Entani T, Iwano M, Shiba H, Takayama S, Fukui K (1999) Centromeric localization of an S-RNase gene in Petunia hybrida Vilm. Theor Appl Genet 99:391–397

    Article  CAS  Google Scholar 

  • Entani T, Iwano M, Shiba H, Che F, 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 

  • Foote HC, Ride JP, Franklin-Tong VE, Walker EA, Lawrence MJ, Franklin FCH (1994) Cloning and expression of a distinctive class of self-incompatibility (S-) gene from Papaver rhoeas L. Proc Natl Acad Sci USA 91:2265–2269

    CAS  PubMed  Google Scholar 

  • Frey M, Tavantzis SM, Saedler H (1989) The maize En/Spm element transposes in tomato. Mol Gen Genet 217:172–177

    CAS  PubMed  Google Scholar 

  • Fu H, Zheng Z, Dooner HK (2002) Recombination rates between adjacent genic and retrotransposon region in maize vary by 2 orders of magnitude. Proc Natl Acad Sci USA 99:1082–1087

    CAS  PubMed  Google Scholar 

  • Golz JF, Su V, Clarke AE, Newbigin EA (1999) A molecular description of mutations affecting the pollen component of the Nicotiana alata S locus. Genetics 152:1123–1135

    CAS  PubMed  Google Scholar 

  • Golz JF, Clarke AE, Newbegin E (2000) Mutational approaches to the study of self-incompatibility: revisiting the pollen part mutations. Ann Bot 85:95–103

    Article  Google Scholar 

  • Golz JF, Oh HY, Su V, Kusaba M, Newbigin E (2001) Genetics analysis of Nicotiana pollen-part mutant 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 

  • Hammond-Kosack KE, Tang S, Harrison K, Jones JD (1998) The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product Avr 9. Plant Cell 10:1251–1266

    Article  CAS  PubMed  Google Scholar 

  • Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatiblity RNases. Proc Natl Acad Sci USA 98:13167–13171

    Article  CAS  PubMed  Google Scholar 

  • Kachroo A, Schopfer CR, Nasrallah ME, Nasrallah JB (2001) Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 293 1824–1826

    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 

  • Lawrence MJ, Lane MD, O'Donnell S, Franklin-Tong VE (1993) The population genetics of the self-incompatibility polymorphism in Papaver rhoeas. V. Cross-classification of the S-alleles of samples from three natural populations. Heredity 71:581–590

    Google Scholar 

  • Li JH, Nass N, Kusaba M, Dodds PN, Treloar N, Clarke AE, Newbigin E (2000) A genetic map of the Nicotiana alata S locus that includes three pollen-expressed genes. Theor Appl Genet 100:956–964

    Article  CAS  Google Scholar 

  • Liu YG, Whitter RF (1994) Rapid preparation of megabase plant DNA from nuclei in agarose plugs and microbeads. Nucleic Acids Res 22:2168–2169

    Google Scholar 

  • Liu YG, Shirano Y, Fukaki H, Yanai Y, Tasaka M (1999) Complementation of plant mutants with large genomic DNA fragments by a transformation-competent artificial chromosome vector accelerates positional cloning. Proc Natl Acad Sci USA 96:6535–6540

    CAS  PubMed  Google Scholar 

  • Liu YG, Nagaki K, Fujita M, Kawaura K, Uozumi M, Ogihara Y (2000) Development of an efficient maintenance and screening system for large-insert genomic DNA libraries of hexaploid wheat in transformation-competent artificial chromosome (TAC) vector. Plant J 23:687–695

    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 

  • Ma W, Zhou J, Lai Z, Zhang Y, Xue Y (2002) The self-incompatibility (S) locus is located in a pericentromeric region in Antirrhinum. Acta Bot Sin 45:47–52

    Google Scholar 

  • Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436

    CAS  PubMed  Google Scholar 

  • May G, Matzke E (1995) Recombination and variation at the mating-type of Coprinus-cinereus. Mol Biol Evol 12:794–802

    CAS  Google Scholar 

  • McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342:955–957

    CAS  PubMed  Google Scholar 

  • McCubbin AG, Kao TH (2000) Molecular recognition and response in pollen and pistil interactions. Annu Rev Cell Dev Biol 16:333–364

    CAS  PubMed  Google Scholar 

  • McCubbin AG, Wang X, Kao TH (2000) Identification of self-incompatibility (S-) locus linked pollen cDNA markers in Petunia inflata. Genome 43:619–627

    Article  CAS  PubMed  Google Scholar 

  • Michelmore RW, Meyers BC, (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130

    CAS  PubMed  Google Scholar 

  • Nacken WK, Piotrowiak R, Suedler H, Sommer H (1991) The transposable element Tam1 from Antirrhinum majus shows structural homology to the maize transposon En/Spm and has no sequence specificity of insertion. Mol Gen Genet 228:201–208

    CAS  PubMed  Google Scholar 

  • Nettancourt D de (2001) Incompatibility and incongruity in wild and cultivated plants, 2nd edn. Springer, Berlin Heidelberg New York

  • O'hUigin C (1995) Quantifying the degree of convergence in primate MHC-DRB genes. Immunol Rev 143:123–140

    CAS  PubMed  Google Scholar 

  • Pandy KK (1965) Centric chromosome fragments and pollen-part mutation of the incompatibility gene in Nicotiana alata. Nature 206:792–795

    Google Scholar 

  • Richman AD, Uyenoyama MK, Kohn JR (1996) S-allele diversity in a natural population of Physalis crassifolia (Solanaceae) (ground cherry) assessed by RT-PCR. Heredity 76:497–505

    CAS  PubMed  Google Scholar 

  • Rizzon C, Marais G, Gouy M, Biemont C (2002) Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res 12:400–407

    CAS  PubMed  Google Scholar 

  • Royo J, Nass N, Matton DP, Okamto S, Clarke AE, Newbigin E (1996) A retrotransposon-like sequence linked to the S-locus of Nicotiana alata is expressed in styles in response to touch. Mol Gen Genet 250:180–188

    Article  CAS  PubMed  Google Scholar 

  • Sassa H, Nishio T, Kowyama Y, Hirano H, Koba T (1996) Self-incompatibility (S) alleles of the Rosaceae encode members of a distinct class of the T2/S ribonuclease superfamily. Mol Gen Genet 250:547–557

    Article  CAS  PubMed  Google Scholar 

  • Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700

    CAS  PubMed  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 

  • Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB (1991) Molecular cloning of a putative receptor protein kinase encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci USA 88:8816–8820

    CAS  PubMed  Google Scholar 

  • Steinbachs JE, Holsinger KE (2002) S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. Mol Biol Evol 19:825–829

    CAS  PubMed  Google Scholar 

  • Suzuki G, Kai N, Hirose T, Fukui K, Nishio T (1999) 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 3:391–400

    Google Scholar 

  • Takayama S, Shimosato H, Shiba H, Funata M, Che FS, Watanabe M, Iwano M, Isogai A (2001) Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413:534–536

    Article  CAS  PubMed  Google Scholar 

  • Ushijima K, Sassa H, Hirano H (1998) Characterization of the flanking regions of S-RNase genes of Japanese pear (Pyrus serotina) and apple (Malus×domestica). Gene 211:159–167

    Article  CAS  PubMed  Google Scholar 

  • Ushijima K, Sassa H, Dandekar A, Gradziel T, Tao R, Hirano H (2003) Structure 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

    Article  CAS  PubMed  Google Scholar 

  • Wei F, Wing RA, Wise RP (2002) Genome dynamics and evolution of the Mla (Powdery Mildew) resistance locus in barley. Plant Cell 14:1903–1917

    Google Scholar 

  • Wheeler MJ, Franklin-Tong VE, Franklin FCH (2001) The molecular and genetics basis of pollen-pistil interactions. New Phytol 151:565–584

    Article  CAS  Google Scholar 

  • Xue Y, Carpenter R, Dickinson HG, Coen ES (1996) Origin of allelic diversity in Antirrhinum S locus RNases. Plant Cell 8:805–814

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to E.S. Coen and R. Carpenter for providing Antirrhinum plants and constant support and Y. Liu for help in constructing TAC library. We also thank J. Huang, H. Qiao and H. Wang and, in particular, an anonymous reviewer for their helpful comments on the manuscript. The work was supported by the Chinese Academy of Sciences and the National Natural Science Foundation of China (39825103).

Author information

Author notes

  1. Wenshi Ma

    Present address: School of Life Sciences, Hebei Normal University, 050016, Shijiazhuang, Hebei Province, China

Authors and Affiliations

  1. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, 100080, Beijing , China

    Junli Zhou, Fei Wang, Wenshi Ma, Yansheng Zhang & Yongbiao Xue

  2. National Center for Gene Research, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 500 Caobao Road, 200233, Shanghai , China

    Bin Han

Authors
  1. Junli Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenshi Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yansheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bin Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yongbiao Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yongbiao Xue.

Additional information

Sequence data from this article have been deposited with the EMBL/GenBank databases under accession numbers AJ300474, AJ515534, AJ515536 and AJ515535

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhou, J., Wang, F., Ma, W. et al. Structural and transcriptional analysis of S-locus F-box genes in Antirrhinum . Sex Plant Reprod 16, 165–177 (2003). https://doi.org/10.1007/s00497-003-0185-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-003-0185-5

Keywords

Search

Navigation