Skip to main content
SpringerLink
Log in

Characterisation of novel S-alleles from cherry (Prunus avium L.)

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

In plant populations exhibiting gametophytic self-incompatibility, individuals harbouring rare S alleles are likely to have a reproductive advantage over individuals having more common alleles. Consequently, determination of the self-incompatibility haplotype of individuals is essential for genetic studies and the development of informed management strategies. This study characterises six new S alleles identified in wild cherry (Prunus avium L.). Investigations to determine the S genotype of individuals in recently planted woodland through length polymorphisms of introns associated with the stylar S-RNase gene and the pollen SFB gene revealed six S intron profiles which did not correspond to those of known S alleles. These are now attributed to S 27 to S 32 . Consensus primers, annealing in the S-RNase sequence coding for the signal peptide and C5 regions, were used to isolate the S-RNase alleles associated with the novel S intron profiles. The proteins corresponding to the new alleles were separated by isoelectric focusing from stylar extracts and their pI values determined. Similarities between the deduced amino acid sequence for the new alleles isolated and other cherry S-RNase sequences available on the databases ranged from 40% to 86%. Amplification products for SFB introns ranged from 172 to 208bp. New sequence regions exposed to positive selection were identified and the significance of the PS3 region reinforced. A phylogenetic relationship between P. avium S-RNases for S 10 and S 13 and between corresponding SFB alleles may indicate co-evolution of allele specificities of these two genes.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bošković R, Tobutt KR (1996) Correlation of stylar ribonuclease zymograms with incompatibility alleles in sweet cherry. Euphytica 90:245–250

    Article  Google Scholar 

  • Bošković R, Tobutt KR (2001) Genotyping cherry cultivars assigned to incompatibility groups, by analysing stylar ribonucleases. Theor Appl Genet 103:475–485

    Article  Google Scholar 

  • Bošković RI, Wolfram B, Tobutt KR, Cerovic R, Sonneveld T (2006) Inheritance and interactions of incompatibility alleles in the tetraploid soar cherry. TAG 112:315–326

    Article  PubMed  Google Scholar 

  • Castric V, Vekemans H (2004) Plant self-incompatibility in natural populations: a critical assessment of recent theoretical and empirical advances. Mol Ecol 13:2873–2889

    Article  PubMed  CAS  Google Scholar 

  • Chung BYW, Simons C, Firth AE, Brown CM, Hellens RP (2006) Effect of 5′UTR introns on gene expression in Arabidopsis thaliana. BMC Genomics 7:120

    Article  PubMed  Google Scholar 

  • Crane MB, Brown AG (1937) Incompatibility and sterility in the sweet cherry, Prunus avium L. J Pomol Hortic Sci 15:86–116

    Google Scholar 

  • Crane MB, Lawrence WJC (1929) Genetical and cytological aspects of incompatibility and sterility in cultivated fruits. J Pomol Hortic Sci 17:276–301

    Google Scholar 

  • De Cuyper B, Sonneveld T, Tobutt KR (2005) Determining self-incompatibility genotypes in Belgian wild cherries. Mol Ecol 14:945–955

    Article  PubMed  Google Scholar 

  • de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin

    Google Scholar 

  • Ducci F, Santi F (1998) The distribution of clones in managed and unmanaged populations of wild cherry (Prunus avium). Can J For Res 27:1998–2004

    Article  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  PubMed  CAS  Google Scholar 

  • Franklin-Tong N, Franklin FCH (2003) Gametophytic self-incompatibility inhibits pollen tube growth using different mechanisms. Trends Plant Sci 8:598–605

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ikeda K, Igic B, Ushijima K, Yamane H, Hauck NR, Nakano R et al (2004) Primary structural features of the S haplotype-specific F-box protein, SFB, in Prunus. Sex Plant Reprod 16:235–243

    Article  CAS  Google Scholar 

  • Ishimizu T, Endo T, Yamaguchi-Kabata Y, Nakamura KT, Sakiyama F, Norioka S (1998) Identification of regions in which positive selection may operate in S-RNase of Rosaceae, Implication for S-allele-specific recognition sites in S-RNase. FEBS Lett 440:337–342

    Article  PubMed  CAS  Google Scholar 

  • Kato S, Mukai Y (2004) Allelic diversity of S-RNase at the self-incompatibility locus in natural flowering cherry populations (Prunus lannesiana var. speciosa). Heredity 92:249–256

    Article  PubMed  CAS  Google Scholar 

  • Ma RC, Oliveira MM (2002) Evolutionary analysis of S-RNase genes from Rosaceae species. Mol Genet Genom 267:71–78

    Article  CAS  Google Scholar 

  • McClure B (2006) New views of S-RNase-based self-incompatibility. Curr Opin Plant Biol 9:639–646

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ortega E, Boskovic RI, Sargent DJ, Tobutt KR (2006) Analysis of S-RNase alleles of almond (Prunus dulcis): characterization of new sequences, resolution of synonyms and evidence of intragenic recombination. MGG 276:413–426

    Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Romero C, Vilanova S, Burgos L, Martinez-Calvo J, Vicente M, Llacer G, Badenes ML (2004) Analysis of the S-locus structure in Prunus armeniaca L. Identification of S-haplotype specific S-RNase and F-box genes. Plant Mol Biol 56:145–157

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sanchez-DelBarrio J, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Sassa H, Nishio T, Kowyama Y, Hirano H, Koba T, Ikehashi H (1996) Self incompatibility (S) alleles of the Rosaceae encode members of a distinct class of the T-2/S ribonuclease superfamily. Mol Gen Genet 250:547–557

    PubMed  CAS  Google Scholar 

  • Schueler S, Tusch A, Scholz F (2006) Comparative analysis of the within-population genetic structure in wild cherry (Prunus avium L.) at the self-incompatibility locus and nuclear microsatellites. Mol Ecol 15:3231–3243

    Article  PubMed  CAS  Google Scholar 

  • Sonneveld T, Robbins TP, Boskovic R, Tobutt KR (2001) Cloning of six cherry self-incompatibility alleles and development of allele-specific PCR detection. Theor Appl Genet 102:1046–1055

    Article  CAS  Google Scholar 

  • Sonneveld T, Tobutt KR, Robbins TP (2003) Allele-specific PCR detection of sweet cherry self-incompatibility (S) alleles S1 to S16 using consensus and allele-specific primers. Theor Appl Genet 107:1059–1070

    Article  PubMed  CAS  Google Scholar 

  • Sonneveld T, Robbins TP, Tobutt KR (2006) Improved discrimination of self-incompatibility S-RNase alleles in cherry and high throughput genotyping by automated sizing of first intron PCR products. Plant Breed 125:305–307

    Article  CAS  Google Scholar 

  • Sonneveld T, Tobutt KR, Vaughan SP, Robbins TP (2005) Loss of pollen-S function in two self-compatible selections of Prunus avium is associated with deletion/mutation of an S haplotype-specific F-box gene. Plant Cell 17:37–51

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Stoeckel S, Grange J, Fernandex-Manjarres FJ, Bilger I, Frascaria-Lacoste N, Mariette S (2006) Heterozygote excess in a self-incompatible and partially clonal forest tree species Prunus avium L. Mol Ecol 15:2109–2118

    Article  PubMed  CAS  Google Scholar 

  • Šurbanovski N, Tobutt KR, Konstantinović M, Maksimović V, Sargent DJ, Stevanović V et al (2007) Self-incompatibility of Prunus tenella and evidence that reproductively isolated species of Prunus have different SFB alleles coupled with an identical S-RNase allele. Plant J 50:723–734

    Article  PubMed  Google Scholar 

  • Tao R, Yamane H, Sugiura A, Murayama H, Sassa H, Mori H (1999) Molecular typing of S-alleles through identification, characterization and cDNA cloning for S-RNases in sweet cherry. J Am Soc Hortic Sci 124:224–233

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Ushijima K, Sassa H, Tao R, Yamane H, Dandekar AM, Gradziel TM et al (1998) Cloning and characterization of cDNAs encoding S-RNases from almond (Prunus dulcis): primary structural features and sequence diversity of the S-RNases in Rosaceae. Mol Gen Genet 260:261–268

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Ushijima K, Yamane H, Watari A, Kakehi E, Ikeda K, Hauck NR, Iezzoni AF, Tao RT (2004) The S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume. Plant J 39:573–586

    Article  PubMed  CAS  Google Scholar 

  • Vaughan SP, Russell K (2004) Characterisation of novel microsatellites and development of multiplex PCR for large-scale population studies in wild cherry, Prunus avium L. Mol Ecol Notes 4:429–431

    Article  CAS  Google Scholar 

  • Vaughan SP, Russell K, Sargent DJ, Tobutt KR (2006) Isolation of S locus F-box alleles in Prunus avium and their application in a novel method to determine self-incompatibility genotype. Theor Appl Genet 112:856–866

    Article  PubMed  CAS  Google Scholar 

  • Vaughan SP, Cottrell JE, Moodley DJ, Connelly T, Russell K (2007a) Distribution and fine-scale spatial-genetic structure in British wild cherry (Prunus avium L). Heredity 98:274–283

    Article  PubMed  CAS  Google Scholar 

  • Vaughan SP, Cottrell JE, Moodley DJ, Connelly T, Russell K (2007b) Clonal structure and recruitment in British wild cherry (Prunus avium L). For Ecol Man 242:419–430

    Article  Google Scholar 

  • Wiersma PA, Wu Z, Zhou L, Hampson C, Kappel F (2001) Identification of new self-incompatibility alleles in sweet cherry (Prunus avium L.) and clarification of incompatibility groups by PCR and sequencing analysis. Theor Appl Genet 102:700–708

    Article  CAS  Google Scholar 

  • Wunsch A, Hormaza JI (2004) Cloning and characterization of genomic DNA sequences of four self-incompatibility alleles in sweet cherry (Prunus avium L.). Theor Appl Genet 108:299–305

    Article  PubMed  CAS  Google Scholar 

  • Yamane H, Ikeda K, Ushijima K, Sassa H, Tao R (2003a) 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  PubMed  CAS  Google Scholar 

  • Yamane H, Ushijima K, Sassa H, Tao R (2003b) The use of the S haplotype-specific F-box protein gene, SFB as a molecular marker for S-haplotypes and self-compatibility in Japanese apricot (Prunus mume). Theor Appl Genet 107:1357–1361

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by funding from Defra and the Forestry Commission (Grant No.WD0502). The authors would also like to thank Bart De Cuyper and Dr. Tineke Sonneveld for provision of primers and P. avium material and for helpful discussions. Radovan Bošković acknowledges a grant from the Mount Trust.

Author information

Author notes

  1. S. P. Vaughan

    Present address: Rothamsted Research, Harpenden, Herts, AL52JQ, UK

Authors and Affiliations

  1. East Malling Research, New Road, East Malling, Kent, ME19 6BJ, UK

    S. P. Vaughan, R. I. Bošković, K. Russell & K. R. Tobutt

  2. Imperial College at Wye, Ashford, Kent, TN25 6BJ, UK

    R. I. Bošković

  3. Instituto Valenciano de Investigaciones Agrarias (IVIA), Carretera Moncada-Náquera, km 4.5, 46113, Moncada, Valencia, Spain

    A. Gisbert-Climent

Authors
  1. S. P. Vaughan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. I. Bošković
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Gisbert-Climent
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Russell
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. R. Tobutt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. P. Vaughan.

Additional information

Communicated by A. Abbott

The nucleotide sequences reported in this paper have been submitted to the EMBL/GenBank database under the following accession numbers: S 27 (DQ266439), S 28 (DQ266440), S 29 (DQ266441), S 30 (DQ266442), S 31 (DQ266443), S 32 (DQ266444).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vaughan, S.P., Bošković, R.I., Gisbert-Climent, A. et al. Characterisation of novel S-alleles from cherry (Prunus avium L.). Tree Genetics & Genomes 4, 531–541 (2008). https://doi.org/10.1007/s11295-007-0129-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-007-0129-6

Keywords

Search

Navigation