Skip to main content
Log in

Two Different Prunus SFB Alleles Have the Same Function in the Self-incompatibility Reaction

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Many species in the families of Rosaceae, Solanaceae, and Scrophulariaceae exhibit gametophytic self-incompatibility, a phenomenon controlled by two polymorphic genes at the S-locus, style-S (S-RNase) and pollen-S (SFB). Sequences of both genes show high levels of diversity, characteristic of genes involved in recognition of self-incompatibility systems in plants. In this study, S 24 -RNase and SFB 24 alleles were cloned from Prunus armeniaca cv. Chuanzhihong (Chinese apricot). Sequence comparisons of deduced amino acid sequences revealed that the P. armeniaca S 24 -haplotype has different SFB alleles, but shares a single S-RNase allele with P. armeniaca S 4 -haplotype. Moreover, P. armeniaca S 24 -RNase haplotype has a single and three different alleles with S 1 -RNase of P. tenella (dwarf almond) and S 1 -RNase of P. mira (smooth pit peach), respectively. The functionalities of SFB 24 and SFB 4 have been evaluated by pollen tube growth and controlled field tests of P. tenella and P. mira. Genetic analysis of the two intercrosses showed that progenies segregated 1:1 into two S-genotype classes, which is consistent with the expected ratio for semi-compatibility. These findings imply that the allelic function of the S 24 -haplotype is identical to that of the S 4 -haplotype in a self-incompatibility reaction. Thus, these two Prunus S-haplotypes are in fact two neutral variants of the same S-haplotype. The evolution of the S-allele is also discussed in terms of both functions and differences between S 24 - and S 4 -haplotypes in Prunus.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bokszczanin K, Palucha A, Przybyla AA (2009) Description of a new trans-generic Skb-RNase allele in apple. Euphytica 166:83–94

    Article  CAS  Google Scholar 

  • Burgos L, Pérez-Tornero O, Ballester J, Olmos E (1998) Detection and inheritance of stylar ribonucleases associated with incompatibility alleles in apricot. Sex Plant Reprod 11:153–158

    Article  CAS  Google Scholar 

  • Chen XS, Wu Y, Chen MX, He TM, Feng JR, Liang Q, Liu W, Yang HH, Zhang LJ (2006) Inheritance and correlation of self-compatibility and other yield components in the apricot hybrid F1 populations. Euphytica 150:69–74

    Article  Google Scholar 

  • Chookajorn T, Kachroo A, Ripoll DR, Clark AG, Nasrallah JB (2004) Specificity determinants and diversification of the Brassica self-incompatibility pollen ligand. Proc Natl Acad Sci USA 101:911–917

    Article  PubMed  CAS  Google Scholar 

  • Crane MB, Lawrence WJC (1929) Genetical and cytological aspects of incompatibility and sterility in cultivated fruits. J Pomol Hortic Sci 7:276–301

    Google Scholar 

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

    Book  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry 19:11–15

    Google Scholar 

  • Fisher R (1961) A model for the generation of self-sterility alleles. J Theor Biol 1:411–414

    PubMed  CAS  Google Scholar 

  • Gu C, Zhang SL, Huang SX, Heng W, Liu QZ, Wu HQ, Wu J (2010) Identification of S-genotypes in Chinese cherry cultivars (Prunus pseudocerasus LindI.). Tree Genet Genomes 6:579–590

    Article  Google Scholar 

  • Halász J, Pedryc A, Hegedus A (2007) Origin and dissemination of the pollen-part mutated SC haplotype which confers self-compatibility in apricot (Prunus armeniaca). New Phytol 176:792–803

    Article  PubMed  Google Scholar 

  • Heng W, Wu HQ, Chen QX, Wu J, Zhang SJ, Zhang SL (2008) Identification of S-genotypes and novel S-RNase alleles in Prunus mume. J Hortic Sci Biotechnol 83:689–694

    CAS  Google Scholar 

  • Heng W, Wu J, Wu H, Cao Y, Nishio T, Zhang SL (2011) Recognition specificity of self-incompatibility in Pyrus and Malus. Mol Breeding 28:549–557

    Article  CAS  Google Scholar 

  • Ikeda K, Igic B, Ushijima K, Yamane H, Hauck NR, Nakano R, Sassa H, Iezzoni AF, Kohn JR, Tao R (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 

  • Ikeda K, Ushijima K, Yamane H, Tao R, Hauck NR, Sebolt AM, Iezzoni AF (2005) Linkage and physical distances between S-haplotype S-RNase and SFB genes in sweet cherry. Sex Plant Reprod 17:289–296

    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 

  • Kakui H, Kato M, Ushijima K, Kitaguchi M, Kato S, Sassa H (2011) Sequence divergence and loss-of-function phenotypes of S locus F-box brothers (SFBB) genes are consistent with non-self recognition by multiple pollen determinants in self-incompatibility of Japanese pear (Pyrus pyrifolia). Plant J 68:1028–1038

    Article  PubMed  CAS  Google Scholar 

  • Kubo K, Entani T, Takara A, Wang N, Fields AM, Hua Z, Toyoda M, Kawashima S, Ando T, Isogai A, Kao TH, Takayama S (2010) Collaborative non-self recognition system in S-RNase-based self-incompatibility. Science 330:796–799

    Article  PubMed  CAS  Google Scholar 

  • Lewis D (1949) Structure of the self-incompatibility gene. II. Induced mutation rate. Heredity 3:339–355

    Article  PubMed  CAS  Google Scholar 

  • Lewis D (1951) Structure of the self-incompatibility gene. III. Types of spotaneous an induced mutation. Heredity 5:399–414

    Article  Google Scholar 

  • Marchese A, Boskovic RI, Caruso T, Raimondo A, Cutuli M, Tobutt KR (2007) A new self-compatibility haplotype in the sweet cherry 'Kronio', S 5 ', attributable to a pollen-part mutation in the SFB gene. J Exp Bot 58:4347–4356

    Article  PubMed  CAS  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

    PubMed  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

    PubMed  CAS  Google Scholar 

  • Matton DP, Luu DT, Morse D, Cappadocia M (2000) Establishing a paradigm for the generation of new S Alleles. Plant Cell 12:313–315

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • McClure BA, Gray JE, Anderson MA, Clarke AE (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347:757–760

    Article  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 

  • Sanzol J (2010) Two neutral variants segregating at the gametophytic self-incompatibility locus of European pear (Pyrus communis L.) (Rosaceae, Pyrinae). Plant Biol 12:800–805

    Article  PubMed  CAS  Google Scholar 

  • Sassa H, Hirano H, Ikehashi H (1992) Self-incompatibility-related RNases in styles of Japanese pear (Pyrus serotina Rehd.). Plant Cell Physiol 33:811–814

    CAS  Google Scholar 

  • Sonneveld T, Robbins TP, Bošković 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, 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 

  • Šurbanovski N, Tobutt KR, Konstantinović M, Maksimović V, Sargent DJ, Stevanović V, Bošković RI (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 

  • Sutherland BG, Tobutt KR, Robbins TP (2008) Trans-specific S-RNase and SFB alleles in Prunus self-incompatibility haplotypes. Mol Genet Genomics 279:95–106

    Article  PubMed  CAS  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 

  • Tao R, Watari A, Hanada T, Habu T, Yaegaki H, Yamaguchi M, Yamane H (2007) Self-compatible peach (Prunus persica) has mutant versions of the S haplotypes found in self-incompatible Prunus species. Plant Mol Biol 63:109–123

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    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 R (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 

  • Uyenoyama MK, Newbigin E (2000) Evolutionary dynamics of dual-specificity self-incompatibility alleles. Plant Cell 12:310–311

    PubMed  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 

  • Verica JA, McCubbin AG, Kao T (1998) Are the hypervariable regions of S RNases sufficient for allele-specific recognition of pollen. Plant Cell 10:314–317

    Article  PubMed  CAS  Google Scholar 

  • Vilanova S, Badenes ML, Burgos L, Martinez-Calvo J, Llacer G, Romero C (2006) Self-compatibility of two apricot selections is associated with two pollen-part mutations of different nature. Plant Physiol 142:629–641

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Gu C, Zhang SL, Zhang SJ, Wu HQ, Heng W (2009) Identification of S-haplotype-specific S-RNase and SFB alleles in native Chinese apricot (Prunus armeniaca L.). J Hortic Sci Biotechnol 84:645–652

    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

    PubMed  CAS  Google Scholar 

  • Zhang SL, Huang SX, Kitashiba H, Nishio T (2007) Identification of S-haplotype-specific F-box gene in Japanese plum (Prunus salicina Lindl.). Sex Plant Reprod 20:1–8

    Article  Google Scholar 

  • Zhang L, Chen X, Zhang C, Liu X, Ci Z, Zhang H, Wu C, Liu C (2008a) Identification of self-incompatibility (S-) genotypes of Chinese apricot cultivars. Euphytica 160:241–248

    Article  CAS  Google Scholar 

  • Zhang SJ, Huang SX, Heng W, Wu HQ, Wu J, Zhang SL (2008b) Identification of S-genotypes in 17 Chinese cultivars of Japanese plum (Prunus salicina Lindl.) and molecular characterisation of 13 novel S-alleles. J Hortic Sci Biotechnol 83:635–640

    CAS  Google Scholar 

  • Zurek DM, Mou B, Beecher B, McClure B (1997) Exchanging sequence domains between S-RNases from Nicotiana alata disrupts pollen recognition. Plant J 11:797–808

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Fundamental Research Funds for the Central Universities (KYZ200911, KYZ201146).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to J. Wu or S.-L. Zhang.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 5097 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gu, C., Wu, J., Du, YH. et al. Two Different Prunus SFB Alleles Have the Same Function in the Self-incompatibility Reaction. Plant Mol Biol Rep 31, 425–434 (2013). https://doi.org/10.1007/s11105-012-0518-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-012-0518-3

Keywords

Navigation