Skip to main content
SpringerLink
Log in

Molecular analysis of eight SFB alleles and a new SFB-like gene in Prunus pseudocerasus and Prunus speciosa

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

Abstract

This study identified eight S-haplotype-specific F-box genes (SFB alleles) and one S-haplotype-specific F-box-like gene (SFB-like gene) from genomic DNA by PCR combined with cleaved amplified polymorphic sequence markers in Prunus pseudocerasus and Prunus speciosa. The unknown sequences of C-termini were obtained by thermal asymmetric interlaced PCR. The whole nucleotide sequences of these genes were submitted to the EMBL/GenBank database. The SFBs shared typical structural features with SFBs from other Prunus species exhibiting gametophytic self-incompatibility. The deduced amino acid identity ranged from 77.1% to 82.4% among the four PpsSFBs and from 70.4% to 80.2% among the four PspeSFBs. The typical structural features were also detected in the PpsFB, but the sequence polymorphism was lower. The nucleotide identities ranged from 71.3% to 90.3% among the eight introns of the SFBs, the length of these introns varied from 95 to 121 bp and showed few polymorphisms. The distance between these SFBs and the corresponding S-RNases (S-ribonucleases) varied from 33 to 956 bp. Moreover, sequence analysis showed that interspecific amino acid identities in comparison with some other Prunus species were often higher than intraspecific identities, similar to S-RNase alleles. In addition, a similarity comparison found that the deduced amino acid identities among SFB alleles were higher than among S-RNase alleles, and the similarity data showed that the relationships among SFB alleles differed among S-RNase alleles, suggesting that the S-RNase and SFB alleles were separated but correlated during the coevolutionary process.

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
Fig. 6

Similar content being viewed by others

Abbreviations

Pps :

Prunus pseudocerasus

Pspe :

Prunus speciosa

Pa :

Prunus avium

Par :

Prunus armeniaca

Pcer :

Prunus Cerasus

Pd :

Prunus dulcis

Pm :

Prunus mume

Ps :

Prunus salicina

PaxiF1 :

Petunia axillaris

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389

    Article  PubMed  CAS  Google Scholar 

  • Anderson MA, Cornish EC, Mau SL, Williams EG, Hoggart R, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD (1986) Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Nature 321:38–44

    Article  CAS  Google Scholar 

  • Chung BY, 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 

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

    Google Scholar 

  • Deshaies RJ (1999) SCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 15:435–467

    Article  PubMed  CAS  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 

  • 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 

  • 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

    Google Scholar 

  • Huang SX, Wu HQ, Li YR, Wu J, Zhang SJ, Heng W, Zhang SL (2008) Competitive interaction between two functional S-haplotypes confer self-compatibility on tetraploid Chinese cherry (Prunus pseudocerasus Lindl. CV. Nanjing Chuisi). Plant Cell Rep 27:1075–1085

    Article  PubMed  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 N, 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 

  • Kato S, Iwata H, Tsumura Y, Mukai Y (2007) Distribution of S-alleles in island populations of flowering cherry, Prunus lannesiana var. speciosa. Genes Genet Syst 82:65–75

    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  PubMed  CAS  Google Scholar 

  • Li Q, Yin H, Li D, Zhu H, Zhang Y, Zhu W (2007) Isolation and characterization of CMO gene promoter from halophyte Suaeda liaotungensis K. J Genet Genomics 34:355–361

    Article  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 

  • Moriya Y, Yamamoto K, Okada K, Iwanami H, Bessho H, Nakanishi T, Takasaki T (2007) Development of a CAPS marker system for genotyping European pear cultivars harboring 17 S alleles. Plant Cell Rep 26:345–354

    Article  PubMed  CAS  Google Scholar 

  • Newbigin E, Paape T, Kohn JR (2008) RNase-based self-incompatibility: puzzled by pollen S. Plant Cell 20:2286–2292

    Article  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 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    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 

  • 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

    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, Sassa H, Mori H, Gradziel TM, Dandekar AM, Sugiura A (1997) Identification of stylar RNases associated with gametophytic self-incompatibility in almond (Prunus dulcis). Plant Cell Physiol 38:304

    PubMed  CAS  Google Scholar 

  • Thomson 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  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

    Article  PubMed  CAS  Google Scholar 

  • Tsukamoto T, Ando T, Watanabe H, Marchesi E, Kao TH (2005) Duplication of the S-locus F-box gene is associated with breakdown of pollen function in an S-haplotype identified in a natural population of self-incompatible Petunia axillaris. Plant Mol Biol 57:141–153

    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 

  • 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 

  • Vieira J, Teles E, Santos RA, Vieira CP (2008) Recombination at Prunus S-locus region SLFL1 gene. Genetics 180:483–491

    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

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Wang X, McCubbin AG, Kao TH (2003) Genetic mapping and molecular characterization of the self-incompatibility (S) locus in Petunia inflata. Plant Mol Biol 53:565–580

    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

    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

    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 

  • 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 

  • 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

Acknowledgment

We thank American Journal Experts for helping to improve our manuscript. This work was supported by the National Natural Science Foundation of China (31071759) and the National Department Public Benefit Research Foundation (2009030044).

Author information

Authors and Affiliations

  1. College of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, Jiangsu, 210095, People’s Republic of China

    Chao Gu, Jun Wu, Shu-Jun Zhang, Ya-Nan Yang, Hua-Qing Wu & Shao-Ling Zhang

  2. Department of Natural Resource and Environmental Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    M Awais Khan

  3. Key Laboratory for Fruit Biotechnology Breeding of Shandong, Pomological Institute of Shandong, Taian, Shandong, 271000, People’s Republic of China

    Qing-Zhong Liu

Authors
  1. Chao Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shu-Jun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ya-Nan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hua-Qing Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M Awais Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shao-Ling Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qing-Zhong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shao-Ling Zhang or Qing-Zhong Liu.

Additional information

Communicated by A. Abbott

Chao Gu and Jun Wu contributed to this paper equally.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S 1

Phylogenetic trees of eight S-RNase and eight SFB genes identified in this study based on the multiple alignment of the nucleotide sequences using the neighbor-joining method. a Phylogenetic tree of four PpsS-RNase genes, b phylogenetic tree of four PpsSFB genes, c phylogenetic tree of four PspeS-RNase genes, d phylogenetic tree of four PspeSFB genes, e phylogenetic tree of four PpsS-RNase and four PspeS-RNase genes, and f phylogenetic tree of four PpsSFB and four PspeSFB genes (JPEG 90 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gu, C., Wu, J., Zhang, SJ. et al. Molecular analysis of eight SFB alleles and a new SFB-like gene in Prunus pseudocerasus and Prunus speciosa . Tree Genetics & Genomes 7, 891–902 (2011). https://doi.org/10.1007/s11295-011-0382-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-011-0382-6

Keyword

Search

Navigation