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Cloning and mapping multiple S-locus F-box genes in European pear (Pyrus communis L.)

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Abstract

European pear, as well as its close relatives Japanese pear and apple, exhibits S-RNase-based gametophytic self-incompatibility. The male determinant of this self-incompatibility mechanism is a pollen-expressed protein containing an F-box domain; in the genera Petunia (Solanaceae), Antirrhinum (Plantaginaceae), and Prunus (Rosaceae), a single F-box gene determines the pollen S. In apple and Japanese pear, however, multiple S-locus F-box genes were recently identified as candidates for the pollen S, and they were named S-locus F-Box Brothers. These genes were considered good candidates for the pollen S determinant since they exhibit S-haplotype-specific polymorphisms, pollen-specific expression, and linkage to the S-RNase. In the present study, S-locus F-Box Brothers homologs have been cloned from two of the most agronomically important European pear varieties, “Abbé Fétel” (S104-2/S105) and “Max Red Bartlett” (S101/S102), and they have been mapped on a genetic linkage map developed on their progeny. Our results suggest that the number of F-box genes linked to the S-locus of the European pear is higher than expected according with previous reports for apple and Japanese pear, since up to five genes were found to be linked to a single S-haplotype. Moreover, two of these genes exhibited an incomplete linkage to the S-RNase, allowing the identification of low-frequency recombinant haplotypes, generated by a crossing-over event between the two genes. These F-box genes are most likely placed in close proximity of the S-locus but do not belong to it, and they can thus be excluded from being responsible for the determination of pollen S function.

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References

  • Anderson MA, Cornish EC, Mau SL, Williams EG, Hoggart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penschow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE (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 

  • Bredemeijer GMM, Blaas J (1981) S-specific proteins in styles of self-incompatible Nicotiana alata. Theor Appl Genet 59:185–190

    Article  CAS  Google Scholar 

  • Campbell CS, Evans RC, Morgan DR, Dickinson TA, Arsenault MP (2007) Phylogeny of subtribe Pyrinae (formerly the Maloideae, Rosaceae): limited resolution of a complex evolutionary history. Plant Syst Evol 266:119–145

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Dondini L, Pierantoni L, Gaiotti F, Chiodini R, Tartarini S, Bazzi C, Sansavini S (2004) Identifying QTLs for fire-blight resistance via a European pear (Pyrus communis L.) genetic linkage map. Mol Breeding 14:407–418

    Article  CAS  Google Scholar 

  • Dondini L, Pierantoni L, Ancarani V, D’Angelo M, Cho KH, Shin IS, Musacchi S, Kang SJ, Sansavini S (2008) The inheritance of the red colour character in European pear (Pyrus communis L.) and its map position in the mutated cultivar ‘Max Red Bartlett. Plant Breeding 127:524–526

    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 

  • Goldway M, Takasaki T, Sanzol J, Mota M, Zisovich AH, Stern RA, Sansavini S (2009) Renumbering the S-RNase alleles of European pears (Pyrus communis L.) and cloning the S109 RNase allele. Sci Hortic 119:417–422

    Article  CAS  Google Scholar 

  • Hauck NR, Ikeda K, Tao R, Iezzoni AF (2006) The mutated S1-haplotype in sour cherry has an altered S-haplotype-specific F-box protein gene. J Hered 97:514–520

    Article  PubMed  CAS  Google Scholar 

  • Igic B, Smith WA, Robertson KA, Schaal BA, Kohn JR (2007) Studies of self-incompatibility in wild tomatoes: I. S-allele diversity in Solanum chilense Dun. (Solanaceae). Heredity 99:553–561

    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 

  • Ioerger TR, Gohlke JR, Xu B, Kao TH (1991) Primary structural features of the self-incompatibility protein in Solanaceae. Sex Plant Reprod 4:81–87

    Article  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, Tsuzuki T, Koba T, Sassa H (2007) Polymorphism of SFBB-gamma and its use for S genotyping in Japanese pear (Pyrus pyrifolia). Plant Cell Rep 26:1619–1625

    Article  PubMed  CAS  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 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van De Weg E, Gessler C (2002) Development and characterization of 140 new microsatellites in apple Malus × domestica Borkh.). Mol Breeding 10:217–241

    Article  CAS  Google Scholar 

  • Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003) Creating a saturated reference map for the apple (Malus × domestica Borkh.) genome. Theor Appl Genet 106:1497–1508

    PubMed  CAS  Google Scholar 

  • Maguire TL, Collins GG, Sedgley M (1994) A modified CTAB DNA extraction procedure for plants belonging to the family Proteaceae. Plant Mol Biol Rep 12:106–109

    Article  CAS  Google Scholar 

  • Maliepaard C, Alston FH, Van Arkel G, Brown LM, Chevreau E, Dunemann F, Evans KM, Gardiner S, Guilford P, Van Heusden AW, Janse J, Laurens F, Lynn JR, Manganaris AG, Den Nijs APM, Periam N, Rikkerink E, Roche P, Ryder C, Sansavini S, Schmidt H, Tartarini S, Verhaegh JJ, Vrielink-van Ginkel M, King GJ (1998) Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet 97:60–73

    Article  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 

  • Mota M, Tavares L, Oliveira CM (2007) Identification of S-alleles in pear (Pyrus communis L) cv. ‘Rocha’ and other European cultivars. Sci Hortic 113:13–19

    Article  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 

  • Nunes MDS, Santos RAM, Ferreira SM, Vieira J, Vieira CP (2006) Variability patterns and positively selected sites at the gametophytic self-incompatibility pollen SFB gene in a wild self-incompatible Prunus spinosa (Rosaceae) population. New Phytol 172:577–587

    Article  PubMed  CAS  Google Scholar 

  • Patocchi A, Walser M, Tartarini S, Broggini GAL, Gennari F, Sansavini S, Gessler C (2005) Identification by genome scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene Vm. Genome 48:630–636

    Article  PubMed  CAS  Google Scholar 

  • Pierantoni L, Cho KH, Shin IS, Chiodini R, Tartarini S, Dondini L, Kang SJ, Sansavini S (2004) Characterisation and transferability of apple SSRs to two European pear F1 populations. Theor Appl Genet 109:1519–1524

    Article  PubMed  CAS  Google Scholar 

  • Pierantoni L, Dondini L, Cho KH, Shin IS, Gennari F, Chiodini R, Tartarini S, Kang SJ, Sansavini S (2007) Pear scab resistance QTLs via a European pear (Pyrus communis) linkage map. Tree Genet Genomes 4:311–317

    Article  Google Scholar 

  • Potter D, Eriksson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Plant Syst Evol 266:5–43

    Article  Google Scholar 

  • Qiao H, Wang F, Zhao L, Zhou J, Lai Z, Zhang Y, Robbins TP, Xue Y (2004) The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility. Plant Cell 16:2307–2322

    Article  PubMed  CAS  Google Scholar 

  • Sanzol J (2009a) Genomic characterization of self-incompatibility ribonucleases (S-RNases) in European pear cultivars and development of PCR detection for 20 alleles. Tree Genet Genomes 5:393–405

    Article  Google Scholar 

  • Sanzol J (2009b) Pistil-function breakdown in a new S-allele of European pear, S21° confers self-compatibility. Plant Cell Rep 28:457–467

    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. doi:10.1111/j.1438-8677.2009.00277.x

  • Sanzol J, Robbins TP (2008) Combined analysis of S alleles in European pear by fertilization efficiency of pollinations and PCR based S-genotyping: correlation between S phenotypes and S-RNase genotype. J Am Soc Hortic Sci 133:213–224

    Google Scholar 

  • Sanzol J, Sutherland BG, Robbins TP (2006) Identification and characterization of genomic DNA sequences of the S-ribonuclease gene associated with self-incompatibility alleles S1 to S5 in European pear. Plant Breeding 125:513–518

    Article  CAS  Google Scholar 

  • Sassa H, Kakui H, Miyamoto M, Suzuki Y, Hanada T, Ushijima K, Kusaba M, Hirano H, Koba T (2007) S locus F-box brothers: multiple and pollen-specific F-box genes with S haplotype-specific polymorphisms in apple and Japanese pear. Genetics 175:1869–1881

    Article  PubMed  CAS  Google Scholar 

  • Sassa H, Kakui H, Minamikawa M (2010) Pollen-expressed F-box gene family and mechanism of S-RNase-based gametophytic self-incompatibility (GSI) in Rosaceae. Sex Plant Reprod 23:39–43

    Article  PubMed  CAS  Google Scholar 

  • Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao TH (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302–305

    Article  PubMed  CAS  Google Scholar 

  • Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh) genome. Tree Genet Genomes 2:202–224

    Article  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 

  • Takasaki T, Moriya Y, Okada K, Yamamoto K, Iwanami H, Bessho H, Nakanishi T (2006) cDNA cloning of nine S alleles and establishment of a PCR-RFLP system for genotyping European pear cultivars. Theor Appl Genet 112:1543–1552

    Article  PubMed  CAS  Google Scholar 

  • Takebayashi N, Brewer PB, Newbigin E, Uyenoyama MK (2003) Patterns of variation within self-incompatibility loci. Mol Biol Evol 20:1778–1794

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tsukamoto T, Hauck NR, Tao R, Jiang N, Iezzoni AF (2006) Molecular characterization of three non-functional S-haplotypes in sour cherry (Prunus cerasus). Plant Mol Biol 62:371–383

    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 

  • Van Ooijen JW, Voorrips RE (2002) Joinmap 3.0, Software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands

    Google Scholar 

  • Vieira J, Morales-Hojas R, Santos RAM, Vieira CP (2007) Different positively selected sites at the gametophytic self-incompatibility pistil S-RNase gene in the Solanaceae and Rosaceae (Prunus, Pyrus, and Malus). J Mol Evol 65:175–185

    Article  PubMed  CAS  Google Scholar 

  • Vieira J, Fonseca NA, Vieira CP (2009) RNase-Based gametophytic self-incompatibility evolution: questioning the hypothesis of multiple independent recruitments of the S-pollen gene. J Mol Evol 69:32–41

    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 

  • Voorrips RE (2002) MapChart: Software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Tsukamoto T, Yi KW, Wang X, Huang S, McCubbin AG, Kao TH (2004) Chromosome walking in the Petunia inflata self-incompatibility (S-) locus and gene identification in an 881-kb contig containing S2-RNase. Plant Mol Biol 54:727–742

    Article  PubMed  CAS  Google Scholar 

  • Wheeler D, Newbigin E (2007) Expression of 10S-class SLF-like genes in Nicotiana alata pollen and its implications for understanding the pollen factor of the S locus. Genetics 177:2171–2180

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto T, Kimura T, Shoda M, Imai T, Saito T, Sawamura Y, Kotobuki K, Hayashi T, Matsuta N (2002) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor Appl Genet 106:9–18

    PubMed  CAS  Google Scholar 

  • Zisovich AH, Stern RA, Shafir S, Goldway M (2004) Identification of seven S-alleles from the European pear (Pyrus communis) and the determination of compatibility among cultivars. J Hortic Sci Biotech 80:143–146

    Google Scholar 

  • Zisovich AH, Stern RA, Shafir S, Goldway M (2009) Identification of seven haplotype-specific SFBs in European pear (Pyrus communis) and their use as molecular markers. Sci Hortic 121:49–53

    Article  CAS  Google Scholar 

  • Zuccherelli S, Tassinari P, Broothaerts W, Tartarini S, Dondini L, Sansavini S (2002) S-allele characterization in self-incompatible pear (Pyrus communis L.). Sex Plant Reprod 15:153–158

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the PRIN project (MIUR, Rome) 2007 “The productive process in fruit tree species: molecular, physiological and agronomical aspects of floral incompatibility and strategies for its control” and “Ministerio de Ciencia e Innovación de España”—EU-FEDER (project grant CICYT AGL2009-12621-C02-02). J.S. acknowledges the “Instituto de Investigación y Tecnología Agroalimentaria”—INIA_CCAA program and the “Ministerio de Ciencia e Innovación de España”—I3 program for financial support.

Ethical standards and conflict of interest declaration

The authors declare that all the experiments comply with the current laws of the country in which they were performed (Italy, Spain) and that they have no conflict of interests.

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Authors and Affiliations

  1. Dipartimento di Colture Arboree (DCA), Università degli Studi di Bologna, Via Giuseppe Fanin 46, 40127, Bologna, Italy

    Paolo De Franceschi, Luca Pierantoni, Luca Dondini, Marco Grandi & Silviero Sansavini

  2. Unidad de Fruticultura, Centro de Investigación y Tecnología Agroalimentaria de Aragón (CITA), Avenida de Montañana 930, 50059, Zaragoza, Spain

    Javier Sanzol

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  1. Paolo De Franceschi
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  2. Luca Pierantoni
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  5. Javier Sanzol
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  6. Silviero Sansavini
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Correspondence to Paolo De Franceschi.

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Communicated by E. Dirlewanger

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De Franceschi, P., Pierantoni, L., Dondini, L. et al. Cloning and mapping multiple S-locus F-box genes in European pear (Pyrus communis L.). Tree Genetics & Genomes 7, 231–240 (2011). https://doi.org/10.1007/s11295-010-0327-5

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