Skip to main content
SpringerLink
Log in

Physical mapping of a pollen modifier locus controlling self-incompatibility in apricot and synteny analysis within the Rosaceae

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

S-locus products (S-RNase and F-box proteins) are essential for the gametophytic self-incompatibility (GSI) specific recognition in Prunus. However, accumulated genetic evidence suggests that other S-locus unlinked factors are also required for GSI. For instance, GSI breakdown was associated with a pollen-part mutation unlinked to the S-locus in the apricot (Prunus armeniaca L.) cv. ‘Canino’. Fine-mapping of this mutated modifier gene (M-locus) and the synteny analysis of the M-locus within the Rosaceae are here reported. A segregation distortion loci mapping strategy, based on a selectively genotyped population, was used to map the M-locus. In addition, a bacterial artificial chromosome (BAC) contig was constructed for this region using overlapping oligonucleotides probes, and BAC-end sequences (BES) were blasted against Rosaceae genomes to perform micro-synteny analysis. The M-locus was mapped to the distal part of chr.3 flanked by two SSR markers within an interval of 1.8 cM corresponding to ~364 Kb in the peach (Prunus persica L. Batsch) genome. In the integrated genetic-physical map of this region, BES were mapped against the peach scaffold_3 and BACs were anchored to the apricot map. Micro-syntenic blocks were detected in apple (Malus × domestica Borkh.) LG17/9 and strawberry (Fragaria vesca L.) FG6 chromosomes. The M-locus fine-scale mapping provides a solid basis for self-compatibility marker-assisted selection and for positional cloning of the underlying gene, a necessary goal to elucidate the pollen rejection mechanism in Prunus. In a wider context, the syntenic regions identified in peach, apple and strawberry might be useful to interpret GSI evolution in Rosaceae.

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

Similar content being viewed by others

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 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucl Acids Res 27:573–580

    Article  PubMed  CAS  Google Scholar 

  • Bonfield J (2004) Staden package, version 1.4. http://staden.sourceforge.net. Accessed 27 July 2011

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

    Article  CAS  Google Scholar 

  • Boskovic R, Sargent DJ, Tobutt KR (2010) Genetic evidence that two independent S-loci control RNase-based self-incompatibility in diploid strawberry. J Exp Bot 61:755–763

    Article  PubMed  CAS  Google Scholar 

  • Busot GY, McClure B, Ibarra-Sánchez CP, Jiménez-Durán K, Vázquez-Santana S, Cruz-García F (2008) Pollination in Nicotiana alata stimulates synthesis and transfer to the stigmatic surface of NaStEP, a vacuolar Kunitz proteinase inhibitor homologue. J Exp Bot 59:3187–3201

    Article  PubMed  CAS  Google Scholar 

  • Cachi AM, Wünsch A (2011) Characterization and mapping of non-S gametophytic self-compatibility in sweet cherry (Prunus avium L.). J Exp Bot 62:1847–1856

    Article  PubMed  CAS  Google Scholar 

  • Cai W, Reneker J, Chow C, Vaishnav M, Bradley A (1998) An anchored framework BAC map of mouse chromosome 11 assembled using multiplex oligonucleotide hybridization. Genomics 54:387–397

    Article  PubMed  CAS  Google Scholar 

  • Cruz-Garcia FC, Hancock N, Kim D, McClure B (2005) Stylar glycoproteins bind to S-RNase in vitro. Plant J 42:295–304

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Dirlewanger E, Graziano E, Joobeur T, Garriga-Calderé F, Cosson P, Howad W, Arús P (2004) Comparative mapping and marker assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA 101:9891–9896

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang W-C, Grossniklausi U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–660

    Article  PubMed  CAS  Google Scholar 

  • Fernández A, Hanada T, Alonso JM, Yamane H, Tao R, Socías i Company R (2009) A modifier locus affecting the expression of the S-RNase gene could be the cause of breakdown of self-incompatibility in almond. Sex Plant Reprod 22:179–186

    Article  Google Scholar 

  • Goldraij A, Kondo K, Lee CB, Hancock CN, Sivaguru M, Vazquez-Santana S, Kim S, Phillips TE, Cruz-García F, McClure B (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439:805–810

    Article  PubMed  CAS  Google Scholar 

  • Grattapaglia D, Sederoff RR (1994) Genetic linkage maps of Eucalyptus grandis and E. urophylla using a pseudotest-cross strategy and RAPD markers. Genetics 137:1121–1137

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hancock CN, Kent L, McClure BA (2005) The 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J 43:716–723

    Article  PubMed  CAS  Google Scholar 

  • Hilario E, Bennell TF, Rikkerink E (2007) Screening a BAC library with nonradioactive overlapping oligonucleotide (overgo) probes. In: Hilario E, Mackay J (eds) Protocols for nucleic acid analysis by nonradioactive probes (Methods in molecular biology, vol 353). Humana press Inc, Totowa, pp 79–91

  • Hospital F (2003) Marker-assisted breeding. In: Newbury HJ (ed) Plant molecular breeding. Blackwell Publishing Ltd., Oxford, UK, pp 30–59

    Google Scholar 

  • Hua Z, Kao T-h (2006) Identification and characterization of components of a putative Petunia S-locus F-box-containing E3 ligase complex involved in S-RNase based self-incompatibility. Plant Cell 18:2531–2553

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Zhao L, Yang Q, Xue Y (2006) AhSSK1, a novel SKP1-like protein that interacts with the S-locus F-box protein SLF. Plant J 46:780–793

    Article  PubMed  CAS  Google Scholar 

  • Illa E, Sargent DJ, López-Girona E, Bushakra J, Cestaro A, Crowhurst R, Pindo M, Cabrera A, van der Knaap E, Iezzoni A, Gardiner S, Velasco R, Arús P, Chagné D, Troggio M (2011) Comparative analysis of rosaceous genomes and the reconstruction of a putative ancestral genome for the family. BMC Evol Biol 11:9

    Article  PubMed  Google Scholar 

  • Juárez-Díaz JA, McClure B, Vázquez-Santana S, Guevara-García A, León-Mejía P, Márquez-Guzmán J, Cruz–García F (2006) A novel thioredoxin h is secreted in Nicotiana alata and reduces S-RNases in vitro. J Biol Chem 281:3418–3424

    Article  PubMed  Google Scholar 

  • Jung S, Jesudurai C, Staton M, Du Z, Ficklin S, Cho I, Abbott A, Tomkins J, Main D (2004) GDR (genome database for Rosaceae): integrated web resources for Rosaceae genomics and genetics research. BMC Bioinf 5:130

    Article  Google Scholar 

  • Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogen Genome Res 110:462–467

    Article  CAS  Google Scholar 

  • Kondo K, Yamamoto M, Itahashi R, Sato T, Egashira H, Hattori T, Kowyama Y (2002) Insights into the evolution of self-compatibility in Lycopersicon from a study of stylar factors. Plant J 30:143–153

    Article  PubMed  CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175

    Article  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 

  • Lee CB, Kim S, McClure B (2009) A pollen protein, NaPCCP, that binds pistil arabinogalactan proteins also binds phosphatidylinositol 3-phosphate and associates with the pollen tube endomembrane system. Plant Physiol 149:791–802

    Article  PubMed  CAS  Google Scholar 

  • Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows-Wheeler Transform. Bioinformatics 26:589–595

    Article  PubMed  Google Scholar 

  • Maliepaard C, Alston FH, van Arkel G, Brown LM, Chevreau E, Dunemann 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 Nicotiana alata are ribonucleases. Nature 342:955–957

    Article  PubMed  CAS  Google Scholar 

  • McClure B, Mou B, Canevascini S, Bernatzky R (1999) A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc Natl Acad Sci USA 96:13548–13553

    Article  PubMed  CAS  Google Scholar 

  • McClure BA, Cruz-García F, Beecher B, Sulaman W (2000) Factors affecting inter- and intra-specific pollen rejection in Nicotiana. Ann Bot 85:113–123

    Article  Google Scholar 

  • Minamikawa M, Kakui H, Wang S, Kotoda N, Kikuchi S, Koba T, Sassa H (2010) Apple S locus region represents a large cluster of related, polymorphic and pollen-specific F-box genes. Plant Mol Biol 74:143–154

    Article  PubMed  CAS  Google Scholar 

  • Movahedi S, Van de Peer Y, Vandepoele K (2011) Comparative network analysis reveals that tissue specificity and gene function are important factors influencing the mode of expression evolution in Arabidopsis and rice. Plant Physiol 156:1316–1330

    Article  PubMed  CAS  Google Scholar 

  • Murase K, Shiba H, Iwano M, Che F-S, Watanabe M, Isogai A, Takayama S (2004) A membrane-anchored protein kinase involved in Brassica self-incompatibility signalling. Science 303:1516–1519

    Article  PubMed  CAS  Google Scholar 

  • Puerta AR, Ushijima K, Koba T, Sassa H (2009) Identification and functional analysis of pistil self-incompatibility factor HT-B of Petunia. J Exp Bot 60:1309–1318

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols (methods in molecular biology, vol 132). Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labelling of PCR fragments. Nat Biotechnol 18:233–234

    Article  PubMed  CAS  Google Scholar 

  • Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkert O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, Burns P, Davis TM, Slovin JP, Bassil N, Hellens RP, Evans C, Harkins T, Kodira C, Desany B, Crasta OR, Jensen RV, Allan AC, Michael TP, Setubal JC, Celton J-M, Rees DJG, Williams KP, Holt SH, Ruiz Rojas JJ, Chatterjee M, Liu B, Silva H, Meisel L, Adato A, Filichkin SA, Troggio M, Viola R, Ashman T-L, Wang H, Dharmawardhana P, Elser J, Raja R, Priest HD, Bryant DW Jr, Fox SE, Givan SA, Wilhelm LJ, Naithani S, Christoffel A, Salama DY, Carter J, Lopez Girona E, Zdepski A, Wang W, Kerstetter RA, Schwab W, Korban SS, Davik J, Monfort A, Denoyes-Rothan B, Arus P, Mittler R, Flinn B, Aharoni A, Bennetzen JL, Salzberg SL, Dickerman AW, Velasco R, Borodovsky M, Veilleux RE, Folta KM (2010) The genome of woodland strawberry (Fragaria vesca). Nature Genet 43:109–116

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sims TL, Ordanic M (2001) Identification of a S-ribonuclease-binding protein in Petunia hybrida. Plant Mol Biol 47:771–783

    Article  PubMed  CAS  Google Scholar 

  • Smit AFA, Hubley R, Green P (1996) RepeatMasker Open-3.0. Computer Program. http://www.repeatmasker.org

  • Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JGR, Korf I, Lapp H, Lehväslaiho H, Matsalla C, Mungall CJ, Osborne BI, Pocock MR, Schattner P, Senger M, Stein LD, Stupka E, Wilkinson MD, Birney E (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12:1611–1618

    Article  PubMed  CAS  Google Scholar 

  • Tao R, Iezzoni AF (2010) The S-RNase-based gametophytic self-incompatibility system in Prunus exhibits distinct genetic molecular features. Sci Hort 124:423–433

    Article  CAS  Google Scholar 

  • Thomson D, Henry R (1995) Single-step protocol for preparation of plant tissue for analysis by PCR. Biotechniques 19:394–400

    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 (2001) JoinMap®3.0, Software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C-E, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nature Genet 42:833–839

    Article  PubMed  CAS  Google Scholar 

  • Vilanova S, Romero C, Abernathy D, Abbott AG, Burgos L, Llácer G, Badenes ML (2003) Construction and application of a bacterial artificial chromosome (BAC) library of Prunus armeniaca L. for the identification of clones linked to the self-incompatibility locus. Mol Genet Genomics 269:685–691

    Article  PubMed  CAS  Google Scholar 

  • Vilanova S, Romero C, Burgos L, Llácer G, Badenes ML (2005) Identification of self-(in)compatiblity alleles in apricot (Prunus armeniaca L.) by PCR and sequence analysis. J Am Soc Hort Sci 130:893–898

    CAS  Google Scholar 

  • Vilanova S, Badenes ML, Burgos L, Martínez-Calvo J, Llácer G, Romero C (2006) Self-compatibility of two apricot selections is associated with two pollen-part mutations of different nature. Plant Physiol 42:629–641

    Article  Google Scholar 

  • Wang Y, Zhang W-Z, Song L-F, Zou J–J, Su Z, Wu W-H (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211

    Article  PubMed  CAS  Google Scholar 

  • Wünsch A, Hormaza JI (2004) Genetic and molecular analysis in Cristobalina sweet cherry, a spontaneous self-compatible mutant. Sex Plant Reprod 17:203–210

    Article  Google Scholar 

  • Wünsch A, Tao R, Hormaza JI (2010) Self-compatibility in ‘Cristobalina’ sweet cherry is not associated with duplications or modified transcription levels of S-locus genes. Plant Cell Rep 29:715–721

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Yamane H, Tao R (2009) Molecular basis of self-(in)compatibility and current status of S-genotyping in Rosaceous fruit trees. J Jpn Soc Hort Sci 78:137–157

    Article  CAS  Google Scholar 

  • Yamane H, Ikeda K, Hauck NR, Iezzoni AF, Tao R (2003) Self-incompatibility (S) locus region of the mutated S 6-haplotype of sour cherry (Prunus cerasus) contains a functional pollen S allele and a non-functional pistil S allele. J Exp Bot 54:2431–2437

    Article  PubMed  CAS  Google Scholar 

  • Zhao L, Huang J, Zhao Z, Li Q, Sims TL, Xue Y (2010) The Skp-like protein SSK is required for cross-pollen compatibility in S-RNase-based self-incompatibility. Plant J 62:52–63

    Article  PubMed  CAS  Google Scholar 

  • Zheng XH, Lu F, Wang Z-Y, Zhong F, Hoover J, Mural R (2005) Using shared genomic synteny and shared protein functions to enhance the identification of orthologous gene pairs. Bioinformatics 21:703–710

    Article  PubMed  CAS  Google Scholar 

  • Zhu C, Zhang YM (2007) An EM algorithm for mapping distortion segregation loci. BMC Genet 8:82

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the ‘Ministerio de Educación y Ciencia’, Research projects AGL2007-60709 and AGL2010-19208. We thank Bruce McClure for review and helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. Instituto Valenciano de Investigaciones Agrarias (IVIA), Apartado Oficial, 46113, Moncada, Valencia, Spain

    Elena Zuriaga, Laura Molina, María Luisa Badenes & Carlos Romero

Authors
  1. Elena Zuriaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura Molina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. María Luisa Badenes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carlos Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carlos Romero.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1056 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zuriaga, E., Molina, L., Badenes, M.L. et al. Physical mapping of a pollen modifier locus controlling self-incompatibility in apricot and synteny analysis within the Rosaceae. Plant Mol Biol 79, 229–242 (2012). https://doi.org/10.1007/s11103-012-9908-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-012-9908-z

Keywords

Search

Navigation