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Plant Cell Reports

, Volume 29, Issue 7, pp 715–721 | Cite as

Self-compatibility in ‘Cristobalina’ sweet cherry is not associated with duplications or modified transcription levels of S-locus genes

  • A. WünschEmail author
  • R. Tao
  • J. I. Hormaza
Original Paper

Abstract

Sweet cherry shows S-RNase-based gametophytic self-incompatibility, which prevents self- and cross-fertilization between genetically related individuals. The specificity of the self-incompatible reaction is determined by two genes located in the S-locus. These encode a pistil-expressed ribonuclease (S-RNase) that inhibits self pollen tube growth, and a pollen-expressed F-box protein (SFB) that may be involved in the cytotoxicity of self-S-RNases. Initial genetic and pollination studies in a self-compatible sweet cherry cultivar, ‘Cristobalina’ (S 3 S 6), showed that self-compatibility was caused by the loss of pollen function of both haplotypes (S 3 and S 6). In this study, we further characterize self-compatibility in this genotype by molecular analysis of the S-locus. DNA blot analyses using S-RNase and SFB probes show no duplications of ‘Cristobalina’ S-locus genes or differences in the restriction patterns when compared with self-incompatible cultivars with the same S-genotype. Furthermore, reverse transcriptase-PCR of S-locus genes and quantitative reverse transcription-PCR of SFBs revealed no differences at the transcription level when compared with a self-incompatible genotype. The results of this study show that no differences at the S-locus can be correlated with self-compatibility, indicating the possible involvement of non-S-locus modifiers in self-incompatibility breakdown in this cultivar.

Keywords

Prunus avium Gametophytic self-incompatibility Pollen part mutant 

Notes

Acknowledgments

This work was financed by a JSPS Postdoctoral Fellowship awarded to A.W. and research projects JSPS-CSIC: 2004JP0087, Spanish Ministry of Education AGL2007-60130/AGR and INIA- RTA2006-00118.

References

  1. Bošković R, Tobutt KR (1996) Correlation of stylar ribonuclease zymograms with incompatibility alleles in sweet cherry. Euphytica 90:245–250CrossRefGoogle Scholar
  2. Calabrese F, Fenech L, Raimondo A (1984) Kronio: una cultivar di cilegio molto precoce e utocompatibile. Frutticoltura 46:27–30Google Scholar
  3. Crane MB, Lawrence JC (1929) Genetical and cytological aspects of incompatibility and sterility in cultivated fruits. J Pomol Hortic Sci 7:276–301Google Scholar
  4. De Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants, 2nd edn. Springer, BerlinGoogle Scholar
  5. Entani T, Iwano M, Shiba H, Che F-S, 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 8:203–213CrossRefPubMedGoogle Scholar
  6. Fernández i Martí A, Hanada T, Alonso JM, Yamane H, Ryutaro T, Socias 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. doi: 10.1007/s00497-009-0102-7
  7. Goldraij A, Kondo K, Katsuhiko L, Christopher BH, Nathan C, Sivaguru M, Vazquez-Santana S, Kim S, Phillips TE, Cruz-Garcia F, McClure B (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439:805–810CrossRefPubMedGoogle Scholar
  8. Golz JF, Clarke AE, Newbigin E (1999) A molecular description of mutations affecting the pollen component of the Nicotiana alata S-locus. Genetics 152:1123–1135PubMedGoogle Scholar
  9. Golz JF, Clarke AE, Newbigin E (2000) Mutational approaches to the study of self-incompatibility: revising pollen-part mutants. Ann Bot 85:95–103CrossRefGoogle Scholar
  10. Hanada T, Fukuta K, Yamane H, Esumi T, Tao R, Gradziel TM, Dandekar AM, Marti AFI, Alonso JM (2009) Cloning and characterization of a self-compatible S-f Haplotype in almond [Prunus dulcis (Mill.) DA Webb. syn. P. amygdalus Batsch] to resolve previous confusion in its S-f-RNase sequence. Hortscience 44:609–613Google Scholar
  11. Hauck NR, Yamane H, Tao R, Iezzoni AF (2002) Self-compatibility and incompatibility in tetraploid sour cherry (Prunus cerasus L.). Sex Plant Reprod 15:39–46CrossRefGoogle Scholar
  12. Hauck NR, Yamane H, Tao R, Iezzoni AF (2006) Accumulation of nonfunctional S-haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus. Genetics 172:1191–1198CrossRefPubMedGoogle Scholar
  13. Herrero J (coord.) (1964) Cartografía de las variedades frutales de hueso y pepita. CSIC Aula Dei, ZaragozaGoogle Scholar
  14. Hua ZH, Kao TH (2006) Identification and characterization of components of a putative S-locus F-box containing E3 ligase complex involved in S-RNase-based-self-incompatibility. Plant Cell 18:2531–2553CrossRefPubMedGoogle Scholar
  15. Hua ZH, Fields A, Kao TH (2008) Biochemical models for S-RNase-based self-incompatibility. Mol Plant 1:575–585CrossRefPubMedGoogle Scholar
  16. 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 46:780–793CrossRefPubMedGoogle Scholar
  17. Huang SX, Wu HQ, Li YR, Wu J, Zhang SJ, Heng W, Zhang SL (2009) Competitive interaction between two functional S-haplotypes confer self-compatibility on tetraploid Chinese cherry (Prunus pseudocerasus Lindl. CV. Nanjing Chuisi). Plant Cell Rep 27:1075–7085CrossRefGoogle Scholar
  18. Hugard J (1978) Origine du pollen et varietes pollinisatrices. Le Fruit Belge 381:11–32Google Scholar
  19. 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 16:235–243CrossRefGoogle Scholar
  20. 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 58:4347–4356CrossRefPubMedGoogle Scholar
  21. McClure B (2009) Darwin’s foundation for investigating self-incompatibility and the progress toward a physiological model for S-RNase-based SI. J Exp Bot 60:1069–1081CrossRefPubMedGoogle Scholar
  22. McClure B, Frankling-Tong V (2006) Gametophytic self-incompatibility: understanding the cellular mechanisms involved in ‘self’ pollen tube inhibition. Planta 224:233–245CrossRefPubMedGoogle Scholar
  23. McClure BA, Gray JE, Anderson MA, Clarke AE (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347:757–760CrossRefGoogle Scholar
  24. McClure BA, Mou B, Canevascini S, Bernatzky R (1999) A small asparagines-rich protein required for S-allele specific pollen rejection in Nicotiana. Proc Natl Acad Sci 96:13548–13553CrossRefPubMedGoogle Scholar
  25. Sims TL, Ordanic M (2001) Identification of a S-ribonuclease-binding protein in Petunia hybrida. Plant Mol Biol 47:771–783CrossRefPubMedGoogle Scholar
  26. 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 17:37–51CrossRefPubMedGoogle Scholar
  27. Tao R, Iezzoni AF (2010) The S-RNase-based gametophytic self-incompatibility system in Prunus exhibits distinct genetic and molecular features. Scientia Horticulturae 124:423–433CrossRefGoogle Scholar
  28. 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 38:304–311PubMedGoogle Scholar
  29. 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 124:224–233Google Scholar
  30. Ushijima K, Sassa H, Tao R, Yamane H, Dandekar AM, Gradziel TM, Hirano H (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 260:261–268CrossRefPubMedGoogle Scholar
  31. Ushijima K, Sassa H, Tamura M, Kusaba M, Tao R, Gradziel TM, Dandekar AM, Hirano H (2001) Characterization of the S-locus region of almond (Prunus dulcis): Analysis of a somaclonal mutant and a cosmid contig for S haplotype. Genetics 158:379–386PubMedGoogle Scholar
  32. Ushijima K, Sassa H, Dandekar HM, 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 15:771–781CrossRefPubMedGoogle Scholar
  33. 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 39:573–586CrossRefPubMedGoogle Scholar
  34. 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 142:629–641CrossRefPubMedGoogle Scholar
  35. Watari A, Hanada T, Yamane H, Esumi T, Tao R, Yaegaki H, Yamaguchi M, Beppu K, Kataoka I (2007) A low transcriptional level of S-e-RNase in the S-e-haplotype confers self-compatibility in Japanese plum. J Am Soc Hortic Sci 132:396–406Google Scholar
  36. Wünsch A, Hormaza JI (2004a) Genetic and molecular analysis in Cristobalina sweet cherry: a spontaneous self-compatible mutant. Sex Plant Reprod 17:203–210CrossRefGoogle Scholar
  37. Wünsch A, Hormaza JI (2004b) S-allele identification in sweet cherry cultivars by PCR analysis. Plant Breed 127:327–331CrossRefGoogle Scholar
  38. Xue Y, Zhang Y, Yang Q, Li Q, Cheng Z, Dickinson HG (2009) Genetic features of a pollen-part mutation suggest an inhibitory role for the Antirrhinum pollen self-incompatibility determinant. Plant Mol Biol 70:499–509CrossRefPubMedGoogle Scholar
  39. Yamane H, Tao R (2009) Molecular basis of self-(in)compatibility and current status of S-genotyping in rosaceous fruit trees. J Jpn Soc Hortic Sci 78:137–157CrossRefGoogle Scholar
  40. Yamane H, Ikeda K, Ushijima K, Sassa H, Tao R (2003) 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 44:764–769CrossRefPubMedGoogle Scholar
  41. Zhang HB, Zhao X, Ding X, Paterson AH, Wing RA (1995) Preparation of megabase-size DNA from plant nuclei. Plant J 7:175–184CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Centro de Investigación y Tecnología Agroalimentaria de AragónZaragozaSpain
  2. 2.Graduate School of AgricultureKyoto UniversityKyotoJapan
  3. 3.Instituto de Hortofruticultura Subtropical y Mediterránea “La Mayora”, Estación Experimental “La Mayora”Universidad de Málaga Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC)MalagaSpain

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