Abstract
Self-incompatibility in the genus Prunus is controlled by two genes at the S-locus, S-RNase and SFB. Both genes exhibit the high polymorphism and high sequence diversity characteristic of plant self-incompatibility systems. Deduced polypeptide sequences of three myrobalan and three domestic plum S-RNases showed over 97% identity with S-RNases from other Prunus species, including almond, sweet cherry, Japanese apricot and Japanese plum. The second intron, which is generally highly polymorphic between alleles was also remarkably well conserved within these S-allele pairs. Degenerate consensus primers were developed and used to amplify and sequence the co-adapted polymorphic SFB alleles. Sequence comparisons also indicated high degrees of polypeptide sequence identity between three myrobalan and the three domestic plum SFB alleles and the corresponding Prunus SFB alleles. We discuss these trans-specific allele identities in terms of S-allele function, evolution of new allele specificities and Prunus taxonomy and speciation.
Similar content being viewed by others
References
Beppu K, Takemoto Y, Yamane H, Yaegaki, Yamaguchi M, Kataota I, Tao R (2003) Determination of S-haplotypes of Japanese plum (Prunus salicina Lindl.) cultivars by PCR and cross-pollination tests. J Hortic Sci Biotechnol 78:315–318
Bortiri E, Oh S-H, Jiang J, Baggett S, Granger A, Weeks C, Buckingham M, Potter G, Parfitt DE (2001) Phylogeny and systematics of Prunus (Rosaceae) as determined by sequence analysis of ITS and the chloroplast trnL-trnF spacer DNA. Syst Bot 26:797–807
Bošković R, Tobutt KR (1996) Correlation of stylar ribonuclease zymograms with incompatibility alleles in sweet cherry. Euphytica 90:245–250
Certal AC, Almeida RC, Bošković R, Oliveira MM, Feijó JA (2002) Structural and molecular analysis of self-incompatibility in almond (Prunus dulcis). Sex Plant Reprod 15:13–20
Clapham AR, Tutin TG, Moore DM (1987) Flora of the British Isles. 3 edn. Cambridge University Press, Cambridge
Crane MB, Lawrence WJC (1929) Genetical and cytological aspects of incompatibility and sterility in cultivated fruits. J Pomol 7:276–301
Dayhoff MO (1979) Atlas of protein sequence and structure. Volume 5. National Biomedical Research Foundation, Washington DC
De Cuyper B, Sonneveld T, Tobutt KR (2005) Determining self-incompatibility genotypes in Belgian wild cherries. Mol Ecol 14:945–955
Despres C, Saba-El-Leil M, Rivard SR, Morse D, Cappadocia M (1994) Molecular cloning of two Solanum chacoense S-alleles and a hypothesis concerning their evolution. Sex Plant Reprod 7:169–176
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochem Bull 19:11–15
Entani T, Iwano M, Shiba H, Takayama S, Fukui K, Isogai A (2003) Comparative analysis of the self-incompatibility (S-) locus region of Prunus mume: identification of pollen-expressed F-box gene with allelic diversity. Genes Cells 8:203–213
Eryomine GV (1990) New data on origin of Prunus domestica L. Acta Hortic 283:27–29
Faust M, Surányi D (1999) Origin and dissemination of plums. Hortic Rev 23:179–231
Halász J, Hegedus A, Hermán R, Stefanovits-Bányai É, Pedryc A (2005) New self-incompatibility alleles in apricot (Prunus armeniaca L.) revealed by stylar ribonuclease assay and S-PCR analysis. Euphytica 145:57–66
Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci USA 98:13167–13171
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
Ioerger TR, Clark AG, Kao T-H (1990) Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Natl Acad Sci USA 87:9732–9735
Ishimizu T, Shinkawa T, Sakiyama F, Norioka S (1998) Primary structural features of rosaceous S-RNases associated with gametophytic self-incompatibility. Plant Mol Biol 37:931–941
Klein J (1987) Origin of major histocompatibility complex polymorphism—the transspecies hypothesis. Human Immunol 19:155–162
Ladizinsky G (1999) On the origin of almond. Genet Resour Crop Evol 46:143–147
Lai Z, Ma W, Han B, Liang L, Zhang Y, Hong G, Xue Y (2002) An F-box gene linked to a self-incompatibility (S) locus in Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol Biol 50:29–42
Lecouls AC, Bergougnoux V, Rubio-Cabetas M-J, Bosselut N, Voisin R, Poessel J-L, Faurobert M, Bonnet A, Salesses G, Dirlewanger E, Esmenjaud D (2004) Marker-assisted selection for the wide-spectrum resistance to root-knot nematodes conferred by the Ma gene from myrobalan plum (Prunus cerasifera) in interspecific material. Theor Appl Genet 13:113–124
Lewis D (1949) Structure of the self-incompatibility gene II. Induced mutation rate. Heredity 3:339–355
Lu Y (2001) Roles of lineage sorting and phylogenetic relationship in the genetic diversity at the self-incompatibility locus of Solanaceae. Heredity 86:195–205
Matton DP, Luu D-T, Xike Q, Laublin G, O’Brien M, Maes O, Morse D, Cappadocia M (1999) Production of and S-RNase with dual specificity suggests a novel hypothesis for the generation of new S-alleles. Plant Cell 9:2087–2097
Matton DB, Luu D-T, Morse D (2000) Establishing a paradigm for the generation of new S-alleles. Plant Cell 12:313–315
Ortega E, Sutherland BG, Dicenta F, Bošković R, Tobutt KR (2005) Determination of incompatibility genotypes in almond using first and second intron consensus primers: detection of new S alleles and correction of reported S genotypes. Plant Breed 124:188–196
Ortega E, Bošković RI, Sargent DJ, Tobutt KR (2006) Analysis of S-RNase alleles in almond (Prunus dulcis): characterization of new sequences, resolution of synonyms and evidence of intragenic recombination. Mol Genet Genomics 276:413–426
Qiao H, Wang F, Zhao L, Lai Z, Zhang Y, Huang J, Zhang Y, Xue Y (2004) The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility. Plant Cell 16:2307–2322
Rehder A (1940) Manual of cultivated trees and shrubs hardy in North America. 2nd edn. Macmillan, New York
Richman AD, Kohn JR (1996) Learning from rejection: the evolutionary biology of single-locus incompatibility. Trends Ecol Evol 11:497–502
Roalson ER, McCubbin AG (2003) S-RNases and sexual incompatibility: structure, functions and evolutionary perspectives. Mol Phylogenet Evol 29:490–506
Saba-El-Leil MK, Rivard S, Morse D, Cappadocia M (1994) The S 11 and S 13 self-incompatibility alleles in Solanum chacoense Bitt. are remarkably similar. Plant Mol Biol 24:571–583
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
Sonneveld T (2002) The molecular genetics of self-incompatibility in sweet cherry (Prunus avium). PhD thesis, University of Nottingham, UK
Sonneveld T, RobbinsTP, 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
Sonneveld T, Tobutt KR, Robbins TP (2003) Allele-specific PCR detection of sweet cherry self-incompatibility (S) alleles S 1 to S 16 using consensus and allele-specific primers. Theor Appl Genet 107:1059–1070
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
Šurbanovski N, Tobutt KR, Konstantinović M, Maksimović, Sargent DJ, Stefanović V, Ortega E, Bošković R (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
Sutherland BG (2005) The molecular genetics of self-incompatibility in plums. PhD thesis, University of Nottingham, UK
Sutherland BG, Tobutt KR, Robbins TP (2004a) Primers amplifying a range of Prunus S-alleles. Plant Breed 123:582–584
Sutherland BG, Tobutt KR, Robbins TP (2004b) Molecular genetics of self-incompatibility in plums. Acta Hortic 663:557–562
Sutherland BG, Tobutt KR, Robbins TP (2007) Molecular genotyping of self-incompatible plum cultivars. Acta Hort 734:47–52
Steinbachs JE, Holsinger KE (2002) S-RNase mediated gametophytic self-incompatibility is ancestral in eudicots. Mol Biol Evol 19:825–829
Tao R, Yamane H, Sugiura A, Murayama H, Sassa H, Mori H (1999) Molecular typing of S-alleles through identification, characterisation and cDNA cloning for S-RNases in sweet cherry. J Am Soc Hort Sci 124:224–233
Tao R, Habu T, Namba A, Yamane H, Fuyuhiro F, Iwamoto K, Sugiura A (2002) Inheritance of Sf-RNase in Japanese apricot (Prunus mume) and its relation to self-incompatibility. Theor Appl Genet 105:222–228
Tobutt KR, Sonneveld T, Bošković R (2001) Cherry (in)compatibility genotypes—harmonisation of recent results from UK, Canada, Germany, Japan and USA. Eucarpia Fruit Breeding Section Newsletter Nr 5, July 2001
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 260:261–268
Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Gradziel TM, 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
Ushijima K, Yamane H, Watari A, Kaheki 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
Uyenoyama MK, Newbigin E (2000) Evolutionary dynamics of dual-specificity self-incompatibility alleles. Plant Cell 12:310–312
Wright S (1939) The distribution of self-sterility alleles in populations. Genetics 24:538–552
Wu J, Saupe SJ, Glass L (1998) Evidence of balancing selection operating at the het-c heterokaryon incompatibility locus in a group of filamentous fungi. Proc Natl Acad Sci USA 95:12398–12403
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
Acknowledgments
We thank Dr Encarna Ortega at CEBAS-CSIC (Spain) and Dr Simon Vaughan (EMR) for providing SFB allele sequence data for almond and sweet cherry. Thanks also to Emma-Jane Lamont at the National Fruit Collections at Brogdale (UK), Dr Encarna Ortega (CEBAS-CSIC) and Dr Yoshihiko Sato at the National Institute of Fruit Tree Science (Japan) for supplying Prunus material, and to Javier-Maria de Vera y Asensio for help with preparing the graphics. Bruce Sutherland gratefully acknowledges a PhD studentship from the University of Nottingham and the East Malling Trust for Horticultural Research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Herrmann.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sutherland, B.G., Tobutt, K.R. & Robbins, T.P. Trans-specific S-RNase and SFB alleles in Prunus self-incompatibility haplotypes. Mol Genet Genomics 279, 95–106 (2008). https://doi.org/10.1007/s00438-007-0300-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-007-0300-7