Abstract
Many species in the families of Rosaceae, Solanaceae, and Scrophulariaceae exhibit gametophytic self-incompatibility, a phenomenon controlled by two polymorphic genes at the S-locus, style-S (S-RNase) and pollen-S (SFB). Sequences of both genes show high levels of diversity, characteristic of genes involved in recognition of self-incompatibility systems in plants. In this study, S 24 -RNase and SFB 24 alleles were cloned from Prunus armeniaca cv. Chuanzhihong (Chinese apricot). Sequence comparisons of deduced amino acid sequences revealed that the P. armeniaca S 24 -haplotype has different SFB alleles, but shares a single S-RNase allele with P. armeniaca S 4 -haplotype. Moreover, P. armeniaca S 24 -RNase haplotype has a single and three different alleles with S 1 -RNase of P. tenella (dwarf almond) and S 1 -RNase of P. mira (smooth pit peach), respectively. The functionalities of SFB 24 and SFB 4 have been evaluated by pollen tube growth and controlled field tests of P. tenella and P. mira. Genetic analysis of the two intercrosses showed that progenies segregated 1:1 into two S-genotype classes, which is consistent with the expected ratio for semi-compatibility. These findings imply that the allelic function of the S 24 -haplotype is identical to that of the S 4 -haplotype in a self-incompatibility reaction. Thus, these two Prunus S-haplotypes are in fact two neutral variants of the same S-haplotype. The evolution of the S-allele is also discussed in terms of both functions and differences between S 24 - and S 4 -haplotypes in Prunus.
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References
Bokszczanin K, Palucha A, Przybyla AA (2009) Description of a new trans-generic Skb-RNase allele in apple. Euphytica 166:83–94
Burgos L, Pérez-Tornero O, Ballester J, Olmos E (1998) Detection and inheritance of stylar ribonucleases associated with incompatibility alleles in apricot. Sex Plant Reprod 11:153–158
Chen XS, Wu Y, Chen MX, He TM, Feng JR, Liang Q, Liu W, Yang HH, Zhang LJ (2006) Inheritance and correlation of self-compatibility and other yield components in the apricot hybrid F1 populations. Euphytica 150:69–74
Chookajorn T, Kachroo A, Ripoll DR, Clark AG, Nasrallah JB (2004) Specificity determinants and diversification of the Brassica self-incompatibility pollen ligand. Proc Natl Acad Sci USA 101:911–917
Crane MB, Lawrence WJC (1929) Genetical and cytological aspects of incompatibility and sterility in cultivated fruits. J Pomol Hortic Sci 7:276–301
De Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry 19:11–15
Fisher R (1961) A model for the generation of self-sterility alleles. J Theor Biol 1:411–414
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
Halász J, Pedryc A, Hegedus A (2007) Origin and dissemination of the pollen-part mutated SC haplotype which confers self-compatibility in apricot (Prunus armeniaca). New Phytol 176:792–803
Heng W, Wu HQ, Chen QX, Wu J, Zhang SJ, Zhang SL (2008) Identification of S-genotypes and novel S-RNase alleles in Prunus mume. J Hortic Sci Biotechnol 83:689–694
Heng W, Wu J, Wu H, Cao Y, Nishio T, Zhang SL (2011) Recognition specificity of self-incompatibility in Pyrus and Malus. Mol Breeding 28:549–557
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
Ikeda K, Ushijima K, Yamane H, Tao R, Hauck NR, 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
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
Kakui H, Kato M, Ushijima K, Kitaguchi M, Kato S, Sassa H (2011) Sequence divergence and loss-of-function phenotypes of S locus F-box brothers (SFBB) genes are consistent with non-self recognition by multiple pollen determinants in self-incompatibility of Japanese pear (Pyrus pyrifolia). Plant J 68:1028–1038
Kubo K, Entani T, Takara A, Wang N, Fields AM, Hua Z, Toyoda M, Kawashima S, Ando T, Isogai A, Kao TH, Takayama S (2010) Collaborative non-self recognition system in S-RNase-based self-incompatibility. Science 330:796–799
Lewis D (1949) Structure of the self-incompatibility gene. II. Induced mutation rate. Heredity 3:339–355
Lewis D (1951) Structure of the self-incompatibility gene. III. Types of spotaneous an induced mutation. Heredity 5:399–414
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 58:4347–4356
Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M (1997) Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9:1757–1766
Matton DP, Luu DT, Xike Q, Laublin G, O'Brien M, Maes O, Morse D, Cappadocia M (1999) Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles. Plant Cell 11:2087–2097
Matton DP, Luu DT, Morse D, Cappadocia M (2000) Establishing a paradigm for the generation of new S Alleles. Plant Cell 12:313–315
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
McClure BA, Gray JE, Anderson MA, Clarke AE (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347:757–760
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
Sanzol J (2010) Two neutral variants segregating at the gametophytic self-incompatibility locus of European pear (Pyrus communis L.) (Rosaceae, Pyrinae). Plant Biol 12:800–805
Sassa H, Hirano H, Ikehashi H (1992) Self-incompatibility-related RNases in styles of Japanese pear (Pyrus serotina Rehd.). Plant Cell Physiol 33:811–814
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
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 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
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
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 124:224–233
Tao R, Watari A, Hanada T, Habu T, Yaegaki H, Yamaguchi M, Yamane H (2007) Self-compatible peach (Prunus persica) has mutant versions of the S haplotypes found in self-incompatible Prunus species. Plant Mol Biol 63:109–123
Thompson 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
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 25:4876–4882
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
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
Uyenoyama MK, Newbigin E (2000) Evolutionary dynamics of dual-specificity self-incompatibility alleles. Plant Cell 12:310–311
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
Verica JA, McCubbin AG, Kao T (1998) Are the hypervariable regions of S RNases sufficient for allele-specific recognition of pollen. Plant Cell 10:314–317
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
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
Xue Y, Carpenter R, Dickinson HG, Coen ES (1996) Origin of allelic diversity in Antirrhinum S locus RNases. Plant Cell 8:805–814
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
Zhang L, Chen X, Zhang C, Liu X, Ci Z, Zhang H, Wu C, Liu C (2008a) Identification of self-incompatibility (S-) genotypes of Chinese apricot cultivars. Euphytica 160:241–248
Zhang SJ, Huang SX, Heng W, Wu HQ, Wu J, Zhang SL (2008b) Identification of S-genotypes in 17 Chinese cultivars of Japanese plum (Prunus salicina Lindl.) and molecular characterisation of 13 novel S-alleles. J Hortic Sci Biotechnol 83:635–640
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
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This work was supported by Fundamental Research Funds for the Central Universities (KYZ200911, KYZ201146).
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Gu, C., Wu, J., Du, YH. et al. Two Different Prunus SFB Alleles Have the Same Function in the Self-incompatibility Reaction. Plant Mol Biol Rep 31, 425–434 (2013). https://doi.org/10.1007/s11105-012-0518-3
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DOI: https://doi.org/10.1007/s11105-012-0518-3