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Molecular and Evolutionary Characterization of Pollen S Determinant (SFB Alleles) in Four Diploid and Hexaploid Plum Species (Prunus spp.)

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Abstract

In more than 60 families of angiosperms, the self- and cross-fertilization is avoided through a complex widespread genetic system called self-incompatibility (SI). One of the major puzzling issues concerning the SI is the evolution of this system in species with complex polyploid genomes. Among plums, one of the first fruits species to attract human interest, polyploid species represent enormous genetic potential, which can be exploited in breeding programs. However, molecular studies in these species are very scarce due to the complexity of their genome. In order to study the SFB gene [the male component of gametophytic self-incompatibility system (GSI)] in plum species, 36 plum accessions belonging to diploid and hexaploid species were used. A total of 19 different alleles were identified; 1 of them was revealed after analyzing sequences. Peptide sequence analysis allowed identifying the five domains features of the SFB gene. Polymorphism analysis showed a subtle difference between domesticated and open pollinated Tunisian accessions and suggested a probable influence of the ploidy level. Divergence analysis between studied sequences showed that a new specificity may appear after 5.3% of divergence at synonymous sites between pairs of sequences in Prunus insititia, 6% in Prunus cerasifera, 8% and 9% in Prunus domestica and Prunus salicina respectively. Furthermore, sites under positive selection, the ones more likely to be responsible for specificity determination, were identified. A positive and significant Pearson correlation was found between the divergence between sequences, divergence time, fixed substitutions (MK test), and PSS number. These results supported the model assuming that functionally distinct proteins have arisen not as a result of chance fixation of neutral variants, but rather as a result of positive Darwinian selection. Further, the role that plays recombination can not be ruled out, since a rate of 0.08 recombination event per polymorphic sites was identified.

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Data Availability

The data sets supporting this article have been uploaded as part of the Supporting Information. The nucleotide sequence data of the SFB gene for Prunus species were deposited in the GeneBank nucleotide sequence databases with the accession numbers KU728959–KU728994.

Abbreviations

Bs:

Bootstrap value

C :

Conservation level between nucleotide sequences

GSI:

Gametophytic self-incompatibility system

K A :

Divergence between alleles at non-synonymous sites

K S :

Divergence between alleles at synonymous sites

MK:

McDonald and Kreitman test

Myr:

Million years

P A :

Polymorphism at non-synonymous sites

P S :

Polymorphism at synonymous sites

PSS:

Positively selected sites

R m :

Minimum number of recombination

R NS :

Rate of new specificity appearance

SFB:

S-haplotype-specific F-box

SI:

Self-incompatibility system

S-RNase:

S-Ribonuclease

T div :

Divergence time

References

  • Abdallah D, Baraket G, Ben Tamarzizt H, Ben Mustapha S, Salhi-Hannachi A (2016) Identification, evolutionary patterns and intragenic recombination of the gametophytic self incompatibility pollen gene (SFB) in Tunisian Prunus species (Rosaceae). Plant Mol Biol Rep 34:339–352

    Google Scholar 

  • Abdallah D, Baraket G, Perez V, Ben Mustapha S, Salhi Hannachi A, Hormaza I (2019) Analysis of self-incompatibility and genetic diversity in diploid and hexaploid plum genotypes. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00896

    Article  PubMed  PubMed Central  Google Scholar 

  • Aguiar B, Vieira J, Cunha AE, Fonseca NA, Iezzoni A, van Nocker S et al (2015) Convergent evolution at the gametophytic self-incompatibility system in Malus and Prunus. PLoS ONE 10:e0126138

    PubMed  PubMed Central  Google Scholar 

  • Akagi T, Henry IM, Morimoto T, Tao R (2016) Insights into the Prunus-specific S-RNase-based self-incompatibility system from a genome-wide analysis of the evolutionary radiation of S locus-related F-box genes. Plant Cell Physiol 57(6):1281–1294

    CAS  PubMed  Google Scholar 

  • Bonferroni CE (1936) Teoriastatisticadelleclassi e calcolodelleprobabilità. Pubbl R Ist Super Sci Econ Commer Firenze 8:3–62

    Google Scholar 

  • Botu M, Sarpe C, Cosmulescu S (2002) The genetic control of pollen fertility, pollinizing and fruit set for the Prunus domestica L. plum cultivars. Acta Hortic 577:139–145

    Google Scholar 

  • Castric V, Vekemans X (2004) Plant self-incompatibility in natural populations: a critical assessment of recent theoretical and empirical advances. Mol Ecol 13:2873–2889

    CAS  PubMed  Google Scholar 

  • Charlesworth D, Vekemans X, Castric V, Glemin S (2005) Plant self-incompatibility systems: a molecular evolutionary perspective. N Phytol 168:61–69

    CAS  Google Scholar 

  • Das B, Ahmed N, Singh P (2011) Prunus diversity–early and present development: a review. Int J Biodivers Conserv 14:721–734

    Google Scholar 

  • De Candolle A (1964) Origin of cultivated plants. Hafner Publ. Co., New York

    Google Scholar 

  • De Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants, 2nd edn. Springer, Berlin

    Google Scholar 

  • Decroocq V, Hagen LS, Favé MG, Eyquard JP, Pierronnet A (2004) Microsatellite markers in the hexaploid Prunus domestica species and parentage lineage of three European plum cultivars using nuclear and chloroplast simple-sequence repeats. Mol Breed 13:135–142

    CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1987) Isolation of DNA from fresh plant tissue. Focus 12:13–15

    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

    CAS  PubMed  Google Scholar 

  • Fisher RA (1929) Tests of significance in harmonic analysis. Proc R Soc Lond A 125(796):54–59

    Google Scholar 

  • Gu C, Lu W, Korban SS, Han Y (2015) Identification and characterization of S-RNase genes and S-genotypes in Prunus and Malus species. Can J Plant Sci 95:1–13

    Google Scholar 

  • Halász J, Kurilla A, Hegedûs A (2014) Preliminary characterization of the self-incompatibility genotypes of European plum (Prunus domestica L.) cultivars. Int J Hortic Sci 20:23–26

    Google Scholar 

  • Halász J, Makovics-Zsoha N, Szöke F, Ercilis S, Hegedüs A (2017) Simple sequence repeat and S-locus genotyping to explore genetic variability in polyploid Prunus spinosa and P. insititia. Biochem Genet 55:22–33

    PubMed  Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9

    Google Scholar 

  • Hammer LB, Kossek EE, Yragui NL, Bodner TE, Hanson GC (2009) Development and validation of a multidimensional measure of family support supervisor behaviors (FSSB). J Manag 35:837–856

    Google Scholar 

  • Hudson RR, Kreitman M, Aquadé M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159

    CAS  PubMed  PubMed Central  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

    CAS  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro H (ed) Mammalian protein metabolism. Academic, New York, pp 21–32

    Google Scholar 

  • Kato S, Mukai Y (2004) Allelic diversity of S-RNase at the self-incompatibility locus in natural flowering cherry populations (Prunus lannesiana var. speciosa). Heredity 92:249–256

    CAS  PubMed  Google Scholar 

  • Kota-Dombrovska I, Lâcis G (2013) Evaluation of self-incompatibility locus diversity of domestic plum (Prunus domestica L.) using DNA-based S-genotyping. Proc Latv Acad Sci B 67(2, 683):109–115.

    Google Scholar 

  • Kumar S, Gadagkar SR (2001) Disparity Index: a simple statistic to measure and test the homogeneity of substitution patterns between molecular sequences. Genetics 158:1321–1327

    CAS  PubMed  PubMed Central  Google Scholar 

  • McCubbin AG, Wang X, Kao T-H (2000) Identification of self-incompatibility (S-) locus linked pollen cDNA markers in Petunia inflata. Genome 43:619–627

    CAS  PubMed  Google Scholar 

  • Mcdonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654

    CAS  PubMed  Google Scholar 

  • Mestre L, Reig G, Betrán J, Moreno MA (2017) Influence of plum rootstocks on agronomic performance, leaf mineral nutrition and fruit quality of ‘Catherina’ peach cultivar in heavy-calcareous soil conditions. Span J Agric Res 15(1):e0901

    Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    CAS  PubMed  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    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. N Phytol 172:577–587

    CAS  Google Scholar 

  • OECD (2002) Consensus Document on the Biology of Prunus spp. (Stone fruits), vol 1. Environment Directorate, OECD, Paris, p 42

  • Ortega E, Bošković R, Sargent DJ, Tobutt KR (2006) Analysis of S-RNase alleles of almond (Prunus dulcis): characterization of new sequences, resolution of synonyms and evidence of intragenic recommendation. Mol Gen Genet 276:413–426

    CAS  Google Scholar 

  • Reig G, Jiménez S, Mestre L, Font iForcada C, Betrán JA, Moreno MA (2018) Horticultural, leaf mineral and fruit quality traits of two ‘Greengage’ plum cultivars budded on plum based rootstocks in Mediterranean conditions. Sci Hortic 232:84–91

    CAS  Google Scholar 

  • Rozas J, Sánchez-del Barrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analysis and other methods. Bioinformatics 19:2496–2497

    CAS  PubMed  Google Scholar 

  • Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum evolution trees. Mol Biol Evol 9:945–967

    CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sassa H (2016) Molecular mechanism of the S-RNase-based gametophytic self-incompatibility in fruit trees of Rosaceae. Breed Sci 66:116–121

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sawyer SA, Hartlt DL (1992) Population genetics of polymorphism and divergence. Genetics 132:1161–1176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson J, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX window interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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): analysis of a somaclonal mutant and a cosmid contig for an S haplotype. Genetics 158:771–781

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uyenoyama MK (1997) Genealogical structure among alleles regulating self-incompatibility in natural populations of flowering plants. Genetics 147:1389–1400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vieira J, Ferreira PG, Aguiar B, Fonseca NA, Vieira CP (2010) Evolutionary patterns at the RNase based gametophytic self-incompatibility system in two divergent Rosaceae groups (Maloideae and Prunus). BMC Evol Biol 10:200

    PubMed  PubMed Central  Google Scholar 

  • Vieira J, Fonseca NA, Santos RAM, Habu T, Tao R, Vieira CP (2008a) The number, age, sharing and relatedness of S-locus specificities in Prunus. Genet Res 90:17–26

    CAS  Google Scholar 

  • Vieira J, Teles E, Santos RAM, Vieira CP (2008b) Recombination at Prunus S-locus region SLFL1 gene. Genetics 180:483–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vieira CP, Charlesworth D, Vieira J (2003) Evidence for rare recombination at the gametophytic selfincompatibility locus. Heredity 91:262–267

    CAS  PubMed  Google Scholar 

  • Wright S (1939) The distribution of self-sterility alleles in populations. The University of Chicago, Chicago

    Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373

    CAS  PubMed  Google Scholar 

  • Zeng B, Wang J, Hao Q, Yu Z, Abudukayoumu A, Tang Y, Zhang X, Ma X (2019) Identification of a novel SBP1-containing SCF SFB complex in wild dwarf almond (Prunus tenella). Front Genet 10:1019

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Kitashiba N (2007) Identification of S-haplotype-specific F-box gene in Japanese plum (Prunus salicina Lindl). Sex Plant Reprod 20:1–8

    Google Scholar 

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Acknowledgements

The authors would like to gratefully thank ‘Sodon collection’ (Bou-Selem, Tunisia), Tunisian farmers and the ‘EEAD-CSIC Prunus bank germplasm’ (Zaragoza, Spain) for kindly providing plant material. We gratefully acknowledge V. Guajardo for critical review of the manuscript.

Funding

This research was supported by the Tunisian ‘Ministère de l’Enseignement supérieur et de la Recherche Scientifique’ and the Project PCI ref. AP/038338/11, funded by the ‘Agencia Española de Cooperación Internacional para el Desarrollo-AECID’of the Spanish Ministry of Foreign Affairs and Cooperation.

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DA performed the experiments and statistical analyses, developed the genetic analyses and wrote the manuscript. GB provided some plant material, discussed and corrected the content. SBM developed some molecular tests. MAM and ASH offered experimental instructions, supervised and provided editorial advice.

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Correspondence to Amel Salhi Hannachi.

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Abdallah, D., Baraket, G., Ben Mustapha, S. et al. Molecular and Evolutionary Characterization of Pollen S Determinant (SFB Alleles) in Four Diploid and Hexaploid Plum Species (Prunus spp.). Biochem Genet 59, 42–61 (2021). https://doi.org/10.1007/s10528-020-09990-x

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