Skip to main content
Log in

Self-(in)compatibility in Tunisian apple accessions [Malus domestica. Borkh]: S-genotypes identification and pollen tube growth analysis

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Self-incompatibility studies have revealed a potential use of Tunisian apple resources for crop improvement and modern breeding programs and a likely correlation between the pollen tube growth and flowering period.

Abstractss

Apples [Malus domestica. Borkh] exhibit an S-RNase-based gametophytic self-incompatibility (GSI) system. Four primer combinations were used to S-genotype eighteen Tunisian local apple accessions and twelve introduced accessions that served as references. Within the Tunisian local accessions, S2, S3, S7, and S28 S-alleles were the most frequent and were assigned to 14 S-genotypes; among them, S7S28, S3S7, S2S5, and S2S3 were the most abundant. PCA plot showed that population structuring was affected by the S-alleles frequencies and revealed a modern origin of the Tunisian varieties rather than being ancient ones. Nonetheless, the results obtained with 17 SSR markers showed a separate grouping of local Tunisian accessions that calls into question the hypothesis discussed. Pollination experiments showed that the pollen started to germinate within 24 h of pollination but 48 h after pollination in the “El Fessi” accession. The first pollen tubes arrived in the styles within 36 h of pollination in two early flowering accessions known as “Arbi” and “Bokri”, and after 72 h of pollination in late flowering “El Fessi” and 48 h after pollination in remaining accessions. The first pollen tube arrests were observed in accessions “Arbi” and “Bokri” within 84 h of pollination, within 108 h of pollination in “El Fessi” and within 108 h of pollination in remaining accessions. In the apple accession called “Boutabgaya,” the pollen tubes reached the base of the style within 120 h of pollination without being aborted. Nevertheless, the self-compatible nature of “Boutabgaya” needs more studies to be confirmed. However, our results revealed the malfunction of the female component of the GSI in this accession. To conclude, this work paved the path for further studies to enhance the insight (i) into the relation between the flowering period and the pollen tube growth, (ii) self-compatible nature of “Boutabgaya”, and (iii) the origin of the Tunisian apple.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

Authors declare that all data are included within the manuscript and fully available without restriction.

References

  • Abdallah D, Baraket G, Perez V, Ben Mustapha S, Salhi Hannachi A, Hormaza JI (2019a) Analysis of self-incompatibility and genetic diversity in diploid and hexaploid plum genotypes. Front Plant Sci 10:896. https://doi.org/10.3389/fpls.2019.00896

    Article  PubMed  PubMed Central  Google Scholar 

  • Abdallah D, Baraket G, Ben Mustapha S, Angeles Moreno M, Salhi HA (2019b) Molecular and evolutionary characterization of pollen S determinant (SFB alleles) in four diploid and hexaploid plum species [Prunus.spp.]. Biochem Genet. https://doi.org/10.1007/s10528-020-09990-x

    Article  PubMed  Google Scholar 

  • Abdallah D, Baraket G, Perez V, Salhi Hannachi A, Hormaza JI (2020) Self-compatibility in peach [Prunus persica (L.) Batsch]: patterns of diversity surrounding the S-locus and analysis of SFB alleles. Hortic Res. https://doi.org/10.1038/s41438-020-00392-

    Article  PubMed  PubMed Central  Google Scholar 

  • Aguiar B, Vieira J, Ae C, Na F, Iezzoni A, Van Nocker S et al (2015) Convergent evolution at the gametophytic self-incompatibility system in malus and Prunus. PLoS ONE 10(5):e0126138

    Article  PubMed  PubMed Central  Google Scholar 

  • Baggiolini M (1952) Les stades repères dans le développement annuel de la vigne et leur utilisation pratique. Revue Romande D’agriculture Et D’arboriculture 8(1):4–6

    Google Scholar 

  • Balti I (2015) Etude de la diversité génétique du pommier cultivé (Malus domestica Borkh.) en Tunisie à laide des marqueurs moléculaires SCoT et CDDP. Mastère de génétique moléculaire et biotechnologie. Bibliothèque de la Faculté des Sciences de Tunis. Université Tunis el Manar

  • Balti I (2022) Analyse du polymorphisme moléculaire et étude transcriptomique des gènes des fleurs et du fruit chez le pommier (Malus domestica Borkh.). thése de doctorat en Sciences biologiques. Bibliothèque de la Faculté des Sciences de Tunis. Université Tunis el Manar

  • Baraket G, Abdallah D, Ben Mustapha S, Hannachi-Salhi A (2019) Combination of simple sequence repeat, S-locus polymorphism and morphology to draw a taxonomic key for Tunisian plum species (Prunus.spp.). Biochem Genet 57:673. https://doi.org/10.1007/s10528-019-09922-4

    Article  CAS  PubMed  Google Scholar 

  • Baraket G, Abdallah D, Boukhalfa Y, Ben Mustapha S, Salhi-Hannachi A (2021) Analysis of genetic diversity andwater-stress tolerance in Tunisian plums [Prunus.spp.; Rosacea]. Sci Hortic. https://doi.org/10.1016/j.scienta.2021.110141

    Article  Google Scholar 

  • Brancher TL, Hawerroth MC, Kvitschal MV, Manenti DC, Guidolin AF (2020) Self-incompatibility alleles in important genotypes for apple breeding in Brazil. CBAB 20(4):e28652041

    Article  CAS  Google Scholar 

  • Broothaerts W, Van Nerum I (2003) Apple self-incompatibility genotypes: an overview. Acta Hortic 622:379–387

    Article  CAS  Google Scholar 

  • Broothaerts W, Ga J, Proost P, Wf B (1995) cDNA cloning and molecular analysis of two self-incompatibility alleles from apple. Plant Mol Biol 27:499–511

    Article  CAS  PubMed  Google Scholar 

  • Broothaerts W, Van Nerum I, Keulemans J (2004) Update on and review of the incompatibility (S-) genotypes of apple cultivars. Hortic Sci 39:943–947

    CAS  Google Scholar 

  • Byrne DH (2002) Peach breeding trends: a world wide perspective. Acta Hortic 592:49–59

    Article  Google Scholar 

  • Chikh-Rouhou H, Mezghani N, Mnasri S, Mezghani N, Garces-Claver A (2021) Assessing the genetic diversity and population structure of a Tunisian melon (Cucumis melo L.) collection using phenotypic traits and SSR molecular markers. Agronomy 11:1121

    Article  Google Scholar 

  • De Franceschi P, Cova V, Tartarini S, Dondini L (2016) Characterization of a new apple S-RNase allele and its linkage with the Rvi5 gene for scab resistance. Mol Breeding 36:1–11

    Article  Google Scholar 

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

    Google Scholar 

  • Gianfranceschi L, Seglias N, Tarchini R, Komjanc M, Gessler C (1998) Simple sequence repeats for the genetic analysis of apple. Theor Appl Genet 96:1069–1076

    Article  CAS  Google Scholar 

  • Górnás P, Mišina I, Ikase L (2022) Crab apple (Malus spp.) seed tocopherol profile: impact of genotype, species purpose and rootstock. Agronomy 12:2736

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Guerra M, Rodrigo J, Lopez-Corrales M, Wünsch A (2009) S-RNase genotyping and incompatibility group assignment by PCR and pollination experiments in Japanese plum. Plant Breed 128:304–311

    Article  CAS  Google Scholar 

  • Hack H, Bleiholder H, Buhr L, Meier U, Schnock-Fricke U, Weber E, Witzenberger A (1992) Einheitliche Codierung der phänologischen Entwicklungsstadien mono- und dikotyler Pflanzen. Erweiterte BBCH-Skala, Allgemein. Nachrichtenbl. Deut. Pflanzenschutzd. 44 (12):265–270

  • Halasz J, Hegedus A, Gyorgy Z, Pallinger E, Toth M (2011) S-genotyping of old apple cultivars from the Carpathian basin: methodological, breeding and evolutionary aspects. Tree Genet Genomes 7:1135–1145

    Article  Google Scholar 

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

    Google Scholar 

  • Hedhly A, Hormaza J, Herrero M (2003) The effect of temperature on stigmatic receptivity in sweet cherry (Prunus avium L.). Plant Cell Environ 26:1673–1680

    Article  Google Scholar 

  • Hedhly A, Hormaza J, Herrero M (2005) The effect of temperature on pollen germination, pollen tube growth, and stigmatic receptivity in peach. Plant Biol 7:476–483

    Article  CAS  PubMed  Google Scholar 

  • Jahed KR, Hirst PM (2017) Pollen tube growth and fruit set in apple. HortScience 52(8):1054–1059

    Article  Google Scholar 

  • Janssens GA, Goderis IJ, Brokaert WF, Broothaerts W (1995) A molecular method for S-allele identification in apple based on allele-specific PCR. Theor Appl Gen 91:691–698

    Article  CAS  Google Scholar 

  • Jefferies CJ, Belcher AR (1974) A fluorescent brightener used for pollen tube identification in vivo. Stain Technol 49:199–202

    Article  CAS  PubMed  Google Scholar 

  • Kim H, Hattori G, Hirata Y, Kim D, Hwang J, Shin Y, Nou I (2006) Determination of self-lncompatibility genotypes of Korean apple cultivars based on S-RNase PCR. J Plant Biol 49:448–454

    Article  CAS  Google Scholar 

  • Kim H, Kakui H, Kotoda N, Hirata Y, Koba T, Sassa H (2009) Determination of partial genomic sequences and development of a CAPS system of the S-RNase gene for the identification of 22 S haplotypes of apple (Malus domestica Borkh.). Mol Breed 23:463–472

    Article  CAS  Google Scholar 

  • Kimura M, Crow F (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komori S, Soejima J, Abe K, Kotoda N, Kato H (2000) Analysis of S-allele genotypes and genetic diversity in the apple. Acta Hortic 538:83–86

    Article  Google Scholar 

  • Lancashire PD, Bleiholder H, Van Den Boom T, Langelüddeke P, Stauss R, Weber E, Witzenberger A (1991) A uniform decimal code for growth stages of crops and weeds. Ann Appl Biol 119:561–601

    Article  Google Scholar 

  • Larsen B, Ørgaard M, Tb T-A, Pedersen C (2016) A high-throughput method for genotyping S-RNase alleles in apple. Mol Breeding 36:24

    Article  Google Scholar 

  • Lewontin RC (1972) The opportionment of Humen Diversity. In: Dobzhansky T, Hecht MK, Steere WC (eds) Evolutionary biology. Springer, New York

    Google Scholar 

  • Liebhard R, Gianfranceschi L, Koller B, Ryder Cd, Tarchini R, Weg E, Van De Gessler C (2002) Development and characterization of 140 new microsatellites in apple (Malus domestica Borkh.). Mol Breeding 10:217–241

    Article  CAS  Google Scholar 

  • Linskens HF, Esser K (1957) Uber eine spezifische anfarbung der pollen schlauche im griffel und die zahl der kallosepfropfen nach selbstung und fremdung. Naturwiss 44:16

    Article  Google Scholar 

  • López-Girona E, Dr B, Mem S, Alvares S, Tl B et al (2021) A high-throughput S-RNase genotyping method for apple. Fruit Res 1:10

    Article  Google Scholar 

  • Losada JM, Herrero M (2012) Arabinogalactan-protein secretion is associated with the acquisition of stigmatic receptivity in the apple flower. Ann Bot 110:573–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marone D, Russo MA, Mores A, Ficco DBM, Laidò G, Mastrangelo AM, Borrelli GM (2021) Importance of landraces in cereal breeding for stress tolerance. Plants 10:1267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto S, Komori S, Kitahara K, Imazu S, Soejima J (1999) S-genotypes of 15 apple cultivars and self-compatibility of ‘Megumi.’ J Jpn Soc Hortic Sci 68:236–241

    Article  CAS  Google Scholar 

  • Matsumoto S, Eguchi T, Bessho H, Abe K (2007) Determination and confirmation of S-RNase genotypes of apple pollinators and cultivars. J Hortic Sci Biotech 82:323–329

    Article  CAS  Google Scholar 

  • Melounova M, Vejl P, Sedlak P, Blazek J, Zoufala J, Milec Z, Blazkova H (2005) Alleles controlling apple skin colour and incompatibility in new Czech apple varieties with different degrees of resistance against Venturia inaequalis CKE. PSE 51:65–73

    CAS  Google Scholar 

  • Nabli M (2011) La flore de la Tunisie, Mise à jour 2011

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70(12):3321–3323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nybom H, Sehic J, Garkava-Gustavsson L (2008) Self-incompatibility alleles of 104 apple cultivars grown in Northern Europe. J Hortic Sci Biotec 83:339–344

    Article  Google Scholar 

  • Okuno T (2000) S-RNase from Malus domestica, cultivar starking delicious. GenBank submission no. AB017636

  • Raspé O, Kohn JR (2002) S-allele diversity in Sorbus aucuparia and Crataegus monogyna (Rosaceae: Maloideae). Heredity 88:458–465

    Article  PubMed  Google Scholar 

  • Razifard H, Ramos A, Della Valle AL, Bodary C, Goetz E, Manser EJ et al (2020) Evidence for complex domestication history of the cultivated tomato in Latin America. Mol Biol Evol 37:1118–1132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigo J, Herrero M (1996) Evaluation of pollination as the cause of erratic fruit set in apricot Moniqui. J Hortic Sci 71:801–805

    Article  Google Scholar 

  • Roeder S, Serra S, Musacchi S (2021) Effective pollination period and parentage effect on pollen tube growth in apple. Plants 10:1618

    Article  PubMed  PubMed Central  Google Scholar 

  • Saddoud DO, Amar FB, Rahmani SM, Taranto F, Montemurro C, Miazzi MM (2022) The status of genetic resources and olive breeding in Tunisia. Plants 11:1759

    Article  Google Scholar 

  • Sakurai K, Brown SK, Weeden NF (1997) Determining the selfincompatibility alleles of Japanese apple cultivars. Hortic Sci 32:1258–1259

    Google Scholar 

  • Sakurai K, Brown SK, Weeden NF (2000) Self-incompatibility alleles of apple cultivars and advanced selections. Hortic Sci 35:116–119

    CAS  Google Scholar 

  • Sangam LD, Salvatore C, Matthew WB, Hari DU, Ashok KA, Rodomiro O (2016) Landrace germoplasm for improving yield and abiotic stress adaptation. Trends Plant Sci 21:31–42

    Article  Google Scholar 

  • Sanzol J (2009) Pistil-function breakdown in a new S-allele of European pear, S21, confers self-compatibility. Plant Cell Rep 28:457–467

    Article  CAS  PubMed  Google Scholar 

  • Sassa H, Mase N, Hirano H, Ikehashi H (1994) Identification of self-incompatibility-related glycoproteins in styles of apple (Malus × domestica). Theor Appl Genet 89:201–205

    Article  CAS  PubMed  Google Scholar 

  • Scorza R, Sherman WB (1996) Peaches. In: Janick J, Moore JN (eds) Fruit breeding vol I. Tree and tropical fruits. John Wiley & Sons Inc., New York, pp 325–440

    Google Scholar 

  • Serra S, Roeder S, Sheick R, Musacchi S (2022) Pistil biology of ‘WA 38’ apple and effect of pollen source on pollen tube growth and fruit set. Agronomy 12:123

    Article  Google Scholar 

  • Sheick R, Serra S, Tillman J, Luby J, Evans K et al (2020) Characterization of a novel S-RNase allele and genotyping of new apple cultivars. Sci Hortic 273:109630

    Article  CAS  Google Scholar 

  • Stoeckel S, Grange J, Fernández-Manjarres JF, Bilger I, Frascaria-Lacoste N, Mariette S (2006) Heterozygote excess in a self-incompatible and partially clonal forest tree species Prunus avium L. Mol Ecol 15:2109–2118

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vieira J, Morales-Hojas R, Santos RA, Vieira CP (2007) Different positively selected sites at the gametophytic self-incompatibility pistil S-RNase gene in the Solanaceae and Rosaceae (Prunus, Pyrus, and Malus). J Mol Evol 65:175–185

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank to the collections technicians and Tunisian farmers for kindly providing plant materials. We would like to express our gratitude to Ms. Yosra Bchir (the Higher Institute of Languages of Tunis ISLT), for her diligent review of this work.

Funding

This research was supported by the Tunisian ‘MINISTRY OF HIGHER EDUCATION AND SCIENTIFIC RESEARCH ‘

Author information

Authors and Affiliations

Authors

Contributions

DA performed the experiments, performed statistical analyses, developed the genetic analyses, and wrote the manuscript. SBM performed the pollination experiments and the microscope observations. IB provided some plant materials and performed SSR amplification. ASH and GB provided experimental instructions, supervised the work, and assisted in writing the manuscript.

Corresponding author

Correspondence to Donia Abdallah.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Stefan de Folter.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdallah, D., Ben Mustapha, S., Balti, I. et al. Self-(in)compatibility in Tunisian apple accessions [Malus domestica. Borkh]: S-genotypes identification and pollen tube growth analysis. Planta 259, 137 (2024). https://doi.org/10.1007/s00425-024-04418-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-024-04418-x

Keywords

Navigation