Skip to main content

Molecular Determination of Denomination Confusion Among the Main Cultivated Fig Trees (Ficus carica L.) in Morocco

Abstract

Fig (Ficus carica L.) is one of the most emblematic trees in the Mediterranean region. Over time its propagation is carried out via stem cuttings, a procedure that favors the occurrence of varietal confusion among genotypes when it is not controlled. DNA fingerprinting using molecular primers such as simple sequence repeats (SSR) has become an important tool for germplasm characterization and authentication of varieties. To assess the intra-varietal genetic diversity among four main varietal types that are widely cultivated in northern Morocco, we performed SSR analysis of many prospected clones of each cultivar. Using six SSR loci that revealed 30 alleles, we distinguished between the four varietal types. The number of alleles per SSR varied from three to ten and the heterozygosity rate ranged from 85% to 96%. Hierarchical classification has shown that clones having the same denomination belong to the same group despite their geographical origins, except “Ghouddan” clones that were classified into two different groups with a similarity coefficient ranging from 0.35 to 0.92. Factorial analysis of correspondence confirmed the presence of an obvious phylogeographical structuring based on geographical locations (Ouazzane and Taounate). Polyclonality or varietal confusion was confirmed for the “Nabout” and “Ghouddan” types and the authenticity for the “El Qouti” and “Massari” types. These outputs may be referred to somaclonal variations or synonymies/homonymies confusion.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Achtak H, Oukabli A, Ater M, Santoni S, Kjellberg F, Khadari B (2009) Microsatellite markers as reliable tools for fig cultivar identification. J Am Soc Hort Sci 134:624–631

    Article  Google Scholar 

  • Aradhya MK, Stover E, Velasco D, Koehmstedt A (2010) Genetic structure and differentiation in cultivated fig (Ficus carica L.). Genetica 138:681–694

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Baraket G, Chatti K, Saddoud O, Mars M, Marrakchi M, Ttrifi M, Salhi-Hannachi A (2009) Genetic analysis of Tunisian fig (Ficus carica L.) cultivars using amplified fragment length polymorphism (AFLP) markers. Sci Hortic 120:487–492

    CAS  Article  Google Scholar 

  • Belkhir K (1999) GENETIX, version 4.0. CNRS UPR 9060. Laboratoire Génome, Populations, Interactions, Montpellier

    Google Scholar 

  • Cabrita L, Apostolova E, Neves A, Marreiros A, Leitão J (2014) Genetic diversity assessment of the almond (Prunus dulcis (Mill.) DA Webb) traditional germplasm of Algarve, Portugal, using molecular markers. Plant Genet Resour 12(S1):S164–S167

    Article  Google Scholar 

  • Cabrita LF, Aksoy U, Hepaksoy S, Leitão JM (2001) Suitability of isozyme, RAPD and AFLP markers to assess genetic differences and relatedness among fig (Ficus carica L.) clones. Sci Hortic 87:261–273

    CAS  Article  Google Scholar 

  • Çalişkan O, Polat AA (2012) Morphological diversity among fig (Ficus carica L.) accessions sampled from the Eastern Mediterranean Region of Turkey. Turk J Agric For 36(2):179–193

    Google Scholar 

  • Cavanna M, Marinoni DT, Bounous G, Botta R (2008) Genetic diversity in ancient apple germplasm from northwest Italy. J Hortic Sci Biotech 83(5):549–554

    Article  Google Scholar 

  • Chatti K, Saddoud O, Salhi-Hannachi A, Mars M, Marrakchi M, Trifi M (2007) Analysis of genetic diversity and relationships in a Tunisian fig (Ficus carica) germplasm collection by random amplified microsatellite polymorphisms. J Integr Plant Biol 49(3):386–391

    CAS  Article  Google Scholar 

  • Chatti K, Salhi-Hannachi A, Mars M, Marrakchi M, Trifi M (2004) Genetic diversity and phylogenic relationships in Tunisian fig (Ficus carica L.) cultivars mediated by RAPD. Biol Tunisie 1(2):1–4

    Google Scholar 

  • Ciarmiello LF, Piccirillo P, Carillo P, De Luca A, Woodrow P (2015) Determination of the genetic relatedness of fig (Ficus carica L.) accessions using RAPD fingerprint and their agro-morphological characterization. S Afr J Bot 97:40–47

    CAS  Article  Google Scholar 

  • Condit IJ (1947) The fig. Chronica Botanica Co Waltham, p 222

    Google Scholar 

  • Condit IJ (1955) Fig varieties: a monograph. Hilgardia 23:323–538

    Article  Google Scholar 

  • Condit IJ (1969) Ficus; the exotic species. Univ California Div Agric Sci, Berkely (363p)

    Google Scholar 

  • Cxalisxkan O, Polat AA (2008) Fruit characteristics of fig cultivars and genotypes grown in Turkey. Sci Hortic 115:360–367

    Article  Google Scholar 

  • Dalkilicx Z, Mestav HO, Gunver-Dalkilicx G, Kocatas H (2011) Genetic diversity of male fig (Ficus carica caprificus L.) genotypes with random amplified polymorphic DNA (RAPD) markers. Afr J Biot 10(4):519–526

    Google Scholar 

  • Essid A, Aljane F, Ferchichi A, Hormaza JI (2015) Analysis of genetic diversity of Tunisian caprifig (Ficus carica L.) accessions using simple sequence repeat (SSR) markers. Hereditas 152(1):1

    PubMed  PubMed Central  Article  Google Scholar 

  • Fachinello JC, Hoffmann A, Nachtigal JC (2005) Propagação de plantas frutíferas. Embrapa Informação Tecnológica (221 p)

    Google Scholar 

  • FAOSTAT (2018) Food and Agriculture Organization statistical database. 436. http://faostat.fao.org/default.aspx. Accessed 13 Sept 2020

  • Ferguson L, Michailides TJ, Shorey HH (1990) The California fig industry. Hortic Rev 12:409–490

    Google Scholar 

  • Giraldo E, Viruel M, López-corrales M, Hormaza JI (2005) Characterisation and cross-species transferability of microsatellites in the common fig (Ficus carica L.). J Hortic Sci Biotech 80(2):217–224

    CAS  Article  Google Scholar 

  • Giraldo E, Lopez-Corrales M, Hormaza JI (2008) Optimization of the management of an ex-situ germplasm bank in common fig with SSRs. J Am Soc Hortic Sci 133(1):69–77

    CAS  Article  Google Scholar 

  • Giraldo E, Lopez Corrales M, Hormaza JI (2010) Selection of the most discriminating morphological qualitative variables for characterization of fig germplasm. J Am Soc Hortic Sci 135:240–249

    Article  Google Scholar 

  • Hmimsa Y, Aumeeruddy-Thomas Y, Ater M (2017) Une forme spontanée de figuier (Ficus carica L.), le nābūt. Rev Ethnoecol (Supplement 1). https://doi.org/10.4000/ethnoecologie.3186

    Article  Google Scholar 

  • IPGRI, CIHEAM (2003) Descriptors for fig. International Plant Genetic Resources Institute, International Centre for Advanced Mediterranean Agronomic Studies, Rome Paris (52pp)

    Google Scholar 

  • Khadari B (2010) Ex situ management of fig (Ficus carica L.) genetic resources: towards the establishment of the Mediterranean reference collection. XXVIII International Horticultural Congress on Science and Horticulture for People (IHC2010): International Symposium on the 940, pp 67–74

    Google Scholar 

  • Khadari B, Hochu I, Santoni S, Kjellberg F (2001) Identification and characterization of microsatellite loci in the common fig (Ficus carica L.) and representative species of the genus Ficus. Mol Ecol Resour 1:191–193

    CAS  Article  Google Scholar 

  • Khadari B, Oukabli A, Ater M, Mamouni A, Roger JP, Kjellberg F (2004) Molecular characterization of Morrocan fig germoplasm using Inter Simple Sequence Repeat and Simple Sequence Repeat markers to establish a reference collection. Hort Sci 40:29–32

    Google Scholar 

  • Khadari B, Oukabli A, Ater M, Mamouni A, Roger JP, Kjellberg F (2005) Molecular characterization of Moroccan fig germplasm using intersimple sequence repeat and simple sequence repeat markers to establish a reference collection. HortScience 40(1):29–32

    CAS  Article  Google Scholar 

  • Khoshbakht K, Hammer K (2006) Savadkouh (Iran)—an evolutionary center for fruit trees and shrubs. Genet Resour Crop Evol 53:641–651

    Article  Google Scholar 

  • Krausel R (1953) Frankfurter Reigen. Nat Volk 83:80–86

    Google Scholar 

  • Lansky E, Paavilainen H (2010) Figs, 1st edn. CRC Press, Boca Raton, p 1

    Book  Google Scholar 

  • Merrill ED (1943) Some aspects of taxonomy. Torreya 43:50–64

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  PubMed  Article  Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76(10):5269–5273

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Oukabli A, Khadari B (2005) Caractérisation des variétés polyclonales marocaines de figuiers, Ficus carica L. Fruits 60(1):47–54

    CAS  Article  Google Scholar 

  • Rajapakse S (2002) Progress in application of molecular markers to genetic improvement of horticultural crops. In: XXVI International Horticultural Congress: Biotechnology in Horticultural Crop Improvement: Achievements, Opportunities and 625, pp 29–36

    Google Scholar 

  • Raymond M, Rousset F (1995a) Genpop: population genetics software for exact test and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Raymond M, Rousset F (1995b) An exact test for population differentiation. Evolution 49:1280–1283

    PubMed  Article  Google Scholar 

  • Rekik I, Salimonti A, Kamoun NG, Muzzalupo I, Lepais O, Gerber S, Perri E, Rebai A (2008) Characterization and identification of Tunisian olive tree varieties by microsatellite markers. HortScience 43(5):1371–1376

    Article  Google Scholar 

  • Rohlf FJ (2002) NTSYS-pc Numerical Taxonomy System, ver. 2.1. Exeter Publishing Ltd. Setauket, New York

    Google Scholar 

  • Rønsted N, Salvo G, Savolainen V (2007) Biogeographical and phylogenetic origins of African fig species (Ficus section Galoglychia). Mol Phylogenet Evol 43(1):190–201

    PubMed  Article  Google Scholar 

  • Sadder MT, Atteyyeh AF (2006) Molecular assessment of polymorphism among local Jordanian genotypes of the common fig (Ficus carica L.). Sci Hortic 107:347–351

    CAS  Article  Google Scholar 

  • Saddoud O, Salhi-Hannachi A, Chatti K, Mars M, Rhouma A, Marrakchi M, Trifi M (2005) Tunisian fig (Ficus carica L.) genetic diversity and cultivars identification mediated by microsatellites markers. Fruits 60:143–153

    CAS  Article  Google Scholar 

  • Saddoud O, Chatti K, Salhi-Hannachi A, Mars M, Rhouma A, Marrakchi M, Trifi M (2007) Genetic diversity of Tunisian figs (Ficus carica L.) as revealed by nuclear microsatellites. Hereditas 144(4):149–157

    CAS  PubMed  Article  Google Scholar 

  • Saddoud O, Baraket G, Chatti K, Trifi M, Marrakchi M, Mars M, Salhi-Hannachi A (2011) Using morphological characters and simple sequence repeat (SSR) markers to characterize Tunisian fig (Ficus carica L.) cultivars. Acta Biol Cracov Ser Bot 53:7–14

    Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81(24):8014–8018. https://doi.org/10.1073/pnas.81.24.8014

    CAS  Article  Google Scholar 

  • Salhi-Hannachi A, Trifi M, Zehdi S, Mars M, Rhouma A, Marrakchi M (2004) Inter simple sequence repeat fingerprintings to assess genetic diversity in Tunisian fig (Ficus carica L.). Genet Resour Crop Evol 51:269–275

    CAS  Article  Google Scholar 

  • Salhi-Hannachi A, Chatti K, Mars M, Marrakchi M, Trifi M (2005) Comparative analysis of genetic diversity in two collections figs cultivars based on random amplified polymorphic DNA and inter Simple Sequence repeats fingerprints. Genet Resour Crop Evol 52:563–573

    Article  CAS  Google Scholar 

  • Salhi-hannachi A, Chatti K, Saddoud O, Messaoud M, Rhouma A, Marrakchi M, Trifi M (2006) Genetic diversity of different tunisian fig (Ficus carica l.) collections revealed by rapd fingerprints. Hereditas 143:15–22

    PubMed  Article  Google Scholar 

  • Sata N (1944) A monographic study of the genus Ficus from the point of view of economic botany. Inst of Hort and Econ Bot, Taihoku Imp Univ, Contrib. No. 32

    Google Scholar 

  • Singh D, Singh B, Goel RK (2011) Traditional uses, phytochemistry and pharmacology of Ficus religiosa: a review. J Ethnopharmacol 134:565–583

    CAS  PubMed  Article  Google Scholar 

  • Solomon A, Golubowicz S, Yablowicz Z, Grossman S, Bergman M, Gottlieb HE, Altman A, Kerem Z, Flaishman MA (2006) Antioxidant activities and anthocyanin content of fresh fruits of common fig (Ficus carica L.). Agric Food Chem 54:7717–7723

    CAS  Article  Google Scholar 

  • Soriano Niebla JJ (2004) Hortelanos de la Sierra de Cádiz: Las variedades locales y el conocimiento campesino sobre el manejo de los recursos fitogenéticos. Mancomunidad de Municipios Sierra de Cádiz, Red Andaluza de Semillas y Junta de Andalucía, Sevilla

    Google Scholar 

  • Storey WB et al (1975) Figs. In: Janick J, Moore J (eds) Advances in fruit breeding. Purdue University Press, Indiana, pp 568–589

    Google Scholar 

  • Tixier MH, Sourdille P, Röder M, Leroy P, Bernard M (1997) Detection of wheat microsatellites using a non radioactive silver-nitrate staining method. J Genet Plant Breed 51:175–178

    CAS  Google Scholar 

  • Vidaud J, Baccaunaud M, Caraglio Y, Hutin C, Roger JP (1997) Le figuier. Centre Technique et Interprofessionnel des fruits et de légumes (Ctif), Paris (263 p)

    Google Scholar 

  • Watson L, Dallwitz MJ (2004) The families of flowering plants: descriptions, illustrations, identification, and information retrieval. http://delta-intkey.com/angio/www/index.htm. Accessed June 2019

  • Zukovskij PM (1950) Ficus. Cultivated plants and their wild relatives. State Publishing House Sov Sci Mosc, pp 58–59

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

J. Charafi designed the methodology of the research, provided the technical support for designing and conducting the research, performed the statistical analysis, and contributed to the writing of this paper. Z. El Kettabi and K. Houmanat contributed to the laboratory analysis, interpretation of the data, and the writing of the manuscript. Z. Messaoudi, L. Ait Haddou, and H. Outghouliast collected samples and performed the review. A. Mamouni assisted in the processing of samples and data and performed the review. M. Tahiri analyzed samples and carried out laboratory manipulations.

Corresponding author

Correspondence to Jamal Charafi.

Ethics declarations

Conflict of interest

J. Charafi, K. Houmanat, Z. El Kettabi, Z. Messaoudi, L. Ait Haddou, H. Outghouliast, A. Mamouni and M. Tahiri declare that they have no competing interests.

Additional information

I, Jamal CHARAFI, testify on behalf of all co-authors that our article submitted to Erwerbs-Obstbau: (1) has not been published previously, and it is not under consideration for publication elsewhere; (2) the contents of the manuscript are original and have never been published or submitted elsewhere; (3) the manuscript is not currently being considered for publication in another journal; (4) all authors have been personally and actively involved in substantive work leading to the manuscript, and will hold themselves jointly and individually responsible for its content.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Charafi, J., Houmanat, K., El Kettabi, Z. et al. Molecular Determination of Denomination Confusion Among the Main Cultivated Fig Trees (Ficus carica L.) in Morocco. Erwerbs-Obstbau (2022). https://doi.org/10.1007/s10341-022-00715-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10341-022-00715-5

Keywords

  • Ficus carica L.
  • SSR markers
  • Homonymy
  • Synonymy
  • Somaclonal variations