Skip to main content

Genetic diversity and structure of Fusarium oxysporum f.sp. lentis isolates from Iran, Syria and Algeria

European Journal of Plant Pathology volume 153, pages 1019–1029 (2019)Cite this article

Abstract

Lentil is an important cool season food legume. Vascular wilt incited by Fusarium oxysporum f.sp. lentis (FOL) is the most important disease of lentil worldwide. Knowledge of pathogen genetic structure is crucial to develop effective control strategies. In this study, the genetic structure of a collection of FOL isolates from Iran, Syria and Algeria was analysed using SSR markers. Eight markers were developed in this study and constitute a valuable resource for future molecular studies in FOL. Our results showed that there is a high molecular variation within regions, with isolates from North West Iran showing the highest gene diversity. Variation among regions also exists, with Iranian populations differing significantly from non-Iranian ones, having some private alleles. The clustering of isolates was well in agreement in both distance-based and model-based approaches suggesting the presence of seven ancestral FOL lineages, being three present exclusively in Iran while the others were distributed across all the regions. These results suggest that Iran could be a regional center of origin for FOL.

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

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2

References

  • Al-Husien, N. H., Hamwieh, A., Ahmed, S., & Bayaa, B. (2017). Genetic diversity of Fusarium oxysporum f.sp. lentis population affecting lentil in Syria. Journal of Phytopathology, 165, 306–312.

    Article  CAS  Google Scholar 

  • Baayen, R. P., O'Donnell, K., Bonants, P. J. M., Cigelnik, E., Kroon, L. P. N. M., Roebroeck, E. J. A., & Waalwijk, C. (2000). Gene genealogies and AFLP analysis in the Fusarium oxysporum complex identify monophyletic and non-monophyletic formae speciales causing wilt and rot diseases. Phytopathology, 90, 891–900.

    Article  CAS  PubMed  Google Scholar 

  • Bao, J. R., Fravel, D. R., O'Neill, N. R., Lazarovits, G., & van Berkum, P. (2002). Genetic analysis of pathogenic and non-pathogenic Fusarium oxysporum from tomato plants. Canadian Journal of Botany, 80, 271–279.

    Article  CAS  Google Scholar 

  • Bayaa, B., Erskine, W., & Hamdi, A. (1995). Evaluation of a wild lentil collection for resistance to vascular wilt. Genetic Resources and Crop Evolution, 42, 231–235.

    Article  Google Scholar 

  • Bayaa, B., Kumari, S. G., Akkaya, A., & Erskine, W. (1998). Survey of major biotic stresses of lentil in south-east Antalia, Turkey. Phytopathologia Mediterranea, 37, 88–95.

    Google Scholar 

  • Baysal, Ö., Siragusa, M., Ikten, H., Polat, E., Gümrükcü, E., Yigit, F., Carimi, F., & Teixeria da Silva, J. A. (2009). Fusarium oxysporum f. sp. lycopersici races and their genetic discrimination by molecular markers in West Mediterranean region of Turkey. Physiological and Molecular Plant Patholgy, 74, 68–75.

    Article  CAS  Google Scholar 

  • Belabid, L., & Fortas, Z. (2002). Virulence and vegetative compatibility of Algerian isolates of Fusarium oxysporum f. sp. lentis. Phytopathologia Mediterranea, 41, 179–187.

    Google Scholar 

  • Belabid, L., Baum, M., Fortas, Z., Bouznad, Z., & Eujayl, I. (2004). Pathogenic and genetic characterization of Algerian isolates of Fusarium oxysporum f. sp. lentis by RAPD and AFLP analysis. African Journal of Biotechnology, 3(1), 25–31.

    Article  CAS  Google Scholar 

  • Bentley, S., Pegg, K. G., & Dale, J. L. (1994). Optimization of RAPD-fingerprinting to analyze genetic variation within populations of Fusarium oxysporum f. sp. cubense. Journal of Phytopathology, 142, 64–78.

    Article  CAS  Google Scholar 

  • Bogale, M., Wingfield, B. D., Wingfield, M. J., & Steenkamp, T. (2005). Simple sequence repeat for species in Fusarium oxysporum complex. Molecular Ecology Notes, 5, 622–624.

    Article  CAS  Google Scholar 

  • Bogale, M., Wingfield, B. D., Wingfield, M. J., & Steenkamp, E. T. (2006). Characterization of Fusarium oxysporum isolates from Ethiopia using AFLP, SSR and DNA sequence analyses. Fungal Diversity, 51–66.

  • Bowcock, A. M., Ruizlinares, A., Tomfohrde, J., et al. (1994). High resolution of human evolutionary trees with polymorphic microsatellites. Nature, 368, 455–457.

  • Chen, W., Basandrai, A. K., Basandrai, D., Banniza, S., Bayaa, B., Buchwaldt, L., Davidson, J., Larsen, R., Rubiales, D., & Taylor, P. (2009). Lentil diseases and their management. In W. Erskine et al. (Eds.), The lentil: Botany, production and uses (pp. 262–281). UK: CABI.

    Chapter  Google Scholar 

  • Datta, S., Choudhary, R. G., Shamim, M., Singh, R. K., & Dhar, V. (2011). Molecular diversity in Indian isolates of Fusarium oxysporum f.sp. lentis inciting wilt disease in lentil (Lens culinaris Medik). African Journal of Biotechnology, 10(38), 7314–7323.

    CAS  Google Scholar 

  • Earl Dent, A., & von Holdt, B. M. (2012). STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4(2), 359–361.

    Article  Google Scholar 

  • Erskine, W., & Bayaa, B. (1996). Yield loss, incidence and inoculum density associated with vascular wilt of lentil. Phytopathologia Mediterranea, 36, 24–32.

    Google Scholar 

  • Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14, 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitocondreal DNA restriction sites. Genetics, 131, 479–491.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.

    CAS  Google Scholar 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791. https://doi.org/10.2307/2408678.

    Article  PubMed  Google Scholar 

  • Felsenstein, J. (2004). PHYLIP (Phylogeny Inference Package) Version 3.6. Department of Genomic Sciences, University of Washington, Seattle, WA.

  • Grajal-Martin, M. J., Simon, C. J., & Muehlbauer, F. J. (1993). Use of random amplified polymorphic DNA (RAPD) to characterize race 2 of Fusarium oxysporum f. sp. pisi. Phytopathology, 83, 612–614.

    Article  CAS  Google Scholar 

  • Kalinowski, S. T. (2004). Counting alleles with rarefaction: Private alleles and hierarchical sampling designs. Conservation Genetics, 5, 539–543.

    Article  CAS  Google Scholar 

  • Kalinowski, S. T. (2005). HP-rare: A computer program for performing rarefaction on measures of allelic diversity. Molecular Ecology Notes, 5, 187–189.

    Article  CAS  Google Scholar 

  • Khare, M. N. (1981). Diseases of lentil. In C. Webb & G. Hawtin (Eds.), Lentil (pp. 163–172). UK: CABI.

    Google Scholar 

  • Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A., & Mayrose, I. (2015). Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15, 1179–1191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kraft, J. M., Haware, M. P., Halila, H., & Bayaa, B. (2000). Soilborne diseases and their control. In R. Knight (Ed.), Linking Research and Marketing Opportunities for Pulses in 21 st Century (pp. 457–466). The Netherlands: Kluwer Academic.

    Chapter  Google Scholar 

  • Lassner, M. W., Peterson, P., Yoder, J. I. (1989). Simultaneous amplification of multiple DNA fragments by polymerase chain reaction in the analysis of transgenic plants and their progeny. Plant Molecular Biology Reporter 7(2):116–128.

  • Lievens, B., Houterman, P.M. and Rep, M. (2009). Effector gene screening allows unambiguous identification of Fusarium oxysporum f. sp. lycopersici races and discrimination from other formae speciales. FEMS Microbiology Letters, 300, 201–215.

  • Ma, L. J., van der Does, H. C., Borkovich, K. A., Coleman, J. J., Daboussi, M. J., di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B., Houterman, P. M., Kang, S., Shim, W. B., Woloshuk, C., Xie, X., Xu, J. R., Antoniw, J., Baker, S. E., Bluhm, B. H., Breakspear, A., Brown, D. W., Butchko, R. A. E., Chapman, S., Coulson, R., Coutinho, P. M., Danchin, E. G. J., Diener, A., Gale, L. R., Gardiner, D. M., Goff, S., Hammond-Kosack, K. E., Hilburn, K., Hua-van, A., Jonkers, W., Kazan, K., Kodira, C. D., Koehrsen, M., Kumar, L., Lee, Y. H., Li, L., Manners, J. M., Miranda-Saavedra, D., Mukherjee, M., Park, G., Park, J., Park, S. Y., Proctor, R. H., Regev, A., Ruiz-Roldan, M. C., Sain, D., Sakthikumar, S., Sykes, S., Schwartz, D. C., Turgeon, B. G., Wapinski, I., Yoder, O., Young, S., Zeng, Q., Zhou, S., Galagan, J., Cuomo, C. A., Kistler, H. C., & Rep, M. (2010). Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature, 464, 367–373.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manulis, S., Kogan, N., Reuven, M., & Ben-Yephet, Y. (1994). Use of the RAPD technique for identification of Fusarium oxysporum f. sp. dianthi from carnation. Phytopathology, 84, 98–101.

    Article  Google Scholar 

  • McDonald, B. A., & Linde, C. (2002). The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica, 124, 163–180.

    Article  CAS  Google Scholar 

  • Minch, E., Ruiz-Linares, A., Goldstein, D. B., Feldmann, M. W., CavalliSforza, L. L. (1997). Microsat (version 1.5d): A program for calculating statistics on microsatellite allele data. http://lotka.stanford.edu/ microsat/microsat.html.

  • Mohammadi, N., Goltapeh, E. M., Babaie-Ahari, A., & Pouralibaba, H. (2011). Pathogenic and genetic characterization of Iranian isolates of Fusarium oxysporum f.sp. lentis by ISSR analysis. Journal of Agricultural Technology, 7(1), 63–72.

  • Nelson, P. E., Toussoun, T. A., & Marasas, W. F. O. (1983). Fusarium species: An illustrated manual for identification. USA: The Pennsylvania State University Press.

    Google Scholar 

  • Nourollahi, K., & Madahjalali, M. (2017). Analysis of population genetic structure of Iranian Fusarium oxysporum f. sp. lentis isolates using microsatellite markers. Australasian Plant Pathology, 46, 35–42.

    Article  Google Scholar 

  • O’Donnell, K., Cigelnik, E., & Nirenberg, H. I. (1998). Molecular systematic and14 phylogeography of the Gibberella fujikuroi species complex. Mycologia, 90, 465–493.

    Article  Google Scholar 

  • Pouralibaba, H. R., Rubiales, D., & Fondevilla, S. (2016). Identification of pathotypes in Fusarium oxysporum f.sp. lentis. European Journal of Plant Pathology, 144, 539–549.

    Article  CAS  Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rousset, F. (2008). GENEPOP'007: A complete reimplementation of the GENEPOP software for windows and Linux. Molecular Ecology Resources, 8, 103–106.

    Article  PubMed  Google Scholar 

  • Saghai Maroof, M. A., Zhang, Q., & Biyashev, R. (1995). Comparison of restriction fragment length polymorphisms in wild and cultivated barley. Genome, 38, 298–306.

    Article  Google Scholar 

  • SAS Institute (2004). SAS/STAT® 9.1 User’s Guide. SAS Institute Inc., Cary, NC.

  • Taheri, N., Rastegar Fallahati, R., Jafarpour, B., Bagheri, A. R., & Jahanbakhsh, V. (2010). Pathogenic and genetic characterization of Fusarium oxysporum f.sp. lentis by RAPD and IGS analysis in Khorasan province. World Applied Sciences Journal, 9(3), 239–244.

    CAS  Google Scholar 

  • Torres, A. M., Weeden, N. F., & Martín, A. (1993). Linkage among isozyme, RFLP and RAPD markers in Vicia faba. Theoretical and Applied Genetics, 85, 937–945.

    Article  CAS  PubMed  Google Scholar 

  • Vogelgsang, S., Enkerli, J., Jenny, E., Roffler, S., & Widmer, F. (2011). Characterization of Fusarium poae microsatellite markers on strains from Switzerland and other countries. Journal of Phytopathology, 159, 197–200.

    Article  CAS  Google Scholar 

  • You, F. M., Huo, N. X., Gu, Y. Q., Luo, M. C., Ma, Y. Q., Hane, D., Lazo, G. R., Dvorak, J., & Anderson, O. D. (2008). BatchPrimer3: A high throughput web application for PCR and sequencing primer design. BMC Bioinfomatics, 9, 253.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was carried out based on PhD educational mission No. 3972/200-28/1/1389 of first author from Agricultural Research, Education and Extension Organization (AREEO) of Iran and financially supported by Project AGL2014-52871-R co-financed by FEDER. The authors wish to tanks Professor B. Bayaa, University of Aleppo, Syria, for helping to obtain Algerian isolates of FOL.

Author information

Authors and Affiliations

  1. Institute for Sustainable Agriculture, CSIC, Avda. Menéndez Pidal s/n, 14004, Córdoba, Spain

    Hamid R. Pouralibaba, Ma José Cobos, Diego Rubiales & Sara Fondevilla

  2. Dryland Agricultural Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Maragheh, Iran

    Hamid R. Pouralibaba

  3. Faculty of Agriculture, Department of Seed Science and Technology, University of Zagreb, Svetošimunska 25, 10000, Zagreb, Croatia

    Zlatko Šatović

  4. Centre of Excellence for Biodiversity and Molecular Plant Breeding (CroP-BioDiv), Svetošimunska 25, 10000, Zagreb, Croatia

    Zlatko Šatović

Authors
  1. Hamid R. Pouralibaba
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zlatko Šatović
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ma José Cobos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Diego Rubiales
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sara Fondevilla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hamid R. Pouralibaba.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest. All authors have revised the manuscript and approved its submission.

Research involving human participants and / or animals

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pouralibaba, H.R., Šatović, Z., Cobos, M.J. et al. Genetic diversity and structure of Fusarium oxysporum f.sp. lentis isolates from Iran, Syria and Algeria. Eur J Plant Pathol 153, 1019–1029 (2019). https://doi.org/10.1007/s10658-018-01617-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-018-01617-7

Keywords

  • Lentil (Lens culinaris)
  • Fusarium oxysporum f.sp. lentis
  • Population structure
  • Pathotype
  • SSR