, Volume 47, Issue 2, pp 263–273 | Cite as

The most recent status of genetic structure of Didymella rabiei (Ascochyta rabiei) populations in Turkey and the first genotype profile of the pathogen from the wild ancestor, Cicer reticulatum

  • Hilal OzkilincEmail author
  • Canan Can


Chickpea is an important legume crop cultivated in many locations of Turkey and wild relatives of chickpea naturally grow in the Southeastern Anatolia Region of Turkey. Ascochyta blight caused by Didymella rabiei is one of the most important limiting factors for chickpea production. In this study, we aimed to investigate the genetic structures of D. rabiei samples from wild and domesticated chickpea hosts from different geographical regions. For this purpose, D. rabiei was collected from different geographic regions of Turkey between March and June in 2014 and 2015. Besides, some isolates were obtained from the wild chickpea species, C. pinnatifidum and C. reticulatum. Total, one hundred and two isolates of D. rabiei were genotyped using six sequence tagged microsatellite (STMS) markers. According to the results of molecular variance, the pathogen isolates from different geographic regions showed a significant genetic variation, but, most of which were confined within the populations. The total genetic diversity was estimated to be 0.612 for D. rabiei isolates from chickpea over the country. For the first time, D. rabiei from C. reticulatum, which is the wild ancestor of domesticated chickpea was found in the world and the isolates from C. reticulatum were represented with a single genotype. Isolates from C. pinnatifidum were genetically closer to the isolates from Southeastern Anatolia Region. All the isolates were grouped as one genetic population according to the Bayesian algorithm and presented a mixed distribution based on the principal coordinate analysis (PCoA) of genetic distances. All the results represented and updated the information about the genetic structure of D. rabiei populations across the country by announcing new information about the isolates from wild relatives. In addition, STMS markers were utilized to test whether allele sizes of microstallite loci change during asexual reproduction in infection period within the host. Thus, the changes in pathogen genotype was traced from seed to seedling. To do tracing, chickpea seeds were treated with two different D. rabiei isolates with known STMS multilocus genotypes. Then, pathogen re- isolations were performed from the plants grown from the infected seeds and these re-isolates were genotyped with the same STMS markers. Allele sizes of re-isolates were different from the parental ones for some of the loci which indicated that microsatellite alleles may have changed during multiple cycles of asexual reproduction through host infection.


Didymella rabiei Ascochyta blight STMS Genotyping Pathogen tracking 



This study was supported by TUBITAK 113O071 project. Authors would like to thank Mr. Unal Sevinc for his assistance in genotyping.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abbo, S., Frenkel, O., Sherman, A., & Shtienberg, D. (2007). The sympatric Ascochyta pathosystems of stern legumes, a key for better understanding of pathogen biology. European Journal of Plant Pathology, 119, 111–118.CrossRefGoogle Scholar
  2. Agapow, P. M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101–102.CrossRefGoogle Scholar
  3. Bayraktar, H., Dolar, S., & Tor, M. (2007). Determination of genetic diversity within Ascochyta rabiei (pass.) Labr., the cause of ascochyta blight of chickpea in Turkey. Journal of Plant Pathology, 89, 341–347.Google Scholar
  4. Berger, J., Abbo, S., & Turner, N. C. (2003). Ecogeography of annual wild Cicer species: The perilous state of the world collection. Crop Science, 43, 1076–1090.CrossRefGoogle Scholar
  5. Brown, A. H. D., Feldman, M. W., Nevo, E. (1980). Multilocus structure of natural populations of Hordeum spontaneum. Genetics, 96, 523–536.Google Scholar
  6. Can, C., Ozkilinc, H., Kahraman, A., & Ozkan, H. (2007). First report of Ascochyta rabiei causing Ascochyta blight of Cicer pinnatifidum. Plant Disease, 91, 908.CrossRefGoogle Scholar
  7. Chen, W. (2016). Pulse crop diseases in the Pacific Northwest. Crop Soil, 49, 20–26.CrossRefGoogle Scholar
  8. Chen, X., Ge, J., Ma, D., Ma, L., Liu, W., & Qiang, S. (2017). Characterization and identification of an epidemic strain of Ascochyta rabiei on chickpeas in Northwest China. Journal of Phytopathology, 165, 355–360.CrossRefGoogle Scholar
  9. Dowling, M.E., Bryson, P. K., Boatwright, H. G., Wilson, J. R., Fan, Z., Everhart, S. E., Brannen, P. M., Schnabel, G. (2016). Effect of Fungicide Applications on Population Diversity and Transposon Movement. Phytopathology, 106, (12):1504–1512Google Scholar
  10. Dowling, M. E., Schnabel, G., Boatwright, H. G., & Everhart, S. E. (2017). Novel gene-sequence markers for isolate tracking within Monilinia fructicola lesions. Pest Management Science, 73, 1822–1829.CrossRefGoogle Scholar
  11. Frenkel, O., Peever, T. L., Chilvers, M., Ozkilinc, H., Can, C., Abbo, S., Shitienberg, D., & Sherman, A. (2010). Ecological genetic divergence of the fungal pathogen Didymella rabiei on sympatric wild and domesticated Cicer spp. (chickpea). Applied and Environmental Microbiology, 76, 30–39.CrossRefGoogle Scholar
  12. Geistlinger, J., Maqbool, S., Kaiser, W. J., & Kahl, G. (1997). Detection of microsatellite fingerprint markers and their Mendelian inheritance in Ascochyta rabiei. Mycological Research, 101, 1113–1121.CrossRefGoogle Scholar
  13. Geistlinger, J., Weising, K., Winter, P., & Kahl, G. (2000). Locus-specific microsatellite markers for the fungal chickpea pathogen Didymella rabiei (anamorph) Ascochyta rabiei. Molecular Ecology, 9, 1939–1941.CrossRefGoogle Scholar
  14. Kaiser, W. J., Hannan, R. M., & Muehlbauer, F. J. (1998). First report of Ascochyta blight of Cicer monbretii, a wild perennial chickpea in Bulgaria. Plant Disease, 82, 830.Google Scholar
  15. Ladizinsky, G., & Adler, A. (1976). Genetic relationships among the annual species of Cicer L. Theoretical and Applied Genetics, 48, 197–203.CrossRefGoogle Scholar
  16. Laine, A. L. (2008). Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecology Letters, 11, 327–337.CrossRefGoogle Scholar
  17. Leo, A. E., Ford, R., & Linde, C. C. (2015). Genetic homogeneity of a recently introduced pathogen of chickpea, Ascochyta rabiei, to Australia. Biol Invasionsions, 17, 609–623.CrossRefGoogle Scholar
  18. Leppik, E. E. (1970). Gene centers of plants as sources of disease resistance. Annual Review of Phytopathology, 8, 323–344.CrossRefGoogle Scholar
  19. Lev-Yadun, S., Gopher, A., Abbo, S. (2000). The cradle of agriculture. Science, 288, 1602–1603.Google Scholar
  20. Michalakis, Y., & Excoffier, L. (1996). A generic estimation of population subdivision using distances between alleles with special references for microsatellite loci. Genetics, 142, 1061–1064.Google Scholar
  21. Muzhinji, N., Woodhall, J. W., Truter, M., & van der Waals, E. J. (2018). Relative contribution of seed tuber- and Soilborne inoculum to potato disease development and changes in the population genetic structure of Rhizoctonia solani AG 3-PT under field conditions in South Africa. Plant Disease, 102, 60–66.CrossRefGoogle Scholar
  22. Nei, M. (1973). Analysis of Gene Diversity in Subdivided Populations. Proceedings of the National Academy of Sciences, 70, (12):3321-3323Google Scholar
  23. Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583–590.Google Scholar
  24. Ozkilinc, H., Frenkel, O., Abbo, S., Shtienberg, D., Sherman, A., Ophir, R., & Can, C. (2010). A comparative study of Turkish and Israeli populations of Didymella rabiei, the ascochyta pathogen of chickpea. Plant Pathology, 59, 492–503.CrossRefGoogle Scholar
  25. Ozkilinc, H., Frenkel, O., Shtienberg, D., Abbo, S., Sherman, A., Kahraman, A., & Can, C. (2011). Aggressiveness of eight Didymella rabiei isolates from domesticated and wild chickpea native to Turkey and Israel, a case study. European Journal of Plant Pathology, 131, 529–537.CrossRefGoogle Scholar
  26. Ozkilinc, H., Thomas, K., Abang, M., Peever, T. L. (2015). Population structure and reproductive mode of in Syria. Plant Pathology, 64, (5):1110–1119Google Scholar
  27. Peakall, R., & Smouse, P. E. (2006). GENALEX 6: Genetic analysis in Excell. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.CrossRefGoogle Scholar
  28. Peever, T. L., Salimath, S. S., Su, G., Kaiser, W. J., & Muehlbauer, F. J. (2004). Historical and contemporary multilocus population structure of Ascochyta rabiei (teleomorph: Didymella rabiei) in the Pacific Northwest of the United States. Molecular Ecology, 13, 291–309.CrossRefGoogle Scholar
  29. Peever, T. L., Barve, M. P., Stone, L. J., Kaiser, W. J. (2017). Evolutionary relationships among species infecting wild and cultivated hosts in the legume tribes Cicereae and Vicieae. Mycologia, 99, (1):59–77Google Scholar
  30. Phan, H. T. T., Ford, R., & Taylor, P. J. W. (2003). Population structure of Ascochyta rabiei in Australia based on STMS fingerprints. Fungal Diversity, 13, 111–129.Google Scholar
  31. Prichard, J. K., Stephans, M., Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959. Google Scholar
  32. Prospero, S., Hansen, E. M., Grünwald, N. J., & Winton, L. M. (2007). Population dynamics of the sudden oak death pathogen Phytophthora ramorum in Oregon from 2001 to 2004. Molecular Ecology, 16, 2958–2973.CrossRefGoogle Scholar
  33. Rhaiem, A., Cherif, M., Peever, T. L., & Dyer, P. S. (2008). Population structure and mating system of Ascochyta rabiei in Tunisia: Evidence for the recent introduction of mating type 2. Plant Pathology, 57, 540–551.CrossRefGoogle Scholar
  34. Shah, D., Bergstrom, G. C., & Ueng, P. P. (1995). Initiation of Septoria nodorum blotch epidemics in winter wheat by seedborne Stagonospora nodorum. Phytopathology, 85, 452–457.CrossRefGoogle Scholar
  35. Zhan, J., Mundt, C. C., Hoffer, E., & McDonald, B. A. (2002). Local adaptation and effect of host genotype on the rate of pathogen evolution: An experimental test in a plant pathosystem. Journal of Evolutionary Biology, 15, 634–647.CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Molecular Biology and GeneticsCanakkale Onsekiz Mart UniversityCanakkaleTurkey
  2. 2.Department of BiologyGaziantep UniversityGaziantepTurkey

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