Genetic Diversity Assessment of the Diaporthe cinerascens Causal Agent of Fig Canker Using ISSR Markers

Document Type : Original Article

Authors

1 Department of Plant Protection, School of Agriculture, Shiraz University, Shiraz 7144113131, Iran.

2 Plankton and Microbial Ecology, Leibniz Institute for Freshwater Ecology and Inland Fisheries (IGB), 16775 Neuglobsow, Germany

10.22043/MI.2024.365650.1280

Abstract

Diaporthe cinerascens is a significant plant pathogen that causes canker disease in fig trees. This pathogen is notably dominant in major fig-production areas in Iran, as well as in other fig-producing countries such as Bulgaria, USA (California), Canada, and Italy. In the present study, six Inter-Simple Sequence Repeats (ISSR) markers were used to investigate genetic diversity among representative D. cinerascens isolates, selected based on the variety of their host cultivars, aggressiveness, and morphological features. The discriminating power of each ISSR marker was assessed using 10 parameters including effective multiplex ratio, expected heterozygosis, observed heterozygosity, polymorphic information content, marker index, resolving power, Nei's diversity, Shannon index, polymorphic percentage, and allele number. Among them, M1 primer was the best to detect the variability of the D. cinerascens isolates. The isolates exhibited a high degree of genetic similarity, as evidenced by Jaccard’s similarity coefficients, which ranged from 79% to 100%. Despite the high values of pairwise Jaccard's similarity coefficient among the isolates (at least 79% similarity), they were grouped into four distinct genetic clusters, based on Principal Coordinate Analysis (PCoA) analysis. The observed grouping pattern was found to be partially influenced by their geographical origins and the specific fig cultivars from which the isolates were recovered. Based on ISSR fingerprinting, we provided genetic evidence regarding the clonal structure of D. cinerascens. These results could be critical to understanding Diaporthe canker epidemiology and adopting sustainable management practices for the disease.
 

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Al Shuwaili, F.E.H. 2020. Taxonomic and genetic diversity and pathogenicity of Diaporthe species associated with soybean. (Publication no. 28027066) [Doctoral dissertation, University of Arkansas] ProQuest Dissertations & Theses Global.

Altıntaş, S., Toklu, F., Kafkas, S., Kilian, B., Brandolini, A. et al. 2008. Estimating genetic diversity in durum and bread wheat cultivars from Turkey using AFLP and SAMPL markers. Plant Breeding 127(1): 9–14, https://doi.org/10.1111/j.1439-0523.2007.01424.x

Banihashemi, Z., and Javadi, A. R. 2009. Further investigations on the biology of Phomopsis cinerascens, the cause of fig canker in Iran. Phytopathologia Mediterranea 48: 454–460. https://doi.org/10.17660/actahortic.2008.798.30.

Bolboli, Z., Mostowfizadeh–Ghalamfarsa, R., Jafari, M and Sarkhosh, A. 2022. Susceptibility of fig cultivars to Diaporthe canker in Iran. Plant Pathology: 71: 1–14. https.//doi.org/10.1111/ppa.13687.

Burt, P.J., Rutter, J. and Ramirez, F. 1998. Airborne spore loads and mesoscale dispersal of the fungal pathogens causing Sigatoka diseases in banana and plantain. Aerobiologia 14(2): 209–214. https://doi.org/10.1007/BF02694208.

Carlier, J., Cabrita, L., Leitao, J., Sousa, R., and Sousa, A.  2009. ISSR and AFLP characterization of Phomopsis amygdali (Del.) Tuset & Portilla accessions. Acta Horticulture 912: 645–650. https://doi.org/10.17660/ActaHortic.2011.912.97.

Crous, P. W., Verkley, G. J. M., Groenewald, J. Z., and Houbraken, J. 2019. Westerdijk laboratory manual series 1. fungal biodiversity. Westerdijk Fungal Biodiversity Institute.‏

Ferguson, L., Michailides, T.J., and Shorey, H.H. 1990. The California fig industry. Horticultural Reviews. 12: 409–490. https://doi.org/10.1002/9781118060858.ch9.

Francis, C.Y., Cai and Yang, R. 1999. Popgene version 1.31. A joint project development by University of Alberta and Tim Boyle. Centre for International, available at. http.//ftp microsoft.com/Softlib/Mslfiles.

Gao, Y. F. Liu, W. Duan, Crous, P.W., and Cai, L. 2017. Diaporthe is paraphyletic. IMA Fungus 8(1): 153–187.

Gomes, R.R. Glienke, C. Videira, S.I. R Lombard, L., Groenewald, J.Z. et al. 2013. Diaporthe: a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31: 1–41.

Haghi, Z., Mostowfizadeh-Ghalamfarsa, R., and Edel-Hermann, V. 2020. Genetic diversity of Pythium oligandrum in Iran. Journal of Plant Pathology 102(4): 1197–1204.

Hampson, M.C. 1981. Phomopsis canker on weeping fig in Newfoundland. Canadian Plant Disease Survey 61 (1): 3–5.‏

Koenick, L.B., Vaghefi, N., Knight, N. L., du Toit, L. J., and Pethybridge, S. J.  2019. Genetic diversity and differentiation in Phoma betae populations on table beet in New York and Washington States. Plant Disease 103(7): 1487–1497.

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

Mirsoleimani, Z, and Mostowfizadeh-Ghalamfarsa, R. 2013. Characterization of Phytophthora pistaciae, the causal agent of pistachio gummosis, based on host range, morphology, and ribosomal genome. Phytopathologia Mediterranea 52(3): 501–516.‏

Ogawa, J.M., and English, H. 1991. Disease of Temperate Zone Tree Fruit and Nut Crops. University of California Division of Agriculture and Natural Resources, Publication.

Powell, W., Morgante, M., Andre, C., Hanafey, M., Vogel, J. et al. 1996. The comparison of RFLP, RAPD, AFLP and SSR (microsatellite) markers for germplasm analysis. Molecular Breeding 2: 225–238, https://doi.org/10.1007/BF00564200.

Rieux, A., Soubeyrand, S., Bonnot, F., Klein, E.K., Ngando, J.E. et al. 2014. Long-distance wind-dispersal of spores in a fungal plant pathogen. estimation of anisotropic dispersal kernels from an extensive field experiment. PLOS One 9(8):  e103225. https.//doi.org/10.1371/journal.pone.0103225.

Rohlf, F. J. 2000. NTSYS-pc. Numerical Taxonomy and Multivariate Analysis System Version 2.1. Exeter Publishing Setauket, New York.

Says-Lesage, V., Roeckel-Drevet, P., Viguié, A., Tourvieille, J., Nicolas, P. et al. 2002. Molecular variability within Diaporthe/Phomopsis helianthi from France. Phytopathology 92(3): 308–313. https://doi.org/10.1094/PHYTO.2002.92.3.308

Smith, J. S. C. Chin, E. Shu, H. Smith, O. S. Wall, S. et al. 1997. An evaluation of the utility of SSR loci as molecular markers in maize (Zea mays L.): comparisons with data from RFLPs and pedigree. Theoretical and Applied Genetics 95: 163–173.

Varshney, R.K., Chabane, K., Hendre, P.S. Aggarwal, R.K. and Graner, A. 2007. Comparative assessment of EST-SSR, EST-SNP and AFLP markers for evaluation of genetic diversity and conservation of genetic resources using wild, cultivated and elite barleys. Plant Science 173(6): 638–649. https://doi.org/10.1016/j.plantsci.2007.08.010.

Xiong, T., Zeng, Y., Wang, W., Li, P., Gai, Y. et al. 2021. Abundant genetic diversity and extensive differentiation among geographic populations of the citrus pathogen Diaporthe citri in southern China. Journal of Fungi 7(9): 749.

Yang, Y. Q., Sun, Q., Li, C. M., Chen, H. F., Zhao, F. et al. 2020. Biological Characteristics and genetic diversity of Phomopsis asparagi, causal agent of asparagus stem blight. Plant Disease 104(11): 2898–2904.

References

Al Shuwaili, and F.E.H. 2020. Taxonomic and genetic diversity, and pathogenicity of Diaporthe species associated with soybean. (Publication no. 28027066)  [Doctoral dissertation, University of Arkansas] ProQuest Dissertations & Theses Global.
Altıntaş, S., Toklu, F., Kafkas, S., Kilian, B., Brandolini, A. et al. 2008. Estimating genetic diversity in durum and bread wheat cultivars from Turkey using AFLP and SAMPL markers. Plant Breeding 127(1): 9–14, https://doi.org/10.1111/j.1439-0523.2007.01424.x
Banihashemi, Z., and Javadi, A. R. 2009. Further investigations on the biology of Phomopsis cinerascens, the cause of fig canker in Iran. Phytopathologia Mediterranea 48: 454–460. https://doi.org/10.17660/actahortic.2008.798.30.
Bolboli, Z., Mostowfizadeh–Ghalamfarsa, R., Jafari, M and Sarkhosh, A. 2022. Susceptibility of fig cultivars to Diaporthe canker in Iran. Plant Pathology: 71: 1–14. https.//doi.org/10.1111/ppa.13687.
Burt, P.J., Rutter, J. and Ramirez, F. (1998). Airborne spore loads and mesoscale dispersal of the fungal pathogens causing Sigatoka diseases in banana and plantain. Aerobiologia 14(2): 209–214. https://doi.org/10.1007/BF02694208.
Carlier, J., Cabrita, L., Leitao, J., Sousa, R., and Sousa, A.  2009. ISSR and AFLP characterization of Phomopsis amygdali (Del.) Tuset & Portilla accessions. Acta Horticalture 912: 645–650. https://doi.org/10.17660/ActaHortic.2011.912.97.
Crous, P. W., Verkley, G. J. M., Groenewald, J. Z., and Houbraken, J. 2019. Westerdijk laboratory manual series 1. fungal biodiversity. Westerdijk Fungal Biodiversity Institute.‏
Ferguson, L., Michailides, T.J., and Shorey, H.H. 1990. The California fig industry. Horticultural Reviews. 12: 409–490. https://doi.org/10.1002/9781118060858.ch9.
Francis, C.Y., Cai and Yang, R. 1999. Popgene version 1.31. A joint project development by University of Alberta and Tim Boyle. Centre for International, available at. http.//ftp microsoft.com/Softlib/Mslfiles.
Gao, Y. F. Liu, W. Duan, Crous, P.W., and Cai, L. 2017. Diaporthe is paraphyletic.. IMA Fungus 8(1): 153–187. https://doi.org/10.5598/imafungus.2017.08.01.11
Gomes, R.R. Glienke, C. Videira, S.I. R Lombard, L., Groenewald, J.Z. et al. 2013. Diaporthe : a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31: 1–41. https://doi.org/10.3767/003158513X666844
Haghi, Z., Mostowfizadeh-Ghalamfarsa, R., and Edel-Hermann, V. 2020. Genetic diversity of Pythium oligandrum in Iran. Journal of Plant Pathology 102(4): 1197–1204.
Hampson, M.C. 1981. Phomopsis canker on weeping fig in Newfoundland. Canadian Plant Disease Survey 61 (1): 3–5.‏
Koenick, L.B., Vaghefi, N., Knight, N. L., du Toit, L. J., and Pethybridge, S. J.  2019. Genetic diversity and differentiation in Phoma betae populations on table beet in New York and Washington States. Plant Disease 103(7): 1487–1497. https://doi.org/10.1094/PDIS-09-18-1675-RE
McDonald, B.A. and Linde, C. 2002. The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica 124:163–180. https://doi.org/10.1023/A:1015678432355
Mirsoleimani, Z, and Mostowfizadeh-Ghalamfarsa, R. 2013. Characterization of Phytophthora pistaciae, the causal agent of pistachio gummosis, based on host range, morphology, and ribosomal genome. Phytopathologia Mediterranea 52(3): 501–516.‏
Ogawa, J.M., and English, H. 1991. Disease of Temperate Zone Tree Fruit and Nut Crops. University of California Division of Agriculture and Natural Resources, Publication.
Powell,W., Morgante, M., Andre, C., Hanafey, M., Vogel, J. et al. 1996. The comparison of RFLP, RAPD, AFLP and SSR (microsatellite) markers for germplasm analysis. Molecular Breeding 2: 225–238, https://doi.org/10.1007/BF00564200.
Rieux, A., Soubeyrand, S., Bonnot, F., Klein, E.K., Ngando, J.E. et al. 2014. Long-distance wind-dispersal of spores in a fungal plant pathogen. estimation of anisotropic dispersal kernels from an extensive field experiment. PLOS One 9(8):  e103225. https.//doi.org/10.1371/journal.pone.0103225.
Rohlf, F. J. 2000. NTSYS-pc. Numerical Taxonomy and Multivariate Analysis System Version 2.1. Exeter Publishing Setauket, New York.
Says-Lesage, V., Roeckel-Drevet, P., Viguié, A., Tourvieille, J., Nicolas, P. et al. 2002. Molecular variability within Diaporthe/Phomopsis helianthi from France. Phytopathology 92(3): 308–313. https://doi.org/10.1094/PHYTO.2002.92.3.308
Smith, J. S. C. Chin, E. Shu, H. Smith, O. S. Wall, S. et al. 1997. An evaluation of the utility of SSR loci as molecular markers in maize (Zea mays L.): comparisons with data from RFLPs and pedigree. Theoretical and Applied Genetics 95: 163–173. https://doi.org/10.1007/s001220050544.
Varshney, R.K., Chabane, K., Hendre, P.S. Aggarwal, R.K. and Graner, A. 2007. Comparative assessment of EST-SSR, EST-SNP and AFLP markers for evaluation of genetic diversity and conservation of genetic resources using wild, cultivated and elite barleys. Plant Science 173(6): 638–649. https://doi.org/10.1016/j.plantsci.2007.08.010.
Xiong, T., Zeng, Y., Wang, W., Li, P., Gai, Y. et al. 2021. Abundant genetic diversity and extensive differentiation among geographic populations of the citrus pathogen Diaporthe citri in southern China. Journal of Fungi 7(9): 749.
Yang, Y. Q., Sun, Q., Li, C. M., Chen, H. F., Zhao, F. et al. 2020. Biological Characteristics and genetic diversity of Phomopsis asparagi, causal agent of asparagus stem blight. Plant Disease 104(11): 2898–2904.
Mycologia Iranica
Volume 11, Issue 1
June 2024
Pages 29-37

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