DOI QR코드

DOI QR Code

Genetic Structure of Macrophomina phaseolina Populations, the Causal Agent of Sesame Charcoal Rot Disease in Iran

  • Maryam Dolatkhah (Department of Plant Protection, College of Agriculture, Yasouj University) ;
  • Fariba ghaderi (Department of Plant Protection, College of Agriculture, Yasouj University) ;
  • Abdollah Ahmadpour (Higher Education Center of Shahid Bakeri, Urmia University)
  • Received : 2023.12.12
  • Accepted : 2024.02.29
  • Published : 2024.03.31

Abstract

Charcoal rot disease, caused by the fungus Macrophomina phaseolina, is one of the most important diseases of Sesame (Sesamum indicum) all over the world. However, the population biology of M. phaseolina is poorly understood. In this study, M. phaseolina isolates from five different regions of Iran (Khuzestan, Fars, Bushehr, Hormozgan, and Kohgiluyeh & Boyer-Ahmad provinces) (n=200) were analyzed for genetic variation using inter simple sequence repeats marker. In total, 152 unique haplotypes were identified among the 200 M. phaseolina isolates, and gene diversity (H=0.46-0.84) and genotypic diversity were high in each of the regions. The structure analysis clustered five Iranian populations into two distinct groups, the individuals from group 1 were assigned to the Bushehr population and the individuals from Khuzestan, Fars, Hormozgan and Kohgiluyeh & Boyer-Ahmad were aggregated and formed group 2. The results matched with genetic differentiation and gene flow among regions. Analyses of the distribution of gene diversity within and among five Iranian populations were 61% and 39%, respectively. Our results showed that infected seeds are thought to be the dominant mechanism responsible for the spreading of the pathogen in southern parts of Iran. In summary, it is essential to have local quarantine and prevent seed exchanges between geographical populations to restrict the dispersal of pathogen over long distances and provide certified seeds in Iran.

Keywords

Acknowledgement

The authors thank the Yasouj University for financial support.

References

  1. Aboshosha, S. S., Atta Alla, S. I., El-Korany, A. E. and El-Argawy, E. 2007. Characterization of Macrophomina phaseolina isolates affecting sunflower growth in El-Behera governorate, Egypt. Int. J. Agri. Biol. 9: 807-815.
  2. Aghakhani, M. and Dubey, S. C. 2009. Determination of genetic diversity among Indian isolates of Rhizoctonia bataticola causing dry root rot of chickpea. Antonie Van Leeuwenhoek. 96: 607-619. https://doi.org/10.1007/s10482-009-9375-y
  3. Almeida, A. M., Abdelnoor, R. V., Arias, C. A. A., Carvalho, V. P., Jacoud Filho, D. S., Marin, S. R. et al. 2003. Genotypic diversity among Brazilian isolates of Macrophomina phaseolina revealed by RAPD. Fitopatol. Bras. 28: 279-285. https://doi.org/10.1590/S0100-41582003000300009
  4. Brown, J. K. and Hovmoller, M. S. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297: 537-541. https://doi.org/10.1126/science.1072678
  5. Carbone, I. and Kohn, L. M. 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553-556. https://doi.org/10.1080/00275514.1999.12061051
  6. Carlile, M. J. 1986. Genetic exchange and gene flow: their promotion and prevention. In: Evolutionary Biological of the Fungi, eds. by A. D. M. Rayner and D. Moore, pp. 203-214. Cambridge University Press, Cambridge, UK.
  7. Chattopadadhyay, C., Kolte, S. J. and Waliyar, F. 2019. Diseases of edible oilseed crops. CRC Press, Boca Raton, FL, USA. 293-325 pp.
  8. Chen, R. S., Boeger, J. M. and McDonald, B. A. 1994. Genetic stability in a population of a plant pathogenic fungus over time. Mol. Ecol. 3: 209-218. https://doi.org/10.1111/j.1365-294X.1994.tb00054.x
  9. Crous, P. W., Slippers, B., Wingfield, M. J., Rheeder, J., Marasas, W. F., Philips, A. J. et al. 2006. Phylogenetic lineages in the Botryosphaeriaceae. Stud. Mycol. 55: 235-253. https://doi.org/10.3114/sim.55.1.235
  10. Das, I. K., Fakrudin, B. and Arora, D. K. 2008. RAPD cluster analysis and chlorate sensitivity of some Indian isolates of Macrophomina phaseolina from sorghum and their relationships with pathogenicity. Microbiol. Res. 163: 215-224. https://doi.org/10.1016/j.micres.2006.05.006
  11. Earl, D. A. and VonHoldt, B. M. 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4: 359-361. https://doi.org/10.1007/s12686-011-9548-7
  12. Elmerich, C., Pandey, A. K., Vemula, A., Rathore, A. and Nair, R. M. 2022. Blackgram-Macrophomina phaseolina interactions and identification of novel sources of resistance. Plant Dis. 106: 2911-2919. https://doi.org/10.1094/PDIS-11-21-2588-RE
  13. Ershad, D. 2009. Fungi of Iran. 3rd ed. Iranian Research Institution of Plant Protection, Tehran, Iran.
  14. Evanno, G., Regnaut, S. and Goudet, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14: 2611-2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
  15. Farr, D. F. and Rossman, A. Y. 2023. Fungal databases, systematic mycology and microbiology laboratory. ARS, USDA, Washington, DC, USA.
  16. Farr, D. F., Rossman, A. Y. and Castlebury, L. A. 2024. United States National Fungus Collections Fungus-Host Dataset. URL https://nt.ars-grin.gov/fungaldatabases/ [20 February 2024].
  17. Food and Agriculture Organization of the United Nations (FAO). 2023. FAOSTAT. URL https://www.fao.org/faostat/en/ [24 September 2023].
  18. Ghosh, T., Biswas, M. K., Guin, C. and Roy, P. 2018. A review on characterization, therapeutic approaches and pathogenesis of Macrophomina phaseolina. Plant Cell Biotechnol. Mol. Biol. 19: 72-84.
  19. Goudet, J. 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. J. Hered. 86: 485-486. https://doi.org/10.1093/oxfordjournals.jhered.a111627
  20. Jacobs, K., Bergdahl, D. R., Wingfield, M. J., Halik, S., Seifert, K. A., Bright, D. E. et al. 2004. Leptographium wingfieldii introduced into North America and found associated with exotic Tomicus piniperda and native bark beetles. Mycol. Res. 108: 411-418. https://doi.org/10.1017/S0953756204009748
  21. Khamari, B., Hasmi, S. K., Sahoo, J. P. and Samal, K. C. 2023. ISSR marker based genetic diversity assessment and phenotypic characterization in relation to the pathogenicity of Macrophomina phaseolina isolates in sesame. Indian Phytopathol. 76: 753-765. https://doi.org/10.1007/s42360-023-00652-7
  22. Khamari, B., Hasmi, S. K., Sahoo, J. P., Samal, K. C., Beura, S. K. and Ranasingh, N. 2022. ISSR based genetic diversity and phenotypic characterization in relation to pathogenicity of Macrophomina phaseolina isolated in sesame. AMA. Agric. Mech. Asia Afr. Lat. Am. 53: 7649-7664.
  23. Khan, A. N., Shair, F., Malik, K., Hayat, Z., Khan, M. A., Hafeez, F. Y. et al. 2017. Molecular identification and genetic characterization of Macrophomina phaseolina strains causing pathogenicity on sunflower and chickpea. Front. Microbiol. 8: 1309.
  24. Kumar, P. and Dubey, R. C. 2023. Macrophomina phaseolina: ecobiology, pathology and management. Elsevier, San Diego, CA, USA. 368 pp.
  25. Linhai, W., Yanxin, Z., Donghua, L., Junbin, H., Wenliang, W., Haixia, L. et al. 2011. Variations in the isolates of Macrophomina phaseolina from sesame in China based on amplified fragment length polymorphism (AFLP) and pathogenicity. Afr. J. Microbiol. Res. 5: 5584-5559.
  26. Lodha, S. and Mawar, R. 2020. Population dynamics of Macrophomina phaseolina in relation to disease management: a review. J. Phytopathol. 168: 1-17. https://doi.org/10.1111/jph.12854
  27. Londono, V. O. 2022. Evolutionary genome analysis of the charcoal rot fungus Macrophomina phaseolina for improved disease management under climate change. Michigan State University ProQuest Dissertations Publishing, East Lansing, MI, USA.29999309 pp.
  28. Mahdizadeh, V., Safaie, N. and Goltapeh, E. M. 2012. Genetic diversity of sesame isolates of Macrophomina phaseolina using RAPD and ISSR markers. Trakia J. Sci. 10: 65-74.
  29. Marquez, N., Giachero, M. L., Declerck, S. and Ducasse, D. A. 2021. Macrophomina phaseolina: general characteristics of pathogenicity and methods of control. Front. Plant Sci. 12: 634397.
  30. Mayek-Perez, N., Lopez-Castaneda, C., Gonzalez-Chavira, M., GarciaEspinosa, R., Acosta-Gallegos, J., de la Vega, O. M. et al. 2001. Variability of Mexican isolates of Macrophomina phaseolina based on pathogenesis and AFLP genotype. Physiol. Mol. Plant Pathol. 59: 257-264. https://doi.org/10.1006/pmpp.2001.0361
  31. McDonald, B. A. and Linde, C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40: 349-379.
  32. McDonald, B. A., Pettway, R. E., Chen, R. S., Boeger, J. M. and Martinez, J. P. 1995. The population genetics of Septoria tritici (teleomorph Mycosphaerella graminicola). Can. J. Bot. 73: 292-301. https://doi.org/10.1139/b95-259
  33. Meena, B., Indiragandhi, P. and Ushakumari, R. 2018. Screening of sesame (Sesamum indicum L.) germplasm against major diseases. J. Pharmacogn. Phytochem. 7: 1466-1468.
  34. Meirmans, P. G. and Van Tienderen, P. H. 2004. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4: 792-794. https://doi.org/10.1111/j.1471-8286.2004.00770.x
  35. Min, Y. Y. and Toyota, K. 2019. Occurrence of different kinds of diseases in sesame cultivation in Myanmar and their impact to sesame yield. J. Exp. Agric. Int. 38: 1-9. https://doi.org/10.9734/jeai/2019/v38i430309
  36. Moslemi, M., Ghaderi, F., Karami, S. and Charehgani, H. 2023. Identification and pathogenicity of Macrophomina species in sesame fields from Iran. Trop. Plant Pathol. Online publication. https://doi.org/10.1007/s40858-023-00601-9.
  37. Murray, M. G. and Thompson, W. F. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8: 4321-4325. https://doi.org/10.1093/nar/8.19.4321
  38. Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. U S A 70: 3321-3323. https://doi.org/10.1073/pnas.70.12.3321
  39. Omar, M. R., Abd-Elsalam, K. A., Aly, A. A., El-Samawaty, A. M. A. and Verreet, J. A. 2007. Diversity of Macrophomina phaseolina from cotton in Egypt: analysis of pathogencity, chlorate phenotypes, and molecular characterization. J. Plant Dis. Protect. 114: 196-204.
  40. Peakall, R. and Smouse, P. E. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6: 288-295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
  41. Pickel, B., Dai, N., Maymon, M., Elazar, M., Tanami, Z., Frenkel, O. et al. 2020. Development of a reliable screening technique for determining tolerance to Macrophomina phaseolina in strawberry. Eur. J. Plant Pathol. 157: 707-718. https://doi.org/10.1007/s10658-020-02051-4
  42. Pritchard, J. K., Stephens, M. and Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959. https://doi.org/10.1093/genetics/155.2.945
  43. Purkayastha, S., Kaur, B., Dilbaghi, N. and Chaudhury, A. 2006. Characterization of Macrophomina phaseolina, the charcoal rot pathogen of cluster bean, using conventional techniques and PCR-based molecular markers. Plant Pathol. 55: 106-116.
  44. Rayatpanah, S., Dalili, S. A. and Yasari, E. 2012. Diversity of Macrophomina phaseolina (Tassi) Goid based on chlorate phenotypes and pathogenicity. Int. J. Biol. 4: 54-63. https://doi.org/10.5539/ijb.v4n2P54
  45. Reyes-Franco, M. C., Hernandez-Delgado, S., Beas-Fernandez, R., Medina-Fernandez, M., Simpson, J. and Mayek-Perez, N. 2006. Pathogenic and genetic variability within Macrophomina phaseolina from Mexico and other countries. J. Phytopathol. 154: 447-453. https://doi.org/10.1111/j.1439-0434.2006.01127.x
  46. Reznikov, S., Chiesa, M. A., Pardo, E. M., De Lisi, V., Bogado, N., Gonzalez, V. et al. 2019. Soybean-Macrophomina phaseolinaspecific interactions and identification of a novel source of resistance. Phytopathology 109: 63-73. https://doi.org/10.1094/PHYTO-08-17-0287-R
  47. Roy, A., De, R. K. and Ghosh, S. K. 2008. Diseases of best fiber crops and their management. In: Jute and allied fibre updates, eds. by P. G. Karmakar, S. K. Hazra, T. Ramasubramanian, R. K. Mandal, M. K. Sinha and H. S. Sen, pp. 217-241. Central Research Institute for Jute and Allied Fibers, Barrackpore, India.
  48. Salahlou, R., Safaie, N. and Shams-Bakhsh, M. 2016. Genetic diversity of Macrophomina phaseolina populations, the causal agent of sesame charcoal rot using inter-simple sequence repeat markers. J. Agr. Sci. Tech. 18: 277-287.
  49. Saleh, A. A., Ahmed, H. U., Todd, T. C., Travers, S. E., Zeller, K. A., Leslie, J. F. et al. 2010. Relatedness of Macrophomina phaseolina isolates from tallgrass prairie, maize, soybean and sorghum. Mol. Ecol. 19: 79-91.
  50. Sarr, M. P., Ndiaye, M., Groenewald, J. Z. and Crous, P. W. 2014. Genetic diversity in Macrophomina phaseolina, the causal agent of charcoal rot. Phytopathol. Mediterr. 53: 250-268.
  51. Slatkin, M. 1993. Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47: 264-279. https://doi.org/10.1111/j.1558-5646.1993.tb01215.x
  52. Stukenbrock, E. H., Banke, S. and McDonald, B. A. 2006. Global migration patterns in the fungal wheat pathogen Phaeosphaeria nodorum. Mol. Ecol. 15: 2895-2904. https://doi.org/10.1111/j.1365-294X.2006.02986.x
  53. Su, G., Suh, S. O., Schneider, R. W. and Russin, J. S. 2001. Host specialization in the charcoal rot fungus, Macrophomina phaseolina. Phytopathology 91: 120-126.
  54. Tancic Zivanov, S., Dedic, B., Dimitrijevic, A., Dusanic, N., Jocic, S., Miklic, V. et al. 2019. Analysis of genetic diversity among Macrophomina phaseolina (Tassi) Goid. Isolates from Euro-Asian countries. J. Plant Dis. Prot. 126: 565-573. https://doi.org/10.1007/s41348-019-00260-6
  55. Teklu, D. H., Shimelis, H. and Abady, S. 2022. Genetic improvement in sesame (Sesamum indicum L.): progress and outlook: a review. Agronomy 12: 2144.
  56. Vashisht, P., Yadav, N. K., Kumar, R., Jangra, P. and Indora, J. 2023. Management strategies for charcoal rot of sesame: a review. Int. J. Plant Soil. Sci. 35: 2255-2264. https://doi.org/10.9734/ijpss/2023/v35i193777
  57. Vimal, S. R., Singh, J. S., Arora, N. K. and Singh, S. 2017. Soil-plantmicrobe interactions in stressed agriculture management: a review. Pedosphere 27: 177-192. https://doi.org/10.1016/S1002-0160(17)60309-6
  58. Wang, L., Yu, J., Zhang, Y., You, J., Zhang, X. and Wang, L. 2021. Sinbase 2.0: an updated database to study multi-omics in Sesamum indicum. Phytopathology 10: 272.
  59. White, T. J., Bruns, T., Lee, S. J. W. T. and Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Proto cols: A Guide to Methods and Applications, eds. by M. A. Innis, D. H. Gelfand, J. J. Sninsky and T. J. White, pp. 315-322. Academic Press, New York, NY, USA.
  60. Win, K. T. and Oo, A. Z. 2017. Salt-stress-induced changes in protein profiles in two blackgram (Vigna mungo L.) varieties differing salinity tolerance. Adv. Plants Agric. Res. 7: 00239.
  61. Yadav, R., Kalia, S., Rangan, P., Pradheep, K., Rao, G. P., Kaur, V. et al. 2022. Current research trends and prospects for yield and quality improvement in sesame, an important oilseed crop. Front. Plant Sci. 13: 863521.
  62. Yeh, F. C., Yang, R. C. and Boyle, T. 1997. POPGENE, version 1.32 edn. Software Microsoft Window-Based Freeware for Population Genetic Analysis, Edmonton, Canada.
  63. Yousef, H. 2021. Pathogenic variation and molecular characterization of Macrophomina phaseolina, the cause of sesame charcoal rot. Egypt. J. Phytopathol. 49: 151-165.