DOI QR코드

DOI QR Code

Phylogenetic Analysis of Phaeosphaeria Species Using Mating Type Genes and Distribution of Mating Types in Iran

  • Ghaderi, Fariba (Department of Plant Protection, College of Agriculture, Yasouj University) ;
  • Habibi, Azadeh (Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology) ;
  • Sharifnabi, Bahram (Department of Plant Protection, College of Agriculture, Isfahan University of Technology)
  • Received : 2021.10.18
  • Accepted : 2022.01.20
  • Published : 2022.04.01

Abstract

Phaeosphaeria species are pathogenic on wheat, barley and a wide range of wild grasses. To analyze mating type loci of the Phaeosphaeria species and investigate mating type distribution in Iran, we sequenced mating type loci of 273 Phaeosphaeria isolates including 67 isolates obtained from symptomatic leaves and ears of wheat, barley, and wild grasses from two wheat growing region in Iran as well as 206 isolates from our collection from other regions in Iran which were isolated in our previous studies. Mating type genes phylogeny was successfully used to determine the species identity and relationships among isolates within the Phaeosphaeria spp. complex. In this study, we reported seven new host records for Phaeosphaeria species and the Phaeosphaeria avenaria f. sp. tritici 3 group was first reported from Iran in this study. Mating type distribution among Phaeosphaeria species was determined. Both mating types were present in all sampling regions from Iran. We observed skewed distribution of mating types in one region (Kohgiluyeh va Boyer-Ahmad) and equal distribution in the other region (Bushehr). However, when considering our entire dataset of 273 Iranian Phaeosphaeria isolates, the ratio of mating types was not deviated significantly from 1:1 suggesting possibilities for isolates of opposite mating type to interact and reproduce sexually, although the sexual cycle may infrequently occur in some regions especially when the climatic conditions are unfavorable for teleomorph development.

Keywords

Acknowledgement

The authors would like to acknowledge the financial support of Yasouj University, Iran, under grant number of d99/89/627.

References

  1. Adhikari, T. B., Ali, S., Burlakoti, R. R., Singh, P. K., Mergoum, M. and Goodwin, S. B. 2008. Genetic structure of Phaeosphaeria nodorum populations in the north-central and midwestern United States. Phytopathology 98:101-107. https://doi.org/10.1094/PHYTO-98-1-0101
  2. Bennett, R. S., Yun, S.-H., Lee, T. Y., Turgeon, B. G., Arseniuk, E., Cunfer, B. M. and Bergstrom, G. C. 2003. Identity and conservation of mating type genes in geographically diverse isolates of Phaeosphaeria nodorum. Fungal Genet. Biol. 40:25-37. https://doi.org/10.1016/S1087-1845(03)00062-8
  3. Cowger, C. and Silva-Rojas, H. V. 2006. Frequency of Phaeosphaeria nodorum, the sexual stage of Stagonospora nodorum, on winter wheat in North Carolina. Phytopathology 96:860-866. https://doi.org/10.1094/PHYTO-96-0860
  4. Cunfer, B. M. 2000. Stagonospora and Septoria diseases of barley, oat, and rye. Can. J. Plant Pathol. 22:332-348. https://doi.org/10.1080/07060660009500452
  5. Croll, D., Crous, P. W., Pereira, D., Mordecai, E. A., McDonald, B. A. and Brunner, P. C. 2021. Genome-scale phylogenies reveal relationships among Parastagonospora species infecting domesticated and wild grasses. Persoonia 46:116-128.
  6. Ghaderi, F. and Razavi, M. 2018. Identification of the species Parastagonospora dactylidis on poaceous plants in Iran. Mycol. Iran. 5:35-41.
  7. Ghaderi, F., Sharifnabi, B. and Javan-Nikkhah, M. 2017. Introduction of some species of Parastagonospora on poaceous plants in Iran. Rostaniha 18:150-165.
  8. Ghaderi, F., Sharifnabi, B., Javan-Nikkhah, M., Brunner, P. C. and McDonald, B. A. 2020. SnToxA, SnTox1, and SnTox3 originated in Parastagonospora nodorum in the Fertile Crescent. Plant Pathol. 69:1482-1491. https://doi.org/10.1111/ppa.13233
  9. Halama, P. 2002. Mating relationships between isolates of Phaeosphaeria nodorum (anamorph Stagonospora nodorum) from geographical locations. Eur. J. Plant Pathol. 108:593-596. https://doi.org/10.1023/A:1019933031308
  10. Halama, P. and Lacoste, L. 1992. Etude des conditions optimales permettant la pycniogenese de Phaeosphaeria (Leptosphaeria) nodorum (Mull) Hedj agent de la septoriose du ble [Study of the optimal conditions allowing the pycniogenesis of Phaeosphaeria (Leptosphaeria) nodorum (Mull) Hedj agent of wheat septoria]. Agronomie 12:705-710 (in French). https://doi.org/10.1051/agro:19920905
  11. Keller, S. M., McDermott, J. M., Pettway, R. E., Wolfe, M. S. and McDonald, B. A. 1997a. Gene flow and sexual reproduction in the wheat glume blotch pathogen Phaeosphaeria nodorum (Anamorph Stagonospora nodorum). Phytopathology 87:353-358. https://doi.org/10.1094/PHYTO.1997.87.3.353
  12. Keller, S. M., Wolfe, M. S., McDermott, J. M. and McDonald, B. A. 1997b. High genetic similarity among populations of Phaeosphaeria nodorum across wheat cultivars and regions in Switzerland. Phytopathology 87:1134-1139. https://doi.org/10.1094/PHYTO.1997.87.11.1134
  13. Librado, P. and Rozas, J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452. https://doi.org/10.1093/bioinformatics/btp187
  14. Malkus, A., Chang, P.-F. L., Zuzga, S. M., Chung, K.-R., Shao, J., Cunfer, B. M., Arseniuk, E. and Ueng, P. P. 2006. RNA polymerase II gene (RPB2) encoding the second largest protein subunit in Phaeosphaeria nodorum and P. avenaria. Mycol. Res. 110:1152-1164. https://doi.org/10.1016/j.mycres.2006.07.015
  15. Malkus, A., Reszka, E., Chang, C. J., Arseniuk, E., Chang, P. F. and Ueng, P. P. 2005. Sequence diversity of β-tubulin (tubA) gene in Phaeosphaeria nodorum and P. avenaria. FEMS Microbiol. Lett. 249:49-56. https://doi.org/10.1016/j.femsle.2005.05.049
  16. McDonald, B. A., Miles, J., Nelson, L. R. and Pettway, R. E. 1994. Genetic variability in nuclear DNA in field populations of Stagonospora nodorum. Phytopathology 84:250-255. https://doi.org/10.1094/Phyto-84-250
  17. McDonald, M. C., Razavi, M., Friesen, T. L., Brunner, P. C. and McDonald, B. A. 2012. Phylogenetic and population genetic analyses of Phaeosphaeria nodorum and its close relatives indicate cryptic species and an origin in the Fertile Crescent. Fungal Genet. Biol. 49: 882-895. https://doi.org/10.1016/j.fgb.2012.08.001
  18. 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
  19. Notteghem, J. L. and Silue, D. 1992. Distribution of mating type alleles in Magnaporthe grisea populations pathogenic on rice. Phytopathology 82:421-424. https://doi.org/10.1094/Phyto-82-421
  20. Posada, D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256. https://doi.org/10.1093/molbev/msn083
  21. Quaedvlieg, W., Verkley, G. J., Shin, H. D., Barreto, R. W., Alfenas, A. C., Swart, W. J., Groenewald, J. Z. and Crous, P. W. 2013. Sizing up Septoria. Stud. Mycol. 75:307-390. https://doi.org/10.3114/sim0017
  22. Reszka, E., Chung, K. R., Tekauz, A., Malkus, A., Arseniuk, E., Krupinsky, J. M., Tsang, H. and Ueng, P. P. 2005. Presence of β-glucosidase (bgl1) gene in Phaeosphaeria nodorum and Phaeosphaeria avenaria f.sp. triticea. Can. J. Bot. 83:1001-1014. https://doi.org/10.1139/b05-052
  23. Shaw, D. E. 1957. Studies on Leptosphaeria avenaria f. sp. triticea on cereals and grasses. Can. J. Bot. 35:113-118. https://doi.org/10.1139/b57-012
  24. Shipton, W. A., Boyd, W. J. R., Rosielle, A. A. and Shearer, B. I. 1971. The common Septoria diseases of wheat. Bot. Rev. 37:231-262. https://doi.org/10.1007/BF02858957
  25. Shoemaker, R. A. and Babcock, C. E. 1989. Phaeosphaeria. Can. J. Bot. 67:1500-1599. https://doi.org/10.1139/b89-199
  26. Solomon, P. S., Lowe, R. G., Tan, K. C., Waters, O. D. and Oliver, R. P. 2006. Stagonospora nodorum: cause of stagonospora nodorum blotch of wheat. Mol. Plant Pathol. 7:147-156. https://doi.org/10.1111/j.1364-3703.2006.00326.x
  27. Solomon, P. S., Parker, K., Loughman, R. and Oliver, R. P. 2004. Both mating types of Phaeosphaeria (anamorph Stagonospora) nodorum are present in Western Australia. Eur. J. Plant Pathol. 110:763-766. https://doi.org/10.1023/B:EJPP.0000041565.42836.c1
  28. Sommerhalder, R. J., McDonald, B. A. and Zhan, J. 2006. The frequencies and spatial distribution of mating types in Stagonospora nodorum are consistent with recurring sexual reproduction. Phytopathology 96:234-239. https://doi.org/10.1094/PHYTO-96-0234
  29. Swofford, D. L. 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland, MA, USA.
  30. Turgeon, B. G. 1998. Application of mating type gene technology to problems in fungal biology. Annu. Rev. Phytopathol. 36:115-137. https://doi.org/10.1146/annurev.phyto.36.1.115
  31. Ueng, P. P. and Chen, W. 1994. Genetic differentiation between Phaeosphaeria nodorum and P. avenaria using restriction fragment length polymorphisms. Phytopathology 84:800-806. https://doi.org/10.1094/Phyto-84-800
  32. Ueng, P. P., Dai, Q., Cui, K.-R., Czembor, P. C., Cunfer, B. M., Tsang, H., Arseniuk, E. and Bergstrom, G. C. 2003. Sequence diversity of mating-type genes in Phaeosphaeria avenaria. Curr. Genet. 43:121-130. https://doi.org/10.1007/s00294-003-0377-4
  33. Ueng, P. P., Subramaniam, K., Chen, W., Arseniuk, E., Wang, L., Cheung, A. M., Hoffmann, G. M. and Bergstrom, G. C. 1998. Intraspecific genetic variation of Stagonospora avenae and its differentiation from S. nodorum. Mycol. Res. 102:607-614. https://doi.org/10.1017/S095375629700525X
  34. Vergnes, D. M., Zhanarbekova, A., Renard, M.-E., Duveiller, E. and Maraite, H. 2006. Mating types of Phaeosphaeria nodorum (anamorph Stagonospora nodorum) from Central Asia. J. Phytopathol. 154: 317-319. https://doi.org/10.1111/j.1439-0434.2006.01100.x
  35. Wang, C.-L., Malkus, A., Zuzga, S. M., Chang, P.-F. L., Cunfer, B. M., Arseniuk, E. and Ueng, P. P. 2007. Diversity of the trifunctional histidine biosynthesis gene (his) in cereal Phaeosphaeria species. Genome 50:595-609. https://doi.org/10.1139/G07-038