Skip to main content

Advertisement

Log in

Magnaporthe oryzae Populations Adapted to Finger Millet and Rice Exhibit Distinctive Patterns of Genetic Diversity, Sexuality and Host Interaction

  • Research
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

In this study, host-specific forms of the blast pathogen Magnaporthe oryzae in sub-Saharan Africa (SSA) were characterised from distinct cropping locations using a combination of molecular and biological assays. Finger millet blast populations in East Africa revealed a continuous genetic variation pattern and lack of clonal lineages, with a wide range of haplotypes. M. oryzae populations lacked the grasshopper (grh) element (96%) and appeared distinct to those in Asia. An overall near equal distribution (47–53%) of the mating types MAT1-1 and MAT1-2, high fertility status (84–89%) and the dominance of hermaphrodites (64%) suggest a strong sexual reproductive potential. Differences in pathogen aggressiveness and lack of cultivar incompatibility suggest the importance of quantitative resistance. Rice blast populations in West Africa showed a typical lineage-based structure. Among the nine lineages identified, three comprised ~90% of the isolates. Skewed distribution of the mating types MAT1-1 (29%) and MAT1-2 (71%) was accompanied by low fertility. Clear differences in cultivar compatibility within and between lineages suggest R gene-mediated interactions. Distinctive patterns of genetic diversity, sexual reproductive potential and pathogenicity suggest adaptive divergence of host-specific forms of M. oryzae populations linked to crop domestication and agricultural intensification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Lenne, J. M., Takan, J. P., Mgonja, M. A., Manyasa, E. O., Kaloki, P., Wanyera, N., et al. (2007). Finger millet blast managment: A key entry point for fighting malnutrition and poverty in East Africa. Outlook on Agriculture, 36, 101–108.

    Article  Google Scholar 

  2. Takan, J. P., Akello, B., Esele, P., Manyasa, E. O., Obilana, A. B., Audi, P. O., et al. (2004). Finger millet blast pathogen diversity and management in East Africa: A summary of project activities and outputs. International Sorghum and Millets Newsletter, 45, 66–69.

    Google Scholar 

  3. Mitaru, B. N., Kargia, J. T., & Munene, C. (1993). Finger millet production and utilization in Kenya. In K. W. Riley, S. C. Gupta, A. Seetharam, & J. N. Mushonga (Eds.), Advances in small millets (pp. 247–254). New Delhi: Oxford and IBH.

    Google Scholar 

  4. Africa Rice Center. (2007). Africa rice trends. http://www.warda.org/publications.

  5. Singh, B. N., Jones, M. P., Fomba, S. N., Sere, Y., Sy, A. A., Akator, K., et al. (2000). Breeding for blast resistance in lowland rice in West Africa. In D. Tharreau, M.-H. Lebrun, N. J. Talbot, & J.-L. Notteghem (Eds.), Advances in rice blast research (pp. 112–128). Netherlands: Kluwer Academic.

    Google Scholar 

  6. Levy, M., Romao, J., Marchetti, M. A., & Hamer, J. E. (1991). DNA fingerprinting with a dispersed repeated sequence resolves pathotype diversity in the rice blast fungus. Plant Cell, 3, 95–102.

    Article  CAS  Google Scholar 

  7. Chen, D., Zeigler, R. S., Leung, H., & Nelson, R. J. (1995). Population structure of Pyricularia grisea at two screening sites in the Philippines. Phytopathology, 85, 1011–1020.

    Article  Google Scholar 

  8. Roumen, E., Levy, M., & Notteghem, J. L. (1997). Characterisation of the European pathogen population of Magnaporthe grisea by DNA finger printing and pathotype analysis. European Journal of Plant Pathology, 103, 363–371.

    Article  CAS  Google Scholar 

  9. Correa-Victoria, F. J., Escobar, F., Prado, G., & Aricapa, G. (2000). Population dynamics of the rice blast pathogen in a screening site in Colombia and characterization of resistance. In D. Tharreau, M.-H. Lebrun, N. J. Talbot, & J.-L. Notteghem (Eds.), Advances in rice blast research (pp. 214–220). Netherlands: Kluwer Academic.

    Google Scholar 

  10. Zeigler, R. S., & Correa-Victoria, F. J. (2000). Applying Magnaporthe grisea population analyses for durable rice blast resistance. APSnet feature: Pathogen population genetics and breeding for disease resistance. http://www.apsnet.org/online/feature/.

  11. Viji, G., Gnanamanickam, S. S., & Levy, M. (2000). DNA polymorphisms of isolates of Magnaporthe grisea from India that are pathogenic to finger millet and rice. Mycological Research, 104, 161–167.

    Article  CAS  Google Scholar 

  12. Farman, M. L., & Kim, Y.-S. (2005). Telomere hypervariability in Magnaporthe oryzae. Molecular Plant Pathology, 6, 287–298.

    Article  CAS  Google Scholar 

  13. Couch, B. C., & Kohn, L. M. (2002). A multilocus gene genealogy concordant with host preferences indicates segregation of a new species, Magnaporthe oryzae, from Magnaporthe grisea. Mycologia, 94, 683–693.

    Article  CAS  Google Scholar 

  14. Valent, B., Farall, L., & Chumley, F. G. (1991). Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics, 127, 87–101.

    CAS  Google Scholar 

  15. Kang, S., Chumley, G. F., & Valent, B. (1994). Isolation of mating-type genes of the phytopathogenic fungus Magnaporthe grisea using genomic subtraction. Genetics, 138, 289–296.

    CAS  Google Scholar 

  16. Talhinhas, P., Sreenivasaprasad, S., Neves-Martins, J., & Oliveira, M. H. (2002). Genetic and morphological characterisation of Colletotrichum acutatum causing anthracnose of Lupinus species. Phytopathology, 92, 986–996.

    Article  Google Scholar 

  17. Itoi, S., Mishima, T., Arase, S., & Nozu, M. (1983). Mating behaviour of Japanese isolates of Pyricularia oryzae. Phytopathology, 73, 155–158.

    Article  Google Scholar 

  18. Kumar, J., Nelson, R. J., & Zeigler, R. S. (1999). Population structure and dynamics of Magnaporthe grisea in the Indian Himalayas. Genetics, 152, 971–984.

    CAS  Google Scholar 

  19. Notteghem, J. L., & Silué, D. (1992). Distribution of the mating type alleles in Magnaporthe grisea populations pathogenic on rice. Phytopathology, 82, 421–424.

    Article  Google Scholar 

  20. Ling, K. C., & Ou, S. H. (1969). Standardization of the international race numbers of Pyricularia oryzae. Phytopathology, 59, 339–342.

    Google Scholar 

  21. National Research Council. (1996). Finger millet. In Lost crops in Africa, Vol. 1: Grains (pp. 39–58). National Research Council: Board on Science and Technology for International Development.

  22. Oryokot, J. O. E. (2001). Finger millet (Eleusine coracana (L.) Gaertn). In J. K. Mukiibi (Ed.), Agriculture in Uganda. Crops, Vol. II (pp. 29–41). Uganda: Fountain Publishers/CTA/NARO.

    Google Scholar 

  23. Nangoti, N., Kayobyo, G., & Rees, D. J. (2004). Seed demand and supply in eastern and northern Uganda—implications for government and non-government interventions. Uganda Journal of Agricultural Sciences, 9, 778–784.

    Google Scholar 

  24. Dobinson, K. F., Harris, R. E., & Hamer, J. E. (1993). Grasshopper, a long terminal repeat (LTR) retroelement in the phytopathogenic fungus Magnaporthe grisea. Molecular Plant-Microbe Interactions, 6, 114–126.

    Article  CAS  Google Scholar 

  25. Tanaka, M., Nakayashiki, H., Tosa, Y., & Mayama, S. (2007). The course of evolution of Magnaporthe oryzae Eleusine pathotype inferred from phylogenetic trees and structures of the flanking region of avirulence gene PWL1. Asilomar-fungal genetics conference, California, USA, 20–25 March 2007.

  26. Mekwatanakarn, P., Kositratana, W., Levy, M., & Zeigler, R. S. (2000). Pathotype and avirulence gene diversity of Pyricularia grisea in Thailand as determined by rice lines near-isogenic for major resistance genes. Plant Disease, 84, 60–70.

    Article  Google Scholar 

  27. Correll, J. C., Harp, T. L., Guerber, J. C., Zeigler, R. S., Liu, B., Cartwright, R. D., et al. (2000). Characterisation of Pyricularia grisea in the United States using independent genetic and molecular markers. Phytopathology, 90, 1396–1404.

    Article  CAS  Google Scholar 

  28. Don, L. D., Kusaba, M., Urashima, A. S., Tosa, Y., Nakayashiki, H., & Mayama, S. (1999). Population structure of the rice blast pathogen in Japan examined by DNA fingerprinting. Annals of the Phytopathological Society of Japan, 65, 15–24.

    Article  Google Scholar 

  29. Park, S.-Y., Milgroom, M. G., Han, S.-S., Kang, S., & Lee, Y.-H. (2003). Diversity of pathotypes and DNA fingerprint haplotypes in populations of Magnaporthe grisea in Korea over two decades. Phytopathology, 93, 1378–1385.

    Article  CAS  Google Scholar 

  30. Viji, G., & Gnanamanickam, S. S. (1998). Mating type distribution and fertility status of Magnaporthe grisea populations from various hosts in India. Plant Disease, 82, 36–40.

    Article  Google Scholar 

  31. Mekwatanakarn, P., Kositratana, W., Phromraksa, T., & Zeigler, R. S. (1999). Sexually fertile Magnaporthe grisea rice pathogens in Thailand. Plant Disease, 83, 939–943.

    Article  Google Scholar 

  32. Dayakar, B. V., Narayanan, N. N., & Gnanamanickam, S. S. (2000). Cross compatibility and distribution of mating type alleles of the rice blast fungus Magnaporthe grisea in India. Plant Disease, 84, 700–704.

    Article  Google Scholar 

  33. Viji, G., & Uddin, W. (2002). Distribution of mating type alleles and fertility status of Magnaporthe grisea causing gray leaf spot of perennial ryegrass and St. Augustine grass turf. Plant Disease, 84, 877–884.

    Google Scholar 

  34. Tredway, L. P., Stevenson, K. L., & Burpee, L. L. (2005). Genetic structure of Magnaporthe grisea population associated with St. Augustine grass and tall fescue in Georgia. Phytopathology, 95, 463–471.

    Article  CAS  Google Scholar 

  35. Leslie, J. F., & Klein, K. K. (1996). Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics, 144, 557–567.

    CAS  Google Scholar 

  36. Paoletti, M., Rydholm, C., Schwier, E. U., Anderson, M. J., Szakacs, G., Lutzoni, F., et al. (2005). Evidence for sexuality in the opportunistic fungal pathogen Aspergillus fumigatus. Current Biology, 15, 1242–1248.

    Article  CAS  Google Scholar 

  37. Pande, S., Mukuru, S. Z., King, S. B., & Karunakar, R. I. (1995). Biology of, and resistance to finger millet blast in Kenya and Uganda. In S. Z. Mukuru & S. B. King (Eds.), Proceedings of the eighth EARSAM regional workshop on sorghum and millets, 30 Oct–5 Nov 1992, Sudan (pp. 83–92). Andhra Pradesh: ICRISAT.

  38. Takan, J. P. (2007). A study on the genetic diversity, sexuality and pathogenicity of the finger millet blast pathogen Magnaporthe grisea populations in two East African countries. PhD thesis (pp. 315). UK: University of Exeter.

  39. Somasekhara, Y. M., Viswanath, S., & Anilkumar, T. B. (1991). Evaluation of finger millet [Eleusine coracana (L) Gaertn] cultivars for their reactions to blast (Pyricularia grisea Sacc). Tropical Agriculture, 68, 231–234.

    Google Scholar 

  40. Shetty, S. H., Gopinath, A., & Rajashekar, K. (1985). Relationship of seed-borne inoculum of Pyricularia grisea to incidence of blast of finger millet in the field. Indian Phytopathology, 38, 154–156.

    Google Scholar 

  41. Borromeo, E. S., Nelson, R. J., Bonman, J. M., & Leung, H. (1993). Genetic differentiation among isolates of Pyricularia infecting rice and weed hosts. Phytopathology, 83, 393–399.

    Article  CAS  Google Scholar 

  42. Gnanamanickam, S. S., Lavanya, B., Priyadarsini, V. B., Dayakar, B. V., Leenakumari, D., Sivaraj, R., et al. (2000). Lineage-exclusion resistance breeding: Pyramiding of blast resistance genes for management of rice blast in India. In D. Tharreau, M.-H. Lebrun, N. J. Talbot, & J.-L. Notteghem (Eds.), Advances in rice blast research (pp. 172–179). Netherlands: Kluwer Academic.

    Google Scholar 

  43. Dean, R. A., Talbot, N. J., Ebbole, D. J., Farman, M. L., Mitchell, T. K., Orbach, M. J., et al. (2005). The genome sequence of rice blast fungus Magnaporthe grisea. Nature, 434, 980–986.

    Article  CAS  Google Scholar 

  44. Couch, B. C., Fudal, I., Lebrun, M.-H., Tharreau, D., Valent, B., Kim, P.-V., et al. (2005). Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice. Genetics, 170, 613–630.

    Article  CAS  Google Scholar 

  45. Parlevliet, J. E. (1988). Identification and evaluation of quantitative resistance. In K. L. Leonard & W. E. Fry (Eds.), Plant disease epidemiology. Genetics, resistance, and management (pp. 215–247). New York: McGraw Hill.

    Google Scholar 

  46. Oduori, C. O. A. (2005). The importance and research status of finger millet in Africa. McKnight Foundation Collaborative Crop Research Program workshop on Tef and finger millet: Comparative genomics of the Chloridoid cereal (pp. 12). Biosciences for East and Central Africa (BECA), ILRI, 28–30 June 2005, Nairobi, Kenya.

  47. Talbot, N. J. (2002). Molecular variability studies of Magnaporthe grisea and application in disease control. In F. Kempken (Ed.), The Mycota XI Agricultural applications (pp. 153–169). Berlin: Springer-Verlag.

    Google Scholar 

  48. Zhu, Y., Chen, H., Fan, J., Wang, Y., Li, Y., Chen, J., et al. (2000). Genetic diversity and disease control in rice. Nature, 406, 718–722.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This publication is an output from research projects funded by the United Kingdom Department for International Development (DFID) for the benefit of developing countries. The views expressed are not necessarily those of DFID. Projects R7552, R6738, R8030 and R8445 co-ordinated by S. Sreenivasaprasad supported the PhD programmes of J.P. Takan and J. Chipili. The authors are grateful to M.A. Mgonja, N.M. Wanyera, A. Mead, and colleagues from the ARC-WARDA and ICRISAT national networks for their help with various components of the projects and to Dr. J. Hamer and Dr. S. Kang for providing the M. oryzae reference strain and mating type sequences, respectively. The authors would like to thank F.M. Kimmins, A. Ward, J.M. Lennè and T. Chancellor for their support in the implementation of the projects.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Sreenivasaprasad.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1530 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takan, J.P., Chipili, J., Muthumeenakshi, S. et al. Magnaporthe oryzae Populations Adapted to Finger Millet and Rice Exhibit Distinctive Patterns of Genetic Diversity, Sexuality and Host Interaction. Mol Biotechnol 50, 145–158 (2012). https://doi.org/10.1007/s12033-011-9429-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-011-9429-z

Keywords

Navigation