The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Genetic Variation and Biological Control of Fusarium graminearum Isolated from Wheat in Assiut-Egypt

  • Mahmoud, Amer F. (Department of Plant Pathology, Faculty of Agriculture, Assiut University)
  • Received : 2015.09.22
  • Accepted : 2015.11.30
  • Published : 2016.04.01
Download PDF
⟨ Previous Next ⟩

Abstract

Fusarium graminearum Schwabe causes Fusarium head blight (FHB), a devastating disease that leads to extensive yield and quality loss of wheat and other cereal crops. Twelve isolates of F. graminearum were collected from naturally infected spikes of wheat from Assiut Egypt. These isolates were compared using SRAP. The results indicated distinct genetic groups exist within F. graminearum, and demonstrated that these groups have different biological properties, especially with respect to their pathogenicity on wheat. There were biologically significant differences between the groups; with group (B) isolates being more aggressive towards wheat than groups (A) and (C). Furthermore, Trichoderma harzianum (Rifai) and Bacillus subtilis (Ehrenberg) which isolated from wheat kernels were screened for antagonistic activity against F. graminearum. They significantly reduced the growth of F. graminearum colonies in culture. In order to gain insight into biological control effect in situ, highly antagonistic isolates of T. harzianum and B. subtilis were selected, based on their in vitro effectiveness, for greenhouse test. It was revealed that T. harzianum and B. subtilis significantly reduced FHB severity. The obtained results indicated that T. harzianum and B. subtilis are very effective biocontrol agents that offer potential benefit in FHB and should be harnessed for further biocontrol applications. The accurate analysis of genetic variation and studies of population structures have significant implications for understanding the genetic traits and disease control programs in wheat. This is the first known report of the distribution and genetic variation of F. graminearum on wheat spikes in Assiut Egypt.

Keywords

References

  1. Agarry, O. O., Akinyosoye, F. A. and Adetuyi, F. C. 2005. Antagonistic property of microorganisms associated with cassava (Manihot esculenta Crantz). Afr. J. Biotechnol. 4:627-663. https://doi.org/10.5897/AJB2005.000-3114
  2. Akinsanmi, O. A., Backhouse, D., Simpfendorfer, S. and Chakraborty, S. 2006. Genetic diversity of Australian Fusarium graminearum and F. pseudograminearum. Plant Pathol. 55:494-504. https://doi.org/10.1111/j.1365-3059.2006.01398.x
  3. Alexander, N. J., Hohn, T. M. and McCormick, S. P. 1998. The TRI11 gene of Fusarium sporotrichioides encodes a cytochrome P-450 monooxygenase required for C-15 hydroxylation in trichothecene biosynthesis. Appl. Environ. Microbiol. 64:221-225.
  4. Asak, O. and Shoda, M. 1996. Biocontrol of Rhizoctonia solani causing damping-off disease of tomato with Bacillus subtilis. Appl. Environ. Microbiol. 62:4081-4085.
  5. Bacon, C. W., Yates, I. E., Hinton, D. M. and Meredith, F. 2001. Biological control of Fusarium moniliforme in maize. Environmental Health Perspectives 109:325-332. https://doi.org/10.1289/ehp.01109s2325
  6. Bai, G. H. and Shaner, G. E. 1996. Variation in Fusarium graminearum and cultivar resistance to wheat scab. Plant Dis. 80:975-979. https://doi.org/10.1094/PD-80-0975
  7. Baysal, O., Siragusa, M., Ikten, H., Polat, I., Gumrukcu, E., Yigit, F., Carimi, F. and Teixeira da Silva, J. A. 2009. Fusarium oxysporum f. sp. lycopersici races and their genetic discrimination by molecular markers in West Mediterranean region of Turkey. Physiol. Mol. Plant Pathol. 74:68-75. https://doi.org/10.1016/j.pmpp.2009.09.008
  8. Bell, D. K., Wells, H. D. and Markham, C. R. 1982. In vitro antagonism of Trichoderma species against six fungal plant pathogens. Phytopathology 72:379-382. https://doi.org/10.1094/Phyto-72-379
  9. Benitez, T., Rincon, A. M., Limon, M. C. and Codon, A. C. 2004. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 7:249-260.
  10. Bergey's Manual of Determinative Systematic Bacteriology. 2001. Buchanan R. E. and N. E. Gibbon eds (2nd). The William and Wilkins Co. Baltimore.
  11. Budak, H., Shearman, R. C., Parmaksiz, I. and Dweikat, I. 2004b. Comparative analysis of seeded and vegetative biotype Buffalograsses based on phylogenetic relationships using ISSRs, SSRs, RAPDs, and SRAPs. Theor. Appl. Genet. 109:280-288.
  12. Budak, H., Shearman, R. C., Parmaksiz, I., Gaussoin, R. E., Riordan, T. P. and Dweikat, I. 2004c. Molecular characterization of Buffalograss germplasm using sequence related amplified polymorphism markers. Theor. Appl. Genet. 108:328-334. https://doi.org/10.1007/s00122-003-1428-4
  13. Budak, H., Shearman, R. C., Gaussoin, R. E. and Dweikat, I. 2004a. Application of sequence-related amplified polymorphism markers for characterization of Turfgrass species. HortScience 39:955-958.
  14. Carter, J. P., Razanoor, H. N., Desjardins, A. E. and Nicholson, P. 2000. Variation in Fusarium graminearum isolates from Nepal associated with their host of origin. Plant Pathol. 49: 1-10. https://doi.org/10.1046/j.1365-3059.2000.00440.x
  15. Carter, J. P., Rezanoor, H. N., Holden, D., Desjardins, A. E., Plattner, R. D. and Nicholson, P. 2002. Variation in pathogenicity associated with the genetic diversity of Fusarium graminearum. Eur. J. Plant Pathol. 108:573-583. https://doi.org/10.1023/A:1019921203161
  16. Cavaglieri, L., Orlando, J., Rodriguez, M. I., Chulze, S. and Etcheverry, M. 2005. Biocontrol of Bacillus subtilis against Fusarium verticillioides in vitro and at the maize root level. Res. Microbiol. 156:748-754. https://doi.org/10.1016/j.resmic.2005.03.001
  17. Chan, Y. K., McCormick, W. A. and Seifert, K. A. 2003. Characterization of an antifungal soil bacterium and its antagonistic activities against Fusarium species. Can. J. Microbiol. 49:253-262. https://doi.org/10.1139/w03-033
  18. Chet, I., Inbar, J. and Hadar, I. 1997. Fungal antagonists and mycoparasites. In: The Mycota IV: Environmental and microbial relationships. eds. by Wicklow, D.T. and Soderstrom, B., pp 165-184. Springer-Verlag, Berlin.
  19. Cohen-Kupiec, R. and Chet, I. 1998. The molecular biology of chitin digestion. Current Opinion in Biotechnol. 9:270-277. https://doi.org/10.1016/S0958-1669(98)80058-X
  20. Crane, J., Gibson, D., Vaughan, R. and Bergstrom, G. 2013. Iturin levels on wheat spikes linked to biological control of Fusarium head blight by Bacillus amyloliquefaciens. Phytopathology 103:146-155. https://doi.org/10.1094/PHYTO-07-12-0154-R
  21. Cumagun, C. J. R. and Miedaner, T. 2003. Aggressiveness of 42 isolates of Gibberella zeae (Fusarium graminearum) in wheat under field and greenhouse conditions. J. Plant Dis. Protec. 110:554-559.
  22. Dana, M. M., Limon, M. C., Mejias, R., Mach, R. L., Benitez, T., Pintor-Toro, J. A. and Kubicek, C. P. 2001. Regulation of chitinase 33 (chit33) gene expression in Trichoderma harzianum. Curr. Gene. 38:335-342. https://doi.org/10.1007/s002940000169
  23. Desjardins, A. E. and Hohn, T. M. 1997. Mycotoxins in plant pathogenesis. Mol. Plant-Microbe Interact. 10:147-152. https://doi.org/10.1094/MPMI.1997.10.2.147
  24. Desjardins, A. E., Hohn, T. M. and McCormick, S. P. 1993. Trichothecene biosynthesis in Fusarium species: chemistry, genetics, and significance. Microbiol. Mol. Biol. Rev. 157:595-604.
  25. Desjardins, A. E., Busman, M., Manandhar, G., Jarosz, A. M., Manandhar, H. K. and Proctor, R. H. 2008. Gibberella ear rot of maize (Zea mays) in Nepal: distribution of the mycotoxins nivalenol and deoxynivalenol in naturally and experimentally infected maize. J. Agr. Food Chem. 56:5428-5436. DOI: 10.1021/jf8003702.
  26. Dhingra, O. D. and Sinclair, J. B. 1995. Basic plant pathology methods. second edition, Lewis Publishers, CRC Press, USA, 400-450.
  27. Dinler, G. and Budak, H. 2008. Analysis of expressed sequence tags (ESTs) from Agrostis species obtained using sequence related amplified polymorphism. Biochem. Genet. 46:663-676. https://doi.org/10.1007/s10528-008-9181-7
  28. Dinolfo, M. I., Castanares, E. and Stenglein, S. A. 2015. SRAP as an informative molecular marker to study the Fusarium poae genetic variability. J. Phytopathol. 163:657-663. DOI:10.1111/jph.12301.
  29. Domsch, K. H., Gams, W. and Anderson, T. H. 1980. Compondium of soil fungi. Academic Press. A Subbsidiary of Harcout Brace Jovanovich, Bublishers, London, 1:859 pp.
  30. Elad, Y., Freeman, S. and Monte, E. 2000. Biocontrol agents: In: Mode of action and interaction with other means of control. IOBC wprs Bulletin, Vol 24. Sevilla, Espana.
  31. Estevez de Jensen, C., Percich, J. A. and Graham, P. H. 2002. Integrated management strategies of bean root rot with Bacillus subtilis and Rhizobium in Minnesota, Field Crops Research, 74:107-115. https://doi.org/10.1016/S0378-4290(01)00200-3
  32. Fernando, W. G. D., Zhang, J. X., Dusabenyagasani, M., Guo, X. W., Ahmed, H. and McCallum, B. 2006. Genetic diversity of Gibberella zeae isolates from Manitoba. Plant Dis. 90:1337-1342. https://doi.org/10.1094/PD-90-1337
  33. Gomez, K. A. and Gomez, A. A. 1984. Statistical procedures for agricultural research, 2nd Ed. John Willey. New York, 680 pp.
  34. Goswami, R. S. and Kistler, H. C. 2004. Heading for disaster: Fusarium graminearum on cereal crops. Mol. Plant Pathol. 5:515-525. https://doi.org/10.1111/j.1364-3703.2004.00252.x
  35. Harman, G. E., Howell, C. R., Viterbo, A., Chet, I. and Lorito, M. 2004. Trichoderma species-opportunistic, avirulent plant symbionts. Nat. Reviews Microbiol. 2:43-56. https://doi.org/10.1038/nrmicro797
  36. Howell, C. R. 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis. 87:4-10. https://doi.org/10.1094/PDIS.2003.87.1.4
  37. Ilgen, P., Hadeler, B., Maier, F. J. and Schäfer, W. 2009. Developing kernel and rachis node induce the trichothecene pathway of Fusarium graminearum during wheat head infection. Mol. Plant-Microbe Interact. 22:899-908. https://doi.org/10.1094/MPMI-22-8-0899
  38. Jaccard, P. 1908. Nouvelles rescherches sur la distribution florale. Bulletin de la Societe vaudoise des sciences naturelles 44: 223-270.
  39. Jansen, C., von Wettstein, D., Schafer, W., Kogel, K. H., Felk, A., Maier, F. J. 2005. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc. Natl. Acad. Sci. USA 102:16892-16897. https://doi.org/10.1073/pnas.0508467102
  40. Jochum, C., Osborne, L. and Yuen, G. 2006. Fusarium head blight biological control with Lysobacter enzymogenes strain C3. Biol. Contr. 39:336-344. https://doi.org/10.1016/j.biocontrol.2006.05.004
  41. Khan, N. I., Schisler, D. A., Boehm, M. J., Slininger, P. J. and Bothast, R. J. 2001. Selection and evaluation of microorganisms for biocontrol of Fusarium head blight of wheat incited by Gibberella zeae. Plant Dis. 85:1253-1258. https://doi.org/10.1094/PDIS.2001.85.12.1253
  42. Kimura, M., Kaneko, I., Komiyama, M., Takatsuki, A., Koshino, H., Yoneyama, K. and Yamaguchi, I. 1998. Trichothecene 3-O-acetyltransferase protects both the producing organism and transformed yeast from related mycotoxins. Cloning and characterization of Tri101. J. Biol. Chem. 273:1654-1661. https://doi.org/10.1074/jbc.273.3.1654
  43. Latge, J. P. 2007. The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 66:279-290. https://doi.org/10.1111/j.1365-2958.2007.05872.x
  44. Li, G. and Quiros, C. F. 2001. Sequence-related amplified polymorphism (SRAP), a new marker system based on a simple PCR reaction: its application to mapping and gene tagging in Brassica. Theor. Appl. Genet. 103:455-461. https://doi.org/10.1007/s001220100570
  45. Mahmoud, A. F. and Abo-Elyousr, K. 2014. Genetic diversity and biological control of Rhizoctonia solani associated with root rot of soybean in Assiut governorate, Egypt. J. Plant Physiol. Pathol. 2:1-5.
  46. Manning, B., Southwell, R., Hayman, P. and Moore, K. 2000. 'Fusarium head blight in northern NSW.' NSW Agriculture Research Update, AgDex 110/637.
  47. McMullen, M. P., Jones, R. and Gallenberg, D. 1997. Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis. 81:1340-1348. https://doi.org/10.1094/PDIS.1997.81.12.1340
  48. Melo, I. S. 1998. Agents microbianos de space control de fungus fitopatogenicos. In: Control biologico, eds. by Melo, I.S. and Azevedo, J.L., Jagua Riuna V.1. Brazil: EMBRAPA; p. 17-30.
  49. Mert-Turk, F., Gencer, R. and Kahriman, F. 2014. Chemotyping of the Fusarium graminearum isolates and variation in aggressiveness against wheat heads. J. Animal and Plant Sci. 24:1858-1862.
  50. Mesterhazy, A. 2002. Role of deoxynivalenol in aggressiveness of Fusarium graminearum and F. culmorum and in resistance to Fusarium head blight. Eur. J. Plant Pathol. 108:675-684. https://doi.org/10.1023/A:1020631114063
  51. Meyer, L., Wehner, F. C., Nel, L. H. and Carling, D. E. 1998. Characterization of the crater disease strain of Rhizoctonia solani. Phytopathology 88:366-371. https://doi.org/10.1094/PHYTO.1998.88.4.366
  52. Miedaner, T., Bolduan, C. and Melchinger, A. 2010. Aggressiveness and mycotoxin production of eight isolates each of Fusarium graminearum and Fusarium verticillioides for ear rot on susceptible and resistant early maize inbred lines. Eur. J. Plant Pathol. 127:113-123. https://doi.org/10.1007/s10658-009-9576-2
  53. Miedaner, T., Reinbrecht, C. and Schilling, A. G. 2000. Association among aggressiveness, fungal colonization, and mycotoxin production of 26 isolates of Fusarium graminearum in winter rye head blight. J. Plant Dis. Protec. 107:124-134.
  54. Monte, E. 2001. Understanding Trichoderma: between biotechnology and microbial ecology. Int. Microbiol. 4:1-4.
  55. Mullenborn, C., Steiner, U. and Oerke, E. C. 2007. Disease control with Bacillus brevis: update and future prospects. Proceeding of the 15th International Symposium on Modern Fungicides and Antifungal Compounds, May 6-10, Ramada Treff Hotel, Friendrichroda, Germany.
  56. Mutlu, N., Boyaci, F. H., Gocmen, M. and Abak, K. 2008. Development of SRAP, SRAP-RGA, RAPD and SCAR markers linked with a Fusarium wilt resistance gene in eggplant. Theor. Appl. Genet. 117:1303-1312. https://doi.org/10.1007/s00122-008-0864-6
  57. Nelson, P. E., Toussoun, T. A. and Marasas, W. F. O. 1983. Fusarium species: An illustrated manual for identification. Pennsylvania State University Press, pp 193.
  58. Nirenberg, H. 1981. A simplified method for identifying Fusarium spp. occurring on wheat. Can. J. Botany 59:1599-1609. https://doi.org/10.1139/b81-217
  59. O'Donnell, K., Cigelnik, E., Weber, N. S. and Trappe, J. M. 1997. Phylogenetic relationships among ascomycetous truffles and the true and false morels inferred from 18S and 28S ribosomal DNA sequence analysis. Mycologia 89:48-65. https://doi.org/10.2307/3761172
  60. O'Donnell, K., Kistler, H. C., Tacke, B. K. and Casper, H. H. 2000. Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc. Natl. Acad. Sci. USA 97:7905-7910. https://doi.org/10.1073/pnas.130193297
  61. Perello, A., Simon, M. R. and Arambarri, A. M. 2002. Interactions between foliar pathogens and the saprophytic microflora of the wheat (Triticum aestivum L.) phylloplane. J. Phytopathol. 150:232-243. https://doi.org/10.1046/j.1439-0434.2002.00747.x
  62. Pestka, J. J. and Smolinski, A. T. 2005. Deoxynivalenol: toxicology and potential effects on humans. Journal of Toxicology and Environmental Health Part B: Critical Reviews 8:39-69. https://doi.org/10.1080/10937400590889458
  63. Proctor, R. H., Hohn, T. M. and McCormick, S. P. 1995. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol. Plant-Microbe Interact. 8:593-601. https://doi.org/10.1094/MPMI-8-0593
  64. Rohlf, F. J. 2000. NTSYS-PC: Numerical taxonomy and multivariate analysis system. Version 2.1. New York: Applied Biostatistics.
  65. Schunmacher, R., Stopacher, N., Reithner, B., Omann, M., Zeillinger, S. and Krska, R. 2007. Peptaibol profiles in cultures of Trichoderma atroviride: Detection and characterization by LC-MS/MS. Poceedings of the 15th International Symposium on Modern Fungicides and Antifungal Compounds, May 6-10, Ramada Treff Hotel, Friendrichroda, Germany.
  66. Skinner, F. A. and Lovelock, D. W. 1979. Identification methods for microbiologist (2nd. Ed.). The Soc. For Appl. Bacterial. Technical Series Academic Press London.
  67. Sneath, P. H. A., Mair, N. S., Elisabeth Sharpe, M. and Holt, J. G. 1986. Bergey's manual of systematic bacteriology. Vol. 2. Section 13, Endospore-forming Gram-positive rods and cocci. The Williams and Wilkings Company, Baltimore Md., USA, p. 1105-1207.
  68. Snijders, C. H. A. and Perkowski, J. 1990. Effects of head blight caused by Fusarium culmorum on toxin content and weight of wheat kernels. Phytopathology 80:566-570. https://doi.org/10.1094/Phyto-80-566
  69. Stein, T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56:845-857. https://doi.org/10.1111/j.1365-2958.2005.04587.x
  70. Stockwell, C. A., Bergstrom, G. C. and da. Luz, W. C. 1999. Selection of microbial antagonists for biological control of Fusarium head blight of wheat. Pp. 82-84. Proceedings of the 1999 National Fusarium Head Blight Forum, Michigan State University, University Printing, East Lasting, MI.
  71. Suman, A., Kimbeng, C. A., Edme, S. J. and Veremis, J. 2008. Sequence-related amplified polymorphism (SRAP) markers for assessing genetic relationships and diversity in sugarcane germplasm collections. Plant Genetic Resources: Characterization and Utilization 6:222-231. https://doi.org/10.1017/S147926210899420X
  72. Summerell, B. A., Salleh, B. and Leslie, J. F. 2003. Utilitarian approach to Fusarium identification. Plant Dis. 87:117-128. https://doi.org/10.1094/PDIS.2003.87.2.117
  73. Voigt, K., Cigelnik, E. and O'donnell, K. 1999. Phylogeny and PCR identification of clinically important Zygomycetes based on nuclear ribosomal-DNA sequence data. J. Clin. Microbiol. 37:3957-3964.
  74. Hue, A. G., Voldeng, H. D., Savard, M. E., Fedak, G., Tian, X. and Hsiang, T. 2009. Biological control of Fusarium head blight of wheat with Clonostachys rosea strain ACM941. Can. J. Plant Pathol. 31:169-179. https://doi.org/10.1080/07060660909507590
  75. Zadoks, J. C., Chang, T. T. and Konzak, C. F. 1974. A decimal code for the growth stages of cereals. Weed Res. 14:415-421. https://doi.org/10.1111/j.1365-3180.1974.tb01084.x
  76. Zeller, K. A., Bowden, R. L. and Leslie, J. F. 2004. Population differentiation and recombination in wheat scab populations of Gibberella zeae from the United States. Mol. Ecol. 13:563-571. https://doi.org/10.1046/j.1365-294X.2004.02098.x

Cited by

  1. Suppression of sugar beet damping-off caused by Rhizoctonia solani using bacterial and fungal antagonists vol.49, pp.19-20, 2016, https://doi.org/10.1080/03235408.2016.1245052
  2. Screening of wheat endophytes as biological control agents against Fusarium head blight using two different in vitro tests vol.202, 2017, https://doi.org/10.1016/j.micres.2017.04.014