Advertisement

Occurrence of Fusarium head blight and Fusarium crown rot in Algerian wheat: identification of associated species and assessment of aggressiveness

  • Nora Abdallah-NekacheEmail author
  • Imane Laraba
  • Christine Ducos
  • Christian Barreau
  • Zouaoui Bouznad
  • Houda Boureghda
Article
  • 50 Downloads

Abstract

Fusarium head blight and Fusarium crown rot are two important fungal diseases of wheat worldwide. This research was carried out to study the most important species associated to these two diseases in Algeria. Symptomatic crowns and heads were collected from different wheat growing regions in Algeria. Morphological and molecular identifications showed the occurrence of six fungal species isolated from crowns for the 2 years: Fusarium culmorum (68%), F. pseudograminearum (10%), F. verticillioides (3%), F. avenaceum (2%), Microdochium majus (13%) and M. nivale (4%). Two species only, F. culmorum (94.1%) and F. pseudograminearum (5.9%), were obtained from the heads. Among the Fusarium spp., 30 isolates were chosen for the pathogenicity tests: F. culmorum isolated from symptomatic crowns (n = 10), F. culmorum isolated from blighted heads (n = 10) and F. pseudograminearum (n = 10). Pathogenicity tests were carried out by using three different methods: seed inoculation, soil inoculation and head inoculation. Results showed that F. culmorum isolates were the most aggressive on the wheat seedlings and on the head. However, F. pseudograminearum isolates were the most aggressive on the crown. High correlations were found between Fusarium isolates aggressiveness on the wheat seedlings and on the head for the two F. culmorum groups (FCC: r = 0.89 and FCH: r = 0.85). These results provide a simple in vitro test to predict pathogenicity of the F. culmorum isolates for head blight. This study highlight that F. culmorum is the dominant species associated with FHB and FCR in Algeria. Also, this is the first report concerning the identification of F. pseudograminearum, M. majus, F. verticillioides and F. avenaceum from wheat in Algeria.

Keywords

Fusarium Microdochium Wheat Aggressiveness Algeria 

Notes

Acknowledgments

Nora Abdallah-Nekache thanks the «Comité Mixte d’Evaluation et de Prospective de la cooperation scientifique franco-algérienne » CMEP PHC TASSILI for support through the « Agence Française pour la promotion et l’enseignement supérieur, l’accueil et la mobilité internationale » during the stays at MycSA laboratory, INRA Bordeaux Aquitaine, France. She also thanks Dr. Nadia Boureghda (Ecole Nationale Supérieure d’Agronomie) for the realization of the geographical map of the distribution of the species of Fusarium and Microdochium and the two diseases in the prospected provinces, and Laetitia Pinson-Gadais for reviewing the manuscript before submission.

Compliance with ethical standards

This study was supported by «Comité Mixte d’Evaluation et de Prospective de la cooperation scientifique franco-algérienne » CMEP PHC TASSILI through the « Agence Française pour la promotion et l’enseignement supérieur, l’accueil et la mobilité internationale » and «Ecole Nationale Superieure d’Agronomie», Algeirs, Algeria. The authors declare that they have no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors. For this type of study formal consent is not required. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information.

References

  1. Aguado, A., Savoie, J. M., Chereau, S., Ducos, C., Aguilar, M., Ferrer, N., Aguilar, M., Pinson-Gadais, L., & Richard-Forget, F. (2018). Priming to protect maize from Fusarium verticilliodes and its fumonisin accumulation. Journal of the Science of Food and Agriculture, 99, 64–72.  https://doi.org/10.1002/jsfa.9142. Google Scholar
  2. Agustí-Brisach, C., Raya-Ortega, M. C., Trapero, C., Roca, L. F., Luque, F., López-Moral, A., Fuentes, M., & Trapero, A. (2018). First report of Fusarium pseudograminearum causing crown rot of wheat in Europe. Disease Notes, 102, 1670.Google Scholar
  3. Akinsanmi, O. A., Mitter, V., Simpfendorfer, S., Backhouse, D., & Chakraborty, S. (2004). Identity and pathogenicity of Fusarium spp. isolated from wheat fields in Queensland and northern New South Wales. Australian Journal of Agricultural Research, 55, 97–107.Google Scholar
  4. Aoki, T., & O’Donnell, K. (1999). Morphological and molecular characterization of Fusarium pseudograminearum sp. nov., formerly recognized as the Group 1 population of F. graminearum. Mycologia, 91, 597–609.Google Scholar
  5. Backhouse, D., Abubakar, A. A., Burgess, L. W., Dennis, J. I., Hollaway, G. J., Wildermuth, G. B., Wallwork, H., & Henry, F. J. (2004). Survey of Fusarium species associated with crown rot of wheat and barley in eastern Australia. Australasian Plant Pathology, 33, 255–261.Google Scholar
  6. Balmas, V., Scherm, B., Marcello, A., Beyer, M., Hoffmann, L., Migheli, Q., & Pasquali, M. (2015). Fusarium species and chemotypes associated with Fusarium head blight and Fusarium root rot on wheat in Sardinia. Plant Pathology, 64, 972–979.Google Scholar
  7. Beccari, G., Colasante, V., Tini, F., Senatore, M. T., Prodi, A., Sulyok, M., & Covarelli, L. (2018a). Causal agents of Fusarium head blight of durum wheat (Triticum durum Desf.) in Central Italy and their in vitro biosynthesis of secondary metabolites. Food Microbiology, 70, 17–27.Google Scholar
  8. Beccari, G., Prodi, A., Pisi, A., Nipoti, P., Onofri, A., Nicholson, P., Pfohl, K., Karlovsky, P., Gardiner, D. M., & Covarelli, L. (2018b). Development of three Fusarium crown rot causal agents and systemic translocation of deoxynivalenol following stem base infection of soft wheat. Plant Pathology, 67, 1055–1065.Google Scholar
  9. Bentley, A. R., Cromey, M. G., Farrokhi-Nejad, R., Leslie, J. F., Summerell, B. A., & Burgess, L. W. (2006). Fusarium crown and root rot pathogens associated with wheat and grass stem bases on the South Island of New Zealand. Australasian Plant Pathology, 35, 495–502.Google Scholar
  10. Beyer, M., Pogoda, F., Pallez, M., Lazic, J., Hoffmann, L., & Pasquali, M. (2014). Evidence for a reversible drought induced shift in the species composition of mycotoxin producing Fusarium head blight pathogens isolated from symptomatic wheat heads. International Journal of Food Microbiology, 182-183, 51–56.Google Scholar
  11. Bottalico, A., & Perrone, G. (2002). Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. European Journal of Plant Pathology, 108, 611–624.Google Scholar
  12. Brennan, J. M., Fagan, B., van Maanen, A., Cooke, B. M., & Doohan, F. M. (2003). Studies on in vitro growth and pathogenicity of European Fusarium fungi. European Journal of Plant Pathology, 109, 577–587.Google Scholar
  13. Burgess, L. W., Wearing, A. H., & Toussoun, T. A. (1975). Surveys of the Fusaria associated with crown rot of wheat in eastern Australia. Australian Journal of Agricultural Research, 26, 791–799.Google Scholar
  14. Burgess, L. W., Klein, T. A., Bryden, W. L., & Tobin, N. F. (1987). Head blight of wheat caused by Fusarium graminearum Group I in New South Wales in 1983. Australasian Plant Pathology, 16, 72–78.Google Scholar
  15. Chakraborty, S., Liu, C. J., Mitter, V., Scott, J., Akinsanmi, O. A., Ali, S., Dill-Macky, R., Nicol, J., Backhouse, D., & Simpfendorfer, S. (2006). Pathogen population structure and epidemiology are keys to wheat crown rot and Fusarium head blight management. Australasian Plant Pathology, 35, 643–655.Google Scholar
  16. Chekali, S., Gargouri, S., Berraies, S., Nicol, M. J., & Nasraoui, B. (2013). Impact of Fusarium foot and root rot on yield of cereals in Tunisia. Tunisian Journal of Plant Protection, 8, 75–86.Google Scholar
  17. Covarelli, L., Beccari, G., Steed, A., & Nicholson, P. (2012). Colonization of soft wheat following infection of the stem base by Fusarium culmorum and translocation of deoxynivalenol to the head. Plant Pathology, 61, 1121–1129.Google Scholar
  18. Demirci, E., & Dane, E. (2003). Identification and pathogenicity of Fusarium spp. from stem bases of winter wheat in Erzurum, Turkey. Phytoparasitica, 31, 170–173.Google Scholar
  19. Dyer, A. T., Johnston, R. H., Hogg, A. C., & Johnston, J. A. (2009). Comparison of pathogenicity of the Fusarium crown rot (FCR) complex (F. culmorum, F. pseudograminearum and F.graminearum) on hard red spring and durum wheat. European Journal of Plant Pathology, 125, 387–395.Google Scholar
  20. El Yacoubi, H., Hassikou, R., Badoc, A., Rochdi, A., & Douira, A. (2012). Complexe fongique de la pourriture racinaire du blé tendre au nord-ouest du Maroc. Bulletin de la Société de Pharmacie de Bordeaux, 151, 35–48.Google Scholar
  21. Eslahi, M. R. (2012). Fungi associated with root and crown rot of wheat in Khuzestan province. Iran Journal of Crop Protection, 1, 107–113.Google Scholar
  22. Fernandez, M. R., & Jefferson, G. (2004). Fungal populations in roots and crowns of common and durum wheat in Saskatchewan. Canadian Journal of Plant Pathology, 26, 325–334.Google Scholar
  23. Grey, W. E., & Mathre, D. E. (1984). Reaction of spring barleys to common root rot and its effect on yield components. Canadian Journal of Plant Science, 64, 245–253.Google Scholar
  24. Hollaway, G. J., & Exell, G. K. (2010). Survey of wheat crops for white heads caused by crown rot in Victoria, 1997-2009. Australas. Plant Pathology, 39, 363–367.Google Scholar
  25. Hollaway, G. J., Evans, M. L., Wallwork, H., Dyson, C. B., & McKay, A. C. (2013). Yield loss in cereals, caused by Fusarium culmorum and F. pseudograminearum, is related to fungal DNA in soil prior to planting, rainfall, and cereal type. Plant Disease, 97, 977–982.Google Scholar
  26. Hoshino, T., Xiao, N., & Tkachenko, O. B. (2009). Cold adaptation in the phytopathogenic fungi causing snow molds. Mycoscience, 50, 26–38.Google Scholar
  27. Ioos, R., Belhadj, A., & Menez, M. (2004). Occurrence and distribution of Microdochium nivale and Fusarium species isolated from barley, durum and soft wheat grains in France from 2000 to 2002. Mycopathologia, 158, 351–362.Google Scholar
  28. Ji, L. J., Kong, L. X., Li, Q. S., Wang, L. S., Chen, D., & Ma, P. (2016). First report of Fusarium pseudograminearum causing Fusarium head blight of wheat in Hebei Province, China. Plant Disease, 100, 220.Google Scholar
  29. Kammoun, L. G., Gargouri, S., Hajlaoui, M. R., & Marrakchi, M. (2009). Occurrence and distribution of Microdochium and Fusarium species isolated from durum wheat in northern Tunisia and detection of mycotoxins in naturally infested grain. Journal of Phytopathology, 157, 546–551.Google Scholar
  30. Kammoun, L. G., Gargouri, S., Barreau, C., Richard-Forget, F., & Hajlaoui, M. R. (2010). Trichothecene chemotypes of Fusarium culmorum infecting wheat in Tunisia. International Journal of Food Microbiology, 140, 84–89.Google Scholar
  31. Kelly, A. C., Clear, R. M., O'Donnell, K., McCormick, S., Turkington, T. K., Tekauz, A., Gilbert, J., Kistler, H. C., Busman, M., & Ward, T. J. (2015). Diversity of Fusarium head blight populations and trichothecene toxin types reveals regional differences in pathogen composition and temporal dynamics. Fungal Genetics and Biology, 82, 22–31.Google Scholar
  32. Kezih, R., Bekhouche, F., & Merazka, A. (2014). Some traditional Algerian products from durum wheat. African Journal of Food Science, 8, 30–34.Google Scholar
  33. Kuzdraliński, A., Szczerba, H., Tofil, K., Filipiak, A., Garbarczyk, E., Dziadko, P., Muszyńska, M., & Solarska, E. (2014). Early PCR-based detection of Fusarium culmorum, F. graminearum, F. sporotrichioides and F. poae on stem bases of winter wheat throughout Poland. European Journal of Plant Pathology, 140, 491–502.Google Scholar
  34. Laraba, I., Boureghda, H., Abdallah, N., Bouaicha, O., Obanor, F., Moretti, A., Geiser, D. M., Kim, H. S., McCormick, S. P., Proctor, R. H., Kelly, A. C., Ward, T. J., & O'Donnell, K. (2017). Fungal population genetic structure and mycotoxin potential of the wheat crown rot and head blight pathogen Fusarium culmorum in Algeria. Fungal Genetics and Biology, 103, 34–41.Google Scholar
  35. Lees, A. K., Nicholson, P., Rezanoor, H. N., & Parry, D. W. (1995). Analysis of variation within Microdochium nivale from wheat: evidence for a distinct sub-group. Mycological Research, 99, 103–109.Google Scholar
  36. Leslie, J. F., & Summerell, A. B. (2006). The Fusarium laboratory manual (p. 388). Ames: Blackwell Publishing.Google Scholar
  37. Li, H. L., Yuan, H. X., Fu, B., Xing, X. P., Sun, B. J., & Tang, W. H. (2012). First report of Fusarium pseudograminearum causing crown rot of wheat in Henan China. Plant Disease, 96, 1065.Google Scholar
  38. MADRP. (2016). Ministère de l'agriculture et du développement durable et de la pêche.Google Scholar
  39. Matny, O. N., Bates, S. T., & Song, Z. (2017). Geographic distribution of Fusarium culmorum chemotypes associated with wheat crown rot in Iraq. Journal of Plant Protection Research, 57, 43–49.Google Scholar
  40. McKinney, H. H. (1923). Influence of soil temperature and moisture on infection of wheat seedlings by Helminthosporium sativum. Journal of Agricultural Research, 26, 195–217.Google Scholar
  41. Merhej, J., Boutigny, A., Pinson-Gadais, L., & Richard-Forget, F. (2010). Acidic pH as a determinant of TRI gene expression and trichothecene B biosynthesis in Fusarium graminearum. Food Additives & Contaminants. Part A, Chemistry, Analysis, Control, Exposure & Risk Assessment, 1–8.Google Scholar
  42. Mesterhazy, A. (1983). Breeding wheat for resistance to Fusarium graminearum and F. culmorum. Zeitschrift für Pflanzenzüchtung, 91, 295–311.Google Scholar
  43. Mesterhazy, A. (1984). A laboratory method to predict pathogenicity of Fusarium graminearum in field and resistance of wheat to scab. Acta Phytopathologica Academiae Scientiarum Hungaricae, 19, 205–218.Google Scholar
  44. Nedjraoui, D., & Bédrani, S. (2008). La désertification dans les steppes algériennes : causes, impacts et actions de lutte. VertigO - la revue électronique en sciences de l'environnement, 8. mis en ligne le 01 avril 2008, consulté le 06 November 2018. URL: http://journals.openedition.org/vertigo/5375.  https://doi.org/10.4000/vertigo.5375.
  45. Nicholson, P., & Parry, D. W. (1996). Development and use of a PCR assay to detect Rhizoctonia cerealis the cause of sharp eyespot in wheat. Plant Pathology, 45, 872–883.Google Scholar
  46. Nicholson, P., Lees, A. K.,Maurin, N., Parry, D. W., & Rezanoor, H. N. (1996). Development of a PCR assay to identify and quantify Microdochium nivale var. nivale and Microdochium nivale var. majus in wheat. Physiological and Molecular Plant Pathology, 48, 257–271.Google Scholar
  47. Nicholson, P., Simpson, D. R., Weston, G., Rezanoor, H. N., Lees, A. K., Parry, D. W., & Joyce, D. (1998). Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereal using PCR assays. Physiological and Molecular Plant Pathology, 53, 17–38.Google Scholar
  48. Nicholson, P., Chandler, E., Draeger, R. C., Gosman, N. E., Simpson, D. R., Thomsett, M., & Wilson, A. H. (2003). Molecular tools to study epidemiology and toxicology of Fusarium head blight of cereals. European Journal of Plant Pathology, 109, 691–703.Google Scholar
  49. Nielson, L. K., Justesen, A. F., Jensen, J. D., & Jorgersen, L. N. (2013). Microdochium nivale and Microdochium majus in seed samples of Danish small grains cereals. Crop Protection, 43, 192–200.Google Scholar
  50. Obanor, F., & Chakraborty, S. (2014). Aetiology and toxigenicity of Fusarium graminearum and F. pseudograminearum causing crown rot and head blight in Australia under natural and artificial infection. Plant Pathology, 63, 1218–1229.Google Scholar
  51. Pancaldi, D., Tonti, S., Prodi, A., Salomoni, D., Dal Prà, M., Nipoti, P., Alberti, I., & Pisi, A. (2010). Survey of the main causal agents of Fusarium head blight of durum wheat around Bologna, Northern Italy. Phytopathologia Mediterranea, 49, 258–266.Google Scholar
  52. Parry, D. W., Jenkinson, P., & McLeod, L. (1995). Fusarium ear blight in small grain cereals—a review. Plant Pathology, 44, 207–238.Google Scholar
  53. Pasquali, M., & Migheli, Q. (2014). Genetic approaches to chemotype determination in type B-trichothecene producing Fusaria. International Journal of Food Microbiology, 189, 164–182.Google Scholar
  54. Paulitz, T. C., Smiley, R. W., & Cook, R. J. (2002). Insight into the prevalence and management of soilborne cereal pathogens under direct seeding in the Pacific Northwest, U.S.A. Canadian Journal of Plant Pathology, 24, 416–428.Google Scholar
  55. Pettit, T., Xu, X., & Parry, D. (2003). Association of Fusarium species in the wheat stem rot complex. European Journal of Plant Pathology, 109, 769–774.Google Scholar
  56. Rebib, H., Bouraoui, H., Rouaissi, M., Brygoo, Y., Boudabbous, A., Hajlaoui, M. R., & Sadfi-Zouaoui, N. (2014). Genetic diversity assessed by SSR markers and chemotyping of Fusarium culmorum causal agent of foot and root rot of wheat collected from two different fields in Tunisia. European Journal of Plant Pathology, 139, 481–495.Google Scholar
  57. Saremi, H., Ammarellou, A., & Jafary, H. (2007). Incidence of crown rot disease of wheat caused by Fusarium pseudograminearum as a new new soil born fungal species in North West Iran. Pakistan Journal of Biological Sciences, 10, 3606–3612.Google Scholar
  58. Scheider, N., Guo, J. R., Verreet, J. A., & Beyer, M. (2009). Assessing the intensity of Fusarium-damage in wheat: a comparison of selected disease parameters during disease development and the role of fungicides. Journal of Plant Diseases and Protection, 116, 118–123.Google Scholar
  59. Scherm, B., Balmas, V., Spanu, F., Pani, G., Delogu, G., Pasquali, M., & Migheli, Q. (2013). Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Molecular Plant Pathology, 14, 323–341.Google Scholar
  60. Simpson, D. R., Rezanoor, H. N., Parry, D. W., & Nicholson, P. (2000). Evidence for differential host preference in Microdochium nivale var. majus and Microdochium nivale var. nivale. Plant Pathology, 49, 261–268.Google Scholar
  61. Touati-Hattab, S., Barreau, C., Verdal-Bonnin, M. N., Chereau, S., Richard-Forget, F., Hadjout, S., Mekliche, L., & Bouznad, Z. (2016). Pathogenicity and trichothecenes production of Fusarium culmorum strains causing head blight on wheat and evaluation of resistance of the varieties cultivated in Algeria. European Journal of Plant Pathology, 145, 797–814.Google Scholar
  62. Tronsmo, A. M., Hsiang, T., Okuyama, H., & Nakajima, T. (2001). Low temperature diseases caused by Microdochium nivale. In N. Iriki, D. A. Gaudet, A. M. Tronsmo, N. Matsumoto, M. Yoshida, & A. Nishimune (Eds.), Low temperature plant microbe interactions under snow (pp. 75–86). Japan: Hokkaido National Experiment Station.Google Scholar
  63. Tunali, B., Nicol, J. M., Hodson, D., Uçkun, Z., Büyük, O., Erdurmuş, D., Hekimhan, H., Aktaş, H., Akbudak, M. A., & Bağcı, S. A. (2008). Root and crown rot fungi associated with spring, facultative, and winter wheat in Turkey. Plant Disease, 92, 1299–1306.Google Scholar
  64. Turner, A. S., Lees, A. K., Rezanoor, H. N., & Nicholson, P. (1998). Refinement of PCR-detection of Fusarium avenaceum and evidence from DNA marker studies for phenetic relatedness to Fusarium tricinctum. Plant Pathology, 47, 278–288.Google Scholar
  65. Waalwijk, C., Kastelein, P., Vries, I., Kerenyi, Z., Lee, T., Hesselink, T., Kohl, J., & Kema, G. (2003). Major changes in Fusarium spp. in wheat in the Netherlands. European Journal of Plant Pathology, 109, 743–754.Google Scholar
  66. Windels, C. E. (2000). Economic and social impacts of Fusarium head blight: changing farms and rural communities in the Northern Great Plains. Phytopathology, 90, 17–21.Google Scholar
  67. Yekkour, A., Toumatia, O., Meklat, A., Verheecke, C., Sabaou, N., Zitouni, A., & Mathieu, F. (2015). Deoxynivalenol-producing ability of Fusarium culmorum strains and their impact on infecting barley in Algeria. World Journal of Microbiology and Biotechnology, 31, 875–881.Google Scholar
  68. Zadoks, J. C., Chang, T. T., & Konzak, C. F. (1974). A decimal code for the growth stages of cereals. Weed Research, 14, 415–421.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2019

Authors and Affiliations

  • Nora Abdallah-Nekache
    • 1
    Email author
  • Imane Laraba
    • 1
  • Christine Ducos
    • 2
  • Christian Barreau
    • 2
  • Zouaoui Bouznad
    • 1
  • Houda Boureghda
    • 1
  1. 1.Laboratoire de phytopathologie et de biologie moléculaire, Département de botaniqueEcole Nationale Supérieure AgronomiqueAlgiersAlgeria
  2. 2.UR1264, MycSAInstitut National de la Recherche AgronomiqueBordeauxFrance

Personalised recommendations