DOI QR코드

DOI QR Code

Sensitivity of the Pyrenophora teres Population in Algeria to Quinone outside Inhibitors, Succinate Dehydrogenase Inhibitors and Demethylation Inhibitors

  • Lammari, Hamama-Imene (Phytopathology and Molecular Biology Laboratory, Department of Botany, National High College of Agriculture) ;
  • Rehfus, Alexandra (BASF SE, Agricultural Centre) ;
  • Stammler, Gerd (BASF SE, Agricultural Centre) ;
  • Benslimane, Hamida (Integrative Improvement of Crop Production Laboratory (Amelioration Integrative des Productions Vegetales), Department of Botany, National High College of Agriculture)
  • Received : 2019.09.15
  • Accepted : 2020.04.21
  • Published : 2020.06.01

Abstract

Net blotch of barley caused by Pyrenophora teres (Died.) Drechsler, is one of the most destructive diseases on barley in Algeria. It occurs in two forms: P. teres f. teres and P. teres f. maculata. A total of 212 isolates, obtained from 58 fields sampled in several barley growing areas, were assessed for fungicide sensitivity by target gene analysis. F129L and G137R mitochondrial cytochrome b substitution associated with quinone outside inhibitors (QoIs) resistance, and succinate dehydrogenase inhibitors (SDHIs) related mutations (B-H277, C-N75S, C-G79R, C-H134R, and C-S135R), were analyzed by pyrosequencing. In vitro sensitivity of 45 isolates, towards six fungicides belonging to three chemical groups (QoI, demethylase inhibitor, and SDHI) was tested by microtiter technique. Additionally, sensitivity towards three fungicides (azoxystrobin, fluxapyroxad, and epoxiconazole) was assessed in planta under glasshouse conditions. All tested isolates were QoI-sensitive and SDHI-sensitive, no mutation that confers resistance was identified. EC50 values showed that pyraclostrobin and azoxystrobin are the most efficient fungicides in vitro, whereas fluxapyroxad displayed the best disease inhibition in planta (81% inhibition at 1/9 of the full dose). The EC50 values recorded for each form of net blotch showed no significant difference in efficiency of QoI treatments and propiconazole on each form. However, in the case of fluxapyroxad, epoxiconazole and tebuconazole treatments, analysis showed significant differences in their efficiency. To our knowledge, this study is the first investigation related to mutations associated to QoI and SDHI fungicide resistance in Algerian P. teres population, as well as it is the first evaluation of the sensitivity of P. teres population towards these six fungicides.

Keywords

References

  1. Akhavan, A. 2017. Genetic structure, virulence and fungicide sensitivity of Pyrenophora teres f. teres and P. teres f. maculata populations from western Canada. Ph.D. thesis. University of Alberta, Alberta, Canada.
  2. Allioui, N., Siah, A., Brinis, L., Reignault, P. and Halama, P. 2016. Identification of Qol fungicide-resistant genotypes of the wheat pathogen Zymoseptoria tritici in Algeria. Phytopathol. Mediterr. 55:89-97.
  3. Angelini, R. M. D. M., Pollastro, S. and Faretra, F. 2015. Genetics of fungicide resistance. In: Fungicide resistance in plant pathogens: principles and a guide to practical management, eds. by H. Ishii and D. W. Hollomon, pp. 13-34. Springer Japan, Tokyo, Japan.
  4. Association de Coordination Technique Agricole. 2017. Index phytosanitaire. Association de Coordination Technique Agricole, Paris, France. 1060 pp.
  5. Avenot, H. F. and Michailides, T. J. 2010. Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi. Crop Prot. 29:643-651. https://doi.org/10.1016/j.cropro.2010.02.019
  6. Benbelkacem, A. 1996. Adaptation of cereal cultivars to extreme agroecologic environments of North Africa. Field Crops Res. 45:49-55. https://doi.org/10.1016/0378-4290(95)00058-5
  7. Benbelkacem, A., Benslimane, H., Arkoub, F. Z., Zouaoui, B., Boulif, M. and Aissat, A. 2002. Net blotch and leaf stripe of barley in Algeria: incidence of pathogens, pathological diver sity and resistance to Pyrenophora graminea and P. teres. In: Proceeding of the 2nd Symposium of Barley Foliar Diseases, eds. by A. H. Yahyaoui, L. Brader, A. Tekauz, H. Wallwork and B. Steffenson. ICARDA, Aleppo, Syria.
  8. Boungab, K., Belabid, L., Fortas, Z. and Bayaa, B. 2012. Pathotype diversity among Algerian isolates of Pyrenophora teres f. teres. Phytopathol. Mediterr. 51:577-586.
  9. Brent, K. J. and Hollomon, D. W. 2007. Fungicide resistance: the assessment of the risk. 2nd ed. Fungicide Resistance Action Committee, Brussels, Belgium. 53 pp.
  10. Campbell, G. F. and Crous, P. W. 2002. Fungicide sensitivity of South African net- and spot-type isolates of Pyrenophora teres to ergosterol biosynthesis inhibitors. Australas. Plant Pathol. 31:151-155. https://doi.org/10.1071/AP02005
  11. Direction de la Protection des Vegetaux et des Controles Techniques (DPVCT). 2017. Index des produits phytosanitaires a usage agricole. DPVCT, Algiers, Algeria. 230 pp. (in French).
  12. Fernandez-Ortuno, D., Tores, J. A., de Vicente, A. and Perez-Garcia, A. 2008. Mechanisms of resistance to QoI fungicides in phytopathogenic fungi. Int. Microbiol. 11:1-9.
  13. Fisher, N. and Meunier, B. 2008. Molecular basis of resistance to cytochrome bc1 inhibitors. FEMS Yeast Res. 8:183-192. https://doi.org/10.1111/j.1567-1364.2007.00328.x
  14. Food and Agriculture Organization of the United Nations. 2020. FAOSTAT. http://www.fao.org/faostat/en/#data/QC [23 April 2020].
  15. Fungicide Resistance Action Committee. 2019. QoI working group of FRAC, Minutes of the meeting All crops: December 11th, 2013 Organised by Syngenta in Frankfurt, Germany. URL http://www.frac.info/ [23 April 2020].
  16. Ghalem-Djender, Z., Boukhobza, N., Yallaoui-Yaici, N., Meziani, M., Oumedjkane, K., Mahiddine, D., Ait Ghezali, A., Chaou, L., Kaced, K. and Bouziri, S. 2016. Repartition des varietes de cereales a paille au niveau des zones-ecologiques du nord de l'Algerie et choix varietal [Distribution of straw cereal varieties in the ecological zones of northern Algeria and variety choice]. Cerealiculture 67:43-69 (in French).
  17. Grasso, V., Palermo, S., Sierotzki, H., Garibaldi, A. and Gisi, U. 2006. Cytochrome b gene structure and consequences for resistance to Qo inhibitor fungicides in plant pathogens. Pest Manag. Sci. 62:465-472. https://doi.org/10.1002/ps.1236
  18. Hales, N. 2015. Algeria: grain and feed annual. URL https://apps.fas.usda.gov/newgainapi/api/report/downloadreportbyfilename?filename=Grain%20and%20Feed%20Annual_Algiers_Algeria_4-1-2015.pdf [23 April 2020].
  19. Hobbelen, P. H., Paveley, N. D., Oliver, R. P. and van den Bosch, F. 2013. The usefulness of fungicide mixtures and alternation for delaying the selection for resistance in populations of Mycosphaerella graminicola on winter wheat: a modeling analysis. Phytopathology 103:690-707. https://doi.org/10.1094/PHYTO-06-12-0142-R
  20. Hobbelen, P. H. F., Paveley, N. D. and van den Bosch, F. 2011. Delaying selection for fungicide insensitivity by mixing fungicides at a low and high risk of resistance development: a modeling analysis. Phytopathology 101:1224-1233. https://doi.org/10.1094/PHYTO-10-10-0290
  21. Hobbelen, P. H. F., Paveley, N. D. and van den Bosch, F. 2014. The emergence of resistance to fungicides. PLoS ONE 9:e91910. https://doi.org/10.1371/journal.pone.0091910
  22. Huf, A., Rehfus, A., Lorenz, K. H., Bryson, R., Vogele, R. T. and Stammler, G. 2018. Proposal for a new nomenclature for CYP51 haplotypes in Zymoseptoria tritici and analysis of their distribution in Europe. Plant Pathol. 67:1706-1712. https://doi.org/10.1111/ppa.12891
  23. Lamb, D., Kelly, D. and Kelly, S. 1991. Molecular aspects of azole antifungal action and resistance. Drug Resist. Updat. 2:390-402. https://doi.org/10.1054/drup.1999.0112
  24. Lammari, H.-I., Rehfus, A., Stammler, G., Fellahi, Z. E. A., Benbelkacem, A. and Benslimane, H. 2020. Occurrence and frequency of spot form and net form of net blotch disease of barley in Algeria. J. Plant Dis. Prot. 127:35-42. https://doi.org/10.1007/s41348-019-00278-w
  25. Liu, Z., Ellwood, S. R., Oliver, R. P. and Friesen, T. L. 2011. Pyrenophora teres: profile of an increasingly damaging barley pathogen. Mol. Plant Pathol. 12:1-19. https://doi.org/10.1111/j.1364-3703.2010.00649.x
  26. Lopez-Ruiz, F. J., Perez-Garcia, A., Fernandez-Ortuno, D., Romero, D., Garcia, E., de Vicente, A., Brown, J. K. M. and Tores, J. A. 2010. Sensitivities to DMI fungicides in populations of Podosphaera fusca in south central Spain. Pest Manag. Sci. 66:801-808. https://doi.org/10.1002/ps.1948
  27. MacQueen, J. 1967. Some methods for classification and analysis of multivariate observations. In: Proceedings of the 5th Berkeley Symposium on Mathematical Statistics and Probability, eds. by L. Le Cam and J. Neyman, pp. 281-297. University of California Press, Berkeley, CA, USA.
  28. Mair, W. J., Deng, W., Mullins, J. G. L., West, S., Wang, P., Besharat, N., Ellwood, S. R., Oliver, R. P. and Lopez-Ruiz, F. J. 2016a. Demethylase inhibitor fungicide resistance in Pyrenophora teres f. sp. teres associated with target site modification and inducible overexpression of Cyp51. Front. Microbiol. 7:1279.
  29. Mair, W., Lopez-Ruiz, F., Stammler, G., Clark, W., Burnett, F., Hollomon, D., Ishii, H., Thind, T. S., Brown, J. K. M., Fraaije, B., Cools, H., Shaw, M., Fillinger, S., Walker, A.-S., Mellado, E., Schnabel, G., Mehl, A. and Oliver, R. P. 2016b. Proposal, for a unified nomenclaturefor target-site mutations associated withresistance to fungicides. Pest Manag. Sci. 72:1449-1459. https://doi.org/10.1002/ps.4301
  30. Marzani, Q. A., Swarbrick, P. and Rossall, S. 2013. Correlation of the F129L mutation in Pyrenophora teres, the pathogen of net blotch of barley, with the efficacy of QoI fungicides. IOSR J. Agric. Vet. Sci. 3:66-72. https://doi.org/10.9790/2380-0346672
  31. McDonald, B. A. and Linde, C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349-379. https://doi.org/10.1146/annurev.phyto.40.120501.101443
  32. Meamiche Neddaf, H., Aouini, L., Bouznad, Z. and Kema, G. H. J. 2017. Equal distribution of mating type alleles and the presence of strobilurin resistance in Algerian Zymoseptoria tritici field populations. Plant Dis. 101:544-549. https://doi.org/10.1094/PDIS-03-16-0298-RE
  33. Observatoire National des filieres Agricoles et Agroalimentaires. 2019. Bilan du commerce exterieur algerien des cereales, 2018 [Algerian cereals external trade balance, 2018]. Ministere de l'Agriculture, du Developpement Rural et de la Peche, Algeria. 6 pp. (in French).
  34. Peltonen, S., Jalli M., Kammiovirta, K. and Karjalainen, R. 1996. Genetic variation in Drechslera teres populations as indicated by RAPD markers. Ann. Appl. Biol. 128:465-477. https://doi.org/10.1111/j.1744-7348.1996.tb07107.x
  35. Rahal-Bouziane, H. 2015. L'orge en Algerie: passe, present et importance pour la securite alimentaire face, aux nouveaux defis [Barley in Algeria: past, present and importance for food security in the face of new challenges]. Rech. Agron. 27:7-24 (In French).
  36. Reddy, P. P. 2013. Recent advances in crop protection. Springer India, New Delhi, India. 259 pp.
  37. Reguieg, M. M., Labdi, M., Benbelkacem, A., Hamou, M., Maatougui, M. E. H., Grando, S. and Ceccarelli, S. 2013. First experience on participatory barley breeding in Algeria. J. Crop Improv. 27:469-486. https://doi.org/10.1080/15427528.2013.794756
  38. Rehfus, A. 2018. Analysis of the emerging situation of resistance to succinate dehydrogenase inhibitors in Pyrenophora teres and Zymoseptoria tritici in Europe. Ph.D. thesis. University of Hohenheim, Stuttgart, Germany.
  39. Rehfus, A., Matusinsky, P., Strobel, D., Bryson, R. and Stammler, G. 2019. Mutations in target genes of succinate dehydrogenase inhibitors and demethylation inhibitors in Ramularia collo-cygni in Europe. J. Plant Dis. Prot. 126:447-459. https://doi.org/10.1007/s41348-019-00246-4
  40. Rehfus, A., Miessner, S., Achenbach, J., Strobel, D., Bryson, R. and Stammler, G. 2016. Emergence of succinate dehydrogenase inhibitor resistance of Pyrenophora teres in Europe. Pest Manag. Sci. 72:1977-1988. https://doi.org/10.1002/ps.4244
  41. Russell, P. E. 2002. Sensitivity baselines in fungicide resistance research and management. FRAC Monograph, no. 3. Crop Life International, Brussels, Belgium. 56 pp.
  42. Sayoud, R., Ezzahiri, B. and Bouznad, Z. 1999. Les maladies des cereales et des legumineuses alimentaires au Maghreb [Diseases of cereals and pulses in the Maghreb]. ITGC, Alger, Algeria. 64 pp. (in French).
  43. Semar, M., Strobel, D., Koch, A., Klappach, K. and Stammler, G. 2007. Field efficacy of pyraclostrobin against populations of Pyrenophora teres containing the F129L mutation in the cytochrome b gene. J. Plant Dis. Prot. 114:117-119. https://doi.org/10.1007/BF03356718
  44. Sierotzki, H., Frey, R., Wullschleger, J., Palermo, S., Karlin, S., Godwin, J. and Gisi, U. 2007. Cytochrome b gene sequence and structure of Pyrenophora teres and P. tritici-repentis and implications for QoI resistance. Pest Manag. Sci. 63:225-233. https://doi.org/10.1002/ps.1330
  45. Speakman, J. B. and Pommer, E.-H. 1986. A simple method for producing large volumes of Pyrenophora teres spore suspension. Bull. Br. Mycol. Soc. 20:129-130. https://doi.org/10.1016/s0007-1528(86)80041-4
  46. Srivastava, K. D. and Tewari A. K. 2002. Fungal disease of wheat and barley: foliar diseases. In: Disease of field crops, eds. by V. K. Gupta and Y. S. Paul, pp. 58-78. Indus Publishing Company, New Delhi, India.
  47. Steinhauer, D., Salat, M., Frey, R., Mosbach, A., Luksch, T., Balmer, D., Hansen, R., Widdison, S., Logan, G., Dietrich, R. A., Kema, G. H. J., Bieri, S., Sierotzki, H., Torriani, S. F. F. and Scalliet, G. 2019. A dispensable paralog of succinate dehydrogenase subunit C mediates standing resistance towards a subclass of SDHI fungicides in Zymoseptoria tritici. PLoS Pathog. 15:e1007780. https://doi.org/10.1371/journal.ppat.1007780
  48. Stepanovic, M., Rekanovic, E., Milijasevic-Marcic, S., Potocnik, I., Todorovic, B. and Stepanovic, J. 2016. Field efficacy of different fungicide mixtures in control of net blotch on barley. Pestic. Phytomed. 31:51-57. https://doi.org/10.2298/PIF1602051S
  49. Tucker, M., Lopez-Ruiz, F., Jayasena, K. and Oliver, R. 2015. Origin of fungicide-resistant barley powdery mildew in Western Australia: lessons to be learned. In: Fungicide resistance in plant pathogens: principles and a guide to practical management, eds. by H. Ishii and D. W. Hollomon, pp. 329-340. Springer Japan, Tokyo, Japan.
  50. Tuffery, S. 2012. Data mining et statistique decisionnelle: l'intelligence des donnees [Data mining and decision statistics: data intelligence]. Editions Technip, Paris, France. 826 pp.
  51. van den Berg, F., van den Bosch, F. and Paveley, N. D. 2013. Optimal fungicide application timings for disease control are also an effective anti-resistance strategy: a case study for Zymoseptoria tritici (Mycosphaerella graminicola) on wheat. Phytopathology 103:1209-1219. https://doi.org/10.1094/PHYTO-03-13-0061-R
  52. Van den Bosch, F., Paveley, N., van den Berg, F., Hobbelen, P. and Oliver, R. 2014. Mixtures as a fungicide resistance management tactic. Phytopathology 104:1264-1273. https://doi.org/10.1094/PHYTO-04-14-0121-RVW
  53. Weibull, J., Walther, U., Sato, K., Habekuss, A., Kopahnke, D. and Proeseler, G. 2003. Diversity in resistance to biotic stresses. In: Developments in plant genetics and breeding, vol. 7. Diversity in barley (Hordeum vulgare), eds. by R. von Bothmer, T. van Hintum, H. Knupffer, and K. Sato, pp. 143-178. Elsevier Science, Amsterdam, The Netherlands.
  54. Yamashita, M. and Fraaije, B. 2018. Non-target site SDHI resistance is present as standing genetic variation in field populations of Zymoseptoria tritici. Pest Manag. Sci. 74:672-681. https://doi.org/10.1002/ps.4761