PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

doi: 10.15389/agrobiology.2019.5.875eng

UDC: 632.952:632.95.025.8

Acknowledgements:
Supported financially by Russian Scientific Foundation (project No. 18-16-00084)

 

FUNGICIDE RESISTANCE OF PLANT PATHOGENIC FUNGI AND THEIR CHEMOSENSITIZATION AS A TOOL TO INCREASE ANTI-DISEASE EFFECTS OF TRIAZOLES AND STROBILURINES (review)

L.A. Shcherbakova

All-Russian Research Institute of Phytopathology, 5, ul. Institut, pos. Bol’shie Vyazemy, Odintsovskii Region,Moscow Province, 143050 Russia, e-mail larisavniif@yahoo.com (✉ corresponding author)

ORCID:
Shcherbakova L.A. orcid.org/0000-0003-0254-379Х

Received December 14, 2018

 

The chemical method for plant protection is still the most reliable way to provide the high yield of economically significant crops and ensure its quality. In the world agriculture, at least 150 different fungicidal compounds with different mechanisms of action are now used, and the number of products developed and registered on their basis is much more. Triazoles and strobilurins belong to fungicides, which have expanded the opportunities to control causative agents of the most damaging diseases (D. Fernández-Ortuño et al., 2008). Nevertheless, multiple applications of fungicides during each new growing season are often required to achieve an effective control of fungal and oomycete pathogens. Such extensive applications of fungicides exacerbate negative impact on environment, and promote developing the resistance by these pathogens, representing the most disturbing consequence of fungicidal treatments (J.A. Lucas et al., 2015) that makes them relatively short-lived and eventually uneconomical (K.J. Brent et al., 2007; R.P. Oliver, 2014). Attempts to combat resistant forms of plant pathogenic fungi and oomycetes by increasing the dosage of fungicides and treatment numbers are futile, as they cause accumulation of more and more resistant strains in fungal populations. Therefore, control of these pathogens by minimal effective dosages of fungicides, without any decrease in the fungicidal efficacy, and search for ways to overcome the plant pathogen resistance to fungicides are dominant trends in plant protection for current sustainable agriculture. At the same time, the rejection of modern fungicides with high and medium risk of the resistance, including strobilurins and triazoles, does not seem to be practically rational, since they provide a highly effective control of a wide range of diseases and have several other advantages (A.V. Filippov et al., 2016). Chemosensitization of plant pathogens by natural compounds to increase efficacy of fungicidal treatments is an approach to solving the aforementioned problems. Chemosensitization can be accomplished by combining a commercial fungicide with a certain non- or marginally fungicidal substance at concentrations where, alone, neither compounds would be effective, while after their co-application a synergistic fungicidal effect is achieved, sometimes at a level significantly exceeding that of the fungicide dosages to which resistant strains are insensitive (B.C. Campbell et al., 2012; V.G. Dzhavakhiya et al., 2012). Since biochemical and structural targets of chemosensitizing substances differ from those targeted by fungicides, chemosensitization do not contribute to the selection of resistant pathogenic form, and reduces the toxic impact on the environment by lowering effective dosage levels of toxic fungicides. In this review, the promise of chemosensitization as an antiresistant strategy to improve efficacy of the protective fungicide effect is exemplified by experiments with several economically significant phytopathogenic fungi, which sensitivity to strobilurins and triazoles was demonstrated to enhance significantly by co-application of these fungicides with secondary plant or microbial metabolites and their synthetic analogues. In addition, the problem of the development of resistance in plant pathogenic fungi and the methods for its management are briefly described, information on the types and main mechanisms of resistance, in particular, those responsible for resistance to triazoles and strobilurins as well as data on the mechanisms of action of some chemosensitizers are presented.

Keywords: chemosensitization, plant pathogenic fungi, resistance to fungicides, triazoles, strobilurins, fungicide stress-responsive metabolic pathways, resistance overcoming.

 

REFERENCES

  1. Moore D., Robson G., Trinci A. Fungi as pathogens of plants. In: 21st Century guidebook to fungi. Cambridge University Press, Cambridge, 2000: 67-391 CrossRef
  2. Filippov A.V. Zashchita i karantin rastenii, 2012, 5: 61-88 (in Russ.).   
  3. Lucas J.A., Hawkins N.J., Fraaije B.A. The evolution of fungicide resistance. Advances in Applied Microbiology, 2015, 90: 29-92 CrossRef
  4. Oliver R.P. A reassessment of the risk of rust fungi developing resistance to fungicides. Pest. Manag. Sci.,2014, 70: 1641-1645 CrossRef
  5. Steffens J.J., Pell E.J., Tien M. Mechanisms of fungicide resistance in phytopathogenic fungi. Current Opinion in Biotechnology, 1996, 7(3): 348-355 CrossRef
  6. Brent K.J., Hollomon D.W. Fungicide resistance in crop pathogens: how can it be managed? Fungicide Resistance Action Committee, Brussels, 2007.
  7. Deising H.B., Reimann S., Pascholati S.F. Mechanisms and significance of fungicide resistance. Brazilian Journal of Microbiology, 2008, 39: 286-295 CrossRef
  8. Campbell B.C., Chan K.L., Kim J.H. Chemosensitization as a means to augment commercial antifungal agents. Frontiers in Microbiology, 2012, 3: 79 CrossRef
  9. Mundaca-Shah C., Ogawa V.A., Nicholson A. The global momentum to counter antimicrobial resistance. In: Combating antimicrobial resistance: a one health approach to a global threat: Proceedings of a Workshop. National Academies of Sciences, Engineering, and Medicine, The National Academies Press, Washington, DC, 2017: 5-12 CrossRef
  10. FRAC Code List ©*2019. Available https://www.frac.info/docs/default-source/pub-lications/frac-code-list/frac-code-list-2019.pdf. No date.
  11. Fernández-Ortuño D., Torés J.A., de Vicente A., Pérez-García A. Mechanisms of resistance to QoI fungicides in phytopathogenic fungi. International Microbiology, 2008, 11: 1-9 CrossRef
  12. Ma Z., Michailides T.J. Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes inphytopathogenic fungi. Crop Protection, 2005, 24: 853-863 CrossRef
  13. Shkel' T.V., Vasilevskaya A.V., Gilep A.A., Chernovetskii M.A., Luk'yanenko I.G., Usanov S.A. Trudy Belorusskogo gosudarstvennogo universiteta, 2013, 8(1): 152-158 (in Russ.).   
  14. Balba H. Review of strobilurin fungicide chemicals. Journal of Environmental Science and Health, Part B, 2007, 42: 441-451 CrossRef
  15. Brent K.J. Historical perspectives of fungicide resistance.In: Fungicide resistance in crop protection: risk and management. T.S. Thind (ed.). CABI, Wallingford, UK, 2012: 3-20 CrossRef
  16. Russell P.E. Fungicide Resistance Action Committee (FRAC). Outlooks on Pest Management, 2006, 17(2): 90-92 CrossRef
  17. Walker A.-S., Auclair C., Gredt M., Leroux P. First occurrence of resistance to strobilurin fungicides in Microdochium nivale and Microdochium majus from French naturally infected wheat grains. Pest Manag. Sci., 2009, 65(8): 906-915 CrossRef
  18. Bardas G.A., Veloukas T., Koutita O., Karaoglanidis G.S. Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups. Pest Manag. Sci.,2010, 66(9): 967-973 CrossRef
  19. Takagaki M., Kaku K., Watanabe S., Kawai K., Shimizu T., Sawada H., Kumakura K., Nagayama K. Mechanism of resistance to carpropamid in Magnaporthe grisea. Pest Manag. Sci., 2004, 60(9): 921-926 CrossRef
  20. Hauslanden H., Adolf B., Leiminger J. Evidence of strobilurine resistant isolates of A. solani and A. alternata in Germany. PPO-Special Report, 2015, 17:  93-100.
  21. Cheval P., Siah A., Bomble M., Popper A.D., Reignault P., Halama P. Evolution of QoI resistance of the wheat pathogen Zymoseptoria tritici in Northern France. Crop Protection, 2017, 92: 131-133 CrossRef
  22. Edin E., Andersson B. The early blight situation in Sweden — species abundance and strobilurin sensitivity. PPO-Special Report, 2014, 16: 83-84.
  23. Davidse L.C., Looijen D., Turkensteen L.J., Wal D. Occurrence of metalaxyl-resistant strains of Phytophthora infestans in Dutch potato fields.Netherlands Journal of Plant Pathology, 1981, 87(2): 65-68 CrossRef   
  24. Taylor R.J., Salas B., Secor G.A., Rivera V., Gudmestad N.C. Sensitivity of North American isolates of Phytophthora erythroseptica and Pythium ultimum to mefenoxam (metalaxyl). Plant Disease, 2002, 86(7): 797-802 CrossRef 
  25. Gisi U., Sierotzki H., Cook A., McCaffery A. Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Manag. Sci., 2002,58(9): 859-867 CrossRef
  26. Bartlett D.W., Clough J.M., Godwin J.R., Hall A.A., Hamer M., Parr-Dobrzanski B. The strobilurin fungicides. Pest Manag. Sci., 2002,58(7): 649-662 CrossRef
  27. Mavroeidi V.I., Shaw M.W. Sensitivity distributions and cross-resistance patterns of Mycosphaerella graminicola to fluquinconazole, prochloraz and azoxystrobin over a period of 9 years. Crop Protection, 2005, 24(3): 259-266 CrossRef
  28. Hobbelen P.H.F., Paveley N.D., Fraaije B.A., Lucas J.A., van den Bosch F. Derivation and testing of a model to predict selection for fungicide resistance. Plant Pathology, 2011, 60(2): 304-313 CrossRef
  29. Filippov A.V., Kuznetsova M.A., Rogozhin A.N. Kartofel' i ovoshchi, 2016, 4: 26-28 (in Russ.).   
  30. Zwiers L.H., Stergiopoulos I., Gielkens M.M., Goodall S.D., de Waard M.A. ABC transporters of the wheat pathogen Mycosphaerella graminicola function as protectants against biotic and xenobiotic toxic compounds. Mol. Gen. Genomics, 2003, 269: 499-507 CrossRef
  31. de Waard M.A., Andrade A.C., Hayashi K., Schoonbeek H., Stergiopoulos I., Zwiers L.-H. Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Manag. Sci., 2006, 62(3): 195-207 CrossRef
  32. Hayashi K., Schoonbeek H.J., de Waard M.A. Bcmfs1, a novel major facilitator superfamily transporter from Botrytis cinerea, provides tolerance towards the natural toxic compounds camptothecin and cercosporin and towards fungicides. Applied and Environmental Microbiology, 2002, 68: 4996-5004 CrossRef
  33. Schnabel G., Jones A.L. The 14a-demethylase (CYP51A1) gene is overexpressed in Venturia inaequalis strains resistant to myclobutanil. Phytopathology, 2001, 91: 102-110 CrossRef
  34. Steinfeld U., Sierotzki H., Parisi S., Poirey S., Gisi U. Sensitivity of mitochondrial respiration to different inhibitors in Venturia inaequalis. Pest Manag. Sci., 2001, 57(9): 787-796 CrossRef
  35. Miguez M., Reeve C., Wood P.M., Hollomon D.W. Alternative oxidase reduces the sensitivity of Mycospherella graminicola to QOI fungicides. Pest Manag. Sci., 2004, 60(1): 3-7 CrossRef
  36. Limpert E. Frequencies of virulence and fungicide resistance in the European barley mildew population in 1985. Journal of Phytopathology, 2008, 119(4): 298-311 CrossRef
  37. Leroux P., Walker A.-S. Multiple mechanisms account for resistance to sterol 14a-de-methylation inhibitors in field isolates of Mycosphaerella graminicola. Pest Manag. Sci.,2011, 67(1): 44-59 CrossRef
  38. Pasche J.S., Wharam C.M., Gudmestad N.C. Shift in sensitivity of Alternaria solani in response to QoI fungicides. Plant Disease, 2004, 88(2): 181-187 CrossRef
  39. Peters R.D., Drake K.A., Gudmestad N.C., Pasche J.S., Shinners-Carnelley T. First report of reduced sensitivity to a QoI fungicide in isolates of Alternaria solani causing early blight of potato in Canada. Plant Disease, 2008, 92(12): 1707-1707 CrossRef
  40. Edin E., Liljeroth E., Andersson B. Long term field sampling in Sweden reveals a shift in occurrence of cytochrome b genotype and amino acid substitution F129L in Alternaria solani, together with a high incidence of the G143A substitution in Alternaria alternata. Eur. J. Plant Pathol., 2019, 155: 1-15 CrossRef
  41. Price C.L., Parker J.E., Warrilow A.G.S., Kelly D.E., Kelly S.L. Azole fungicides — understanding resistance mechanisms in agricultural fungal pathogens. Pest Manag. Sci., 2015, 71(8): 1054-1058 CrossRef
  42. Torriani S.F.F., Frey R., Buitrago C., Wullschleger J., Waldner M., Kuehn R., Scalliet G., Sierotzki H. Succinate-dehydrogenase inhibitor (SDHI) resistance evolution in plant pathogens. In: Modern fungicides and antifungal compounds, Vol. VIII.  H.B. Deising,  B. Fraaije, A. Mehl, E.C. Oerke, H. Sierotzki, G. Stammler (eds.). Deutsche Phytomedizinische Gesellschaft, Braunschweig, 2017: 89-94.
  43. Sierotzki H., Wullschleger J., Gisi U. Point mutation in sytochrome b gene conferring resistance to strobilurin fungicides in Erysiphe graminis f. sp. tritici field isolates. Pesticide Biochemistry and Physiology, 2000, 68: 107-112 CrossRef
  44. Frey R., Lindenberger N., Brunner P.C., Torriani S.F.F. The evolution of Zymoseptoria tritici sensitivity to triazole fungicides. Abstracts of 19th Int. RHB Symposium on Modern Fungicides and Antifungal Compounds. Friedrichroda, 2019: 88.
  45. Chen C., Wang J., Luo Q., Yuan S., Zhou M. Characterization and fitness of carbendazim-resistant strains of Fusarium graminearum (wheat scab). Pest Manag. Sci., 2007, 63(12): 1201-1207 CrossRef
  46. Pasche J.S., Piche L.M., Gudmestad N.C. Effect of the F129L mutation in Alternaria solani on fungicides affecting mitochondrial respiration. Plant Disease, 2005, 89(3): 269-278 CrossRef
  47. Adolf B., Leiminger J., Hausladen H. The F129L mutation of the cytochrome b gene in German A. solani isolates and its impact on their sensitivity towards QoI fungicides. PPO-Special Report, 2014, 16: 195-196.
  48. Leiminger J.H., Adolf B., Hausladen H. Occurrence of the F129L mutation in Alternaria solani populations in Germany in response to QoI application, and its effect on sensitivity. Plant Pathology, 2014, 63(3): 640-650 CrossRef
  49. Jung G., Sang H., Hulvey J., Chang T., Popko J. Multidrug resistance conferred by xenobiotic detoxification in the ascomycete fungus Sclerotinia. In: Modern fungicides and antifungal compounds, Vol. VIII. H.B. Deising, B. Fraaije, A. Mehl, E.C. Oerke, H. Sierotzki, G. Stammler (eds.). Deutsche Phytomedizinische Gesellschaft, Braunschweig, 2017: 101-106.
  50. Marzani A., Swarbrick P., Rossall S. Correlation of the F129L mutation in Pyrenophora teres, the pathogen of net blotch of barley, with the efficacy of QoI fungicides. IOSR Journal of Agriculture and Veterinary Science, 2013, 3(4): 66-72 CrossRef
  51. Eisermann I., Gottschling D., Kemen E., Karlovsky P., Deising H.B., Wirsel S.G.R. A single amino acid exchange in the novel transcription factor Azr1 governs azole tolerance of Fusarium graminearum. Abstracts of 19th Int. RHB Symposium on Modern Fungicides and Antifungal Compounds. Friedrichroda, 2019: 99.
  52. Proactive Fungicide Resistance Avoidance. Pesticide Environmental Stewardship. Available https://pesticidestewardship.org/resistance/fungicide-resistance/proactive-fungicide-resistance-avoidance/. Accessed 27.09.2019.
  53. Dowley L.J., Griffin D., O’Sullivan E. Two decades of monitoring Irish populations of Phytophthora infestans for phenylamide resistance. Potato Research, 2002, 45: 79-84 CrossRef
  54. Cooke L.R., Little G. Potato late blight control with fluazinam and the current status of phenylamide resistance in Northern Ireland. PPO-Special Report, 2006, 11: 175-184.
  55. Beckerman J.L., Sundin G.W., Rosenberger D.A. Do some IPM concepts contribute to the development of fungicide resistance? Lessons learned from the apple scab pathosystem in the United States. Pest Manag. Sci., 2014, 71(3): 331-342 CrossRef
  56. Battistini G., Ciriani A., Cavina F., Prodi A., Collina M. Strobilurin sensitivity of Zymoseptoria tritici Italian strains.In: Modern fungicides and antifungal compounds, Vol. VIII. H.B. Deising,  B. Fraaije, A. Mehl, E.C. Oerke, H. Sierotzki, G. Stammler (eds.). Deutsche Phytomedizinische Gesellschaft, Braunschweig, 2017: 263-264.
  57. Jørgensen L.N., Matzen N., Semaskiene R., Korbas M., Danielewicz J., Glazek M., Maumene C., Rodemann B., Weigand S., Hess M., Blake J., Clark B., Kildea S., Bataille C., Ban R. Azoles have different strengths and perform diversely across Europe.In: Modern fungicides and antifungal compounds, Vol. VIII. H.B. Deising,  B. Fraaije, A. Mehl, E.C. Oerke, H. Sierotzki, G. Stammler (eds.). Deutsche Phytomedizinische Gesellschaft, Braunschweig, 2017: 129-134.
  58. Hemaiswarya S., Kruthiventi A.K., Doble M. Synergism between natural products and antibiotics against infectious diseases. Phytomedicine, 2008, 15(8): 639-652 CrossRef
  59. Shabbits J.A., Hu Y., Mayer L.D. Tumor chemosensitization strategies based on apoptosis manipulations. Molecular Cancer Therapeutics, 2003,2(8): 805-813.
  60. Wagner H., Ulrich-Merzenich G. Synergy research: Approaching a new generation of phytopharmaceuticals. Phytomedicine, 2009,16(2-3): 97-110 CrossRef
  61. Dzhavakhiya V., Shcherbakova L., Semina Y., Zhemchuzhina N., Campbell B. Chemosensitization of plant pathogenic fungi to agricultural fungicides. Frontiers in Microbiology, 2012, 3: 87 CrossRef
  62. Kim K., Lee Y., Ha A., Kim J.-I., Park A.R., Yu N.H., Son H., Choi G.J., Park H.W., Lee C.W., Lee T., Lee Y.-W., Kim J.-C. Chemosensitization of Fusarium graminearum to chemical fungicides using cyclic lipopeptides produced by Bacillus amyloliquefaciens strain JCK-12. Frontiers in Plant Science, 2017, 8: 2010 CrossRef
  63. Wink M. Evolutionary advantage and molecular modes of action of multicomponent mixtures used in phytomedicine. Current Drug Metabolism, 2008,9(1)0: 996-1009 CrossRef
  64. Kim J.H., Mahoney N., Chan K., Molyneux R.J., May G.S., Campbell B.C. Chemosensitization of fungal pathogens to antimicrobial agents using benzo analogs. FEMS Microbiology Letters, 2008, 281(1): 64-72 CrossRef
  65. Dzhavakhiya V.G., Voinova T.M., Statsyuk N.V., Shcherbakova L.A. Sensitization of plant pathogenic fungi to the tebuconazole-based commercial fungicide using some analogues of natural amino acids. AIP Conference Proceedings, 2019, 2063(1): 030005 CrossRef
  66. Kim J., Campbell B., Mahoney N., Chan K., Molyneux R., May G. Chemosensitization prevents tolerance of Aspergillus fumigatus to antimycotic drugs. Biochemical and Biophysical Research Communications, 2008, 372(1): 266-271 CrossRef
  67. Bang K.H., Lee D.W., Park H.M., Rhee Y.H. Inhibition of fungal cell wall synthesizing enzymes by trans-cinnamaldehyde. Bioscience, Biotechnology, and Biochemistry, 2000,64(5): 1061-1063 CrossRef
  68. Yen T.B., Chang S.T. Synergistic effects of cinnamaldehyde in combination with eugenol against wood decay fungi. Bioresource Technology, 2008,99(1): 232-236 CrossRef
  69. Kim J.H., Campbell B.C., Mahoney N., Chan K.L., Molyneux R.J., May G.S. Enhanced activity of strobilurin and fludioxonil by using berberine and phenolic compounds to target fungal antioxidative stress response. Letters in Applied Microbiology, 2007, 45(2): 134-141 CrossRef
  70. Kim J.H., Campbell B.C., Mahoney N., Chan K.L., Molyneux R.J., May G.S. Enhancement of fludioxonil fungicidal activity by disrupting cellular glutathione homeostasis with 2,5-dihydroxybenzoic acid. FEMS Microbiology Letters, 2007, 270(2): 284-290 CrossRef
  71. Eschenauer G., Depestel D.D., Carver P.L. Comparison of echinocandin antifungals. Therapeutics and Clinical Risk Management, 2007,3(1): 71-97 CrossRef
  72. Hsu F.L., Chang H.T., Chang S.T. Evaluation of antifungal properties of octyl gallate and its synergy with cinnamaldehyde. Bioresource Technology, 2007,98(4): 734-738   CrossRef
  73. Kim J.H., Campbell B.C., Mahoney N., Chan K.L., Molyneux R.J., Xiao C.L. Use of chemosensitization to overcome fludioxonil resistance in Penicillium expansum. Letters in Applied Microbiology, 2010, 51(2): 177-183 CrossRef
  74. Kartashov M.I., Shcherbakova L.A., Dzhavakhiya V.G. In vitro enhancement of the sensitivity to tebuconazole in Bipolaris sorokiniana, a causative agent of cereal root rots, by a microbial metabolite 6-demethylmevinolin. Abstracts of 19th Int. RHB Symposium on Modern Fungicides and Antifungal Compounds. Friedrichroda, 2019: 48.
  75. Kartashov M.I., Shcherbakova L.A., Statsyuk N.V., Dzhavakhiya V.G. So-application of difenoconazole with thymol results in suppression of a Parastagonospora nodorum mutant strain resistant to this triazole. Advances in Engineering Research, 2019, 183: 1-5.
  76. Shcherbakova L.A., Syomina Yu.V., Arslanova L.R., Nazarova T.A., Dzhavakhiya V.G. Metabolites secreted by a nonpathogenic Fusarium sambucinum inhabiting wheat rhizosphere enhance fungicidal effect of some triazoles against Parastagonospora nodorum. AIP Conference Proceedings, 2019, 2063(1): 030018 CrossRef
  77. Faria N.C.G., Kim J.H., Goncalves L., Martins M., Chan K.L., Campbell B.C. Enhanced activity of antifungal drugs using natural phenolics against yeast strains of Candida and Cryptococcus. Letters in Applied Microbiology, 2011, 52(5): 506-513 CrossRef
  78. Kim J.H., Mahoney N., Chan K.L., Campbell B.C., Haff R.P., Stanker L.H. Use of benzo analogs to enhance antimycotic activity of kresoxim methyl for control of aflatoxigenic fungal pathogens. Frontiers in Microbiology, 2014, 5: 87 CrossRef
  79. Kim J.H., Campbell B.C., Mahoney N., Chan K.L., Molyneux R.J. Chemosensitization of aflatoxigenic fungi to antimycin A and strobilurin using salicylaldehyde, a volatile natural compound targeting cellular antioxidation system. Mycopathologia, 2011, 171: 291-298 CrossRef
  80. Kim J.H., Chang P.K., Chan K.L., Faria N.C.G., Mahoney N., Kim Y.K., Martins M. de L., Campbell B.C. Enhancement of commercial antifungal agents by kojic acid. Int. J. Mol. Sci., 2012, 13(11): 13867-13880 CrossRef
  81. Kim J.H., Chan K.L. Augmenting the antifungal activity of an oxidizing agent with kojic acid: control of Penicillium strains infecting crops. Molecules,2014, 19: 18448-18464 CrossRef
  82. Dzhavakhiya V.G., Kempbel B.K., Shcherbakova L.A., Arslanova L.R., Zhemchuzhina N.S., Drozdova E.I., Semina Yu.V. Kompozitnyi preparat fungitsidnogo deistviya dlya zashchity rastenii ot patogenov, v tom chisle rezistentnykh k kommercheskim fungitsidam. GNU VNIIF Rossel'khozakademii (RF). Patent № RU 2 548 191 C1. Zayavl. 24.12.2013. Opubl. 20.04.2015. Byul. № 11 [A fungicidal composite preparation for protecting plants from pathogens, including those resistant to commercial fungicides. GNU VNIIF Russian Agricultural Academy (RF). Patent № RU 2 548 191 C1.Appl. 24.12.2013. Publ. 20.04.2015. Bul. № 11] (in Russ.).  

 

back

 


CONTENTS

 

 

Full article PDF (Rus)

Full article PDF (Eng)