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In vitro toxicity of alternative oxidase inhibitors salicylhydroxamic acid and propyl gallate on Fusicladium effusum

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Abstract

Pecan scab, caused by the fungus Fusicladium effusum (syn. Cladosporium caryigenum and Fusicladosporium effusum), is the most devastating disease of the commercial pecan (Carya illinoinensis) production in Southeastern United States. Disease control depends primarily on multiple applications of fungicides per season. Fungicides available for scab control include those in the quinone outside inhibitor (QoI) group. QoI fungicides have a high level of resistance risk and in vitro sensitivity assays are essential to monitor development of resistance in populations of F. effusum. In vitro assays were conducted to determine sensitivity of F. effusum to the QoI fungicide azoxystrobin. In vitro assays were conducted with and without the addition of salicylhydroxamic acid (SHAM) to inhibit alternative oxidase (AOX) and eliminate the rescue impact of AOX on fungal respiration in the presence of QoI fungicides. When 0.653 mM SHAM was added to the medium, growth of a majority of the isolates was significantly reduced, even in the absence of fungicide. Of the 89 isolates tested, only 21 showed a dose response to azoxystrobin. Growth of the other 68 isolates was insufficient to measure a dose response. Only 18 isolates showed a clear dose response to azoxystrobin both with and without SHAM, but the calculated EC50 values were significantly different (P < 0.0001). Further experiments were performed to investigate the effects of different concentrations of SHAM and another AOX inhibitor, propyl gallate (PG) on hyphal growth derived from mycelial fragments of F. effusum in liquid medium in microtiter plates and hyphal growth derived from germinated conidia on solid medium in the absence of fungicide. Even at the lowest concentrations tested, both SHAM and PG (0.01 and 0.25 mM, respectively) inhibited hyphal growth of F. effusum in liquid medium and on solid medium. These results suggest the role of AOX and possible auxiliary toxicity of these inhibitors in F. effusum physiology. Due to the toxic effects of these AOX inhibitors on F. effusum in vitro, future sensitivity profiling for QoIs will be performed without the addition of these inhibitors.

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References

  • Avila-Adame C, Köller W (2003) Impact of alternative respiration and target-site mutations on responses of germinating conidia of Magnaporthe grisea to Qo-inhibiting fungicides. Pest Manag Sci 59:303–309

    Article  CAS  PubMed  Google Scholar 

  • Avila-Adame C, Olaya G, Köller W (2003) Characterization of Colletotrichum graminicola isolates resistant to strobilurin-related QoI fungicides. Plant Dis 87:1426–1432

    Article  CAS  Google Scholar 

  • Baek HS, Rho HS, Yoo JW, Ahn SM, Lee JY, Lee J, Kim M, Kim DH, Chang IS (2008) The inhibitory effect of new hydroxamic acid derivatives on melanogenesis. Bull Korean Chem Soc 29:43–46

    Article  CAS  Google Scholar 

  • Beck A, Ritschel AK, Schubert K, Braun U, Triebel D (2005) Phylogenetic relationships of the anamorphic genus Fusicladium s. lat. as inferred by ITS nrDNA data. Mycol Prog 4:111–116

    Article  Google Scholar 

  • Braun U, Crous PW, Dugan F, Groenewald JZ, de Hoog GS (2003) Phylogeny and taxonomy of Cladosporium-like hyphomycetes, including Davidiella gen. nov., the teleomorph of Cladosporium s. str. Mycol Prog 2:3–18

    Article  Google Scholar 

  • Cancro R (2000) Sensitivity of Cladosporium caryigenum isolates to kresoxim-methyl. Dissertation, University of Georgia

  • Cancro R, Stevenson KL (2000) Comparison of in vivo and in vitro assays for sensitivity of Cladosporium caryigenum to kresoxim-methyl. Phytopathology 90:S11

    Google Scholar 

  • Faure D, Bouillant M, Bally R (1995) Comparative study of substrates and inhibitors of Azospirillum ipoferum and Pyricularia oryzae laccases. Appl Environ Microbiol 61:1144–1146

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gottwald TR (1985) Influence of temperature, leaf wetness period, leaf age, and spore concentration on infection of pecan leaves by conidia of Cladosporium caryigenum. Phytopathology 75:190–194

    Article  Google Scholar 

  • Herms S, Seehuas K, Koehle H, Conrath U (2002) A strobilurin fungicide enhances the resistance of tobacco against Tobacco Mosaic Virus and Pseudomonas syringae pv tabaci. Plant Physiol 130:120–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsiao K, Bornman CH (1993) Salicylhydroxamic acid mimics esterase-like action. J Exp Bot 44:1847–1849

    Article  CAS  Google Scholar 

  • Ishii H, Fountaine J, Chung W, Kansako M, Nishimura K, Takahashi K, Oshima M (2009) Characterisation of QoI-resistant field isolates of Botrytis cinerea from citrus and strawberry. Pest Manag Sci 65:916–922

    Article  CAS  PubMed  Google Scholar 

  • Jones S, Pethybridge S, Hay F, Groom T, Wilson C (2007) Baseline sensitivity of Australian Phoma ligulicola isolates from pyrethrum to azoxystrobin and difenoconazole. J Phytopathol 155:377–380

    Article  CAS  Google Scholar 

  • Kameko I, Ishii H (2009) Effect of azoxystrobin on activities of antioxidant enzymes and alternative oxidase in wheat head blight pathogens Fusarium graminearum and Microdochium nivale. J Gen Plant Pathol 75:388–398

    Article  Google Scholar 

  • Kim Y, Dixon EW, Vincelli P, Farman ML (2003) Field resistance to strobilurin (QoI) fungicides in Pyricularia grisea caused by mutations in the mitochondrial cytochrome b gene. Phytopathology 93:891–900

    Article  CAS  PubMed  Google Scholar 

  • Köhle H, Grossmann K, Jabs T, Gerhard M, Kaiser W, Glaab J, Conrath U, Seehaus K, Herms S (2002) Physiological effects of the strobilurin fungicide F 500 on plants. In: Dehne HW, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds III. Agro Concept GmbH, Bonn, pp 61–74

    Google Scholar 

  • Köller W, Parker DM, Turechek WW, Avila-Adame C, Cronshaw K (2004) A two phase resistance response of Venturia inaequalis populations to the QoI fungicides kresoxim-methyl and trifloxystrobin. Plant Dis 88:534–544

    Article  Google Scholar 

  • Malandrakis AA, Markoglou AN, Nikou DC, Vontas JG, Ziogas BN (2006) Biological and molecular characterization of laboratory mutants of Cercospora beticola resistant to Qo inhibitors. Eur J Plant Pathol 116:155–166

    Article  Google Scholar 

  • Markoglou AN, Malandrakis AA, Vitoratos AG, Ziogas BN (2006) Characterization of laboratory mutants of Botrytis cinerea resistant to QoI fungicides. Eur J Plant Pathol 115:149–162

    Article  CAS  Google Scholar 

  • Nason MA, Farrar J, Bartlett D (2007) Strobilurin fungicides induce changes in photosynthetic gas exchange that do not improve water use efficiency of plants grown under conditions of water stress. Pest Manag Sci 63:1191–1200

    Article  CAS  PubMed  Google Scholar 

  • Pasche JS, Wharam CM, Gudmestad NC (2004) Shift in sensitivity of Alternaria solani in response to QoI fungicides. Plant Dis 88:181–187

    Article  CAS  Google Scholar 

  • Schubert K, Braun U (2002) Fusicladium effusum. In: IMI descriptions of fungi and bacteria, CAB International, Surrey, p 1514

  • Schubert K, Ritschel A, Braun U (2003) A monograph of Fusicladium s. lat. (hyphomycetes). Schlechtendalia 9:1–132

    Google Scholar 

  • Seyran M, Nischwitz C, Lewis KJ, Gitaitis RD, Brenneman TB, Stevenson KL (2009) Phylogeny of the pecan scab fungus Fusicladium effusum G. Winter based on cytochrome b gene sequence. Mycol Progress. doi:10.1007/s11557-009-0638-9

  • Steinfeld U, Sierotzki H, Parisi S, Poirey S, Gisi U (2001) Sensitivity of mitocondrial respiration to different inhibitors in Venturia inaequalis. Pest Manag Sci 57:787–796

    Article  CAS  PubMed  Google Scholar 

  • Stevenson KL (1999) Fungicide resistance management in pecans. In: The pecan industry: current situation and future challenges, third national pecan workshop proceedings, USDA-ARS, pp 1–6

  • Tsukamoto K, Itakura H, Sato K, Fukuyama K, Miura S, Takahashi S, Ikezawa H, Hosoya T (1999) Binding of salicylhydroxamic acid and several aromatic donor molecules to Arthromyces ramosus peroxidase, investigated by x-ray crystallography, optical difference spectroscopy, NMR relaxation, molecular dynamics, and kinetics. Biochemistry 38:12558–12568

    Article  CAS  PubMed  Google Scholar 

  • Turechek WW, Stevenson KL (1998) Effects of host resistance, temperature, leaf wetness, and leaf age on infection and lesion development of pecan scab. Phytopathology 88:1294–1301

    Article  CAS  PubMed  Google Scholar 

  • Walker A, Auclair C, Gredt M, Leroux P (2009) First occurrence of resistance to strobilurin fungicides in Microdochium nivale and Microdochium majus from French naturally infected wheat grains. Pest Manag Sci 65:906–915

    Article  CAS  PubMed  Google Scholar 

  • Wood PM, Hollomon DW (2003) Review a critical evaluation of the role of alternative oxidase in the performance of strobilurin and related fungicides acting at the Qo site of Complex III. Pest Manag Sci 59:499–511

    Article  CAS  PubMed  Google Scholar 

  • Ypema HL, Gold RE (1999) Kresoxim-methyl modification of a naturally occuring compound to produce a new fungicide. Plant Dis 83:4–19

    Article  CAS  Google Scholar 

  • Ziogas BN, Baldwin BC, Young JE (1997) Alternative respiration: a biochemical mechanism of resistance to azoxystrobin (ICIA 5504) in Septoria tritici. Pestic Sci 50:28–34

    Article  CAS  Google Scholar 

  • Ziogas BN, Markoglou AN, Tzima A (2002) A non-Mendelian inheritance of resistance to strobilurin fungicides in Ustilago maydis. Pest Manag Sci 58:908–916

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We acknowledge Bonnie Evans and Andrew Moore for technical assistance, and Sidney Law and Tim Varnadore for assistance in locating orchards for sampling. Financial support provided by E. I. Du Pont de Nemours and Company, Inc., United Phosphorus Inc., and the Georgia Agricultural Commodity Commission for Pecans is also appreciated.

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Authors and Affiliations

  1. Department of Plant Pathology, Coastal Plain Experiment Station, The University of Georgia, P.O. Box 748, Tifton, GA, 31793, USA

    Murat Seyran, Timothy B. Brenneman & Katherine L. Stevenson

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  1. Murat Seyran
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  2. Timothy B. Brenneman
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  3. Katherine L. Stevenson
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Correspondence to Katherine L. Stevenson.

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Communicated by K. J. Gorman.

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Seyran, M., Brenneman, T.B. & Stevenson, K.L. In vitro toxicity of alternative oxidase inhibitors salicylhydroxamic acid and propyl gallate on Fusicladium effusum . J Pest Sci 83, 421–427 (2010). https://doi.org/10.1007/s10340-010-0312-7

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  • DOI: https://doi.org/10.1007/s10340-010-0312-7

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