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Differential susceptibility to the mycoparasite Paraphaeosphaeria minitans among Sclerotinia sclerotiorum isolates

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Abstract

The mycoparasitic fungus Paraphaeosphaeria minitans (formerly Coniothyrium minitans), is increasingly used by farmers to reduce soilborne inoculum of Sclerotinia sclerotiorum. In France, its field efficacy tends to be higher in the North than in the South, leading to the hypothesis of possible regional differences in the susceptibility of the pathogen to the biocontrol agent. A standardized assay was developed and four quantitative criteria were used to assess the susceptibility to P. minitans of 75 S. sclerotiorum isolates collected from different regions of France. There was no significant difference between the group of isolates from the North and that from the South, but wide differences were observed among isolates, with consistent responses for all quantitative criteria. This study suggests that biocontrol efficacy might vary locally depending on the frequency of less susceptible isolates and it brings to attention the possibility that selection pressure could lead to a gradual increase in the frequency of less susceptible isolates, as this biocontrol method becomes widely adopted by farmers. To our knowledge, this is the first report of the variable susceptibility of S. sclerotiorum to a commercialized strain of P. minitans and the first detailed characterization of a large group of isolates from France for traits related to fitness, such as mycelial growth and production of sclerotia.

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References

  • Adams PB (1990) The potential of mycoparasites for biological control of plant diseases. Annual Review of Phytopathology 28:59–72

    Article  CAS  PubMed  Google Scholar 

  • Adams P, Ayers W (1979) Ecology of Sclerotinia species. Phytopathology 69:896–899

    Article  Google Scholar 

  • Anas O (1987) Recovery of fungi and arthropods from sclerotia of Sclerotinia sclerotiorum in Quebec muck soils. Phytopathology 77:327–331

    Article  Google Scholar 

  • Anas O, Reeleder R (1988) Consumption of sclerotia of Sclerotinia sclerotiorum by larvae of Bradysia coprophila: influence of soil factors and interactions between larvae and Trichoderma viride. Soil Biology and Biochemistry 20:619–624

    Article  Google Scholar 

  • Bardin M, Ajouz S, Comby M, Lopez-Ferber M, Graillot B, Siegwart M, Nicot PC (2015) Is the efficacy of biological control against plant diseases likely to be more durable than that of chemical pesticides? Frontiers in Plant Science 6:566

    Article  PubMed  PubMed Central  Google Scholar 

  • Bell AA, Liu L, Reidy B, Davis RM, Subbarao KV (1998) Mechanisms of subsurface drip irrigation-mediated suppression of lettuce drop caused by Sclerotinia minor. Phytopathology 88:252–259

    Article  CAS  PubMed  Google Scholar 

  • Bitsadze N, Siebold M, Koopmann B, von Tiedemann A (2015) Single and combined colonization of Sclerotinia sclerotiorum sclerotia by the fungal mycoparasites Coniothyrium minitans and Microsphaeropsis ochracea. Plant Pathology 64:690–700

    Article  CAS  Google Scholar 

  • Bolton MD, Thomma BPHJ, Nelson BD (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Molecular Plant Pathology 7:1–16

    Article  CAS  PubMed  Google Scholar 

  • Budge SP, Whipps JM (2001) Potential for integrated control of Sclerotinia sclerotiorum in glasshouse lettuce using Coniothyrium minitans and reduced fungicide application. Phytopathology 91:221–227

    Article  CAS  PubMed  Google Scholar 

  • Budge SP, McQuilken MP, Fenlon JS, Whipps JM (1995) Use of Coniothyrium minitans and Gliocladium virens for biological control of Sclerotinia sclerotiorum in glasshouse lettuce. Biological Control 5:513–522

    Article  Google Scholar 

  • Campbell W (1947) A new species of Coniothyrium parasitic on sclerotia. Mycologia 39:190–195

    Article  Google Scholar 

  • Carpenter MA, Stewart A, Ridgway HJ (2005) Identification of novel Trichoderma hamatum genes expressed during mycoparasitism using subtractive hybridisation. FEMS Microbiology Letters 251:105–112

    Article  CAS  PubMed  Google Scholar 

  • Chitrampalam P, Figuli P, Matheron M, Subbarao K, Pryor BM (2008) Biocontrol of lettuce drop caused by Sclerotinia sclerotiorum and S. minor in desert agroecosystems. Plant Disease 92:1625–1634

    Article  CAS  PubMed  Google Scholar 

  • Chitrampalam P, Cox CA, Turini TA, Pryor BM (2010) Efficacy of Coniothyrium minitans on lettuce drop caused by Sclerotinia minor in desert agroecosystem. Biological Control 55:92–96

    Article  Google Scholar 

  • Clarkson JP, Staveley J, Phelps K, Young CS, Whipps JM (2003) Ascospore release and survival in Sclerotinia sclerotiorum. Mycological Research 107:213–222

    Article  PubMed  Google Scholar 

  • Clarkson JP, Fawcett L, Anthony SG, Young C (2014) A model for Sclerotinia sclerotiorum infection and disease development in lettuce, based on the effects of temperature, relative humidity and ascospore density. PLoS One 9:e94049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coley-Smith J, Cooke R (1971) Survival and germination of fungal sclerotia. Annual Review of Phytopathology 9:65–92

    Article  Google Scholar 

  • Ćosić J, Jurković D, Vrandečić K, Kaučić D (2012) Survival of buried Sclerotinia sclerotiorum sclerotia in undisturbed soil. Helia 35:73–78

    Article  Google Scholar 

  • De Vrije T, Antoine N, Buitelaar R, Bruckner S, Dissevelt M, Durand A, Gerlagh M, Jones E, Lüth P, Oostra J (2001) The fungal biocontrol agent Coniothyrium minitans: production by solid-state fermentation, application and marketing. Applied Microbiology and Biotechnology 56:58–68

    Article  PubMed  Google Scholar 

  • Derbyshire MC, Denton-Giles M (2016) The control of sclerotinia stem rot on oilseed rape (Brassica napus): current practices and future opportunities. Plant Pathology 65:859–877

    Article  CAS  Google Scholar 

  • Duncan RW, Dilantha Fernando WG, Rashid KY (2006) Time and burial depth influencing the viability and bacterial colonization of sclerotia of Sclerotinia sclerotiorum. Soil Biology and Biochemistry 38:275–284

    Article  CAS  Google Scholar 

  • Elsheshtawi M, Elkhaky MT, Sayed SR, Bahkali AH, Mohammed AA, Gambhir D, Mansour AS, Elgorban AM (2017) Integrated control of white rot disease on beans caused by Sclerotinia sclerotiorum using Contans® and reduced fungicides application. Saudi Journal of Biological Sciences 24:405–409

    Article  CAS  PubMed  Google Scholar 

  • Gao XN, Han QM, Chen YF, Qin HQ, Huang LL, Kang ZS (2014) Biological control of oilseed rape Sclerotinia stem rot by Bacillus subtilis strain Em7. Biocontrol Science and Technology 24:39–52

    Article  Google Scholar 

  • Geraldine AM, Lopes FAC, Carvalho DDC, Barbosa ET, Rodrigues AR, Brandão RS, Ulhoa CJ, Lobo Junior M (2013) Cell wall-degrading enzymes and parasitism of sclerotia are key factors on field biocontrol of white mold by Trichoderma spp. Biological Control 67:308–316

    Article  CAS  Google Scholar 

  • Gerlagh M, Goossen-van de Geijn HM, Fokkema NJ, Vereijken PFG (1999) Long-term biosanitation by application of Coniothyrium minitans on Sclerotinia sclerotiorum-infected crops. Phytopathology 89:141–147

    Article  CAS  PubMed  Google Scholar 

  • Gracia-Garza JA, Reeleder RD, Paulitz TC (1997) Degradation of sclerotia of Sclerotinia sclerotiorum by fungus gnats (Bradysia coprophila) and the biocontrol fungi Trichoderma spp. Soil Biology and Biochemistry 29:123–129

    Article  CAS  Google Scholar 

  • Huang HC, Erickson RS (2000) Soil treatment with fungal agents for control of apothecia of Sclerotinia sclerotiorum in bean and pea crops. Plant Pathology Bulletin 9:53–58

    CAS  Google Scholar 

  • Huang Y, Xie X, Yang L, Zhang J, Li G, Jiang D (2011) Susceptibility of Sclerotinia sclerotiorum strains different in oxalate production to infection by the mycoparasite Coniothyrium minitans. World Journal of Microbiology and Biotechnology 27:2799–2805

    Article  CAS  Google Scholar 

  • Jones E, Mead A, Whipps J (2003) Evaluation of different Coniothyrium minitans inoculum sources and application rates on apothecial production and infection of Sclerotinia sclerotiorum sclerotia. Soil Biology and Biochemistry 35:409–419

    Article  CAS  Google Scholar 

  • Jones E, Mead A, Whipps J (2004) Effect of inoculum type and timing of application of Coniothyrium minitans on Sclerotinia sclerotiorum: control of sclerotinia disease in glasshouse lettuce. Plant Pathology 53:611–620

    Article  Google Scholar 

  • Jones EE, Stewart A, Whipps JM (2011) Water potential affects Coniothyrium minitans growth, germination and parasitism of Sclerotinia sclerotiorum sclerotia. Fungal Biology 115:871–881

    Article  PubMed  Google Scholar 

  • Kamal MM, Lindbeck KD, Savocchia S, Ash GJ (2015) Biological control of sclerotinia stem rot of canola using antagonistic bacteria. Plant Pathology 64:1375–1384

    Article  CAS  Google Scholar 

  • Kora C, McDonald MR, Boland GJ (2008) New progress in the integrated management of sclerotinia rot of carrot. In: Ciancio A, Mukerji KG (eds) Integrated Management of Diseases Caused by Fungi, Phytoplasma and Bacteria. Springer Netherlands, Dordrecht, pp 243–270

    Chapter  Google Scholar 

  • Lehner MS, Lima RC, Carneiro JES, Paula TJ, Vieira RF, Mizubuti ESG (2016) Similar aggressiveness of phenotypically and genotypically distinct isolates of Sclerotinia sclerotiorum. Plant Disease 100:360–366

    Article  CAS  PubMed  Google Scholar 

  • Lehner MS, Del Ponte EM, Gugino BK, Kikkert JR, Pethybridge SJ (2017) Sensitivity and efficacy of boscalid, fluazinam, and thiophanate-methyl for white mold control in snap bean in New York. Plant Disease 101:1253–1258

    Article  CAS  PubMed  Google Scholar 

  • Leyronas C, Duffaud M, Nicot PC (2012) Compared efficiency of the isolation methods for Botrytis cinerea. Mycology: An International Journal on Fungal Biology 3:221–225

    Google Scholar 

  • Leyronas C, Troulet C, Duffaud M, Villeneuve F, Benigni M, Leignez S, Nicot PC (2018) First report of Sclerotinia subarctica in France detected with a rapid PCR-based test. Canadian Journal of Plant Pathology 40:1–6

    Article  CAS  Google Scholar 

  • McCredie TA, Sivasithamparam K (1985) Fungi mycoparasitic on sclerotia of Sclerotinia sclerotiorum in some Western Australian soils. Transactions of the British Mycological Society 84:736–739

    Article  Google Scholar 

  • McLaren D, Huang H, Rimmer S (1996) Control of apothecial production of Sclerotinia sclerotiorum by Coniothyrium minitans and Talaromyces flavus. Plant Disease 80:1373–1378

    Article  Google Scholar 

  • Nicot P, Bardin M, Alabouvette C, Köhl J (2011) Potential of biological control based on published research. 1. Protection against plant pathogens of selected crops. In: Nicot P (ed) Classical and augmentative biological control against diseases and pests: critical status analysis and review of factors influencing their success. IOBC/WPRS, Zürich, pp 1–11

    Google Scholar 

  • Nicot PC, Avril F, Duffaud M, Leyronas C, Troulet C, Villeneuve F, Bardin M (2016) Are there regional differences in the susceptibility of Sclerotinia sclerotiorum strains to Coniothyrium minitans? IOBC WPRS Bulletin 117:83–87

    Google Scholar 

  • Öhberg H, Bång U (2010) Biological control of clover rot on red clover by Coniothyrium minitans under natural and controlled climatic conditions. Biocontrol Science and Technology 20:25–36

    Article  Google Scholar 

  • Partridge DE, Sutton TB, Jordan DL (2006) Effect of environmental factors and pesticides on mycoparasitism of Sclerotinia minor by Coniothyrium minitans. Plant Disease 90:1407–1412

    Article  CAS  PubMed  Google Scholar 

  • Rabeendran N, Jones EE, Moot DJ, Stewart A (2006) Biocontrol of Sclerotinia lettuce drop by Coniothyrium minitans and Trichoderma hamatum. Biological Control 39:352–362

    Article  Google Scholar 

  • Sandys-Winsch C, Whipps JM, Gerlagh M, Kruse M (1993) World distribution of the sclerotial mycoparasite Coniothyrium minitans. Mycological Research 97:1175–1178

    Article  Google Scholar 

  • Shrestha U, Augé RM, Butler DM (2016) A meta-analysis of the impact of anaerobic soil disinfestation on pest suppression and yield of horticultural crops. Frontiers in Plant Science 7:1254

    PubMed  PubMed Central  Google Scholar 

  • Steadman J (1979) Control of plant diseases caused by Sclerotinia species. Phytopathology 69:904–907

    Article  CAS  Google Scholar 

  • Trutmann P, Keane PJ, Merriman PR (1980) Reduction of sclerotial inoculum of Sclerotinia sclerotiorum with Coniothyrium minitans. Soil Biology and Biochemistry 12:461–465

    Article  Google Scholar 

  • Trutmann P, Keane PJ, Merriman PR (1982) Biological control of Sclerotinia sclerotiorum on aerial parts of plants by the hyperparasite Coniothyrium minitans. Transactions of the British Mycological Society 78:521–529

    Article  Google Scholar 

  • Turner GJ, Tribe HT (1976) On Coniothyrium minitans and its parasitism of Sclerotinia species. Transactions of the British Mycological Society 66:97–105

    Article  Google Scholar 

  • Van Beneden S, Leenknegt I, França SC, Höfte M (2010) Improved control of lettuce drop caused by Sclerotinia sclerotiorum using Contans combined with lignin or a reduced fungicide application. Crop Protection 29:168–174

    Article  CAS  Google Scholar 

  • Verkley GJM, Dukik K, Renfurm R, Göker M, Stielow JB (2014) Novel genera and species of coniothyrium-like fungi in Montagnulaceae (Ascomycota). Persoonia : Molecular Phylogeny and Evolution of Fungi 32:25–51

    Article  CAS  Google Scholar 

  • von Tiedemann A, Hedke K, Mögling R (2001) Abbauverhalten von Sklerotien der Weißstängeligkeit bei Einsatz von Contans. Raps 1:1–3

    Google Scholar 

  • Whipps JM, Budge SP (1990) Screening for sclerotial mycoparasites of Sclerotinia sclerotiorum. Mycological Research 94:607–612

    Article  Google Scholar 

  • Willbur JF, Fall ML, Bloomingdale C, Byrne AM, Chapman SA, Isard SA, Magarey RD, McCaghey MM, Mueller BD, Russo JM, Schlegel J, Chilvers MI, Mueller DS, Kabbage M, Smith DL (2018) Weather-based models for assessing the risk of Sclerotinia sclerotiorum apothecial presence in soybean (Glycine max) fields. Plant Disease 102:73–84

    Article  PubMed  Google Scholar 

  • Wu BM, Subbarao KV, Liu YB (2008) Comparative survival of sclerotia of Sclerotinia minor and S. sclerotiorum. Phytopathology 98:659–665

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Li G, Zhang J, Jiang D, Chen W (2011) Compatibility of Coniothyrium minitans with compound fertilizer in suppression of Sclerotinia sclerotiorum. Biological Control 59:221–227

    Article  Google Scholar 

  • Zeng W, Kirk W, Hao J (2012a) Field management of Sclerotinia stem rot of soybean using biological control agents. Biological Control 60:141–147

    Article  Google Scholar 

  • Zeng W, Wang D, Kirk W, Hao J (2012b) Use of Coniothyrium minitans and other microorganisms for reducing Sclerotinia sclerotiorum. Biological Control 60:225–232

    Article  Google Scholar 

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Acknowledgements

This work was supported in part by funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement N° 633184 (“EUCLID” project) and by a CASDAR grant from the French Ministry of Agriculture together with the Scientific Interest Group “GIS PICLég” (“ScleroLeg” project). The authors thank all the field experimenters of the French technical institutes (CTIFL, ACPEL, APEF, CEFEL, Invenio, SILEBAN, Terres Inovia UNILET) who collaborated in the project and who collected the isolates used in the present study.

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  1. Pathologie végétale, INRA, 84140, Montfavet, France

    Philippe C. Nicot, Félicie Avril, Magali Duffaud, Christel Leyronas, Claire Troulet & Marc Bardin

  2. CTIFL, centre de Lanxade, 28 Route des Nébouts, F-24130, Prigonrieux, France

    François Villeneuve

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  1. Philippe C. Nicot
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  2. Félicie Avril
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Correspondence to Philippe C. Nicot.

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Nicot, P.C., Avril, F., Duffaud, M. et al. Differential susceptibility to the mycoparasite Paraphaeosphaeria minitans among Sclerotinia sclerotiorum isolates. Trop. plant pathol. 44, 82–93 (2019). https://doi.org/10.1007/s40858-018-0256-7

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