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Survey of entomopathogenic and mycoparasitic fungi in the soil of onion and garlic fields in the Czech Republic and Israel

Abstract

Bulb crops are attacked by various soil-dwelling pests and pathogens. Entomopathogenic (EPFs) and mycoparasitic fungi (MPFs) which are distributed in natural and agricultural soils worldwide can play an important role as natural enemies of bulb pests. The species richness and density of these fungi in onion and garlic fields have not been investigated. The aim of this study was to determine the occurrence of EPFs and MPFs in soils where these crops were grown and compared the data from sites of the Czech Republic and Israel. Methods of fungi isolation and quantification were based on elution of soil samples by water and cultivation using selective media with dodine for EPFs and cultivation using potato dextrose agar with chloramphenicol for MPFs. Entomopathogenic fungi Beauveria spp., Isaria spp., Lecanicillium spp., Metarhizium spp., Purpureocillium spp. and mycoparasitic fungi Trichoderma spp. were isolated from soil samples in both countries. The highest density was observed in the genus Metarhizium in both countries. Metarhizium spp. were most abundant in the site Mlýn Podhora in the Czech Republic. The average density of colony-forming units (CFU) per 1 mL of soil sample was 1.47 × 104. The lowest density was observed in the genus Beauveria in both countries, up to 5.93 × 102 CFU per 1 mL of soil sample. Soils in the Czech Republic contained about ten times higher number of EPFs compared to Israel. Rather higher prevalence of MPFs was also found in the Czech Republic. Possible reasons for within and between countries variability in EPFs and MPFs occurrence are discussed.

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Data availability

The authors confirm that the data supporting the findings of this study are available within the article and from the corresponding author on reasonable request.

Abbreviations

EPFs:

Entomopathogenic fungi

MPFs:

Mycoparasitic fungi

References

  • Anwar W, Ali S, Nawaz K, Iftikhar S, Javed MA, Hashem A, Alqarawi AA, Abd Allah EF, Akhter A (2018) Entomopathogenic fungus Clonostachys rosea as a biocontrol agent against whitefly (Bemisia tabaci). Biocontrol Sci Technol 28:750–760. https://doi.org/10.1080/09583157.2018.1487030

  • Augustyniuk-Kram A, Kram KJ (2012) Entomopathogenic Fungi as an important natural regulator of insect outbreaks in forests (review). In: Blanco JA (ed) Forest ecosystems—more than just trees. InTech, pp 265–294

  • Bidochka MJ, Kasperski JE, Wild GA (1998) Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Can J Bot 76:1198–1204. https://doi.org/10.1139/b98-115

    Article  Google Scholar 

  • Brožová J (2010) Mycoparasitic fungi Trichoderma spp. in plant protection—review. Plant Protect Sci 40:63–74. https://doi.org/10.17221/459-PPS

  • Bueno-Pallero FÁ, Blanco-Pérez R, Vicente-Díez I, Rodríguez Martín JA, Dionísio L, Campos-Herrera R (2020) Patterns of occurrence and activity of entomopathogenic fungi in the Algarve (Portugal) using different isolation methods. Insects 11:352. https://doi.org/10.3390/insects11060352

    Article  PubMed Central  Google Scholar 

  • Bunbury-Blanchette AL, Walker AK (2019) Trichoderma species show biocontrol potential in dual culture and greenhouse bioassays against Fusarium basal rot of onion. Biol Control 130:127–135. https://doi.org/10.1016/j.biocontrol.2018.11.007

    Article  Google Scholar 

  • Canfora L, Malusà E, Tkaczuk C, Tartanus M, Łabanowska BH, Pinzari F (2016) Development of a method for detection and quantification of B. brongniartii and B. bassiana in soil. Sci Rep 6:22933. https://doi.org/10.1038/srep22933

  • Charnley AK, Collins SA (2007) Entomopathogenic fungi and their role in pest control. In: Kubicek CP, Druzhinina IS (eds) Environmental and microbial relationships. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 159–187

    Google Scholar 

  • Chase AR, Osborne LS, Ferguson VM (1986) Selective Isolation of the Entomopathogenic Fungi Beauveria bassiana and Metarhizium anisopliae from an Artificial Potting Medium. Fla Entomol 69:285. https://doi.org/10.2307/3494930

    Article  Google Scholar 

  • Czech Meteorological Services (2021) Environmental data. https://www.chmi.cz. Accessed 10 November 2021

  • Degani O, Dor S (2021) Trichoderma biological control to protect sensitive maize hybrids against late wilt disease in the field. JoF 7:315. https://doi.org/10.3390/jof7040315

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Díaz A, Okabe K, Eckenrode CJ, Villani MG, Oconnor BM (2000) Biology, ecology, and management of the bulb mites of the genus Rhizoglyphus (Acari: Acaridae). Exp Appl Acarol 24:85–113. https://doi.org/10.1023/A:1006304300657

    Article  PubMed  Google Scholar 

  • Domsch KH, Gams W, Anderson TH (1980) Compendium of soil fungi. Academic Press, London, New York

    Google Scholar 

  • Elad Y, Chet I, Henis Y (1981) A selective medium for improving quantitative isolation of Trichoderma spp. from soil. Phytoparasitica 9:59–67. https://doi.org/10.1007/BF03158330

    Article  Google Scholar 

  • El-Mougy NS, Abdel-Kader MM (2019) Biocontrol measures against onion basal rot incidence under natural field conditions. J Plant Pathol 101:579–586. https://doi.org/10.1007/s42161-018-00237-8

    Article  Google Scholar 

  • FAO Crops FAOSTAT (2021) Countries—select all; regions—world + (total); elements—production quantity; items—garlic and onion; years—2019. https://www.fao.org/home/en/. Accessed 11 May 2021

  • Fuxa JR (1995) Biorational Pest control agents: formulation and delivery. American Chemical Society, Washington, DC

    Google Scholar 

  • Gams W, Bissett J (2002) Trichoderma and Gliocladium. Volume 1: basic biology, taxonomy and genetics. CRC Press

  • Gerson U, Gafni A, Paz Z, Sztejnberg A (2008) A tale of three acaropathogenic fungi in Israel: Hirsutella, Meira and Acaromyces. Exp Appl Acarol 46:183–194. https://doi.org/10.1007/s10493-008-9202-6

    CAS  Article  PubMed  Google Scholar 

  • Ghosh SK, Pal S (2016) Entomopathogenic potential of Trichoderma longibrachiatum and its comparative evaluation with malathion against the insect pest Leucinodes orbonalis. Environ Monit Assess 188:37. https://doi.org/10.1007/s10661-015-5053-x

    CAS  Article  PubMed  Google Scholar 

  • Goettel MS, Inglis GD (1997) Manual of techniques in insect pathology. Press, San Diego, Calif, Acad

    Google Scholar 

  • Goettel MS, Koike M, Kim JJ, Aiuchi D, Shinya R, Brodeur J (2008) Potential of Lecanicillium spp. for management of insects, nematodes and plant diseases. J Invertebr Pathol 98:256–261. https://doi.org/10.1016/j.jip.2008.01.009

    CAS  Article  PubMed  Google Scholar 

  • Gupta SC, Leathers TD, Wicklow DT (1993) Hydrolytic enzymes secreted by Paecilomyces lilacinus cultured on sclerotia of Aspergillus flavus. Appl Microbiol Biotechnol 39:99–103. https://doi.org/10.1007/BF00166856

    CAS  Article  Google Scholar 

  • Hall RA (1976) A bioassay of the pathogenicity of Verticillium lecanii conidiospores on the aphid, Macrosiphoniella sanborni. J Invertebr Pathol 27:41–48. https://doi.org/10.1016/0022-2011(76)90026-4

    Article  Google Scholar 

  • Harman GE, Kubicek CP (eds) (2002) Trichoderma and Gliocladium. Volume 1: Basic biology, taxonomy and genetics. CRC Press

  • Hossain L, Rahman R, Khan MS (2017) Alternatives of Pesticides. In: Khan MS, Rahman MS (eds) Pesticide residue in foods. Springer International Publishing, Cham, pp 147–165

    Chapter  Google Scholar 

  • Hue AG, Voldeng HD, Savard ME, Fedak G, Tian X, Hsiang T (2009) Biological control of Fusarium head blight of wheat with Clonostachys rosea strain ACM941. Can J Plant Pathol 31:169–179. https://doi.org/10.1080/07060660909507590

    Article  Google Scholar 

  • Humber RA (2012) Identification of entomopathogenic fungi. In: Lacey LA (ed) Manual of techniques in invertebrate pathology. Academic Press, London, UK, pp 151–157

  • Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford, pp 23–69

    Chapter  Google Scholar 

  • Inglis GD, Enkerli J, Goettel MS (2012) Manual of techniques in invertebrate pathology, 2nd edn. Academic Press imprint of Elsevier Science, Oxford, New York

    Google Scholar 

  • Israel Meteorological Services (2021) Environmental data. https://ims.gov.il/en/SurfaceObservations. Accessed 14 November 2021

  • Jensen B, Knudsen IMB, Jensen DF (2000) Biological seed treatment of cereals with fresh and long-term stored formulations of Clonostachys rosea: Biocontrol efficacy against Fusarium culmorum. Eur J Plant Pathol 106:233–242. https://doi.org/10.1023/A:1008794626600

    Article  Google Scholar 

  • Jensen B, Knudsen IMB, Jensen DF (2002) Survival of conidia of Clonostachys rosea on stored barley seeds and their biocontrol efficacy against seed-borne Bipolaris sorokiniana. Biocontrol Sci Technol 12:427–441. https://doi.org/10.1080/09583150220146013

    Article  Google Scholar 

  • Jensen B, Knudsen IMB, Madsen M, Jensen DF (2004) Biopriming of infected carrot seed with an antagonist, Clonostachys rosea, selected for control of Seedborne Alternaria spp. Phytopathology 94:551–560. https://doi.org/10.1094/PHYTO.2004.94.6.551

    Article  PubMed  Google Scholar 

  • Keller S, Zimmermann G (1989) Mycopathogens of soil insects. Elsevier

    Book  Google Scholar 

  • Keller S, Kessler P, Schweizer C (2003) Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metharhizium anisopliae. Biocontrol 48:307–319. https://doi.org/10.1023/A:1023646207455

    Article  Google Scholar 

  • Kenneth R, Muttath TI, Gerson U (1979) Hirsutella thompsonii, a fungal pathogen of mites. I. Biology of the fungus in vitro. Ann Appl Biol 91:21–28

    Article  Google Scholar 

  • Keyser CA, Jensen B, Meyling NV (2016) Dual effects of Metarhizium spp. and Clonostachys rosea against an insect and a seed-borne pathogen in wheat: dual effects of Metarhizium spp. and Clonostachys rosea. Pest Manag Sci 72:517–526. https://doi.org/10.1002/ps.4015

    CAS  Article  PubMed  Google Scholar 

  • Klingen I, Eilenberg J, Meadow R (2002) Effects of farming system, field margins and bait insect on the occurrence of insect pathogenic fungi in soils. Agric Ecosyst Environ 91:191–198. https://doi.org/10.1016/S0167-8809(01)00227-4

    Article  Google Scholar 

  • Konopická J, Bohatá A, Nermuť J, Jozová E, Mráček Z, Palevsky E, Zemek R (2021) Efficacy of soil isolates of entomopathogenic fungi against the bulb mite, Rhizoglyphus robini (Acari: Acaridae). Syst Appl Acarol 1149–1167. https://doi.org/10.11158/saa.26.6.11

  • Krauss U, Hidalgo E, Arroyo C, Piper SR (2004) Interaction Between the Entomopathogens Beauveria bassiana, Metarhizium anisopliae and Paecilomyces fumosoroseus and the Mycoparasites Clonostachys spp., Trichoderma harzianum and Lecanicillium lecanii. Biocontrol Sci Technol 14:331–346. https://doi.org/10.1080/09583150410001665196

    Article  Google Scholar 

  • Landa Z, Horňák P, Charvátová H, Osborne LS (2002) Distribution, Occurrence and potential use of entomopathogenic fungi in arable soils in Czech Republic. In: Proceedings of international conference ISTRO “Current trends in the research of soil environment.” pp 195–201

  • Latch GCM, Falloon RE (1976) Studies on the use of Metarhizium anisopliae to control Oryctes rhinoceros. Entomophaga 21:39–48. https://doi.org/10.1007/BF02372014

    Article  Google Scholar 

  • Lawande KE, Khar, A, Mahajan V, Srinivas PS, Sankar V, Singh RP (2009) Onion and garlic research in India. J Hortic Sci 91–119

  • Lebiush-Mordechai S, Erlich O, Maymon M, Freeman S, Ben-David T, Ofek T, Palevsky E, Tsror Lahkin L (2014) Bulb and Root Rot in Lily (Lilium longiflorum) and Onion (Allium cepa) in Israel. J Phytopathol 162:466–471. https://doi.org/10.1111/jph.12214

    Article  Google Scholar 

  • Majchrowska-Safaryan A, Tkaczuk C (2021) Abundance of entomopathogenic fungi in leaf litter and soil layers in forested habitats in Poland. Insects 12:134. https://doi.org/10.3390/insects12020134

    Article  PubMed  PubMed Central  Google Scholar 

  • Marti GA, Lastra CCL, Pelizza SA, García JJ (2006) Isolation of Paecilomyces lilacinus (Thom) Samson (Ascomycota: Hypocreales) from the Chagas disease vector, Triatoma infestans Klug (Hemiptera: Reduviidae) in an endemic area in Argentina. Mycopathologia 162:369–372. https://doi.org/10.1007/s11046-006-0072-3

    Article  PubMed  Google Scholar 

  • McDonald MR, de los Angeles Jaime M, Hovius MHY (2004) Management of diseases of onions and garlic. In: Naqvi SAMH (ed) Diseases of fruits and vegetables: vol II. Springer Netherlands, Dordrecht, pp 149–200

  • McGuire AV, Northfield TD (2020) Tropical occurrence and agricultural importance of Beauveria bassiana and Metarhizium anisopliae. Front Sustain Food Syst 4:6. https://doi.org/10.3389/fsufs.2020.00006

    Article  Google Scholar 

  • Medo J, Cagáň Ľ (2011) Factors affecting the occurrence of entomopathogenic fungi in soils of Slovakia as revealed using two methods. Biol Control 59:200–208. https://doi.org/10.1016/j.biocontrol.2011.07.020

    Article  Google Scholar 

  • Meyling NV, Eilenberg J (2006) Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem. Agric Ecosyst Environ 113:336–341. https://doi.org/10.1016/j.agee.2005.10.011

    Article  Google Scholar 

  • Meyling NV, Eilenberg J (2007) Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol Control 43:145–155. https://doi.org/10.1016/j.biocontrol.2007.07.007

    Article  Google Scholar 

  • Mishra RK, Jaiswal KR, Kumar D, Saabale PR, Singh A (2014) Management of major diseases and insect pests of onion and garlic: a comprehensive review. J Plant Breed Crop Sci 6:160–170. https://doi.org/10.5897/JPBCS2014.0467

    Article  Google Scholar 

  • Mohammed AA, Younus AS, Ali AN (2021) Efficacy of Clonostachys rosea, as a promising entomopathogenic fungus, against coleopteran stored product insect pests under laboratory conditions. Egypt J Biol Pest Control 31:55. https://doi.org/10.1186/s41938-021-00405-6

    Article  Google Scholar 

  • Moino A Jr, Alves SB (1999) EFEITO ANTAGÔNICO DE Trichoderma sp. NO DESENVOLVIMENTO DE Beauveria bassiana (Bals.) Vuill. e Metarhizium anisopliae (Metsch.) Sorok. Sci Agric (piracicaba, Braz) 56:217–224. https://doi.org/10.1590/S0103-90161999000100029

    Article  Google Scholar 

  • Nygren K, Dubey M, Zapparata A, Iqbal M, Tzelepis GD, Durling MB, Jensen DF, Karlsson M (2018) The mycoparasitic fungus Clonostachys rosea responds with both common and specific gene expression during interspecific interactions with fungal prey. Evol Appl 11:931–949. https://doi.org/10.1111/eva.12609

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Ofek T, Gal S, Inbar M, Lebiush-Mordechai S, Tsror L, Palevsky E (2014) The role of onion-associated fungi in bulb mite infestation and damage to onion seedlings. Exp Appl Acarol 62:437–448. https://doi.org/10.1007/s10493-013-9750-2

    Article  PubMed  Google Scholar 

  • Okabe K, Amano H (1991) Penetration and Population Growth of the Robine Bulb Mite, Rhizoglyphus robini CLAPAREDE (Acari:Acaridae), on healthy and Fusarium-Infected Rakkyo Bulbs. Appl Entomol Zool 26:129–136. https://doi.org/10.1303/aez.26.129

    Article  Google Scholar 

  • Ownley BH, Gwinn KD, Vega FE (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. Biocontrol 55:113–128. https://doi.org/10.1007/s10526-009-9241-x

    Article  Google Scholar 

  • Paz Z, Burdman S, Gerson U, Sztejnberg A (2007a) Antagonistic effects of the endophytic fungus Meira geulakonigii on the citrus rust mite Phyllocoptruta oleivora: fungal antagonism of rust mite. J Appl Microbiol 103:2570–2579. https://doi.org/10.1111/j.1365-2672.2007.03512.x

    CAS  Article  PubMed  Google Scholar 

  • Paz Z, Gerson U, Sztejnberg A (2007b) Assaying three new fungi against citrus mites in the laboratory, and a field trial. Biocontrol 52:855–862. https://doi.org/10.1007/s10526-006-9060-2

    Article  Google Scholar 

  • Paz Z, Bilkis I, Gerson U, Kerem Z, Sztejnberg A (2011) Argovin, a novel natural product secreted by the fungus Meira argovae, is antagonistic to mites: a novel mycotoxin affecting the citrus rust mite. Entomol Exp Appl 140:247–253. https://doi.org/10.1111/j.1570-7458.2011.01155.x

    CAS  Article  Google Scholar 

  • Podder D, Ghosh SKr, (2019) A new application of Trichoderma asperellum as an anopheline larvicide for ecofriendly management in medical science. Sci Rep 9:1108. https://doi.org/10.1038/s41598-018-37108-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Prenerová E, Zemek R, Weyda F, Volter L (2009) Entomopathogenic fungi isolated from soil in the vicinity of Cameraria ohridella infested horse chestnut trees. In: Ehlers RU, Crickmore N, Enkerli J, Glazer I, Lopez-Ferber M, Tkaczuk C (eds) IOBC/WPRS Bulletin, pp 321–324

  • Quesada-Moraga E, Navas-Cortés JA, Maranhao EAA, Ortiz-Urquiza A, Santiago-Álvarez C (2007) Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycol Res 111:947–966. https://doi.org/10.1016/j.mycres.2007.06.006

    Article  PubMed  Google Scholar 

  • Rabeendran N, Jones EE, Stewart A (1998) Isolation and in vitro screening of soil fungi for biological control of Sclerotinia sclerotiorum. pnzppc 51:102–106. https://doi.org/10.30843/nzpp.1998.51.11666

  • Rath AC, Koen TB, Yip HY (1992) The influence of abiotic factors on the distribution and abundance of Metarhizium anisopliae in Tasmanian pasture soils. Mycol Res 96:378–384. https://doi.org/10.1016/S0953-7562(09)80956-8

    Article  Google Scholar 

  • Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98. https://doi.org/10.3852/mycologia.97.1.84

    CAS  Article  Google Scholar 

  • Rehner SA, Minnis AM, Sung G-H, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073. https://doi.org/10.3852/10-302

    Article  PubMed  Google Scholar 

  • Ribeiro WRC, Butler EE (1992) Isolation of mycoparasitic species of Pythium with spiny oogonia from soil in California. Mycol Res 96:857–862. https://doi.org/10.1016/S0953-7562(09)81031-9

    Article  Google Scholar 

  • Rodríguez MA, Cabrera G, Gozzo FC, Eberlin MN, Godeas A (2011) Clonostachys rosea BAFC3874 as a Sclerotinia sclerotiorum antagonist: mechanisms involved and potential as a biocontrol agent: Clonostachys rosea as a Sclerotinia sclerotiorum antagonist. J Appl Microbiol 110:1177–1186. https://doi.org/10.1111/j.1365-2672.2011.04970.x

    Article  PubMed  Google Scholar 

  • Rombach MC, Humber RA, Roberts DW (1986) Metarhizium flavoviride var. minus, var. nov., a pathogen of plant- and leafhoppers on rice in the Philippines and Solomon Islands. Mycotaxon 1986:87–92

  • Samson RA, Evans HC, Latgé J-P (1988) Atlas of entomopathogenic fungi. Springer, Berlin Heidelberg, Berlin, Heidelberg

    Book  Google Scholar 

  • Sánchez-Peña SR, Lara JS-J, Medina RF (2011) Occurrence of entomopathogenic fungi from agricultural and natural ecosystems in Saltillo, México, and their virulence towards thrips and whiteflies. J Insect Sci 11:1–10. https://doi.org/10.1673/031.011.0101

    Article  PubMed  PubMed Central  Google Scholar 

  • Scheepmaker JWA, Butt TM (2010) Natural and released inoculum levels of entomopathogenic fungal biocontrol agents in soil in relation to risk assessment and in accordance with EU regulations. Biocontrol Sci Technol 20:503–552. https://doi.org/10.1080/09583150903545035

    Article  Google Scholar 

  • Sharifi-Rad J, Mnayer D, Tabanelli G, Stojanović-Radić ZZ, Sharifi-Rad M, Yousaf Z, Vallone L, Setzer WN, Iriti M (2016) Plants of the genus Allium as antibacterial agents: from tradition to pharmacy. Cell Mol Biol (Noisy-le-grand) 62:57–68

  • Sharma L, Bohra N, Rajput VD, Quiroz-Figueroa FR, Singh RK, Marques G (2020) Advances in entomopathogen Isolation: a case of bacteria and fungi. Microorganisms 9:16. https://doi.org/10.3390/microorganisms9010016

    CAS  Article  PubMed Central  Google Scholar 

  • Sharma L, Oliveira I, Torres L, Marques G (2018) Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria-Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana). MC 38:1–23. https://doi.org/10.3897/mycokeys.38.26790

  • Siegel S, Castellan NJ (2003) Nonparametric statistics for the behavioral sciences, 2nd edn. [reprinted]. McGraw-Hill, Boston, Mass

  • Šimáčková K, Kročáková J, Bohatá A, Herrero N (2014) Diversity and distribution of entomopathogenic fungi in Czech Republic soils. In: 47th Annual meeting of the society for invertebrate pathology and international congress on invertebrate pathology and microbial control. Mainz, p 103

  • Steenberg T (1997) Natural occurrence of Beauveria bassiana (Bals.) Vuill. with focus on infectivity to Sitona species and other insects in lucerne. Dissertation, The Royal Veterinary and Agricultural University

  • Tkaczuk C, Król A, Majchrowska-Safaryan A, Niecewicz Ł (2014) The occurrence of entomopathogenic fungi in soils from fields cultivated in a conventional and organic system. J Ecol Eng 2014:137–144. https://doi.org/10.12911/22998993.1125468

  • Tsui CKM, Woodhall J, Chen W, Lévesque CA, Lau A, Schoen CD, Baschien C, Najafzadeh MJ, de Hoog S (2011) Molecular techniques for pathogen identification and fungus detection in the environment. IMA Fungus 2011:177–89. https://doi.org/10.5598/imafungus.2011.02.02.09

  • Vänninen I (1996) Distribution and occurrence of four entomopathogenic fungi in Finland: effect of geographical location, habitat type and soil type. Mycol Res 100:93–101. https://doi.org/10.1016/S0953-7562(96)80106-7

    Article  Google Scholar 

  • Vänninen I, Tyni-Juslin J, Hokkanen H (2000) Persistence of augmented Metarhizium anisopliae and Beauveria bassiana in Finnish agricultural soils. Biocontrol 45:201–222. https://doi.org/10.1023/A:1009998919531

    Article  Google Scholar 

  • Wen C, Xiong H, Wen J, Wen X, Wang C (2020) Trichoderma species attract Coptotermes formosanus and antagonize termite pathogen Metarhizium anisopliae. Front Microbiol 11:653. https://doi.org/10.3389/fmicb.2020.00653

    Article  PubMed  PubMed Central  Google Scholar 

  • Whipps JM, Lumsden RD (2001) Commercial use of fungi as plant disease biological control agents: status and prospects. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford, pp 9–22

    Chapter  Google Scholar 

  • Zemek R, Konopická J, Bohatá A (2018) Inoculation of sphagnum-based soil substrate with entomopathogenic fungus Isaria fumosorosea (Hypocreales: Cordycipitaceae). AIP Conf Proc 1954:030009. https://doi.org/10.1063/1.5033389

    CAS  Article  Google Scholar 

  • Zimmermann G (1986) The ‘Galleria bait method’ for detection of entomopathogenic fungi in soil. J Appl Entomol 102:213–215. https://doi.org/10.1111/j.1439-0418.1986.tb00912.x

    Article  Google Scholar 

  • Zimmermann G (2007a) Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Sci Technol 17:879–920. https://doi.org/10.1080/09583150701593963

    Article  Google Scholar 

  • Zimmermann G (2007b) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci Technol 17:553–596. https://doi.org/10.1080/09583150701309006

    Article  Google Scholar 

  • Zimmermann G (2008) The entomopathogenic fungi Isaria farinosa (formerly Paecilomyces farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus): biology, ecology and use in biological control. Biocontrol Sci Technol 18:865–901. https://doi.org/10.1080/09583150802471812

    Article  Google Scholar 

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Acknowledgements

The authors thank the farmers for allowing access to their fields for the collection of soil samples. Mrs. Olga Divišová is thanked for her technical help.

Funding

This research was funded by institutional support RVO: 60077344 and co-financed by Grant Agency of the University of South Bohemia (project No. 018/2018/Z). It was also an integral part of a joint Czech Republic and Israeli project titled ‘New biorational methods applied to control selected pests as an alternative to chemical pesticides to prevent contamination of soil and water resource’, supported by the Ministry of Education, Youth and Sports of the Czech Republic (project No. 8G15006) and the Ministry of Science, Technology and Space, State Israel (project No. 3-13035). Publication of this study was funded by the Technology Agency of the Czech Republic (project No. TP01010022).

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Conceptualization was done by JK and RZ. Methodology was carried out by JK and AB. Soil sampling was done by RZ, EP and JN. Experiments and data collection were carried out by JK. Data analysis was done by JK and RZ. Validation was done by RZ and JN. Writing—original draft preparation were carried out by JK. Writing—review and editing were carried out by JK, RZ and EP. Visualization was done by VP. Supervision was done by RZ and AB. Funding acquisition was done by EP and RZ. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Jana Konopická.

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Konopická, J., Bohatá, A., Palevsky, E. et al. Survey of entomopathogenic and mycoparasitic fungi in the soil of onion and garlic fields in the Czech Republic and Israel. J Plant Dis Prot 129, 271–281 (2022). https://doi.org/10.1007/s41348-021-00557-5

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  • DOI: https://doi.org/10.1007/s41348-021-00557-5

Keywords

  • Alliaceae
  • Soil microorganisms
  • Hypocreales
  • Diversity
  • Metarhizium
  • Trichoderma