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Evaluation of Mycotoxin Production and Phytopathogenicity of the Entomopathogenic Fungi Fusarium caatingaense and F. pernambucanum from Brazil

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Abstract

Fusarium incarnatum-equiseti species complex (FIESC) is considered as one of the richest insecticolous species. Fusarium species synthesize toxic secondary metabolites that are not fully understood. Mycotoxin production and pathogenicity on germinating seeds, seedlings, and leaves must be carefully studied for the use of Fusarium species in the biological control of insect pests. In this study, we evaluated the mycotoxin production and phytopathogenic potential of entomopathogenic strains of Fusarium sulawesiensis (1), F. pernambucanum (3), and F. caatingaense (23). The phytopathogenicity tests of F. caatingaense (URM 6776, URM 6777, URM 6778, URM 6779, and URM 6782) were performed during the development of bean (Phaseolus vulgaris, Vigna unguiculata, and Phaseolus lunatus), and corn (Zea mays) seedlings, using four treatments (soil infestation with the inoculum, spraying on leaves, root dip, and negative control). The mycotoxins, monoacetyl-deoxynivalenols (AcDON), deoxynivalenol (DON), beauvericin (BEA), fusarenone-X (FUS), T-2 toxin (T2), diacetoxyscirpenol (DAS), and zearalenone (ZEA), were detected in the study; BEA (detected in 25 strains) and FUS (detected in 21 strains) were found to be predominant. None of the strains showed any ability to cause disease or virulence in beans and corn. The FIESC strains showed a highly variable production of mycotoxins without the potential to be used as phytopathogenic agents for the cultures tested.

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References

  1. Santos ACS, Trindade JVC, Lima CS, Barbosa RN, Costa AF, Tiago PV, Oliveira NT (2019) Morphology, phylogeny, and sexual stage of Fusarium caatingaense and Fusarium pernambucanum, new species of the Fusarium incarnatum-equiseti species complex associated with insects in Brazil. Mycologia 111:244–259. https://doi.org/10.1080/00275514.2019.1573047

    Article  CAS  PubMed  Google Scholar 

  2. Villani A, Proctor RH, Kim H-S, Brown DW, Logrieco AF, Amatulli MT, Moretti A, Susca A (2019) Variation in secondary metabolite production potential in the Fusarium incarnatum-equiseti species complex revealed by comparative analysis of 13 genomes. BMC Genomics 20:314. https://doi.org/10.1186/s12864-019-5567-7

    Article  PubMed  PubMed Central  Google Scholar 

  3. Summerell BA (2019) Resolving Fusarium: Current status of the genus. Annu Rev Phytopathol 57:323–339. https://doi.org/10.1146/annurev-phyto-082718-100204

    Article  CAS  PubMed  Google Scholar 

  4. Sandoval-Denis M, Guarnaccia V, Polizzi G, Crous PW (2018) Symptomatic Citrus trees reveal a new pathogenic lineage in Fusarium and two new Neocosmospora species. Persoonia 40:1–25. https://doi.org/10.3767/persoonia.2018.40.01

    Article  CAS  PubMed  Google Scholar 

  5. O’Donnell K, Humber RA, Geiser DM, Kang S, Park B, Robert VARG, Crous PW, Johnston PR, Aoki T, Rooney AP, Rehner SA (2012) Phylogenetic diversity of insecticolous fusaria inferred from multilocus DNA sequence data and their molecular identification via FUSARIUM-ID and Fusarium MLST. Mycologia 104:427–445. https://doi.org/10.3852/11-179

    Article  CAS  PubMed  Google Scholar 

  6. Wang MM, Chen Q, Diao YZ, Duan WJ, Cai L (2019) Fusarium incarnatum-equiseti complex from China. Persoonia 43:70–89. https://doi.org/10.3767/persoonia.2019.43.03

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Xia JW, Sandoval-Denis M, Crous PW, Zhang XG, Lombard L (2019) Numbers to names – restyling the Fusarium incarnatum-equiseti species complex. Persoonia 43:186–221. https://doi.org/10.3767/persoonia.2019.43.05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Tiago PV, Medeiros LV, Carneiro Leão MP, Santos ACS, Costa AF, Oliveira NT (2016) Polymorphisms in entomopathogenic fusaria based on inter simple sequence repeats. Biocontrol Sci Techn 26:1401–1410. https://doi.org/10.1080/09583157.2016.1210084

    Article  Google Scholar 

  9. Carneiro-Leão MP, Tiago PV, Medeiros LV, Costa AF, Oliveira NT (2017) Dactylopius opuntiae: control by the Fusarium incarnatum-equiseti species complex and confirmation of mortality by DNA fingerprinting. J Pest Sci 90:925–933. https://doi.org/10.1007/s10340-017-0841-4

    Article  Google Scholar 

  10. Velez BAA, Diniz AG, Barbosa LFS, Santos ACS, Costa AF, Tiago PV (2019) Potential of Fusarium incarnatum-equiseti species complex isolates with Chenopodium ambrosioides and Enterolobium contortisiliquum extracts to control Dactylopius opuntiae. Int J Trop Insect Sci 39:131–138. https://doi.org/10.1007/s42690-019-00014-9

    Article  Google Scholar 

  11. Diniz AG, Barbosa LFS, Santos ACS, Oliveira NT, Costa AF, Carneiro-Leão MP, Tiago PV (2020) Bio-insecticide effect of isolates of Fusarium caatingaense (Sordariomycetes: Hypocreales) combined to botanical extracts against Dactylopius opuntiae (Hemiptera: Dactylopiidae). Biocontrol Sci Technol 30:384–395. https://doi.org/10.1080/09583157.2020.1720601

    Article  Google Scholar 

  12. Fan J-H, Xie Y-P, Xue J-L, Xiong Q, Jiang W-J, Zhang Y-J, Ren Z-M (2014) The strain HEB01 of Fusarium sp., a new pathogen that infects brown soft scale. Ann Microbiol 64:333–341. https://doi.org/10.1007/s13213-013-0668-z

    Article  CAS  Google Scholar 

  13. Addario E, Turchetti T (2011) Parasitic fungi on Dryocosmus kuriphilus in Castanea sativa necrotic galls. Bull Insectol 64:269–273

    Google Scholar 

  14. Ameen MKM (2012) Screening of Fusarium isolates pathogenicity in vitro by using the larvae of Galleria mellonella L. J. Basrah Res (Sciences) 38:19–28

    Google Scholar 

  15. Diniz AG, Cerqueira LVMP, Ribeiro TKO, Costa AF, Tiago PV (2020) Pathogenicity of isolates of Fusarium incarnatum-equiseti Species Complex to Nasutitermes corniger (Blattodea: Termitidae) and Spodoptera frugiperda (Lepidoptera: Noctuidae). Int J Pest Manag.

  16. Sharma A, Chandla VK, Thakur DR (2012) Biodiversity and pathogenicity potential of mycoflora associated with Brahmina coriacea in potato fields of North-Western Indian hills. J Entomol 9:319–331. https://doi.org/10.3923/je.2012.319.331

    Article  Google Scholar 

  17. Majumdar A, Boetel MA, Jaronski ST (2008) Discovery of Fusarium solani as a naturally occurring pathogen of sugarbeet root maggot (Diptera: Ulidiidae) pupae: Prevalence and baseline susceptibility. J Invertebr Pathol 97:1–8. https://doi.org/10.1016/j.jip.2007.05.003

    Article  PubMed  Google Scholar 

  18. Lazo MLSR (2012) Characterization and pathogenicity of entomopathogenic fungi typical of tan eucalyptus stink bug, Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae). Dissertation, Universidade Estadual Paulista.

  19. Liuzzi VC, Mirabelli V, Cimmarusti MT, Haidukowski M, Leslie JF, Logrieco AF, Caliandro R, Fanelli F, Mulè G (2017) Enniatin and beauvericin biosynthesis in Fusarium species: Production profiles and structural determinant prediction. Toxins 9:45. https://doi.org/10.3390/toxins9020045

    Article  CAS  PubMed Central  Google Scholar 

  20. Sharma L, Marques G (2018) Fusarium, an Entomopathogen—A Myth or Reality? Pathogens 7:93. https://doi.org/10.3390/pathogens7040093

    Article  CAS  PubMed Central  Google Scholar 

  21. Avila CF, Moreira GM, Nicolli CP, Gomes LB, Abreu LM, Pfenning LH, Haidukowski M, Moretti A, Logrieco A, Del Ponte EM (2019) Fusarium incarnatum-equiseti species complex associated with Brazilian rice: Phylogeny, morphology and toxigenic potential. Int J Food Microbiol 306:108267. https://doi.org/10.1016/j.ijfoodmicro.2019.108267

    Article  CAS  PubMed  Google Scholar 

  22. O’Donnell K, McCormick SP, Busman M, Proctor RH, Ward TJ, Doehring G, Geiser DM, Alberts JF, Rheeder JP et al (2018) Marasas et al. 1984 Toxigenic Fusarium species: identity and mycotoxicology revisited. Mycologia 110:1058–1080. https://doi.org/10.1080/00275514.2018.1519773

    Article  CAS  PubMed  Google Scholar 

  23. Desjardins AE (2006) Fusarium mycotoxins: chemistry, genetics, and biology. American Phytopathological Society (APS Press), St, Paul

    Google Scholar 

  24. Streit E, Schatzmayr G, Tassis P, Tzika E, Marin D, Taranu I, Tabuc C, Nicolau A, Aprodu I, Puel O, Oswald IP (2012) Current situation of mycotoxin contamination and co-occurrence in animal feed focus on Europe. Toxins 4:788–809. https://doi.org/10.3390/toxins4100788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Panasiuk Ł, Jedziniak P, Pietruszka K, Posyniak A (2020) Simultaneous determination of deoxynivalenol, its modified forms, nivalenol and fusarenone-X in feedstuffs by the liquid chromatography–tandem mass spectrometry method. Toxins 12:362. https://doi.org/10.3390/toxins12060362

    Article  CAS  PubMed Central  Google Scholar 

  26. Caloni F, Fossati P, Anadón A, Bertero A (2020) Beauvericin: The beauty and the beast. Environ Toxicol Pharmacol 75:103349. https://doi.org/10.1016/j.etap.2020.103349

    Article  CAS  PubMed  Google Scholar 

  27. Yang WC, Hsu TC, Cheng KC, Liu JR (2017) Expression of the Clonostachys rosea lactonohydrolase gene by Lactobacillus reuteri to increase its zearalenone-removing ability. Microb Cell Factor 16:69. https://doi.org/10.1186/s12934-017-0687-8

    Article  CAS  Google Scholar 

  28. Wang J, Xie Y (2020) Review on microbial degradation of zearalenone and aflatoxins. Grain Oil Sci Technol 3:117–125. https://doi.org/10.1016/j.gaost.2020.05.002

    Article  Google Scholar 

  29. Perincherry L, Lalak-Kańczugowska J, Stępień Ł (2019) Fusarium-produced mycotoxins in plant-pathogen interactions. Toxins 11:664. https://doi.org/10.3390/toxins11110664

    Article  CAS  PubMed Central  Google Scholar 

  30. Chehri K (2017) Molecular identification of entomopathogenic Fusarium species associated with Tribolium species in stored grains. J Invertebr Pathol 144:1–6. https://doi.org/10.1016/j.jip.2017.01.003

    Article  CAS  PubMed  Google Scholar 

  31. Barros G, Alaniz Zanon MS, Palazzini JM, Haidukowski M, Pascale M, Chulze S (2012) Trichothecenes and zearalenone production by Fusarium equiseti and Fusarium semitectum species isolated from Argentinean soybean. Food Addit Contam A 29:1436–1442. https://doi.org/10.1080/19440049.2012.698397

    Article  CAS  Google Scholar 

  32. Carvalho DDC, Mello SCM, Lobo Júnior M, Silva MC (2011) Controle de Fusarium oxysporum f.sp. phaseoli in vitro e em sementes, e promoção do crescimento inicial do feijoeiro comum por Trichoderma harzianum. Trop Plant Pathol 36:028–034. https://doi.org/10.1590/s1982-56762011000100004

    Article  Google Scholar 

  33. Zhang XY, Yu XX, Yu Z, Xue YF, Qi LP (2014) A simple method based on laboratory inoculum and field inoculum for evaluating potato resistance to black scurf caused by Rhizoctonia solani. Breeding Sci 64:156–163. https://doi.org/10.1270/jsbbs.64.156

    Article  Google Scholar 

  34. Mendes SS, Santos PR, Santana GC, Ribeiro GT, Mesquita JB (2005) Survey, pathogenicity and transmissibility of fungi by sabiá seeds (Mimosa caesalpiniaefolia Benth). Rev Cienc Agron 36:118–122

    Google Scholar 

  35. Karimi R, Owuoche JO, Silim SN (2010) Inheritance of fusarium wilt resistance in pigeonpea [Cajanus cajan (L.) Millspaugh]. Indian J Genet Plant Breed 70:271–276

    Google Scholar 

  36. Silva AN, Azevedo GB, Sobrinho GGR, Novaes QS (2014) Effect of chemical products and use of the Trichoderma spp. for control of Fusarium solani in passion fruit trees. Interciencia 39:398–403

    Google Scholar 

  37. Menezes M, Silva DMW (1997) Guia prático para isolamento de fungos fitopatogênicos. Recife, PE

    Google Scholar 

  38. Sahayaraj K, Namasivayam SKR, Rathi JM (2011) Compatibility of entomopathogenic fungi with extracts of plants and commercial botanicals. Afr J Biotechnol 10:933–938. https://doi.org/10.5897/AJB10.252

    Article  Google Scholar 

  39. Villani A, Moretti A, De Saeger S, Han Z, Di Mavungu JD, Soares CMG, Proctor RH, Venâncio A, Lima N, Stea G, Paciolla C, Logrieco AF, Susca A (2016) A polyphasic approach for characterization of a collection of cereal isolates of the Fusarium incarnatum-equiseti species complex. Int J Food Microbiol 234:24–35. https://doi.org/10.1016/j.ijfoodmicro.2016.06.023

    Article  CAS  PubMed  Google Scholar 

  40. Diniz AG, Cerqueira LVBMP, Ribeiro TKO, Costa AF, Tiago PV (2020) Pathogenicity of isolates of Fusarium incarnatum-equiseti species complex to Nasutitermes corniger (Blattodea: Termitidae) and Spodoptera frugiperda (Lepidoptera: Noctuidae). Int J Pest Manage. https://doi.org/10.1080/09670874.2020.1797232

    Article  Google Scholar 

  41. Logrieco A, Mulè G, Moretti A, Bottalico A (2002) Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. Eur J Plant Pathol 108:597–609. https://doi.org/10.1023/A:1020679029993

    Article  CAS  Google Scholar 

  42. Proctor RH, McCormick SP, Alexander NJ, Desjardins AE (2009) Evidence that a secondary metabolic biosynthetic gene cluster has grown by gene relocation during evolution of the filamentous fungus Fusarium. Mol Microbiol 74:1128–1142. https://doi.org/10.1111/j.1365-2958.2009.06927.x

    Article  CAS  PubMed  Google Scholar 

  43. Paciolla C, Dipierro N, Mulè G, Logrieco A, Dipierro S (2004) The mycotoxins beauvericin and T-2 induce cell death and alteration to the ascorbate metabolism in tomato protoplasts. Physiol Mol Plant Pathol 65:49–56. https://doi.org/10.1016/j.pmpp.2004.07.006

    Article  CAS  Google Scholar 

  44. Shishido M, Miwa C, Usami T, Amemiya Y, Johnson KB (2005) Biological control efficiency of fusarium wilt of tomato by nonpathogenic Fusarium oxysporum Fo-B2 in different environments. Phytopathology 95:1072–1080. https://doi.org/10.1094/phyto-95-1072

    Article  PubMed  Google Scholar 

  45. Edel-Hermann V, Aimé S, Cordier C, Olivain C, Steinberg C, Alabouvette C (2011) Development of a strain specific real-time PCR assay for the detection and quantification of the biological control agent Fo47 in root tissues. FEMS Microbiol Lett 322:34–40. https://doi.org/10.1111/j.1574-6968.2011.02332.x

    Article  CAS  PubMed  Google Scholar 

  46. Aimé S, Alabouvette C, Steinberg C, Olivain C (2013) The endophytic strain Fusarium oxysporum Fo47: a good candidate for priming the defense responses in tomato roots. Mol Plant Microbe Interact 26:918–926. https://doi.org/10.1094/MPMI-12-12-0290-R

    Article  CAS  PubMed  Google Scholar 

  47. Pereira MJZ, Ramalho MAP, Abreu AFB (2008) Strategies for the efficiency of common bean selection for resistance to fusarium wilt. Pesqui Agropecu Bras 43:721–728. https://doi.org/10.1590/S0100-204X2008000600008

    Article  Google Scholar 

  48. Varo A, Raya-Ortega MC, Trapero A (2016) Selection and evaluation of micro-organisms for biocontrol of Verticillium dahliae in olive. J Appl Microbiol 121:767–777. https://doi.org/10.1111/jam.13199

    Article  CAS  PubMed  Google Scholar 

  49. Varo A, Mulero-Aparicio A, Adem M, Roca LF, Raya-Ortega MC, López-Escudero FJ, Trapero A (2017) Screening water extracts and essential oils from Mediterranean plants against Verticillium dahliae in olive. Crop Prot 92:168–175. https://doi.org/10.1016/j.cropro.2016.10.018

    Article  CAS  Google Scholar 

  50. Varo-Suárez A, Raya-Ortega MC, Agustí-Brisach C, García-Ortiz-Civantos C, Fernández-Hernández A, Mulero-Aparicio A, Trapero A (2017) Evaluation of organic amendments from agro-industry waste for the control of verticillium wilt of olive. Plant Pathol 67:860–870. https://doi.org/10.1111/ppa.12798

    Article  CAS  Google Scholar 

  51. Mulero-Aparicio A, Cernava T, Turrà D, Schaefer A, Di Pietro A, López-Escudero FJ, Berg G (2019) The role of volatile organic compounds and rhizosphere competence in mode of action of the non-pathogenic Fusarium oxysporum FO12 toward verticillium wilt. Front Microbiol 10:1808. https://doi.org/10.3389/fmicb.2019.01808

    Article  PubMed  PubMed Central  Google Scholar 

  52. Kavitha T, Nelson R (2013) Exploiting the biocontrol activity of Tricoderma spp against root rot causing phytopathogens. ARPN J Agric Biol Sci 8:571–574

    Google Scholar 

  53. Petrișor C, Paica A, Constantinescu F (2017) Effect of secondary metabolites produced by different Trichoderma spp. isolates against Fusarium oxysporum f. sp. radicis-lycopersici and Fusarium solani. Sci Papers Ser B Hortic LXI:407–411

    Google Scholar 

  54. Mikunthan G, Manjunatha M (2006) Pathogenicity of Fusarium semitectum against crop pests and its biosafety to non-target organisms. Commun Agric Appl Biol Sci 71:465–473

    CAS  PubMed  Google Scholar 

  55. Wenda-Piesik A, Sun Z, Grey WE, Weaver DK, Morrill WL (2009) Mycoses of wheat stem sawfly (Hymenoptera: Cephidae) larvae by Fusarium spp. isolates. Environ Entomol 38:387–394. https://doi.org/10.1603/022.038.0211

    Article  PubMed  Google Scholar 

  56. Santos ACS, Diniz AG, Tiago PV, Oliveira NT (2020) Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects. Fungal Biol Rev 34:41–57. https://doi.org/10.1016/j.fbr.2019.12.002

    Article  Google Scholar 

  57. Wang Q, Xu L (2012) Beauvericin, a bioactive compound produced by fungi: a short review. Molecules 17:2367–2377. https://doi.org/10.3390/molecules17032367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Li C, Zuo C, Deng G, Kuang R, Yang Q, Hu C, Sheng O, Zhang S, Ma L, Wei Y, Yang J, Liu S, Biswas MK, Viljoen A, Yi G (2013) Contamination of bananas with beauvericin and fusaric acid produced by Fusarium oxysporum f sp cubense. PLoS One 8:e70226. https://doi.org/10.1371/journal.pone.0070226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors sincerely thank the Programa de Pós-Graduação em Biologia de Fungos (UFPE), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—Programa Nacional de Pós-Doutorado/Post-Doctorate grant given to the first author [Grant Number 88882.306291/2018-01]), and the Fundação de Amparo à Ciência e Tecnologia de Pernambuco (FACEPE), Brazil for providing scholarships or financial support. We sincerely thank to all members of the Micoteca URM, especially Eliane Barbosa (MSc) and Dr. Renan Barbosa.

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MHCM, NTO, and PVT implemented the project; MHCM, TDS, and CMSM performed the mycotoxin detection; MHC, ACTA, and AFC designed the experiment and analyzed the results of phytopathogenicity; MHCM and JDPB wrote the paper. All the authors reviewed the final version of the paper.

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Correspondence to Marília de H. C. Maciel.

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de H. C. Maciel, M., do Amaral, A.C.T., da Silva, T.D. et al. Evaluation of Mycotoxin Production and Phytopathogenicity of the Entomopathogenic Fungi Fusarium caatingaense and F. pernambucanum from Brazil. Curr Microbiol 78, 1218–1226 (2021). https://doi.org/10.1007/s00284-021-02387-y

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