Skip to main content
SpringerLink
Log in

Antagonistic Potential of Macrolepiota sp. Against Alternaria Solani as Causal Agent of Early Blight Disease in Tomato Plants

Antagonistisches Potenzial von Macrolepiota sp. gegen Alternaria solani als Erreger der Dürrfleckenkrankheit bei Tomaten

  • Original Article
  • Published:
Gesunde Pflanzen Aims and scope Submit manuscript

Abstract

The aim of this study was to identify a Mexican native basidiomycete strain with antagonistic potential against phytopathogenic fungi. The antifungal activity of fifteen isolates against Fusarium oxysporum, Fusarium solani, Colletotrichum truncatum, Colletotrichum coccodes, Colletotrichum sp., Stemphylium solani, Botrytis cinerea, Epicoccum nigrum, Phomopsis sp. and Alternaria solani was studied in vitro using dual culture assay. An isolate of Macrolepiota sp (CS185) exhibited the strongest ability to compete on potato dextrose agar medium (PDA) causing 22.2 up to 46.6% inhibition in seven out of ten pathogens evaluated. The addition of 30% Macrolepiota sp. liquid filtrates (from 7 day-cultures in potato dextrose broth) to PDA plates inhibited 66% of A. solani growth. Application of Macrolepiota sp. CS185 culture fluids to control early blight disease caused in tomato plants by A. solani under greenhouse conditions diminished disease incidence and percent of damage. The length of the stems, the roots and the foliar area increased in the treated plants and, above all, the foliar symptoms decreased by 73%. Sesquiterpene lactones and quinones identified in culture fluids might be responsible for Macrolepiota antifungal activity. This study proves that Macrolepiota sp. CS185 culture filtrates have potential in biocontrol of early blight disease.

Zusammenfassung

Ziel dieser Studie war es, einen in Mexiko heimischen Basidiomycetenstamm mit antagonistischem Potenzial gegen phytopathogene Pilze zu identifizieren. Die antimykotische Aktivität von fünfzehn Isolaten gegen Fusarium oxysporum, Fusarium solani, Colletotrichum truncatum, Colletotrichum coccodes, Colletotrichum sp., Stemphylium solani, Botrytis cinerea, Epicoccum nigrum, Phomopsis sp., und Alternaria solani wurde in vitro unter Verwendung eines Doppelkulturassays untersucht. Ein Isolat von Macrolepiota sp. (CS185) zeigte die stärkste Konkurrenzfähigkeit auf dem Kartoffeldextrose‐Agar‐Medium (PDA), was bei sieben von zehn untersuchten Krankheitserregern zu einer Hemmung von 22,2 bis 46,6 % führte. Die Zugabe von 30 % Macrolepiota sp.-Flüssigfiltrat (aus 7‑Tage-Kulturen in Kartoffeldextrose-Saft) zu PDA-Platten hemmte das Wachstum von A. solani um 66 %. Die Anwendung von Macrolepiota sp. CS185-Kulturflüssigkeiten zur Bekämpfung der durch A. solani unter Gewächshausbedingungen verursachten Dürrfleckenkrankheit bei Tomatenpflanzen verringerte die Häufigkeit und den prozentualen Anteil der Schäden. Die Länge der Stiele, der Wurzeln und der Blattfläche nahm bei den behandelten Pflanzen zu, die Blattsymptome nahmen um 73 % ab. In Kulturflüssigkeiten identifizierte Sesquiterpenlaktone und Chinone könnten für die antimykotische Aktivität von Macrolepiota verantwortlich sein. Diese Studie belegt, dass Macrolepiota sp. CS185-Kulturfiltrate Potenzial zur biologischen Kontrolle der Dürrfleckenkrankheit besitzen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abo-Elyous KA, Abdel-Hafez SI, Abdel-Rahim IR (2014) Isolation of Trichoderma and evaluation of their antagonistic potential against Alternaria porri. J Phytopathol 162(9):567–574. https://doi.org/10.1111/jph.12228

    Article  Google Scholar 

  • Alves MJ, Ferreira IC, Dias J, Teixeira V, Martins A, Pintado M (2013) A review on antifungal activity of mushroom (basidiomycetes) extracts and isolated compounds. Curr Top Med Chem 13:2648–2659. https://doi.org/10.2174/15680266113136660191

    Article  CAS  PubMed  Google Scholar 

  • Astegiano ED, Favaro JC, Bouzo CA (2001) Estimación del área foliar en distintos cultivares de tomate (Lycopersicon esculentum Mill.) utilizando medidas foliares lineales. Investig Agrar Prod Prot Veg 16(2):249–256

    Google Scholar 

  • Baka ZAM (2014) Biological control of the predominant seed-borne fungi of tomato by using plant extracts. J Phytopathol Pest Manag 1:10–22

    Google Scholar 

  • Barneche S, Jorcin G, Cecchetto G, Cerdeiras MP, Vázquez A, Alborés S (2016) Screening for antimicrobial activity of wood rotting higher basidiomycetes mushrooms from Uruguay against phytopathogens. Int J Med Mushrooms 18:261–267. https://doi.org/10.1615/IntJMedMushrooms.v18.i3.90

    Article  PubMed  Google Scholar 

  • Barseghyan GS, Barazani A, Wasser SP (2016) Medicinal mushrooms with anti-phytopathogenic and insecticidal properties. Mushroom Biotechnol. https://doi.org/10.1016/B978-0-12-802794-3.00008-4

    Article  Google Scholar 

  • Bergougnoux V (2014) The history of tomato: from domestication to bio pharming. Biotechnol Adv 32(1):170–189. https://doi.org/10.1016/j.biotechadv.2013.11.003

    Article  CAS  PubMed  Google Scholar 

  • Coy Barrera CA, Parra J, Cuca Suárez LE (2014) Caracterización química del aceite esencial e identificación preliminar de metabolitos secundarios en hojas de la especie raputia heptaphylla (rutaceae). Elementos 4(4):31–39

    Article  Google Scholar 

  • Dias MP, Bastos MS, Xavier VB, Cassel E, Astarita LV, Santarém ER (2017) Plant growth and resistance promoted by Streptomyces spp. in tomato. Plant Physiol Biochem 118:479–493. https://doi.org/10.1016/j.plaphy.2017.07.017

    Article  CAS  PubMed  Google Scholar 

  • Duarte Y, Pino O, Infante D, Sánchez Y, Travieso MD, Martínez B (2013) Efecto in vitro de aceites esenciales sobre Alternaria solani Sorauer. Rev Prot Veg 28(1):54–59

    Google Scholar 

  • Fontenelle AD, Guzzo SD, Lucon CM, Harakava R (2011) Growth promotion and induction of resistance in tomato plant against Xanthomonas euvesicatoria and Alternaria solani by Trichoderma spp. Crop Prot 30(11):1492–1500. https://doi.org/10.1016/j.cropro.2011.07.019

    Article  Google Scholar 

  • Gao Z, Zhang B, Liu H, Han J, Zhang Y (2017) Identification of endophytic Bacillus velezensis ZSY‑1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis cinerea. Biol Control 105:27–39. https://doi.org/10.1016/j.biocontrol.2016.11.007

    Article  Google Scholar 

  • Ghazanfar MU, Raza W, Ahmed KS, Qamar J, Haider N, Rasheed MH (2016) Evaluation of different fungicides against Alternaria solani (Ellis & Martin) Sorauer cause of early blight of tomato under laboratory conditions. Int J Zool Stud 1(5):8–12

    Google Scholar 

  • Gjhorbanpour M, Omidvari M, Abbaszadeh-Dahaji P, Omidvar R, Kariman K (2018) Mechanisms underlying the protective effects of beneficial fungi against plant diseases. Biol Control 117:147–157. https://doi.org/10.1016/j.biocontrol.2017.11.006

    Article  Google Scholar 

  • Imtiaj A, Lee TS (2007) Screening of antibacterial and antifungal activities from Korean wild mushrooms. World J Agric Sci 3(3):316–321

    Google Scholar 

  • Innocenti G, Garibyan NG, Badalyan SM (2002) Antagonistic activity of xylotrophic mushrooms against pathogenic fungi of cereals in dual culture. Phytopathol Mediterr 41(3):220–225

    Google Scholar 

  • Jorcin G, Barneche S, Vázquez A, Cerdeiras MP, Alborés S (2017) Effects of culture conditions on antimicrobial activity of Ganoderma resinaceum (Agaricomycetes) extracts. Int J Med Mushrooms 19(8):737–744. https://doi.org/10.1615/IntJMedMushrooms.2017021217

    Article  PubMed  Google Scholar 

  • Joseph A, Igbinosa OB, Alori ET, Ademiluyi BO, Aluko AP (2017) Effectiveness of Pseudomonas species in the management of tomato early blight pathogen Alternaria solani. Afr J Microbiol Res 11(23):972–976. https://doi.org/10.5897/AJMR2017.8564

    Article  CAS  Google Scholar 

  • Kim KH, Park KM, Choi SU, Lee KR (2009) Macrolepiotin, a new indole alkaloid from Macrolepiota neomastoidea. J Antibiot 62(6):335–338. https://doi.org/10.1038/ja.2009.30

    Article  CAS  PubMed  Google Scholar 

  • Klančnik A, Megušar P, Sterniša M, Jeršek B, Bucar F, Smole Možina S, Kos J, Sabotič J (2017) Aqueous extracts of wild mushrooms show antimicrobial and antiadhesion activities against bacteria and fungi. Phytother Res 31(12):1971–1976. https://doi.org/10.1002/ptr.5934

    Article  CAS  PubMed  Google Scholar 

  • Kosanić M, Ranković B, Rancić A, Stanojković T (2016) Evaluation of metal concentration and antioxidant, antimicrobial, and anticancer potentials of two edible mushrooms Lactarius deliciosus and Macrolepiota procera. J Food Drug Anal 24(3):477–484. https://doi.org/10.1016/j.jfda.2016.01.008

    Article  CAS  PubMed  Google Scholar 

  • Kumar N, Bhardwaj ML, Kumari S, Sharma A, Kansal S (2018) Screening of tomato (Solanum lycopersicum L.) germplasm for growth, yield, resistance against buckeye rot and Alternaria blight severity under mid-hills conditions of Himachal Pradesh. J Pharmacogn Phytochem 7(1):2098–2103

    Google Scholar 

  • Llauradó G, Morris HJ, Ferrera L, Camacho M, Castán L, Lebeque Y, Beltrán Y, Cos P, Bermúdez RC (2015) In-vitro antimicrobial activity and complement/macrophage stimulating effects of a hot-water extract from mycelium of the oyster mushroom Pleurotus sp. Innov Food Sci Emerg Technol 30:177–183. https://doi.org/10.1016/j.ifset.2015.05.002

    Article  CAS  Google Scholar 

  • Luo DQ, Shao HJ, Zhu HJ, Liu JK (2005) Activity in vitro and in vivo against plant pathogenic fungi of grifolin isolated from the basidiomycete Albatrellus dispansus. Z Naturforsch C 60(1/2):50–56. https://doi.org/10.1515/znc-2005-1-210

    Article  CAS  PubMed  Google Scholar 

  • Mohan V, Nivea R, Menon S (2015) Evaluation of ectomycorrhizal fungi as potential bio-control agents against selected plant pathogenic fungi. J Acad Ind Res 3(9):408–412

    CAS  Google Scholar 

  • Muthomi JW, Lengai GM, Wagacha MJ, Narla RD (2017) In vitro activity of plant extracts against some important plant pathogenic fungi of tomato. Aust J Crop Sci 11(6):683–689. https://doi.org/10.21475/ajcs.17.11.06.p399

    Article  CAS  Google Scholar 

  • Oka K, Ishihara A, Sakaguchi N, Nishino S, Parada RY, Nakagiri A, Otani H (2015) Antifungal activity of volatile compounds produced by an edible mushroom Hypsizygus marmoreus against phytopathogenic fungi. J Phytopathol 163(11/12):987–996. https://doi.org/10.1111/jph.12405

    Article  CAS  Google Scholar 

  • Oliva J, Messal M, Wendt L, Elfstrand M (2017) Quantitative interactions between the biocontrol fungus Phlebiopsis gigantea, the forest pathogen Heterobasidion annosum and the fungal community inhabiting Norway spruce stumps. For Ecol Manag 402:253–264. https://doi.org/10.1016/j.foreco.2017.07.046

    Article  Google Scholar 

  • Owaid MN, Al Saeedi SSS, Abed IA, Shahbazi P, Sabaratnam V (2016) Antifungal activities of some Pleurotus species (higher basidiomycetes). Walailak J Sci Tech 14(3):215–224

    Google Scholar 

  • Paramanandham P, Rajkumari J, Pattnaik S, Busi S (2017) Biocontrol potential against Fusarium oxysporum f. sp. lycopersici and Alternaria solani and tomato plant growth due to plant growth—promoting Rhizobacteria. Int J Veg Sci 23(4):294–303. https://doi.org/10.1080/19315260.2016.1271850

    Article  Google Scholar 

  • Pereira E, Santos A, Reis F, Tavares RM, Baptista P, Lino-Neto T, Almeida-Aguiar C (2013) A new effective assay to detect antimicrobial activity of filamentous fungi. Microbiol Res 168(1):1–5. https://doi.org/10.1016/j.micres.2012.06.008

    Article  CAS  PubMed  Google Scholar 

  • Petre CV, Dîrțu AC, Niculaua M, Tănase C (2017) Volatile compounds in the aroma of three species of wood-rotting basidiomycetes and their antifungal potential. J Plant Dev 24:73–83

    Google Scholar 

  • Prajapati HN, Panchal RK, Patel ST (2014) Efficacy of bioagents and biological interaction of Alternaria solani with phylloplane mycoflora of tomato. J Mycopathol Res 52(1):81–86

    Google Scholar 

  • Qi QY, Bao L, Ren JW, Han JJ, Zhang ZY, Li Y, Yao YJ, Cao R, Liu HW (2014) Sterhirsutins A and B, two new heterodimeric sesquiterpenes with a new skeleton from the culture of Stereum hirsutum collected in Tibet Plateau. Org Lett 16(19):5092–5095. https://doi.org/10.1021/ol502441n

    Article  CAS  PubMed  Google Scholar 

  • Radhajeyalakshmi R, Velazhahan R, Prakasam V (2012) In vitro evaluation of solvent extracted compounds from edible macromycetes against phytopathogenic fungi. Arch Phytopathol Plant Prot 45(3):293–300. https://doi.org/10.1080/03235408.2011.559048

    Article  Google Scholar 

  • Ramos-Sandoval RU, Gutiérrez-Soto JG, Rodríguez-Guerra R, Salcedo-Martínez SM, Hernández-Luna CE, Luna-Olvera HA, Jiménez-Bremont JF, Fraire-Velázquez S, León A, Humberto I (2010) Antagonismo de dos ascomicetos contra Phytophthora capsici Leonian, causante de la marchitez del chile (Capsicum annuum L.). Rev Mex Fitopatol 28(2):75–86

    Google Scholar 

  • Robles CA, Ceriani-Nakamurakare E, Slodowicz M, González-Audino P, Carmarán CC (2018) Granulobasidium vellereum (Ellis &Cragin) Jülich, a promising biological control agent. Biol Control 117:99–108. https://doi.org/10.1016/j.biocontrol.2017.10.012

    Article  Google Scholar 

  • Sarkar S, Beura SK, Nandi A, Das S, Dash SK, Senapati N, Pandey G, Patnaik A (2016) Management of Early blight of tomato (Alternaria solani Ellis and Martin) by chemicals and biocontrol agents under field condition. J Mycopathol Res 54(1):81–84. https://www.cabdirect.org/cabdirect/abstract/20163253747

    Google Scholar 

  • Schüffler A (2018) Secondary metabolites of basidiomycetes. In: Physiology and Genetics. Springer, Cham, pp 231–275

    Chapter  Google Scholar 

  • Senatore F (1988) Chemical constituents of some species of Agaricaceae. Biochem Syst Ecol 16(7/8):601–604. https://doi.org/10.1016/0305-1978(88)90070-1

    Article  CAS  Google Scholar 

  • Shen JW, Ma BJ, Li W, Yu HY, Wu TT, Ruan Y (2009) Activity of armillarisin B in vitro against plant pathogenic fungi. Z Naturforsch C 64(11/12):790–792. https://doi.org/10.1515/znc-2009-11-1206

    Article  CAS  PubMed  Google Scholar 

  • Sivanandhan S, Khusro A, Paulraj MG, Ignacimuthu S, AL-Dhabi NA (2017) Biocontrol properties of basidiomycetes: an overview. J Fungi 3(1):2. https://doi.org/10.3390/jof3010002

    Article  CAS  Google Scholar 

  • Survilienë E (2002) Reaction of micromycetes to antagonistic organisms and fungicides in substrate. Biologija 1:14–17

    Google Scholar 

  • Tonucci-Zanardo NM, Pascholati SF, Di Piero RM (2015) In vitro antimicrobial activity of aqueous extracts from Lentinula edodes isolates against Colletotrichum sublineolum and Xanthomonas axonopodis pv. Passiflorae. Summa Phytopathol 4(1):13–20. https://doi.org/10.1590/0100-5405/1995

    Article  Google Scholar 

  • Vahidi H, Kobarfard F, Namjoyan F (2004) Effect of cultivation conditions on growth and antifungal activity of Mycena leptocephala. Afr J Biotechnol 3(11):606–609

    CAS  Google Scholar 

  • Varma PK, Gandhi SK, Surender S (2008) Biological control of Alternaria solani, the causal agent of early blight of tomato. J Biol Control 22(1):67–72

    Google Scholar 

  • Verma A, Kumar S, Shina HA, Jaiswal S (2018) Evaluate the efficacy of bio-control agents and botanicals against early blight of potato caused by Alternaria solani. Pharma Innov J 7(3):28–30

    CAS  Google Scholar 

  • Ying WU, Lu-dan HO, Jie ZH (2016) Inhibitory effects of metabolites from eight strains of Bacillus, Aspergillus, and Streptomyces on Alternaria solani. Jiangsu J Agric Sci 2:9

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Universidad Autónoma de Nuevo León, Facultad de Agronomía, Francisco Villa S/N., Col. Ex Hacienda El Canadá, ZP. 66050, General Escobedo, Nuevo León, Mexico

    Jesús S. Hernández-Ochoa, Guillermo Niño-Medina, Iosvany López-Sandin & Guadalupe Gutiérrez-Soto

  2. Micología Experimental, Dpto. de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428, Ciudad Autónoma de Buenos Aires, Argentina

    Laura N. Levin

  3. Universidad Autónoma de Nuevo León, Facultad de Ciencias Biológicas, Pedro de Alba S/N., Ciudad Universitaria, ZP. 66455, San Nicolás de los Garza, Nuevo León, Mexico

    Carlos E. Hernández-Luna, Juan Francisco Contreras-Cordero & Abelardo Chávez-Montes

Authors
  1. Jesús S. Hernández-Ochoa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura N. Levin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carlos E. Hernández-Luna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan Francisco Contreras-Cordero
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guillermo Niño-Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Abelardo Chávez-Montes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Iosvany López-Sandin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Guadalupe Gutiérrez-Soto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guadalupe Gutiérrez-Soto.

Ethics declarations

Conflict of interest

J.S. Hernández-Ochoa, L.N. Levin, C.E. Hernández-Luna, J.F. Contreras-Cordero, G. Niño-Medina, A. Chávez-Montes, I. López-Sandin and G. Gutiérrez-Soto declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hernández-Ochoa, J.S., Levin, L.N., Hernández-Luna, C.E. et al. Antagonistic Potential of Macrolepiota sp. Against Alternaria Solani as Causal Agent of Early Blight Disease in Tomato Plants. Gesunde Pflanzen 72, 69–76 (2020). https://doi.org/10.1007/s10343-019-00484-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10343-019-00484-4

Keywords

Schlüsselwörter

Search

Navigation