Skip to main content
SpringerLink
Log in

Trichoderma spp. isolates from the rhizosphere of healthy olive trees in northern Algeria and their biocontrol potentials against the olive wilt pathogen, Verticillium dahliae

  • Original research paper
  • Published:
Organic Agriculture Aims and scope Submit manuscript

Abstract

Trichoderma species are known for their ability to control many plant diseases. In this study, fifteen (T1–T15) indigenous strains of Trichoderma spp. isolated from rhizosphere soils of olive in northern Algeria were investigated for their biocontrol potential against eleven strains of Verticillium dahliae, the causal agent of wilting on olive (Olea europea cv. europea L.). Direct and indirect confrontation assays were performed to investigate if isolates of Trichoderma affect mycelium growth. In addition, gas chromatography–mass spectroscopy (GC–MS) was applied to identify the volatile organic compounds (VOCS) produced by the T2 isolate. Besides, Trichoderma isolates were screened for the production of extracellular enzymes on solid medium including chitinases, proteasesand cellulases. Results showed that Trichoderma isolates demonstrated an effective potential in reducing mycelium growth against V. dahliae in vitro. T12 was the highest antagonistic of the Trichoderma isolates by direct confrontation assay method. This isolate exhibited an average inhibition rate of 68.86% against V. dahliae isolates, whereas the evaluation of volatile metabolites effect revealed that inhibition percentage of radial growth varies between 55.26 and 65.93%. Importantly, results showed the presence of 33 compounds detected in the methanolic and hexanic fraction of T2 isolate, including important volatile compounds with antifungal activities such as Undecane, Octadecane, Eicosane, 13-Docosenamide, (Z), Hexadecanamide, 9-Octadecenamide, (Z), Cyclopentanone, 2-methyl, Tetradecanoic acid, propyl ester, Tetradecanoic acid, oleic acid, and n-Hexadecanoic acid. Interestingly, all isolates tested showed chitinolytic, proteolytic and cellulolytic activity. T2 and T12 were the effective Trichoderma isolates showing high chitinase production on solid medium. Besides that, isolates T2 and T6 demonstrated the highest chitinolytic and proteolytic activity with values 0.043 µmol/ml/min and 0.019 µmol/ml/min, respectively. Overall, the isolates, T2, T6, and T12 are the most effective agents against olive wilt pathogen V. dahliae in vitro. Hence, they could be further investigated for biocontrol of olive wilt in vivo.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aarti T, Meenu S (2015) Role of volatile metabolites from Trichoderma citrinoviride in biocontrol of phytopathogens. Int J Res Chem Environ 5:86–95

    Google Scholar 

  • Agrawal T, Kotasthane AS (2012) Chitinolytic assay of indigenous Trichoderma isolates collected from different geographical locations of Chhattisgarh in Central India. Springerplus 1(1):73

    Article  PubMed  PubMed Central  Google Scholar 

  • Akintokun AK, Akande GA, Akintokun PO, Popoola TOS, Babalola AO (2007) Solubilization on insoluble phosphate by organic acid-producing fungi isolated from Nigerian soil. Int J Soil Sci 2(4):301–307. https://doi.org/10.3923/ijss.2007.301.307

    Article  CAS  Google Scholar 

  • Amira MB, Lopez D, Mohamed AT, Khouaja A, Chaar H, Fumanal B, Ribeiro S (2017) Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees. Biol Control 110:70–78

    Article  Google Scholar 

  • Anees MR, Azim S, Ur Rehman M, Jamil S, El Hendawy NA, Al Suhaiban NA (2018) Antifungal potential of Trichoderma strains originated from North Western regions of Pakistan against the plant pathogens. Pak J Bot 50(5):2031–2040

    CAS  Google Scholar 

  • Anita S, Ponmurugan P, Ganesh Babu R (2012) Significance of secondary metabolites and enzymes secreted by Trichoderma atroviride isolates for the biological control of phomopsis canker disease. Afr J Biotech 11(45):10350–10357. https://doi.org/10.5897/ajb12.599

    Article  CAS  Google Scholar 

  • Anke H, Kinn J, Bergquist KE, Sterner O (1991) Production of siderophores by strains of the genusTrichoderma. Biol Met 4(3):176–180

    Article  CAS  Google Scholar 

  • Bach E, Seger GD, dos S, Fernandes G, de C, Lisboa BB, Passaglia LMP (2016) Evaluation of biological control and rhizosphere competence of plant growth promoting bacteria. Appl Soil Ecol 99:141–149

    Article  Google Scholar 

  • Bakker AW, Schippers B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp.-mediated plant growth-stimulation. Soil Biol Biochem 19:451–457

    Article  CAS  Google Scholar 

  • Bedine Boat MA, Sameza ML, Iacomi B, Tchameni SN, Boyom FF (2020) Screening, identification and evaluation of Trichoderma spp. for biocontrol potential of common bean damping-off pathogens. Biocontrol Science and Technology 30(3):228–242

    Article  Google Scholar 

  • Benhamou N, Chet I (1996) Parasitism of sclerotia of Sclerotium rolfsii by Trichoderma harzianum: ultrastructural and cytochemical aspects of the interaction. Phytopathology 86:405–416

    Article  Google Scholar 

  • Berg G, Krechel A, Ditz M, Sikora RA, Ulrich A, Hallmann J (2002) Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51(2):215–229

    Article  Google Scholar 

  • Bissett J (1984) A revision of the genus Trichoderma. I. Section Longibrachiatum sect. nov. Can J Bot 62(5):924–931

    Article  Google Scholar 

  • Bissett J (1991a) A revision of the genus Trichoderma. II. Infrageneric classification. Can J Bot 69(11):2357–2372

    Article  Google Scholar 

  • Bissett J (1991b) A revision of the genus Trichoderma. III. Section Pachybasium. Canadian journal of botany, 69(11), 2373–2417.

  • Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indole acetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burke BA, Nair MG (1989) Antimicrobial/antifungal compositions. United States Utility Patent, US4876277

  • Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91(3):553–556

    Article  CAS  Google Scholar 

  • Carrero-Carrón I, Trapero-Casas JL, Olivares-García C, Monte E, Hermosa R, Jiménez-Díaz RM (2016) Trichoderma asperellum is effective for biocontrol of Verticillium wilt in olive caused by the defoliating pathotype of Verticillium dahliae. Crop Prot 88:45–52

    Article  Google Scholar 

  • Chaverri P, Castlebury LA, Overton BE, Samuels GJ (2003) Hypocrea/Trichoderma: species with conidiophore elongations and green conidia. Mycologia 95:1100–1140

    Article  PubMed  Google Scholar 

  • Cherukupally R, Amballa H, Reddy BN (2017) In vitro screening for enzymatic activity of Trichoderma species for biocontrol potential. Ann Plant Sci 6:1784–1789

    Article  Google Scholar 

  • Chet I, Inbar J, Hadar I (1997) Fungal antagonists and mycoparasites. The mycota IV: environmental and microbial relationships. Springer-Verlag, Berlin, 165–184

  • Choi IY, Hong SB, Yadav MC (2003) Molecular and morphological characterization of green mold, Trichoderma spp isolated from oyster mushrooms. Mycobiology 31(2):74–80

    Article  CAS  Google Scholar 

  • Coley-Smith JR, Ridout CJ, Mitchell CM, Lynch JM (1991) Control of button rot of lettuce (Rhizoctonia solani) using preparations of Trichoderma viride, T. Harzianum or toclofos-methyl. Plant Path 40(3):359–366

    Article  Google Scholar 

  • Collado-Romero M, Mercado-Blanco J, Olivares-García C, Valverde-Corredor A, Jiménez-Díaz RM (2006) Molecular variability within and among Verticillium dahliae vegetative compatibility groups determined by fluorescent amplified fragment length polymorphism and polymerase chain reaction markers. Phytopathology 96(5):485–495

    Article  CAS  PubMed  Google Scholar 

  • Debbi A, Boureghda H, Monte E, Hermosa R (2018) Distribution and genetic variability of Fusarium oxysporum associated with tomato diseases in algeria and a biocontrol strategy with indigenous Trichoderma spp. front. Microbiol 9:282. https://doi.org/10.3389/fmicb.2018.00282

    Article  Google Scholar 

  • de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Saber MK, Thomma BP (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci 109(13):5110–5115

    Article  PubMed  PubMed Central  Google Scholar 

  • De la Cruz-Quiroz R, Roussos S, Rodríguez-Herrera R, Hernandez-Castillo D, Aguilar CN (2018) Growth inhibition of Colletotrichum gloeosporioides and Phytophthora capsici by native Mexican Trichoderma strains. Karbala International Journal of Modern Science 4(2):237–243

    Article  Google Scholar 

  • Dennis C, Webster J (1971) Antagonistic properties of species-groups of Trichoderma. Trans Br Mycol Soc 57:41–48. https://doi.org/10.1016/s0007-1536(71)80078-5

    Article  CAS  Google Scholar 

  • Díaz RJ, Casas JT, Boned J, Landa BB, Cortés JN (2009) Uso de Bioten para la protección biológica de plantones de olivo contra la Verticilosis causada por el patotipo defoliante de Verticillium dahliae. Boletín De Sanidad Vegetal Plagas 35(4):595–615

    Google Scholar 

  • Dubey SC, Tripathi A, Dureja P, Grover A (2011) Characterization of secondary metabolites and enzymes produced by Trichoderma species and their efficacy against plant pathogenic fungi. Indian J Agric Res 81(5):455–461

    CAS  Google Scholar 

  • Elad Y, Williamson B, Tudzynski P, Delen N (2004) Botrytis spp. and diseases they cause in agricultural systems- an introduction. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds) Botrytis, Biology, Pathology and Control. Kluwer Academic Publishers, Netherland, pp 1–8

    Google Scholar 

  • El-Katatny M, Abdelzaher H, Shoulkamy M (2006) Antagonistic actions of Pythium oligandrum and Trichoderma harzianum against phytopathogenic fungi (Fusarium oxysporum and Pythium ultimum var. ultimum). Arch Phytopathol Plant Prot 39(4):289–301. https://doi.org/10.1080/03235400500222396

    Article  Google Scholar 

  • El-Mougy NS, Abdel-Kader MM (2018) Biocontrol measures against onion basal rot incidence under natural field conditions. J Plant Pathol. https://doi.org/10.1007/s42161-018-00237-8

    Article  Google Scholar 

  • Elsherbiny EA, Amin BH, Aleem B, Kingsley KL, Bennett JW (2020) Trichoderma volatile organic compounds as a biofumigation tool against late blight pathogen Phytophthora infestans in postharvest Potato tubers. J Agric Food Chem 68(31):8163–8171

    Article  CAS  PubMed  Google Scholar 

  • El-Sobky MA, Fahmi AI, Eissa RA, El-Zanaty AM (2019) Genetic characterization of Trichoderma spp. isolated from different locations of Menoufia Egypt and assessment of their Antagonistic Ability. J Microb Biochem Technol, 11(1).

  • Ertas A, Yilmaz MA, Firat M (2014) Chemical profile by LC-MS/MS, GC/MS and antioxidant activities of the essential oils and crude extracts of two Euphorbia species. Nat Prod Res 3:1–6

    Google Scholar 

  • Fradin EF, Thomma B (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. alboatrum. Mol Plant Pathol 7(2):71–86. https://doi.org/10.1111/j.1364-3703.2006.00323.x

    Article  CAS  PubMed  Google Scholar 

  • Gams W, Bissett J (1998) Morphology and identification of trichoderma In: Kubicek CP and Harman GE, Eds., Trichoderma and Gliocladium: Basic Biology, Taxonomy and Genetics. London: Taylor& Francis Led, 1, 3–34.

  • Gams W, Bissett J (2002) Morphology and identification of. Trichoderma and Gliocladium, 3–31.

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118

    Article  CAS  PubMed  Google Scholar 

  • Gharbi Y, Triki MA, Trabelsi R, Fendri I, Daayf F, Gdoura R (2015) Genetic structure of Verticillium dahliae isolates infecting olive tree in Tunisia using AFLP, Pathogenicity and PCR markers. Plant Pathol 64:871–879

    Article  Google Scholar 

  • Ghosh SK, Banerjee S, Sengupta C (2017) Bioassay, characterization and estimation of siderophores from some important antagonistic fungi. J Biopest 10(2):105–112

    Article  CAS  Google Scholar 

  • Gibka AJ, Styczynska K (2009) Glinski M (2009) Antimicrobial activity of undecan-3-one, undecan-3-ol and undec-3-yl acetate. Centr Eur J Immunol 34:154–157

    CAS  Google Scholar 

  • Gupta RR, Singal R, Shanker A, Kuhad RC, Saxena RK (1994) A modified plate assay for screening phosphate solubilizing microorganisms. J Gen Appl Microbiol 40:255–260

    Article  CAS  Google Scholar 

  • Hajiegharai B, Torabi-giglou M, Mohammadi MR, Davari M (2008) Biological potential of some Iranian Trichoderma isolates in the control of soil born plant pathogenic fungi. Afr J Biotech 7(8):967–972

    Google Scholar 

  • Hankin L, Anagnostakis SL (1975) The use of solid media for detection of enzyme production by fungi. Mycologia 67:597–607

    Article  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  CAS  PubMed  Google Scholar 

  • Hemerly A (2016) Genetic controls of biomass increase in sugarcane by association with beneficial nitrogen-fixing bacteria. Plant and Animal Genome Conference XXIV. Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

  • Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25

    Article  CAS  PubMed  Google Scholar 

  • Hernandez Castillo FD, Berlanga Padilla AM, Gallegos Morales G, Cepeda Siller M, Rodriguez Herrera R, Aguilar Gonzales CN, Castillo Reyes F (2011) In vitro antagonist action of Trichoderma strains against Sclerotinia sclerotiorum and Sclerotium cepivorum. Am J Agric Biol Sci 6(3):410–417

    Article  Google Scholar 

  • Howe TGB, Ward JM (1976) The utilization of Tween 80 as carbon source by pseudomonas B. J G Microbiol 92:234–235

    Article  CAS  Google Scholar 

  • Hoyos-Carvajal L, Orduz S, Bissett J (2009) Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biol Control 51:409–416

    Article  Google Scholar 

  • Hsouna AB, Trigie M, Mansour RB, Jarraya RM, Damak M, Jaoua S (2011) Chemical composition, cytotoxicity effect and antimicrobial activity of Ceratonia siliqua essential oil with preservative effects against listeria inoculated in minced beef meat. Int J Food Microbiol 148(1):66–72

    Article  PubMed  Google Scholar 

  • Huang XQ, Zhang N, Yong XY, Yang XM, Shen QR (2012) Biocontrol of Rhizoctonia solani damping-off disease in cucumber with Bacillus pumilus SQR-N43. Microbiol Res 167:135–143

    Article  CAS  PubMed  Google Scholar 

  • Intana W, Kheawleng S, Sunpapao A (2021) Trichoderma asperellum T76–14 released volatile organic compounds against postharvest fruit rot in muskmelons (Cucumis melo) caused by Fusarium incarnatum. J Fungi 7(1):46

    Article  CAS  Google Scholar 

  • Isaias CO, Martins I, Silva JBT, Silva JP, Mello SCM (2014) Ação antagônica e de metabólitos bioativos de Trichoderma spp contra os patógenos Sclerotium rolfsii e Verticillium dahliae. Summa Phytopathol 40:(1)34–41

  • Islam MM, Hossain DM, Rahman MME, Suzuki K, Narisawa T, Hossain I, Harada N (2016) Native Trichoderma strains isolated from Bangladesh with broad spectrum antifungal action against fungal phytopathogens. Archives of Phytopathology and Plant Protection 49(1–4):75–93

    Article  CAS  Google Scholar 

  • Jamdar Z, Mohammadi AH, Mohammadi S (2013) Study of antagonistic effects of Trichoderma species on growth of Verticillium dahliae, the causal agent of Verticillium wilt of pistachio under laboratory condition. J Nuts 4(4):53–56

    Google Scholar 

  • Jie WG, Bai L, Yu WJ, Cai BY (2015) Analysis of interspecific relationships between Funneliformis mosseae and Fusarium oxysporum in the continuous cropping of soybean rhizosphere soil during the branching period. Biocontrol Sci Technol 25:1036–1051

    Article  Google Scholar 

  • Jiménez-Díaz RM, Cirulli M, Bubici G, Jiménez-Gasco MM, Antoniou PP, Tjamos EC (2012) Verticillium wilt: a major threat to olive production current status and future prospects for its management. Plant Dis 96:304–329

    Article  PubMed  Google Scholar 

  • Johnson LF, Curl EH (1972) Methods for research on the ecology of soil borne plant pathogens. Burgress Publishing Co., Minneapolis: pp.v+247

  • Kamala TH, Indira S (2012) Biocontrol propreties of indigenous Trichoderma isolates from North-east India against Fusarium oxysporum and Rhizoctonia Solani. Afr J Biotechnol 11(34):8491–8499. https://doi.org/10.5897/AJB11.1938

    Article  CAS  Google Scholar 

  • Karanja E, Boga H, Muigai A, Wamunyokoli F, Kinyua J, Nonoh J (2012) Growth characteristics and production of secondary metabolites from selected novel Streptomyces species isolated from selected Kenyan national parks. In: Scientific conference proceeding

  • Keswani C, Mishra S, Sarma BK (2014) Unraveling the efficient application of secondary metabolites of various Trichoderma. Appl Microbiol Biotechnol 98:533–544

    Article  CAS  PubMed  Google Scholar 

  • Khethr FBH, Ammar S, Saïdana D, Daami M, Chriaa J, Liouane K, Mahjoub MA, Helal AN, Mighri Z (2008) Chemical composition, antibacterial and antifungal activities of Trichoderma sp. growing in Tunisia. Ann Microbiol 58:303. https://doi.org/10.1007/BF03175334

    Article  CAS  Google Scholar 

  • Kubicek CP, Mach RL, Peterbauer CK, Lorito M (2001) Trichoderma: from genes to biocontrol. J Plant Pathol 83:11–23

    CAS  Google Scholar 

  • Kumar PP, Kumaravel S, Lalitha C (2010) Screening of antioxidant activity, total phenolics and GC-MS study of Vitexnegundo. Afr J Biochem Res 4(7):191–195

    Google Scholar 

  • Lalngaihawmi, Bhattacharyya A (2019) Study on the different modes of action of potential Trichoderma spp from banana rhizosphere against Fusarium oxysporum fsp cubense. Int J Curr Microbiol App Sci 8(01):1028–1040. https://doi.org/10.20546/ijcmas.2019.801.112

    Article  CAS  Google Scholar 

  • Lee JT, Bae DW, Park SH, Shim CK, Kwak YS, Kim HK (2001) Occurrence and biological control of postharvest decay in onion caused by fungi. Plant Pathol J 17(3):141–148

    Google Scholar 

  • Li YT, Hwang SG, Huang YM, Huang CH (2018a) Effects of Trichoderma asperellum on nutrient uptake and Fusarium wilt of tomato. Crop Prot 110:275–282

    Article  CAS  Google Scholar 

  • Li Z, Wang T, Luo X, Li X, Xia C, Zhao Y, Cui Z (2018b) Biocontrol potential of Myxococcus sp. strain BS against bacterial soft rot of calla lily caused by Pectobacterium carotovorum. Biol Control 126:36–44

    Article  Google Scholar 

  • López AC, Alvarenga AE, Zapata PD, Luna MF, Villalba LL (2019) Trichoderma spp. from Misiones, Argentina: effective fungi to promote plant growth of the regional crop Ilexparaguariensis St. Hil, Mycology. https://doi.org/10.1080/21501203.2019.1606860

  • López-Escudero FJ, Mercado-Blanco J (2011) Verticillium wilt of olive: a case study to implement an integrated strategy to control soil-borne pathogen. Plant Soil 344:1–50. https://doi.org/10.1007/s11104-010-0629-2

    Article  CAS  Google Scholar 

  • Lunge AG, Patil AS (2012) Characterization of efficient chitinolytic enzyme producing Trichoderma species: a tool for better antagonistic approach. Int J Sci Environ Technol 1(5):377–385

    Google Scholar 

  • Marques E, Martins I, Mello SCM (2017) Antifungal potential of crude extracts of Trichoderma spp. Biota Neotrop 18(1):0418. https://doi.org/10.1590/1676-0611-BN-2017-0418

    Article  Google Scholar 

  • Meena M, Swapnil P, Zehra A, Dubey MK (2017) Antagonistic assessment of Trichoderma spp. by producing volatile and non-volatile compounds against different fungal pathogens. Arch Phytopathol Plant Prot 50(14):629–648

    Article  CAS  Google Scholar 

  • Meera T, Balabaskar P (2012) Isolation and characterization of Pseudomonas fluorescens from rice fields. Int J Food Agric Vet Sci 2(1):113–120

    Google Scholar 

  • Mercado-Blanco J, Rodríguez-Jurado D, Parrilla-Araujo S, Jiménez-Díaz RM (2003) Simultaneous detection of the defoliating and nondefoliating Verticillium dahliae pathotypes in infected olive plants by duplex, nested polymerase chain reaction. Plant Dis 87(12):1487–1494

    Article  CAS  PubMed  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Mohiddin FA, Bashir I, Padder SA, Hamid B (2017) Evaluation of different substrates for mass multiplication of Trichoderma species. J Pharmacogn Phytochem 6(6):563–569

    CAS  Google Scholar 

  • Moraga-Suazo P, Opazo A, Zaldúa S, González G, Sanfuentes E (2011) Evaluation of Trichoderma spp. and Clonostachys spp. strains to control Fusarium circinatum in Pinus radiate Seedlings. Chilean J Agric Res 71:412–417

    Article  Google Scholar 

  • Moya P, Girotti JR, Toledo A, Sisterna MN (2018) Antifungal activity of Trichoderma VOCs against Pyrenophora teres, the causal agent of barley net blotch. J Plant Protect Res 58:45–53

    CAS  Google Scholar 

  • Murthy N, Bleakley B (2012) Simplified method of preparing colloidal chitin used for screening of chitinaseproducing microorganisms. Internet J Microbiol, 10(2), e2bc3.

  • Naing KW, Anees M, Kim SJ, Nam Y, Kim YC, Kim KY (2014) Characterization of antifungal activity of Paenibacillus ehimensis KWN38 against soilborne phytopathogenic fungi belonging to various taxonomic groups. Ann Microbiol 64(1):55–63

    Article  CAS  Google Scholar 

  • Nandhini SU (2015) Gas chromatography–mass spectrometry analysis of bioactive constituents from the marine Streptomyces. Asi J Pharm Clin Res 8:244–246.Ng LC, Ngadin A, Azhari M, Zahari NA (2015) Potential of Trichoderma spp. as biological control agents against bakanae pathogen (Fusarium fujikuroi) in rice. Asian J Plant Pathol 9:46–58

    Google Scholar 

  • Noori MSS, Saud HM (2012) Potential plant growth-promoting activity of Pseudomonas sp. isolated from paddy soil in Malaysia as biocontrol agent. J Plant Pathol Microbiol 3:120. https://doi.org/10.4172/2157-7471.1000120

    Article  CAS  Google Scholar 

  • Pegg GF, Brady BL (2002) Verticillium Wilts. CABI Publishing, New York

    Book  Google Scholar 

  • Pérez-Artés E, García-Pedrajas MD, Bejarano-Alcázar J, Jiménez-Díaz RM (2000) Differentiation of cotton-defoliating and nondefoliating pathotypes of Verticillium dahliae by RAPD and specific PCR analyses. Eur J Plant Pathol 106(6):507–517

    Article  Google Scholar 

  • Ratnakumari YR, Nagamani A, Bhramaramba S, Kumar R, Kumar U, Shaik M (2011) Non-volatile and volatile metabolites of antagonistic Trichoderma against collar rot pathogen of Mentha arvensis. Int J Pharm Biomed Res 2(2):56–58

    Google Scholar 

  • Pohl CH, Kock JL, Thibane VS (2011) Antifungal free fatty acids: a review. Sci Against Microb Pathog Curr Res Technol Adv 1:61–71

    Google Scholar 

  • Raza W, Yuan J, Wu YC, Rajer FU, Huang Q, Shen QR (2015) Biocontrol traits of two Paenibacillus polymyxa strains SQR-21 and WR-2 In response to fusaric acid, a phytotoxin produced by Fusarium species. Plant Pathol 64:1041–1052. https://doi.org/10.1111/ppa.12354

    Article  CAS  Google Scholar 

  • Rifai MA (1969) A revision of the genus Trichoderma. Mycol Pap 116:1–56

    Google Scholar 

  • Ruangwong OU, Wonglom P, Suwannarach N, Kumla J, Thaochan N, Chomnunti P, Sunpapao A (2021) Volatile organic compound from Trichoderma asperelloides TSU1: impact on plant pathogenic fungi. Journal of Fungi 7(3):187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Russell DW, Sambrook J (2001) Molecular cloning: a laboratory manual (Vol. 1, p. 112). Cold Spring Harbor Laboratory, Cold Spring Harbor

  • Samuels GJ (1996) Trichoderma: a review of biology and systematics of the genus. Mycol Res 100(8):923–935

    Article  Google Scholar 

  • Samuels GJ, Dodd SL, Gams W, Castlebury LA, Petrini O (2002) Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia 94(1):146–170

    Article  PubMed  Google Scholar 

  • Saravanakumar K, Arasu VS, Kathiresan K (2013) Effect of Trichoderma on soil phosphate solubilization and growth improvement of Avicennia marina. Aquat Bot 104:101–105. https://doi.org/10.1016/j.aquabot.2012.09.001

    Article  CAS  Google Scholar 

  • Schirmböck M, Lorito M, Wang YL, Hayes CK, Arisan-Atac I, Scala F, Kubicek CP (1994) Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol 60(12):4364–4370

    Article  PubMed  PubMed Central  Google Scholar 

  • Shah S, Nasreen S, Sheikh PA (2012) Cultural and morphological characterization of Trichoderma spp. associated with green mold disease of Pleurotus spp In Kashmir. Res J Microbiol 7:139–144

    Article  Google Scholar 

  • Shahzad M, Nadeem A, Muhammad A, Shafiq UR, Muhammad A, Lixin Z, Muhammad A (2019) Chitinolytic activity of the indigenous trichoderma spp. from the north west of pakistan against the fungal phytopathogens. Pak J Bot 51(2). https://doi.org/10.30848/PJB2(37)

  • Sharmila M, Rajeswari M, Jayashree I (2017) GC-MS analysis of bioactive compounds in the whole plant of ethanolic extract of Ludwigia perennisL. Int J Pharm Sci Rev Res 46(1):124–128

    CAS  Google Scholar 

  • Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43

    Article  CAS  PubMed  Google Scholar 

  • Siddiquee S, Cheong BE, Taslima K, Kausar H, Hasan MdM (2012) Separation and identification of volatile compounds from liquid cultures of Trichoderma harzianum by GC-MS using three different capillary columns. J Chromatogr Sci 50:358–367

    Article  CAS  PubMed  Google Scholar 

  • Singh HB, Singh BN, Singh SP (2012) Exploring different avenues of Trichoderma as a potent bio-fungicidal and plant growth promoting candidate-an overview. Rev Plant Pathol 5:315–426

    Google Scholar 

  • Sivan A, Elad Y, Chet I (1984) Biological control effects of a new isolate of Trichoderma harzianum on Pythium aphanidermatum. Phytopathology 74(4):498–501

    Article  Google Scholar 

  • Sivasithamparam K, Ghisalberti EL (1998) Secondary metabolism in Trichoderma and Gliocladium. Vol. 1, London 139–192

  • Sohrabi M, Zhang L, Zhang K, Ahmetagic A, Wei MQ (2014) Volatile organic compounds as novel markers for the detection of bacterial infections. Clin Microbiol Open Acc 3:151

    Google Scholar 

  • Song M, Yun HY, Kim YH (2014) Antagonistic Bacillus species as a biological control of ginseng root rot caused by Fusarium cf. incarnatum. J Gins Res 38:136–145

    Article  Google Scholar 

  • Thrane C, Jensen DF, Tronsmo A (2000) Substrate colonization, strain competition, enzyme production in vitro, and Biocontrol of Pythium ultimum by Trichoderma spp. Isolates P1 and T3. Eur J Plant Pathol 106:215–225. https://doi.org/10.1023/A:1008798825014

    Article  CAS  Google Scholar 

  • Tondje PR, Roberts DP, Bon MC, Widner T, Samuels GL, Ismaiel A, Begoude AD, Tchana T, Nyemb-Tshomb E, Ndounbe-Nkeng M, Bateman R, Fontem D, Hebbar KP (2007) Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon. Biol Control 43:202–212

    Article  Google Scholar 

  • Vey A, Hoagland RE, Butt TM (2001) Toxic metabolites of fungal biocontrol agents. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CAB International, Bristol, pp 311–346

    Chapter  Google Scholar 

  • Vinale F, Nigro M, Sivasithamparam K, Flematti G, Ghisalberti EL, Ruocco M, Varlese R, Marra R, Lanzuise S, Eid A, Woo SL, Lorito M (2013) Harzianic acid: a novel siderophore from Trichoderma harzianum. FEMS Microbiol Lett 347:123–129

    CAS  PubMed  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL, Woo SL, Nigro M, Marra R, Lombardi N, Pascale A, Ruocco M, Lanzuise S, Manganiello G, Lorito M (2014) Trichoderma secondary metabolites active on plants and fungal pathogens. Open Mycol J 8:127–139

    Article  Google Scholar 

  • Whipps JM (1997) Ecological considerations involved in commercial development of biological control agents for soil-borne diseases. Modern soil microbiology., 525-546.

  • Whipps JM, Lumsden RD (2001) Commercial use of fungi as plant disease biological control agents: status and prospects. Fungal biocontrol agents: progress, problems and potential, 9-22.

  • You J, Zhang J, Wua M, Yang L, Chen W, Li G (2016) Multiple criteria-based screening of Trichoderma isolates for biological control of Botrytis cinerea on tomato. Biol Control 101:31–38

    Article  Google Scholar 

  • Zhang F, Chen C, Zhang F, Gao L, Liu G, Chen L, Fan X, Liu C, Zhang K, He Y, Chen C, Ji X (2017) Trichoderma harzianum containing1-aminocyclopropane-1-carboxylate deaminase and chitinase improved growth and diminished adverse effect caused by Fusarium oxysporum in soybean. J Plant Physiol 210:84–94

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Valorization and Conservation of Biological Resources, Department of Biology, University of M’hamed Bougara, Boumerdes, Algeria

    Abdenaceur Reghmit, Farida Benzina-tihar, Fatma Halouane-Sahir, Zahia Oukali & Nourelhouda Ghozali

  2. Escuela Técnica Superior of Agricultural and Forestry Engineers, Department of Agronomy, University of Córdoba, University Campus of Rabanales, Celestino Mutis Building (C4), 14071, Córdoba, Spain

    Francisco Javier López Escudero

  3. Department of Biological Sciences, Faculty of Nature, Life and Earth Sciences, Akli Mohand Oulhadj University, 10000, Bouira, Algeria

    Souhila Bensmail

Authors
  1. Abdenaceur Reghmit
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Farida Benzina-tihar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francisco Javier López Escudero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fatma Halouane-Sahir
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zahia Oukali
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Souhila Bensmail
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nourelhouda Ghozali
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdenaceur Reghmit.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reghmit, A., Benzina-tihar, F., López Escudero, F. et al. Trichoderma spp. isolates from the rhizosphere of healthy olive trees in northern Algeria and their biocontrol potentials against the olive wilt pathogen, Verticillium dahliae. Org. Agr. 11, 639–657 (2021). https://doi.org/10.1007/s13165-021-00371-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13165-021-00371-1

Keywords

Search

Navigation