Biological control of Verticillium wilt and growth promotion in peach by endophytic and rhizospheric soil fungi from stone fruit trees

Document Type : Original Article

Authors

1 Department of Plant Protection, College of Agriculture, Bu-Ali Sina University, Hamedan, Iran

2 Department of Plant Protection, Faculty of Crop Science, Sari Agricultural Sciences and Natural Resources University, Sari, Iran.

3 Department of Soil Science, College of Agriculture, Bu-Ali Sina University, Hamedan, Iran

4 Department of Pathobiology, Faculty of Veterinary Sciences, Bu-Ali Sina University, Hamedan, Iran

10.22043/MI.2024.364757.1274

Abstract

Verticillium wilt of stone fruit trees caused by Verticillium dahliae occurs worldwide and causes serious economic losses. Control of Verticillium is difficult and costly due to its wide host range and resistant soil-borne microsclerotia. Also, increased concerns about agrochemicals have encouraged the development of biocontrol strategies. In this study, we evaluated antagonistic fungi for biocontrol of V. dahliae in vitro and greenhouse. A total of 85 endophytic and rhizospheric fungal isolates of peach and other stone fruit trees were isolated in the west Azarbaijan province, Iran. The identified fungi included Alternaria, Aspergillus, Aureobasidium, Clonostachys, Cryptococcus, Fusarium, Penicillium, and Trichoderma. The potential control of the isolates was initially evaluated by a dual culture assay. Furthermore, the antagonistic activity of fungi metabolites on the germination of microsclerotia both in vitro and in the soil was evaluated. In total, Trichoderma asperellum AE66 showed the highest inhibitory activity (73.85%) and was selected for greenhouse experiments. In the greenhouse assay on peach, T. asperellum AE66 not only reduced the progress of Verticillium wilt but also its severity. Moreover, the plant growth was promoted. These findings suggest that biocontrol provides a potentially effective strategy for the management of Verticillium wilt.

Keywords


Aleandri MP, Chilosi G, Bruni N, Tomassini A, Vettraino AM, Vannini A. 2015. Use of nursery potting mixes amended with local Trichoderma isolates with multiple complementary mechanisms to control soil-borne diseases. Crop Protection 67: 269-78.
Angelopoulou DJ, Naska EJ, Paplomatas EJ, Tjamos SE. 2014. Biological control agents (BCAs) of Verticillium wilt: influence of application rates and delivery method on plant protection, triggering of host defense mechanisms and rhizosphere populations of BCAs. Plant Pathology 63: 1062–1069.
Aranda S, Montes-Borrego M, Jiménez-Díaz RM, et al. 2011. Microbial communities associated with the root system of wild olives (Olea europaea L. subsp. europaea var. sylvestris) are good reservoirs of bacteria with antagonistic potential against Verticillium dahliae. Plant and Soil 343: 329–345.
Ausher R, Katan J, Ovadia S. 1975. An improved selective medium for the isolation of Verticillium dahliae. Phytoparasitica 3: 133-137.
Berg G, Fritze A, Roskot N, Smalla K. 2001. Evaluation of potential biocontrol rhizobacteria from different host plants of Verticillium dahliae Kleb. Journal of Applied Microbiology 91: 963–971.
Campbell CL, Madden LV. 1990. Introduction to Plant Disease Epidemiology. John Wiley, New York, USA. 531 p.
Carbone I, Kohn LM. 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553-556.
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 Protection 88: 45-52.
Chandelier A, Laurent F, Dantinne D, Mariage L, Etienne M, Cavelier M. 2003. Genetic and molecular characterization of Verticillium dahliae isolates from woody ornamentals in Belgian nurseries. European Journal of Plant Pathology 109: 943–952.
D’Ercole N, Nipoti P, Di Pillo L, Gavina F. 2000. In vitro and in vivo tests of Trichoderma spp. as a biocontrol agent of Verticillium dahliae Kleb. in eggplants. In: Advances in Verticillium: Research and Disease Management; Tjamos EC, Rowe RC, Heale JB, Fravel DR, Eds.; APS Press: St. Paul, MN, USA, 2000; pp. 260–263. 
Davet P. 1979. A technique for analyzing soil populations of Trichoderma spp. and Gliocladium virens. Annual Review of Phytopathology 11: 529-534.
Deketelaere S, Tyvaert L, França SC, Höfte M. 2017. Desirable traits of a good biocontrol agent against Verticillium wilt. Frontiers in Microbiology 8: 1186.
FAO 2023. Faostat, Production Statistics. http://faostat. fao.org.
Fradin EF, Thomma BP. 2006. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Molecular Plant Pathology 7: 71–86.
García M, Arriagada C, García-Romera I, Ocampo JA. 2011. Are plant cell wall hydrolysing enzymes of saprobe fungi implicated in the biological control of the Verticillium dahliae pathogenesis. Crop Protection 30: 85– 87.
Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61: 1323-30.
Hamim A, Miche L, Douaik A, Mrabet R, Ouhammou A, Duponnois R, Hafidi M. 2017. Diversity of fungal assemblages in roots of Ericaceae in two Mediterranean contrasting ecosystems. Comptes Rendus Biologies 340: 226-37.
Hawke M, Lazarovits G. 1994. Production and manipulation of individual microsclerotia of Verticillium dahliae for use in studies of survival. Phytopathology 84: 883-890.
Hermosa R, Viterbo A, Chet I, Monte E. 2012. Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158: 17e25.
Hong SB, Cho HS, Shin HD, Frisvad JC, Samson RA. 2006. Novel Neosartorya species isolated from soil in Korea. International Journal of Systematic and Evolutionary Microbiology 56: 477–486.
Inderbitzin P, Bostock RM, Davis RM, Usami T, Platt HW, Subbarao KV. 2011. Phylogenetics and taxonomy of the fungal vascular wilt pathogen Verticillium, with the descriptions of five new species. PLoS one 6: e28341.
Jabnoun-Khiareddine H, Daami-Remadi M, Ayed F, El-Mahjoub M. 2009. Biological control of tomato Verticillium wilt by using indigenous Trichoderma spp. The African Journal of Plant Science and Biotechnology 3: 26-36.
Leslie JF, Summerell BA. 2006. The Fusarium Laboratory Manual. Ames, Iowa, USA: Blackwell Publishing; 2006. 387 p.
Li J, Zingen-Sell I, Buchenauer H. 1996. Induction of resistance of cotton plants to Verticillium wilt and of tomato plants to Fusarium wilt by 3-aminobutyric acid and methyl jasmonate. Journal of Plant Diseases and Protection 103: 288-299.
Lorito M, Woo SL, Harman GE, Monte E. 2010. Translational research on Trichoderma: from omics to the field. Annual Review of Phytopathology 48: 395-417.
Lurie S, Crisosto CH. 2005. Chilling injury in peach and nectarine. Postharvest biology and technology 37: 195-208.
Maldonado-González MM, Schilirò E, Prieto P, Mercado-Blanco J. 2015. Endophytic colonization and biocontrol performance of Pseudomonas fluorescens PICF7 in olive (Olea europaea L.) are determined neither by pyoverdine production nor swimming motility. Environmental Microbiology 17: 3139–3153.
Markakis EA, Tjamos SE, Antoniou PP, Paplomatas EJ, Tjamos EC. 2016. Biological control of Verticillium wilt of olive by Paenibacillus alvei, strain K165. Biocontrol 61: 93–303
Marois J, Johnston S, Dunn M, Papavizas G. 1982. Biological control of Verticillium wilt of eggplant in the field. Plant Disease 66: 1166-1168.
Mercado-Blanco J, Rodrıguez-Jurado D, Hervás A, Jiménez-Dıaz RM. 2004. Suppression of Verticillium wilt in olive planting stocks by root-associated fluorescent Pseudomonas spp. Biological Control 30: 474–486.
Möller E, Bahnweg G, Sandermann H, Geiger H. 1992. A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Research 20: 6115.
Müller H, Berg G. 2008. Impact of formulation procedures on the effect of the biocontrol agent Serratia plymuthica HRO-C48 on Verticillium wilt in oilseed rape. Biocontrol 53: 905-16.
Naraghi L, Heydari A, Ershad D. 2006. Sporulation and survival of Talaromyces flavus on different plant material residues for biological control of cotton wilt caused by Verticillium dahliae. Iranian Journal of Plant Pathology 42: 382-397.
Narisawa K, Kawamata H, Currah RS, Hashiba T. 2002. Suppression of Verticillium wilt in eggplant by some fungal root endophytes. European Journal of Plant Pathology 108: 103–109.
Prieto P, Navarro-Raya C, Valverde-Corredor A, Amyotte SG, Dobinson KF, Mercado-Blanco J. 2009. Colonization process of olive tissues by Verticillium dahliae and its greenhouse interaction with the biocontrol root endophyte Pseudomonas fluorescens PICF7. Microbial Biotechnology 2: 499–511.
Royse DJ, Ries SM. 1978. The influence of fungi isolated from peach twigs on the pathogenicity of Cytosporacinata. Phytopathology 63: 603- 607.
Ruano-Rosa D, Prieto P, Rincón AM, Gómez-Rodríguez MV, Valderrama R, Barroso JB, et al. 2016. Fate of Trichoderma harzianum in the olive rhizosphere: time course of the root colonization process and interaction with the fungal pathogen Verticillium dahliae. Biocontrol 61: 269–282.
Rubio MB, Quijada NM, Perez E, Domínguez S, Monte E, Hermosa R. 2014. Identifying Trichoderma parareesei beneficial qualities for plants. Applied and Environmental Microbiology 80: 1864e1873.
Samson RA. 1994. Taxonomy—Current Concepts of Aspergillus Systematics. In: Smith JE (eds) Aspergillus. Biotechnology Handbooks, vol 7. Springer, Boston, MA.
Samuels GJ, Ismaiel A, Mulaw TB, et al. 2012. The Longibrachiatum clade of Trichoderma: a revision with new species. Fungal Diversity 55: 77–108.
Sanei SJ, Razavi SE. 2011. Suppression of Verticillium wilt of olive by Pseudomonas fluorescens. Journal of Experimental Agriculture International 8: 294-305.
Schroers HJ. 2001. A monograph of Bionectria (Ascomycota, Hypocreales, Bionectriaceae) and its Clonostachys anamorphs, Centraalbureau voor Schimmelcultures. 214 pp.
Simmons EG. 2007. Alternaria: An Indentification Manual. CBS Biodiversity Series 6. 775 pp. 
Slusarski C, Pietr SJ. 2009. Combined application of dazomet and Trichoderma asperellum as an efficient alternative to methyl bromide in controlling the soil-borne disease complex of bell pepper. Crop Protection 28: 668–674.
Stapleton J, Paplomatas E, Wakeman R, De Vay J. 1993. Establishment of apricot and almond trees using soil mulching with transparent (solarization) and black polyethylene film: effects on Verticillium wilt and tree health. Plant Pathology 42: 333-338.
Taghdi Y, Hermosa R, Dominguez S, Rubio MB, Essalmani H, Nicolas C, Monte E. 2015. Effectiveness of composts and Trichoderma isolates for control of Fusarium wilt of tomato. Phytopathologia Mediterranea 1: 232-40.
Talboys P. 1960. A culture‐medium aiding the identification of Verticillium albo‐atrum and V. dahliae. Plant Pathology 9: 57-58.
Tjamos EC, Fravel DR. 1997. Distribution and establishment of the biocontrol fungus Talaromyces flavus in soil and on roots of solanaceous crops. Crop Protection 16: 135–139.
Tjamos EC, Biris DA, Paplomatas EJ. 1991. Recovery of olive trees from Verticillium wilt after individual application of soil solarization in established olive orchards. Plant Disease 75: 557-562.
Varo A, Raya-Ortega MC, Trapero A. 2016. Selection and evaluation of micro-organisms for biocontrol of Verticillium dahliae in olive. Journal of Applied Microbiology 121: 767–777.
Veloso J, Díaz J. 2012. Fusarium oxysporum Fo47 confers protection to pepper plants against Verticillium dahliae and Phytophthora capsici, and induces the expression of defence genes. Plant Pathology 61: 281–288.
Visagie CM, Houbraken J, Frisvad JC, Hong SB, Klaassen CH, Perrone G, Seifert KA, Varga J, Yaguchi T, Samson RA. 2014. Identification and nomenclature of the genus Penicillium. Studies in Mycology 78: 343-71.
White TJ, Bruns T, Lee SJWT, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 18: 315–322.
Zhang Q, Yang L, Zhang J, Wu M, Chen W, Jiang D, et al. 2015. Production of anti-fungal volatiles by non-pathogenic Fusarium oxysporum and its efficacy in suppression of Verticillium wilt of cotton. Plant and Soil 392: 101–114.
Zhou L, Hu Q, Johansson A, Dixelius C. 2006. Verticillium longisporum and V. dahliae: infection and disease in Brassica napus. Plant Pathology 55: 137–144