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Suppressive biomasses and antagonist bacteria for an eco-compatible control of Verticillium dahliae on nursery-grown olive plants

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Abstract

Two organic amendments (OMW-M1 and OMW-M2), based on olive mill wastes (OMWs) subjected to advanced processes of aerobic static storage or composting, were tested for their suppressive activity against Verticillium dahliae, the causal agent of olive Verticillium wilt. OMW-M1 and OMW-M2 drastically inhibited the pathogen growth in vitro and then were further tested in suppressive pot experiments. The amendments, mixed at 15 % (v/v) with a nursery standard plant-growth matrix, were tested alone or in combination with two biocontrol bacteria (Bacillus amyloliquefaciens and Burkholderia cepacia) selected from suppressive soils. All mixtures were artificially contaminated with V. dahliae microsclerotia (MS), the density of which was periodically monitored by either a semi-selective medium or a specific real-time Polymerase Chain Reaction technique. In plant-less pot assays conducted in a growth chamber, OMW-M1 was the most effective amendment, reducing V. dahliae MS density by 100 % after 90 days with respect to the untreated control. In nursery experiments with pot-growing olive plants, OMW-M1, particularly when combined with the biocontrol bacteria, confirmed its strong suppressive activity reducing up to 100 % the density of V. dahliae MS in the rhizosphere behaving even better than a commercial biofungicide (Trichoderma asperellum TV1) used as a control. The best combined treatment also reduced plant mortality and increased root and shoot extension. It is concluded that organic amendments from stabilized olive mill by-products showed positive agronomic and phytosanitary properties on pot-growing olive plants and, particularly when enriched with biocontrol agents, they are potentially suitable for use in sustainable agriculture.

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References

  • Alburquerque JA, Gonzálvez J, García D, Cegarra J (2007) Effects of a compost made from the solid by-product (“alperujo”) of the two-phase centrifugation system for olive oil extraction and cotton gin waste on growth and nutrient content of ryegrass (Lolium perenne L.). Bioresource Technol 98(4):940–945

    Article  CAS  Google Scholar 

  • Alfano G, Belli C, Lustrato G, Ranalli G (2008) Pile composting of two-phase centrifuged olive husks residues: technical solutions and quality of cured compost. Bioresource Technol 99(11):4694–4701

    Article  CAS  Google Scholar 

  • Alfano G, Lustrato G, Lima G, Vitullo D, Delfine S, Tognetti R, Ranalli G (2009a) Physico-Chemical, microbiological, agronomical, and phytopathological aspects in the recycling of olive waste composted residues. In: Martin-Gil J (ed) Dynamic soil dynamic plant, special issue 1, compost part II. Global Science Books, Isleworth, pp 64–72

    Google Scholar 

  • Alfano G, Lustrato G, Lima G, Ranalli G (2009b) Present and future perspectives of olive residues composting in the Mediterranean basin (CompMed). Invited review. In: Martin-Gil J (ed) Dynamic soil dynamic plant, special Issue 1, Compost Part II. Global Science Books, Isleworth, pp 39–56

  • Altieri R, Esposito A (2008) Olive orchard amended with two experimental olive mill wastes mixtures: effects on soil organic carbon, plant growth and yield. Bioresource Technol 99(17):8390–8393

    Article  CAS  Google Scholar 

  • Altieri R, Esposito A (2010) Evaluation of the fertilizing effect of olive mill waste compost in short-term crops. Int Biodeter Biodegr 64(2):124–128

    Article  CAS  Google Scholar 

  • Altieri R, Pepi M, Esposito A, Fontanazza G (2005) Chemical and microbiological characterization of olive mill wastes based substrata produced by the (O.Mi.By.P.) technology (Olive Mill By-Products Processor) and their grounds amendment. In: Proceedings International Seminar: “The Role and Importance of Integrated Soil and Water Management for Orchards Development”, Mosciano S. Angelo, Teramo, Italy, 9–10 May 2004, Fao Land Water Bull. n.10, 91–101

  • Berg G, Opelt K, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K (2006) The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiol Ecol 56(2):250–261

    Article  CAS  Google Scholar 

  • Borrero C, Ordovása J, Trillasb MI, Avilésa M (2006) Tomato Fusarium wilt suppressiveness. The relationship between the organic plant growth media and their microbial communities as characterised by Biolog®. Soil Biol Biochem 38(7):1631–1637

    Article  CAS  Google Scholar 

  • Boulter JI, Trevors JT, Boland GJ (2002) Microbial studies of compost: bacterial identifications, and their potential for turfglass pathogens suppression. World J Microb Biot 18:661–671

    Article  CAS  Google Scholar 

  • Cullen DW, Lees AK, Toth IK, Duncan JM (2001) Conventional PCR and real-time quantitative PCR detection of Helminthosporium solani in soil and potato tubers. Eur J Plant Pathol 107:387–398

    Article  CAS  Google Scholar 

  • De Costa DM, Samarasinghe SST, Dias HRD, Dissanayake DMN (2008) Control of rice sheath blight by phyllosphere epiphytic microbial antagonists. Phytoparasitica 36(1):52–65

    Article  Google Scholar 

  • De Curtis F, Lima G, Vitullo D, De Cicco V (2010) Biocontrol of Rhizoctonia solani and Sclerotium rolfsii on tomato by delivering antagonistic bacteria through a drip irrigation system. Crop Prot 29(7):663–670

    Article  Google Scholar 

  • DIVAPRA (Dipartimento di Valorizzazione e Protezione delle Risorse Agro-forestali, Sez. Chimica Agraria, Università di Torino), IPLA (Istituto per le Piante da Legno e l’Ambiente) (1992) Metodi di analisi dei compost, Assessorato Ambiente Regione Piemonte (ed), Torino, IT

  • DL 75/2010 (2010) Decreto Legislativo 29 aprile 2010, n. 75 of Italian Republic “Riordino e revisione della disciplina in materia di fertilizzanti”, a norma dell’articolo 13 della Legge 7 luglio 2009 n. 88, Gazzetta Ufficiale n. 121—Supplemento Ordinario n.106, Roma, May 26th

  • Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent Pseudomonas. Nat Rev Microbiol 3:307–319

    Article  CAS  Google Scholar 

  • Hawke MA, Lazarovits G (1994) Production and manipulation of individual microsclerotia of Verticillium dahliae for use in studies of survival. Phytopathology 84(9):883–890

    Article  Google Scholar 

  • Huang J, Li H, Yuan H (2006) Effect of organic amendments on Verticillium wilt of cotton. Crop Prot 25(11):1167–1173

    Article  Google Scholar 

  • Huisman OC (1988) Seasonal colonization of roots of field-grown cotton by Verticillium dahliae and V. tricorpus. Phytopathology 78(6):708–716

    Article  Google Scholar 

  • IOOC (International Olive Oil Council) (2012) Olivae 117, pp 42 Available from: http://www.internationaloliveoil.org/store/index/48-olivae-publications (last accessed November 2012)

  • Jiménez-Díaz RM, Tjamos EC, Cirulli M (1998) Verticillium wilt of major tree hosts: olive. In: Hiemstra JA, Harris DC (eds) A compendium of Verticillium wilts in tree species Pousen and Looijen. Wageningen, The Netherlands, pp 13–16

    Google Scholar 

  • Lima G, De Cicco V (2006) Integrated strategies to enhance biological control of postharvest diseases. In: Benkeblia N, Shiomi N (eds) Advances in post-harvest technologies for horticultural crops, vol 1., Research SignpostKerala, India, pp 173–194

    Google Scholar 

  • Lima G, De Curtis F, Donghia AM, Nigro F (2007) Comparison between real time PCR and semi-selective medium in monitoring Verticillium dahliae microsclerotia in the olive rhizosphere and suppression of the pathogen by compost. IOBC/WPRS Bull 30(9):221–224

    Google Scholar 

  • Lima G, Piedimonte D, De Curtis F, Elgelane A, Nigro F, D’Onghia AM, Alfano G, Ranalli G (2008) Suppressive effect of cured compost from olive oil by-products towards Verticillium dahliae and other fungal pathogens. Acta Hortic 791:585–591

    Google Scholar 

  • López-Piñeiro A, Murillo S, Barreto C, Muñoz A, Rato JM, Albarrán A, García A (2007) Changes in organic matter and residual effect of amendment with two-phase olive-mill waste on degraded agricultural soils. Sci Total Environ 378(1–2):84–89

    Article  Google Scholar 

  • Malandraki I, Tjamos SE, Pantelides IS, Paplomatas EJ (2008) Thermal inactivation of compost suppressiveness implicates possible biological factors in disease management. Biol Control 44(2):180–187

    Article  Google Scholar 

  • Martin FN (2003) Development of alternative strategies for management of soilborne pathogens currently controlled with methyl bromide. Annu Rev Phytopathol 41:325–350

    Article  CAS  Google Scholar 

  • Mercado-Blanco J, Rodriguez-Jurado D, Hervas A, Jiménez-Díaz RM (2004) Suppression of Verticillium wilt in olive planting stocks by root-associated fluorescent Pseudomonas spp. Biol Control 30:474–486

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Nelson EB, Boehm MJ (2002) Microbial mechanics of composted induced disease suppression. Part II. Biocycle 43(7):45–47

    Google Scholar 

  • Nigro F, Schena L, Gallone P (2002) Real-time diagnosis of Verticillium wilt of olive by Scorpion-PCR. In: Proceedings International Conference Oliviculture, VI Giornate Scientifiche SOI, Spoleto, Italy, April 23–25, pp 454–461

  • Nigro F, Gallone P, Romanazzi G, Schena L, Ippolito A, Salerno MG (2005) Incidence of Verticillium wilt on olive in Apulia and genetic diversity of Verticillium dahliae isolates from infected trees. J Plant Pathol 87(1):13–23

    CAS  Google Scholar 

  • Noble R, Coventry E (2005) Suppression of soilborne plant diseases with composts: a review. Biocontrol Sci Techn 15(1):3–20

    Article  Google Scholar 

  • Ntougias S, Papadopolou KK, Zervakis GI, Kavroulakis N, Ehaliotis C (2008) Suppression of soil-borne pathogens of tomato by composts derived from agro-industrial wastes abundant in Mediterranean regions. Biol Fert Soils 44(8):1081–1090

    Article  Google Scholar 

  • Pane C, Spaccini R, Piccolo A, Scala F, Bonanomi G (2011) Compost amendments enhance peat suppressiveness to Pythium ultimum, Rhizoctonia solani and Sclerotinia minor. Biol Control 56(2):115–124

    Article  Google Scholar 

  • Pullman GS, de Vay JE, Garber RH (1981) Soil solarization and thermal death: logarithmic relationship between time and temperature for four soilborne plant pathogens. Phytopathology 71:959–964

    Article  Google Scholar 

  • Ranalli G, Bottura G, Taddei P, Garavani M, Marchetti R, Sorlini C (2001) Composting of solid and sludge residues from agricultural and food industries. Bio-indicators of monitoring and compost maturity. J Environ Sci Heal A 36(4):415–436

    Article  CAS  Google Scholar 

  • Saadi I, Laor Y, Medina S, Krassnovsky A, Raviv M (2010) Compost suppressiveness against Fusarium oxysporum was not reduced after one-year storage under various moisture and temperature conditions. Soil Biol Biochem 42(4):626–634

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA

    Google Scholar 

  • Schena L, Nigro F, Ippolito A (2002) Identification and detection of Rosellinia necatrix by conventional and real-time scorpion-PCR. Eur J Plant Pathol 108:355–366

    Article  CAS  Google Scholar 

  • Schena L, Nigro F, Ippolito A (2004) Real-time PCR detection and quantification of soilborne fungal pathogens: the case of Rosellinia necatrix, Phytophthora nicotianae, P. citrophthora, and Verticillium dahliae. Phytopathol Mediterr 43:273–280

    CAS  Google Scholar 

  • Schoffelmeer EAM, Klis FM, Sietsma JH, Cornelissen BJC (1999) The cell wall of Fusarium oxysporum. Fungal Genet Biol 27(2–3):275–282

    Article  CAS  Google Scholar 

  • Senesi N, Plaza C, Brunetti G, Polo A (2007) A comparative survey of recent results on humic-like fractions in organic amendments and effect on native soil humic substances. Soil Biol Biochem 39(6):1244–1262

    Article  CAS  Google Scholar 

  • Sequi P, De Nobili M, Leita L, Cercignani G (1986) A new index of Humification. Agrochimica 30:175–179

    CAS  Google Scholar 

  • Singleton VL, Sullivan AR, Kramer C (1971) An analysis of wine to indicate aging in wood or treatment with wood chips or tannic acid. Am J Enol Viticult 22:161–197

    CAS  Google Scholar 

  • Skrobek A, Boss D, Défago G, Butt TM, Maurhofer M (2005) Evaluation of different biological test system to assess the toxicity of metabolites from fungal biocontrol agents. Toxicol Lett 161(1):43–52

    Article  Google Scholar 

  • van der Gaag DJ, van Noort FR, Stapel-Cuijpers LHM, de Kreij C, Termorshuizen AJ, van Rijn E, Zmora-Nahum S, Chen Y (2007) The use of green waste compost in peat-based potting mixtures: fertilization and suppressiveness against soilborne diseases. Sci Hort Amsterdam 114(4):289–297

    Article  Google Scholar 

  • Vitullo D, De Curtis F, Di Pietro A, Lima G (2008) Exploring the interaction between bacterial biocontrol agents and genetically characterized mutants of Fusarium oxysporum. J Plant Pathol 90:42–43

    Google Scholar 

  • Vitullo D, Di Pietro A, Romano A, Lanzotti V, Lima G (2012) Role of new bacterial surfactins in the antifungal interaction between Bacillus amyloliquefaciens and Fusarium oxysporum. Plant Pathol 61(4):689–699

  • Walker DJ, Bernal MP (2008) The effects of olive mill waste compost and poultry manure on the availability and plant uptake of nutrients in a highly saline soil. Bioresource Technol 99(2):396–403

    Article  CAS  Google Scholar 

  • Whitcombe D, Theaker J, Guy SP, Brown T, Little S (1999) Detection of PCR products using self-probing amplicons and fluorescence. Nat Biotechnol 17:804–807

    Article  CAS  Google Scholar 

  • Yaseen T, D’Onghia A, Ippolito A, Nigro F (2009) Microbial antagonists and compost-based growing media affect the growth of olive plantlets and the inoculum density of Verticillium dahliae microsclerotia. In: Proceedings of 10th International Verticillium Symposium, November 16–20, Corfu Island, Hellas, 87

  • Yogev A, Raviv M, Giora K, Hadar Y, Cohen R, Benny K, Katan J (2009) Suppression of bacterial canker of tomato by composts. Crop Prot 28(1):97–103

    Article  Google Scholar 

  • Zucconi F, Pera A, Forte M, de Bertoldi M (1981) Evaluating toxicity of immature compost. Biocycle 22:54–57

    Google Scholar 

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Acknowledgments

The research was supported by (a) the Italian “Ministero dell’Istruzione, dell’Università e della Ricerca”, PRIN project, prot. 20089LSZ2A_003, “Studies on biocontrol agents and their biomolecules to optimize the suppressive activity of natural amendments against soilborne pathogens of horticultural crops”, (b) the Italian “Ministero delle Risorse Agricole e Forestali”, OLVIVA project “Qualificazione del vivaismo olivicolo: caratterizzazione varietale, sanitaria e innovazioni nella tecnica vivaistica” (L499/99 Programmi Interregionali), and (c) the European Union project “LIFE Environment TIRSAV PLUS: LIFE05 ENV/IT/000845”. The authors are grateful to the Parco Scientifico “STAR” of Verona, and SETA SrL, Vigonza, Italy, for producing and supplying the composted substrate OMW-M2, and to the staff of the plant nursery “Verde Molise” Termoli, Italy, for technical assistance and equipment involved in the development of the suppressive experiments on olive plants. The authors also thank Janice Beccaria, from the Faculty of Foreign Languages and Literature at the University of Salento, Lecce, Italy for her valuable assistance in the linguistic revision of the manuscript.

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Vitullo, D., Altieri, R., Esposito, A. et al. Suppressive biomasses and antagonist bacteria for an eco-compatible control of Verticillium dahliae on nursery-grown olive plants. Int. J. Environ. Sci. Technol. 10, 209–220 (2013). https://doi.org/10.1007/s13762-012-0145-4

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