SpringerLink
Log in

Dispersion, persistence, and stability of the biocontrol agent Penicillium frequentans strain 909 after stone fruit tree applications

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The capacity of dispersion, persistence, and stability from biocontrol agents is essential before these organisms can be developed into a commercial product. Interactions that microorganisms establish with stone fruit trees may be beneficial in the exploitation of trees in agriculture as crop production. The natural background levels of Penicillium frequentans strain 909 dispersion, persistence, and stability were assessed after tree applications and postharvest conditions. A fingerprinting-based approach to trace genetic stability of P. frequentans along stored time and its release in the field was developed. P. frequentans was successfully traced and discriminated. This strain was dispersed well in treated trees, persisting in the ecosystem up to 2 weeks and staying genetically stable after 36 months of storage. However, the dispersal of P. frequentans was very limited on around untreated trees and soil. P. frequentans dispersed randomly into the air, and its presence reduced from the first day to disappear completely at 15–21 days after application. Great losses of P. frequentans and its increased dispersal in open field conditions probably resulted from rainfall. Biological control strategies with Pf909 were discussed.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  • Behle RW, Mc Guire MR, Shasha BS (1997) Effects of sunlight and simulated rain on residual activity of Bacillus thuringiensis formulations. J Econ Entomol 90:1560–1566

    Google Scholar 

  • Benson EE, Bremner D (2004) Oxidative stress in the frozen plant: a free radical point of view. In: Fuller B, Lane N, Benson EE (Eds), Life in the frozen state. CRC, FL, pp 205-242.

    Google Scholar 

  • Bonaterra A, Badosa E, Cabrefiga J, Francés J, Montesinos E (2012) Prospects and limitations of microbial pesticides for control of bacterial and fungal pomefruit tree diseases. Trees 26:215–226

    CAS  Google Scholar 

  • Boysen M, Jacobsson GK, Schnürer J (2000). Molecular Identification of Species from the Penicillium roqueforti Group Associated with Spoiled Animal Feed. Appl Environ Microbiol 66: 1523-1526.

    CAS  Google Scholar 

  • Bruns TD, White TJ, Taylor JW (1991) Fungal molecular systematics. Annu Rev Ecol Evol Syst 22:525–564

    Google Scholar 

  • Calvo-Garrido C, Viñas I, Usall J, Rodríguez-Romera M, Ramos MC, Teixidó N (2014) Survival of the biological control agent Candida sake CPA-1 on grapes under the influence of abiotic factors. J Appl Microbiol 117:800–811

    CAS  Google Scholar 

  • Coombes CA (2013) Entomopathogenic fungi for the control of soil-borne life stages of false codling month, Thaumatotibia leucotreta Meyrick (1912) (Lepidoptera: Tortricidae). Dissertation, Rhodes University, Grahamstown, South Africa

  • Day JG, Fleck RA, Benson EE (2000) Cryopreservation-recalcitrance in microalgae: novel approaches to identify and avoid cryo-injury. J Appl Phycol 12:369–377

    Google Scholar 

  • De Cal A, M-Sagasta E, Melgarejo P (1990) Biological control of peach twig blight (Monilinia laxa) with Penicillium frequentans. Plant Pathol 39:612–618

    Google Scholar 

  • De Cal A, Larena I, Guijarro B, Melgarejo P (2012) The use of biofungicides for controlling plant diseases to improve food availability. Agriculture 2:109–124

    Google Scholar 

  • De Clercq D, Cognet S, Pujol M, Lepoivre P, Jijakli MH (2003) Development of a SCAR marker and a semi-selective medium for specific quantification of Pichia anomala strain K on apple surface. Postharvest Biol Technol 29:237–247

    Google Scholar 

  • Den Boer PJ (1968) Spreading of risk and stabilization of animal numbers. Acta Biotheor (Leiden) 18:165–194

    Google Scholar 

  • Dupont J, Magnin S, Marti A, Brousse M (1999) Molecular tools for identification of Penicillium starter cultures used in the food industry. Int J Food Microbiol 49:109–118

    CAS  Google Scholar 

  • Fajardo V, González I, López-Calleja I, Martín I, Hernández PE, García T (2006) PCR-RFLP authentication of meats from red deer (Cervus elaphus), fallow deer (Dama dama), roe deer (Capreolus capreolus), cattle (Bos taurus), sheep (Ovis aries), and goat (Capra hircus). J Agri Food Chem 54:1144–1150

    CAS  Google Scholar 

  • Fleck RA (1998) The assessment of cell damage and recovery in cryopreserved freshwater protists. Ph.D. dissertation, University Abertay Dundee, Dundee, UK

  • Fleck RA, Benson EE, Bremner DH, Day JG (2000) Studies of free radical-mediated cryoinjury in the unicellular green alga Euglena gracilis using a non-destructive hydroxyl radical assay: a novel approach for develo** protistan cryopreservation strategies. Free Radic Res 32:157–170

    CAS  Google Scholar 

  • Filho AB,  Alves SB, Augusto NT, Pereira RM, Alves LFA (2001) Stability and Persistence of Two Formulations Containing Anticarsia gemmatalis Nuclear Polyhedrovirus (AgMNPV). Neotropical Entomology 30 (3):411-416

    Google Scholar 

  • Francés J, Bonaterra A, Moreno MC, Cabrefiga J, Badosa E, Montesinos E (2006) Pathogen agressiveness and postharvest biocontrol efficiency in Pantoea agglomerans. Postharvest Biol Technol 39:299–307

    Google Scholar 

  • Garrett K, Dendy S, Frank E, Rouse M, Travers S (2006) Climate change effects on plant disease: genomes to ecosystems. Annu Rev Phytopathol 44:489–509

    CAS  Google Scholar 

  • Gil E, Gallart M, Llorens J, Llop J, Bayer T, Carvalho C (2014) Spray adjustments based on LWA concept in vineyard. Relationship between canopy and coverage for different application settings. In: Proceedings of International Advance in Pesticide Application, Aspects of Applied Biology 122, pp 25–32

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330

    CAS  Google Scholar 

  • Gotor-Vila A, Usall J, Torres R, Solsona C, Teixidó N (2017) Biocontrol products based on Bacillus amyloliquefaciens CPA-8 using fluid-bed spray-drying process to control postharvest brown rot in stone fruit. LWT-Food Sci Technol 82:274e282

    Google Scholar 

  • Guijarro B, Larena I, Melgarejo P, De Cal A (2006) Effect of drying on conidial viability of Penicillium frequentans, a biological control agent against peach brown rot disease caused by Monilinia spp. Biocontrol Sci Tech 16:257–269

    Google Scholar 

  • Guijarro B, Melgarejo P, De Cal A (2007a) Relationship between shelf-life of Penicillium frequentans, a biological agent against brown rot disease, and its efficacy against peach brown rot. Int J Food Microbiol 113:117–124

    CAS  Google Scholar 

  • Guijarro B, Melgarejo P, Torres R, Lamarca N, Usall J, De Cal A (2007b) Effects of different biological formulations of Penicillium frequentans on brown rot of peaches. Biol Control 42:86–96

    Google Scholar 

  • Guijarro B, Melgarejo P, Torres R, Lamarca N, Usal J, De Cal A (2008) Penicillium frequentans population dynamics on peach fruit after its applications against brown rot in orchards. J Appl Microbiol 104:659–671

    CAS  Google Scholar 

  • Guijarro B, Hernández-Escribano L, Larena I, Melgarejo P, De Cal A (2017a) Competition is the mechanism of biocontrol of brown rot in stone fruit by Penicillium frequentans. BioControl 62:557–566

    Google Scholar 

  • Guijarro B, Larena I, Melgarejo P, De Cal A (2017b) Adaptive conditions and safety of the application of Penicillium frequentans as a biocontrol agent on stone fruit. Int J Food Microbiol 254:25–35

    Google Scholar 

  • Guijarro B, Larena I, Melgarejo P, De Cal A (2018) Surfactant effects on wettability of Penicillium frequentans formulations to improve brown rot biocontrol. J Sci Food Agric 98:5832–5840. https://doi.org/10.1002/jsfa.9133

    Article  CAS  Google Scholar 

  • Hunsche M, Damerow L, Schmitz-Eiberger M, Noga G (2007) Mancozeb wash-off from apple seedlings by simulated rainfall as affected by drying time of fungicide deposit and rain characteristics. Crop Prot 26:768–774

    CAS  Google Scholar 

  • Inglis GD, Duke GM, Kanagaratnam P, Johnson DL, Goettel MS (1997) Persistence of Beauveria bassiana in soil following application of conidia through crop canopies. Mem Entomol Soc Can 171:253–263

    Google Scholar 

  • Inyang EN, McCartney HA, Oyejola B, Ibrahim L, Pye BJ, Archer SA, Butt TM (2000) Effect of formulation, application and rain on the persistence of the entomogenous fungus Metarhizium anisopliae on oilseed rape. Mycol Res 104:653–661

    Google Scholar 

  • Jawhar M, Sangawn RS, Arabi MIE (2000) Identification of Drechslera graminea isolates by cultural characters and RAPD analysis. Cereal Res Commun 28:89–93

    Google Scholar 

  • Jonsen ID, Bourchier RS, Roland J (2007) Influence of dispersal, stochasticity, and an Allee effect on the persistence of weed biocontrol introductions. Ecol Model 203:521–526

    Google Scholar 

  • Kean JM, Barlow ND (2000) The effects of density dependence and local dispersal in individual-based stochastic metapopulations. Oikos 88:282–290

    Google Scholar 

  • Kinkel LL,Wilson M, Lindow SE (2000) Plant Species and Plant Incubation Conditions Influence Variability in Epiphytic Bacterial Population Size. Microbial Ecology 39 (1):1-11

    CAS  Google Scholar 

  • Longa CMO, Savazzini F, Tosi S, Elad Y, Pertot I (2009) Evaluating the survival and the environmental fate of the biocontrol agent Trichoderma atroviride strain SC1 in vineyards in Northern Italy. J Appl Microbiol 106:1549–1557

    CAS  Google Scholar 

  • Lund F, Frisvad JC (2003) Penicillium verrucosum in wheat and barley indicates presence of ochratoxin A. J Appl Microbiol 95:1117–1123

    CAS  Google Scholar 

  • Madden LV (1997) Effects of rain on splash dispersal of fungal pathogens. Can J Plant Pathol 19:225–230

    Google Scholar 

  • Melgarejo P, M-Sagasta E (1984) Fungal antagonism in relation to peach. In: Woodbine M (ed) Antimicrob Agriculture. Butterworths, London, pp 127–136

    Google Scholar 

  • Melgarejo P, Carrillo R, M-Sagasta E (1985) Mycoflora of peach twigs flowers and its possible significance in biological control of Monilinia laxa. Trans Br Mycol Soc 85:313–317

    Google Scholar 

  • Melgarejo P, Carrillo R, M-Sagasta E (1986a) Study on the epiphytic mycoflora of peach twigs and flowers. Phytopathol Mediterr 25:68–72

    Google Scholar 

  • Melgarejo P, Carrillo R, M-Sagasta E (1986b) Potential for biological control of Monilinia laxa in peach twigs. Crop Prot 5:422–426

    Google Scholar 

  • Montesinos E (2003) Development, registration and commercialization of microbial pesticides for plant protection. Int Microbiol 6:245–252

    CAS  Google Scholar 

  • Montesinos E, Bonaterra A (1996) Dose-response models in biological control of plant pathogens: an empirical verification. Phytopathology 86:464–472

    Google Scholar 

  • Mortelmans K, Zeiger E (2000) The Ames Salmonella/microsome mutagenicity assay. Mutat Res 455:29–60

    CAS  Google Scholar 

  • Muller J, Day J.G., Harding K, Hepperle D, Lorenz M, Friedl T, (2007) Assessing genetic stability of a range of terrestrial microalgae after cryopreservation using amplified fragment length polymorphism (AFLP). American Journal of Botany 94 (5):799-808

    Google Scholar 

  • Norris RJ, Memmott J, Lovell DJ (2002) The effects of rainfall on the survivorship and establishment of a biocontrol agent. J Appl Ecol 39:226–234

    Google Scholar 

  • Ogawa JM, Zehr EI, Biggs AR (1995) Brown rot. In: Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K, Uyemoto JK (eds) Compendium of stone fruit disease. American Phytopathological Society, St. Paul, pp 7–10

    Google Scholar 

  • Pedersen LH, Skouboe P, Boysen M, Soule J, Rossen L (1997) Detection of Penicillium species in complex food samples using the polymerase chain reaction. Int J Food Microbiol 35:169–177

    CAS  Google Scholar 

  • Peterson SW (2008) Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 100:205–226

    CAS  Google Scholar 

  • Pianzzola M, Moscatelli M, Vero S (2004) Characterization of Penicillium isolates associated with blue mold on apple in Uruguay. Plant Dis 88:23–28

    CAS  Google Scholar 

  • Pietrarelli R, Balestra L, Varvaro GM (2006) Effects of simulated rain on Pseudomonas syringae pv. tomato populations on tomato plants. J Plant Pathol 88:245–251

    Google Scholar 

  • Redondo C, Cubero J, Melgarejo P (2009) Characterization of Penicillium species by ribosomal DNA sequencing and BOX, ERIC and REP-PCR analysis. Mycopathologia 168:11–22

    CAS  Google Scholar 

  • Rojas M, González I, Fajardo V, Martín I, Hernández PE, García T (2009) Authentication of meats from quail (Coturnix coturnix), pheasant (Phasianus colchicus), partridge (Alectoris spp.), and guinea fowl (Numida meleagris) using polymerase chain reaction targeting specific sequences from the mitochondrial 12S rRNA gene. Food Control 20:896–902

    CAS  Google Scholar 

  • Scheepmaker JWA, Butt TM (2010) Natural and released agents in soil in relation to risk assessment and in accordance with EU regulations. Biocontrol Sci Technol 20:503–552

    Google Scholar 

  • Snedecor, G.W., Cochran, W.G., 1980. Statistical Methods, seventh ed. Ames: Iowa State University Press, University Press, Iowa State, USA, pp. 507

  • Soto-Muñoz L, Torres R, Usall J, Viñas I, Dashevskaya S, Teixidó N (2015) Environmental monitoring of the biocontrol agent Pantoea agglomerans CPA-2 applied to citrus fruit at preharvest. Ann Appl Biol 167:250–261

    Google Scholar 

  • Teixidó N, Viñas I, Usall J, Sanchis V, Magan N (1998) Ecophysiological responses of the biocontrol yeast Candida sake to water, temperature and pH stress. J Appl Microbiol 84:192–200

    Google Scholar 

  • Versalovic J, Schneider M, DeBruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence based polymerase chain reaction. Methods Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  • Vilanova L, Teixidó N, Usall J, Balsells-Llauradó M, Gotor-Vila A, Torres R (2018) Environmental fate and behaviour of the biocontrol agent Bacillus amyloliquefaciens CPA-8 after preharvest application to stone fruit. Pest Manag Sci 74:375–383

    CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR - protocols and applications - a laboratory manual. Publisher: Academic Press, pp. 315–322

    Google Scholar 

Download references

Acknowledgements

This work was carried out with financial support from BIOCOMES project (EU FP7 612713). We thank Dr. Spadaro (University of Torino, Italy), Dr. Palou (IVIA, Spain) and Dr. Karaoglanidis, (University of Thessaloniki, Greece), for providing Penicillium glabrum isolates. The authors would like to acknowledge Raquel Castillo for her technical assistance.

Author information

Authors and Affiliations

  1. Department of Plant Protection, INIA, Ctra. de La Coruña Km. 7, 28040, Madrid, Spain

    Belen Guijarro, Inmaculada Larena, Paloma Melgarejo & Antonieta De Cal

  2. IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnologic Agroalimentari de Lleida, 25003, Lleida, Spain

    Laura Vilanova, Rosario Torres, Marta Balsells-Llauradó & Neus Teixidó

Authors
  1. Belen Guijarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Inmaculada Larena
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura Vilanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rosario Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marta Balsells-Llauradó
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Neus Teixidó
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Paloma Melgarejo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Antonieta De Cal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antonieta De Cal.

Additional information

Responsible editor: Diane Purchase

Publisher’s note

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

Electronic supplementary material

Suppl. Fig. 1

RFLP profiles for Penicillium frequentans strain 909 (Pf909) and other P. frequentans isolates with primer pair T10-f/BT2b-r using restriction enzymes (a) Hinf-I; (b) HaeIII; (c) Msel; and (d) MaeII; Lane Ld, 100 bp DNA ladder; lanes 909 positive control Pf909; lanes C negative controls for each enzyme restriction product. Lanes Pg1 to Pg8, GAG, GAI, and GAE Penicillium glabrum (PNG 866 kb)

High resolution image (TIF 282 kb)

Suppl. Fig. 2

Percentage area coverage with dried conidia Penicillium frequentans strain 909 (Pf909DC) spray treatment obtained from the analysis of Water Sensitive Papers (WSPs) using the IMAGEJ program. The WSPs were located on the leaves of the outside and inside canopy of treated and non-treated trees different distances. Pf909DC (107 conidia/mL) was sprayed 3 days before harvest onto nectarine cv Albared orchard at Alpicat (Lleida, Spain). (PNG 199 kb)

High resolution image (TIF 87 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guijarro, B., Larena, I., Vilanova, L. et al. Dispersion, persistence, and stability of the biocontrol agent Penicillium frequentans strain 909 after stone fruit tree applications. Environ Sci Pollut Res 26, 29138–29156 (2019). https://doi.org/10.1007/s11356-019-06023-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-06023-y

Keywords

Search

Navigation