Microbial Ecology

, Volume 56, Issue 4, pp 720–732

Culturable Fungi of Stored ‘Golden Delicious’ Apple Fruits: A One-Season Comparison Study of Organic and Integrated Production Systems in Switzerland

  • José Granado
  • Barbara Thürig
  • Edith Kieffer
  • Liliane Petrini
  • Andreas Flieβbach
  • Lucius Tamm
  • Franco P. Weibel
  • Gabriela S. Wyss
Original Article

Abstract

The effects of organic and integrated production systems on the culturable fungal microflora of stored apple fruits from five matched pairs of certified organic and integrated ‘Golden Delicious’ farms were studied at five representative production sites in Switzerland. Isolated fungi were identified morphologically. Colonization frequency (percentage of apples colonized), abundance (colony numbers), and diversity (taxon richness) were assessed for each orchard. The standard quality of the stored fruits was comparable for both organic and integrated apples and complied with national food hygiene standards. Yeasts (six taxa) and the yeast-like fungus Aureobasidium pullulans were the dominant epiphytes, filamentous fungi (21 taxa) the dominant endophytes. The most common fungi occurred at all sites and belonged to the “white” and “pink” yeasts, yeast-like A. pullulans, filamentous fungi Cladosporium spp., Alternaria spp., and sterile filamentous fungi. Canonical correspondence analysis of the total fungal community revealed a clear differentiation among production systems and sites. Compared to integrated apples, organic apples had significantly higher frequencies of filamentous fungi, abundance of total fungi, and taxon diversity. The effects of the production system on the fungal microflora are most likely due to the different plant protection strategies. The incidence of potential mycotoxin producers such as Penicillium and Alternaria species was not different between production systems. We suggest that higher fungal diversity may generally be associated with organic production and may increase the level of beneficial and antagonistically acting species known for their potential to suppress apple pathogens, which may be an advantage to organic apples, e.g., in respect to natural disease control.

References

  1. 1.
    Andrews JH, Kenerley CM (1978) The effects of a pesticide program on non-target epiphytic microbial populations of apple leaves. Can J Microbiol 24:1058–1072PubMedCrossRefGoogle Scholar
  2. 2.
    Andrews JH, Kenerley CM (1980) Microbial populations associated with buds and young leaves of apple. Can J Bot 58:847–855Google Scholar
  3. 3.
    Andrews JH, Berbee FM, Nordheim EV (1983) Microbial antagonism to the imperfect stage of the apple scab pathogen, Venturia inaequalis. Phytopathology 73:228–234CrossRefGoogle Scholar
  4. 4.
    Avilla J, Riedl H (2003) Integrated fruit production for apples—principles and guidelines. In: Ferree DC, Warrington IJ (eds) Apples: botany, production and uses. CABI Publishing, Wallingford, pp 539–549Google Scholar
  5. 5.
    Bakker GR, Frampton CM, Jaspers MV, Stewart A, Walter M (2002) Assessment of phylloplane micro-organism populations in Canterbury apple orchards. N Z Plant Prot 55:129–134Google Scholar
  6. 6.
    Bayman P, Lebrón LL, Tremblay RL, Lodge DJ (1997) Variation in endophytic fungi from roots and leaves of Lepanthes (orchidaceae). New Phytol 135:143–149CrossRefGoogle Scholar
  7. 7.
    Bio-Suisse (2007) Umbrella organization of Swiss organic farmers, http://www.bio-suisse.ch/en/consumer/bud/index.php
  8. 8.
    Calvente V, Benuzzi D, Obuchowicz N, Hough G, De Tosetti MIS (1999) Changes in surface microflora of apple and pear fruits by application of pesticides and their relation with biocontrol of post-harvest diseases. Agro Food Ind Hi-Tech 10:30–33Google Scholar
  9. 9.
    Carisse O, Philion V, Rolland D, Bernier J (2000) Effect of fall application of fungal antagonists on spring ascospore production of the apple scab pathogen, Venturia inaequalis. Phytopathology 90:31–37CrossRefPubMedGoogle Scholar
  10. 10.
    Chand-Goyal T, Spotts RA (1996) Enumeration of bacterial and yeast colonists of apple fruits and identification of epiphytic yeasts on pear fruits in the Pacific Northwest United States. Microbiol Res 151:427–432PubMedGoogle Scholar
  11. 11.
    Doores S (1983) The microbiology of apples and apple products. Crit Rev Food Sci Nutr 19:133–149PubMedCrossRefGoogle Scholar
  12. 12.
    Droby S, Wisniewski M, El Ghaouth A, Wilson CL (2003) Biological control of postharvest diseases of fruits and vegetables: current achievements and future challenges. Acta Hortic 628:703–713Google Scholar
  13. 13.
    Drusch S, Ragab W (2003) Mycotoxins in fruits, fruit juices, and dried fruits. J Food Prot 66:1514–1527PubMedGoogle Scholar
  14. 14.
    Dugan FM, Lupien SL, Grove GG (2002) Incidence, aggressiveness and in planta interactions of Botrytis cinerea and other filamentous fungi quiescent in grape berries and dormant buds in Central Washington State. J Phytopathol 150:375–381CrossRefGoogle Scholar
  15. 15.
    EC (2007) Council Regulation (EC) No 834/2007 of June 2007 on organic production and labelling of organic products and repealing Regulation (EEC) No 2092/91. Official Journal of the European Communities L189/1 (20.7.2007):1–23Google Scholar
  16. 16.
    Ellis MA (1983) Colonisation of delicious apple fruits by Alternaria spp. and effect of fungicide sprays on moldy-core. Plant Dis 67:150–151CrossRefGoogle Scholar
  17. 17.
    Elmer PAG, Reglinski T (2006) Biosuppression of Botrytis cinerea in grapes. Plant Pathol 55:155–177CrossRefGoogle Scholar
  18. 18.
    Esperschütz J, Gattinger A, Mäder P, Schloter M, Fliessbach A (2007) Response of soil microbial biomass and community structures to conventional and organic farming systems under identical crop rotation. FEMS Microbiol Ecol 61:26–37PubMedCrossRefGoogle Scholar
  19. 19.
    Fan Q, Tian S (2001) Postharvest biological control of grey mold and blue mold on apple by Cryptococcus albidus (Saito) Skinner. Postharvest Biol Technol 21:341–350CrossRefGoogle Scholar
  20. 20.
    FIV (2007) Swiss ordinance on foreign substances and constituents in foods (Verordnung über Fremd-und Inhaltstoffe in Verordnung über Fremd-und Inhaltstoffe in Lebensmitteln, SR 817.021.23, Bern, Swiss Federal Office of Public Health), http://www.admin.ch/ch/d/sr/817_021_23/index.html
  21. 21.
    Fokkema NJ (1976) Antagonism between fungal saprophytes and pathogens on aerial plant surfaces. In: Dickinson CH, Preece TF (eds) Microbiology of aerial plant surfaces. Academic, London, pp 487–506Google Scholar
  22. 22.
    Gattinger A, Höfle MG, Schloter M, Embacher A, Böhme F, Munch JC, Labrenz M (2007) Traditional cattle manure application determines abundance, diversity and activity of methanogenic Archaea in arable European soil. Environ Microbiol 9:612–624PubMedCrossRefGoogle Scholar
  23. 23.
    Gildemacher P, Heijne B, Silvestri M, Houbraken J, Hoekstra E, Theelen B, Boekhout T (2006) Interactions between yeasts, fungicides and apple fruit russeting. FEMS Yeast Res 6:1149–1156PubMedCrossRefGoogle Scholar
  24. 24.
    Gildemacher PR, Heijne B, Houbraken J, Vromans T, Hoekstra ES, Boekhout T (2004) Can phyllosphere yeasts explain the effect of scab fungicides on russeting of Elstar apples? Eur J Plant Pathol 110:929–937CrossRefGoogle Scholar
  25. 25.
    Golubev WI, Ikeda R, Shinoda T, Nakase T (1997) Antifungal activity of Bullera alba (Hanna) Derx. Mycoscience 38:25–29CrossRefGoogle Scholar
  26. 26.
    Golubev WI, Kulakovskaya TV, Golubeva EW (2001) The yeast Pseudozyma fusiformata VKM Y-2821 producing an antifungal glycolipid. Microbiology 70:553–556CrossRefGoogle Scholar
  27. 27.
    Grove GG, Eastwell KC, Jones AL, Sutton TB (2003) Diseases of apple. In: Ferree DC, Warrington IJ (eds) Apples: botany, production and uses. CABI Publishing, Wallingford, pp 459–488Google Scholar
  28. 28.
    HyV (2007) Swiss Ordinance on Food Hygiene (Hygieneverordnung des EDI, SR 817.024.1, Bern, Swiss Federal Office of Public Health), http://www.admin.ch/ch/d/sr/817_024_1/index.html
  29. 29.
    Ippolito A, El Ghaouth A, Wilson CL, Wisniewski M (2000) Control of postharvest decay of apple fruit by Aureobasidium pullulans and induction of defense responses. Postharvest Biol Technol 19:265–272CrossRefGoogle Scholar
  30. 30.
    Janisiewicz WJ, Peterson DL, Bors R (1994) Control of storage decay of apples with Sporobolomyces roseus. Plant Dis 78:466–470Google Scholar
  31. 31.
    Kulakovskaya TV, Shashkov AS, Kulakovskaya EV, Golubev WI (2005) Ustilagic acid secretion by Pseudozyma fusiformata strains. FEMS Yeast Res 5:919–923PubMedCrossRefGoogle Scholar
  32. 32.
    Leibinger W, Breuker B, Hahn M, Mendgen K (1997) Control of postharvest pathogens and colonization of apple surface by antagonistic microorganisms in the field. Phytopathology 87:1103–1110CrossRefPubMedGoogle Scholar
  33. 33.
    Lima G, Spina AM, Castoria R, De Curtis F, De Cicco V (2005) Integration of biocontrol agents and food-grade additives for enhancing protection of stored apples from Penicillium expansum. J Food Prot 68:2100–2106PubMedGoogle Scholar
  34. 34.
    Mäder P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1696PubMedCrossRefGoogle Scholar
  35. 35.
    Matteson MC, Corral-Garcia MR, Momol EA, Burr TJ (1997) Russet of apple fruit caused by Aureobasidium pullulans and Rhodotorula glutinis. Plant Dis 81:337–342CrossRefGoogle Scholar
  36. 36.
    Maxin P, Huyskens-Keil S, Klopp K, Ebert G (2005) Control of postharvest decay in organic grown apples by hot water treatment. Acta Hortic 682:2153–2158Google Scholar
  37. 37.
    Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A (2003) Impact of land use intensity on species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69:2816–2824PubMedCrossRefGoogle Scholar
  38. 38.
    Peck GM, Andrews PK, Richter C, Reganold JP (2005) Internationalization of the organic fruit market: the case of Washington State’s organic apple exports to the European Union. Renew Agric Food Syst 20:101–112CrossRefGoogle Scholar
  39. 39.
    Peck GM, Andrews PK, Reganold JP, Fellman JK (2006) Apple orchard productivity and fruit quality under organic, conventional, and integrated management. HortScience 41:99–107Google Scholar
  40. 40.
    Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 178–197Google Scholar
  41. 41.
    Reganold JP, Glover JD, Andrews PK, Hinman HR (2001) Sustainability of three apple production systems. Nature 410:926–930PubMedCrossRefGoogle Scholar
  42. 42.
    Róth E, Kovács E, Felföldi J (2004) The effect of growing system on the storability of apple. Acta Aliment 33:79–86CrossRefGoogle Scholar
  43. 43.
    Seghers D, Wittebolle L, Top EM, Verstraete W, Siciliano SD (2004) Impact of agricultural practices on the Zea mays L. endophytic community. Appl Environ Microbiol 70:1475–1482Google Scholar
  44. 44.
    Serdani M, Crous PW, Holz G, Petrini O (1998) Endophytic fungi associated with core rot of apples in South Africa, with specific reference to Alternaria species. Sydowia 50:257–271Google Scholar
  45. 45.
    Suisse-Garantie (2007) AMS Agro-Marketing Suisse, http://www.suissegarantie.ch
  46. 46.
    Tamm L, Häseli A, Fuchs JG, Weibel FP, Wyss E (2004) Organic fruit production in humid climates of Europe: bottlenecks and new approaches in disease and pest control. Acta Hortic 638:333–339Google Scholar
  47. 47.
    Teixido N, Usall J, Magan N, Viñas I (1999) Microbial population dynamics on Golden Delicious apples from bud to harvest and effect of fungicide applications. Ann Appl Biol 134:109–116CrossRefGoogle Scholar
  48. 48.
    TerBraak CJF, Smilauer P (2002) Software for canonical community ordination (version 4.5).CANOCO reference manual and CanoDraw for Windows user’s guide. Microcomputer Power, Ithaca, NY, USAGoogle Scholar
  49. 49.
    Tilman D (1999) Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proc Natl Acad Sci U S A 96:5995–6000PubMedCrossRefGoogle Scholar
  50. 50.
    Waipara NW, Obanor FO, Walter M (2002) Impact of phylloplane management on microbial populations. N Z Plant Prot 55:125–128Google Scholar
  51. 51.
    Weibel F, Häseli A (2003) Organic apple production—with emphasis on european experiences. In: Ferree DC, Warrington IJ (eds) Apples: botany, production and uses. CABI Publishing, Wallingford, pp 551–583Google Scholar
  52. 52.
    Weibel FP, Bickel R, Leuthold S, Alföldi T (2000) Are organically grown apples tastier and healthier? A comparative field study using conventional and alternative methods to measure fruit quality. Acta Hortic 517:417–426Google Scholar
  53. 53.
    Weibel FP, Treutter D, Häseli A, Graf U (2004) Sensory and health-related fruit quality of organic apples: a comparative field study over three years using conventional and holistic methods to assess fruit quality. 11th International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing. Fördergemeinschaft Ökologischer Obstbau e. V., Weinsberg, pp 185–195Google Scholar
  54. 54.
    Woody ST, Spear RN, Nordheim EV, Ives AR, Andrews JH (2003) Single-leaf resolution of the temporal population dynamics of Aureobasidium pullulans on apple leaves. Appl Environ Microbiol 69:4892–4900PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • José Granado
    • 1
  • Barbara Thürig
    • 1
  • Edith Kieffer
    • 1
    • 2
  • Liliane Petrini
    • 3
  • Andreas Flieβbach
    • 1
  • Lucius Tamm
    • 1
  • Franco P. Weibel
    • 1
  • Gabriela S. Wyss
    • 1
  1. 1.Research Institute of Organic Agriculture, AckerstrasseFrickSwitzerland
  2. 2.Amt für VerbraucherschutzAarauSwitzerland
  3. 3.ComanoSwitzerland

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