Skip to main content

Resistance in Postharvest Pathogens of Citrus in the United States

  • Chapter
Fungicide Resistance in Plant Pathogens

Abstract

Among citrus postharvest pathogens, fungicide resistance in the United States to date has only been reported for species of Penicillium. Except for the inorganic salts, widespread resistance has developed to all of the older fungicides such as the still registered phenylphenols o-phenylphenol and sodium o-phenylphenate, the methyl benzimidazole carbamate, thiabendazole, and the demethylation inhibitor imazalil. The almost simultaneous introduction of several new compounds in the early 2000s that include the anilinopyrimidine pyrimethanil, the phenylpyrrole fludioxonil, and the quinone outside inhibitor azoxystrobin offered a unique opportunity in keeping the development of resistance to a minimum. Fungicide modes of action could be mixed and rotated from the first introduction before resistance had occurred. Resistance to pyrimethanil, however, has developed in some packinghouse populations of P. digitatum because end users did not follow these guidelines and used the fungicide exclusively. For azoxystrobin, resistance in P. digitatum has only been described for laboratory mutants and for fludioxonil only in mass platings of conidia on selective media in the laboratory or in packinghouse air samplings. Thus, practical resistance to azoxystrobin and fludioxonil has not occurred. Natural resistance frequencies and molecular mechanisms for thiabendazole, imazalil, pyrimethanil, fludioxonil, and azoxystrobin have been studied, and resistant pathogen isolates have been evaluated for their fitness. Anti-resistance strategies focus on sanitation of fruit, equipment, and storage rooms; limitation of pathogen sporulation and spore dispersal; use of fungicide mixtures, pre-mixtures, and rotations; as well as the early detection of resistance.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adaskaveg JE (2004) Evaluation of new postharvest treatments to reduce postharvest decays and improve fruit quality in citrus packinghouse operations. Citrus Research Board, 2004 Annual Report, pp 64–65

    Google Scholar 

  • Adaskaveg JE, Förster H (2010) New developments in postharvest fungicide registrations for edible horticultural crops and use strategies in the United States. In: Prusky D, Gullino ML (eds) Post-harvest pathology: plant pathology in the 21st century: contributions to the 9th international congress. Springer, Dordrecht, pp 107–117

    Google Scholar 

  • Adaskaveg JE, Förster H, Sommer NF (2002) Principles of postharvest pathology and management of decays of edible horticultural crops. In: Kader A (ed) Postharvest technology of horticultural crops, 4th edn, Publication 3311. University of California Agriculture and Natural Resources, Oakland, pp 163–195

    Google Scholar 

  • Adaskaveg JE, Kanetis L, Soto-Estrada A, Förster H (2004) A new era of postharvest decay control in citrus with the simultaneous introduction of three new ‘reduced-risk’ fungicides. Proc Int Soc Citric III:999–1004

    Google Scholar 

  • Barger WR (1928) Sodium bicarbonate as citrus fruit disinfectant. Calif Citrogr 13:164,172–174

    Google Scholar 

  • Baudoin ABAM, Eckert JW (1982) Factors influencing the susceptibility of lemons to infection by Geotrichum candidum. Phytopathology 72:1592–1597

    Article  Google Scholar 

  • Brent KJ (1995) Fungicide resistance in crop pathogens: How can it be managed? FRAC monogr No. 1. GIFAP, Brussels

    Google Scholar 

  • Brent KJ, Hollomon DW (1998) Fungicide resistance: the assessment of risk, FRAC monogr. No. 2. GCPF, Brussels

    Google Scholar 

  • Brent KJ, Hollomon DW (2007) Fungicide resistance in crop pathogens: how can it be managed? 2nd edn, FRAC monogr No. 1. GCPF, Brussels

    Google Scholar 

  • Brown GE, Eckert JW (2000) Penicillium decays – blue mold. In: Timmer LW, Garnsey SM, Graham JH (eds) Compendium of citrus diseases, 2nd edn. American Phytopathological Society Press, St. Paul, p 41

    Google Scholar 

  • Cooke LR, Carlisle DJ, Donaghy C, Quinn M, Perez FM, Deahl KL (2006) The Northern Ireland Phytophthora infestans population 1998–2002 characterized by genotypic and phenotypic markers. Plant Pathol 55:320–330

    Article  CAS  Google Scholar 

  • Davé BA, Kaplan HJ, Petrie JF (1980) The isolation of Penicillium digitatum Sacc. strains tolerant to 2-AB, SOPP, TBZ, and benomyl. Proc Fla State Hortic Soc 93:344–347

    Google Scholar 

  • De Waard MA, Groeneweg H, Van Nistelrooy JGM (1982) Laboratory resistance to fungicides which inhibit ergosterol biosynthesis in Penicillium italicum. Neth J Plant Pathol 88:99–112

    Article  Google Scholar 

  • Eckert JW (1959) Lemon sour rot. Calif Citrogr 45:30–36

    Google Scholar 

  • Eckert JW (1987) Biotypes of Penicillium digitatum with reduced sensitivity to imazalil. Phytopathology 77:1728 (Abstr)

    Google Scholar 

  • Eckert JW (1988) Dynamics of benzimidazole-resistant Penicillia in the development of postharvest decays of citrus and pome fruits. In: Delp CJ (ed) Fungicide resistance in North America. APS Press, St. Paul, pp 31–35

    Google Scholar 

  • Eckert JW, Eaks IL (1989) Postharvest disorders and diseases of citrus fruit. In: Reuther W, Calavan EC, Carman GE (eds) The citrus industry, volume V – crop protection, postharvest technology, and early history of citrus research in California. Publication no. 3326. University of California, Division of Agricultural and Natural Resources, Oakland, pp 179–260

    Google Scholar 

  • Förster H, Adaskaveg JE (2012) Fitness and competitiveness of Penicillium spp. isolates with reduced sensitivity to fludioxonil and pyrimethanil. Phytopathology 102(Suppl 6):S6.9

    Google Scholar 

  • Förster H, Kanetis L, Adaskaveg JE (2004) Spiral gradient dilution, a rapid method for determining growth responses and EC50 values in fungus-fungicide interactions. Phytopathology 94:163–170

    Article  PubMed  Google Scholar 

  • Fritz R, Lanen C, Chapeland-Leclerc F, Leroux P (2003) Effect of the anilinopyrimidine fungicide pyrimethanil on the cystathionine β-lyase of Botrytis cinerea. Pestic Biochem Physiol 77:54–65

    Article  CAS  Google Scholar 

  • Ghosoph JM, Schmidt LS, Margosan DA, Smilanick JL (2007) Imazalil resistance linked to a unique insertion sequence in the PdCYP51 promoter region of Penicillium digitatum. Postharv Biol Technol 44:9–18

    Article  CAS  Google Scholar 

  • Hamamoto H, Hasegawa K, Nakaune R, Lee YJ, Akutsu K, Hibi T (2001) PCR-based detection of sterol demethylation inhibitor-resistant strains of Penicillium digitatum. Pest Manag Sci 57:839–843

    Article  CAS  PubMed  Google Scholar 

  • Harding PR Jr (1962) Differential sensitivity to sodium orthophenylphenate by biphenyl-sensitive and biphenyl-resistant strains of Penicillium digitatum. Plant Dis Rep 46:100–104

    CAS  Google Scholar 

  • Harding PR Jr (1972) Differential sensitivity to thiabendazole by strains of Penicillium italicum and P. digitatum. Plant Dis Rep 56:256–260

    CAS  Google Scholar 

  • Harding PR Jr (1976) R23979, a new imidazole derivative effective against postharvest decay of citrus by molds resistant to thiabendazole, benomyl, and 2-aminobutane. Plant Dis Rep 60:643–646

    CAS  Google Scholar 

  • Hewitt HG (1998) Fungicides in crop protection. CAB International, Cambridge, UK, 221 pp

    Google Scholar 

  • Holmes GJ, Eckert JW (1995) Relative fitness of imazalil-resistant and -sensitive biotypes of Penicillium digitatum. Plant Dis 79:1068–1073

    Article  Google Scholar 

  • Holmes GJ, Eckert JW (1999) Sensitivity of Penicillium digitatum and P. italicum to postharvest citrus fungicides in California. Phytopathology 89:716–721

    Article  CAS  PubMed  Google Scholar 

  • Kader AA (2002) Postharvest technology of horticultural crops, 3rd edn, DANR Publication 3311. University of California, Oakland

    Google Scholar 

  • Kanetis L, Förster H, Adaskaveg JE (2007) Comparative efficacy of the new postharvest fungicides azoxystrobin, fludioxonil, and pyrimethanil for managing citrus green mold. Plant Dis 91:1502–1511

    Article  CAS  Google Scholar 

  • Kanetis L, Förster H, Adaskaveg JE (2008a) Baseline sensitivities for new postharvest fungicides against Penicillium spp. on citrus and multiple resistance evaluations in P. digitatum. Plant Dis 92:301–310

    Article  CAS  Google Scholar 

  • Kanetis L, Förster H, Jones CA, Borkovich KA, Adaskaveg JE (2008b) Characterization of genetic and biochemical mechanisms of fludioxonil and pyrimethanil resistance in field isolates of Penicillium digitatum. Phytopathology 98:205–214

    Article  CAS  PubMed  Google Scholar 

  • Kanetis L, Förster H, Adaskaveg JE (2010) Determination of natural resistance frequencies in Penicillium digitatum using a new air-sampling method and characterization of fludioxonil- and pyrimethanil-resistant isolates. Phytopathology 100:738–746

    Article  CAS  PubMed  Google Scholar 

  • Kendall SJ, Hollomon DW (1998) Fungicide resistance. In: Hutson D, Miyamoto J (eds) Fungicidal activity: chemical and biological approaches to plant protection. Wiley, New York, pp 87–108

    Google Scholar 

  • Koenraadt H, Somerville SC, Jones AL (1992) Characterization of mutations in the beta-tubulin gene of benomyl-resistant field strains of Venturia inaequalis and other plant pathogenic fungi. Phytopathology 82:1348–1354

    Article  Google Scholar 

  • Leroux P, Fritz R, Debieu D, Albertini C, Lanen C, Bach J, Gredt M, Chapeland F (2002) Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Manag Sci 58:876–888

    Article  CAS  PubMed  Google Scholar 

  • Masner P, Muster P, Schmid J (1994) Possible methionine biosynthesis inhibition by pyrimidinamine fungicides. Pestic Sci 42:163–166

    Article  CAS  Google Scholar 

  • McKay AH, Förster H, Adaskaveg JE (2012) Toxicity of selected fungicides to the postharvest pathogens Galactomyces citri-aurantii, G. geotrichum, and Penicillium digitatum and resistance potential to propiconazole. Plant Dis 96:87–96

    Article  CAS  Google Scholar 

  • Muirhead TF (1974) Resistance to benzimidazole fungicides in blue mold of citrus in Queensland. Aust J Exp Agric Anim Husb 14:698–701

    Article  CAS  Google Scholar 

  • Rippon LE, Morris SC (1981) Guazatine control of sour rot in lemons, oranges and tangors under various storage conditions. Sci Hortic 14:245–251

    Article  CAS  Google Scholar 

  • Schmidt LS, Ghosoph JM, Margosan DA, Smilanick JL (2006) Mutation at β-tubulin codon 200 indicated thiabendazole resistance in Penicillium digitatum collected from California citrus packinghouses. Plant Dis 90:765–770

    Article  CAS  Google Scholar 

  • Sierotzki H, Frey R, Wullschleger J, Palermo S, Karlin S, Godwin J, Gisi U (2007) Cytochrome b gene sequence and structure of Pyrenophora teres and P. tritici-repentis and implications for QoI resistance. Pest Manag Sci 63:225–233

    Article  CAS  PubMed  Google Scholar 

  • Suprapta DN, Arai K, Iwai H, Matsuo T (1996) Change in susceptibility of satsuma mandarin fruit to sour rot pathogen (Geotrichum candidum citrus race) with relation to biochemical changes during maturation and storage. Mycoscience 37:209–216

    Article  Google Scholar 

  • Timmer LW, Garnsey SM, Graham JH (2000) Compendium of citrus diseases, 2nd edn. The American Phytopathological Society Press, St. Paul

    Google Scholar 

  • Wild BL (1980) Resistance to citrus green mold Penicillium digitatum Sacc. Doctoral thesis, University of California, Riverside, 89 pp

    Google Scholar 

  • Wild BL (1983) Double resistance by citrus green mould Penicillium digitatum to the fungicides guazatine and benomyl. Ann. Appl. Biol. 103:237-241

    Google Scholar 

  • Zhang Z, Zhu Z, Ma Z, Li H (2009) A molecular mechanism of azoxystrobin resistance in Penicillium digitatum UV mutants and a PCR-based assay for detection of azoxystrobin-resistant strains in packing- or store-house isolates. Int J Food Microbiol 131:157–161

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James E. Adaskaveg .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Japan

About this chapter

Cite this chapter

Adaskaveg, J.E., Förster, H. (2015). Resistance in Postharvest Pathogens of Citrus in the United States. In: Ishii, H., Hollomon, D. (eds) Fungicide Resistance in Plant Pathogens. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55642-8_28

Download citation

Publish with us

Policies and ethics