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Genetic diversity in Monilinia laxa populations in stone fruit species in Hungary

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Abstract

The objectives of this study were firstly, to determine the genetic diversity of Monilinia laxa isolates from Hungary, using the PCR-based inter-simple sequence repeat (ISSR) and randomly amplified polymorphic DNA (RAPD) technique; secondly, to prepare genetic diversity groups based on the dendrograms; and finally, to select some relevant isolates to study their fungicide sensitivity. 55 and 77 random amplified polymorphic ISSR and RAPD markers, of which 23 and 18 were polymorphic and 32 and 59 monomorphic, respectively, were used to assess the genetic diversity and to study the structure of M. laxa populations in Hungary. 27 isolates out of 57 ones were confirmed as M. laxa from several orchards (subpopulations) in three geographical regions, in various inoculum sources and in various hosts, were used. 10 fungicides and 12 isolates selected from genetic diversity groups based on the ISSR dendrograms were used to determine the fungicide sensitivity of the selected isolates. The analysis of population structure revealed that genetic diversity within locations, inoculum sources and host (H S ) accounted for 99 % of the total genetic diversity (H T ), while genetic diversity among locations, inoculum sources and host represented only 1 %. The relative magnitude of gene differentiation between subpopulations (G ST ) and the estimate of the number of migrants per generation (Nm) averaged 0.005–0.009 and 53.9–99.2, respectively, for both ISSR and RAPD data set. The results obtained in dendrograms were in accordance with the gene diversity analysis. Grouping of isolates in the dendrograms was irrespective of whether they came from the same or different geographical locations. There was no relationship between clustering among isolates from inoculum sources and hosts. In the fungicide sensitivity tests, five isolates out of 12 were partly insensitive to boscalid+piraclostrobin, cyprodinil, fenhexamid or prochloraz. Obtained results in genetic diversity of M. laxa populations are discussed together with implications for the management of brown rot.

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References

  • Alfonso C, Raposo R, Melgarejo P (2000) Genetic diversity in Botrytis cinerea populations on vegetable crops in greenhouses in south-eastern Spain. Plant Pathol 49:243–251

    Article  Google Scholar 

  • Boeger JM, Chen RS, McDonald BA (1993) Gene flow between geographic populations of Mycosphaerella graminicola (anamorph Septoria tritici) detected with restriction fragment length polymorphism markers. Phytopathology 83:1148–1154

    Article  CAS  Google Scholar 

  • Byrde RJW, Willetts HJ (1977) The brown rot fungi of fruit: their biology and control. Pergamon, Oxford, UK, p 377

    Google Scholar 

  • Cekic C, Battey NH, Wilkinson MJ (2001) The potential of ISSR-PCR primer-pair combinations for genetic linkage analysis using the seasonal flowering locus in Fragaria as a model. Theor Appl Genet 103:540–546

    Article  CAS  Google Scholar 

  • Colwell RK (2006) EstimateS: statistical estimation of species richness and shared species from samples. Version 8. User’s guide and application. http://purl.oclc.org/estimates

  • Cote M-J, Tardif M-C, Meldrum AJ (2004) Identification of Monilinia fructigena, M. fructicola, M. laxa, and Monilia polystroma on inoculated and naturally infected fruit using multiplex PCR. Plant Dis 88:1219–1225

    Article  CAS  Google Scholar 

  • De Cal A, Melgarejo P (1999) Effects of long-wave UV light on Monilinia growth and identification of species. Plant Dis 83:62–65

    Article  Google Scholar 

  • Di Lenna P, Marciano PM, Magro P (1981) Comparative investigation on morphological and physiological features of three isolates of Botrytis cinerea. J Phytopathol 100:203–211

    Article  Google Scholar 

  • Elmer PAG, Gaunt RE (1994) The biological characteristics of dicarboximide resistant isolates of Monilinia fructicola from New Zealand stone-fruit orchards. Plant Pathol 43:130–137

    Article  Google Scholar 

  • Fan JY, Guo L-Y, Xu JP, Luo Y, Michailides TJ (2010) Genetic diversity of populations of Monilinia fructicola (Fungi, Ascomycota, Helotiales) from China. J Eukar Microbiol 57:206–212

    Article  CAS  Google Scholar 

  • Förster H, Adaskaveg JE (2000) Early brown rot infections in sweet cherry fruit are detected by Monilinia-specific DNA primers. Phytopathology 90:171–178

    Article  Google Scholar 

  • Fulton CE, van Leeuwen GCM, Brown AE (1999) Genetic variation among and within Monilinia species causing brown rot of stone and pome fruits. Eur J Plant Pathol 105:495–500

    Article  Google Scholar 

  • Gell I, Larena I, Melgarejo P (2007) Genetic diversity in Monilinia laxa populations in peach orchards in Spain. J Phytopathol 155:549–556

    Article  CAS  Google Scholar 

  • Gril T, Celar F, Munda A, Javornik B, Jakse J (2008) AFLP analysis of intraspecific variation between Monilinia laxa isolates from different hosts. Plant Dis 92:1616–1624

    Article  CAS  Google Scholar 

  • Gril T, Celar F, Javornik B, Jakse J (2010) Fluorescent AFLP fingerprinting of Monilinia fructicola. J Plant Dis Prot 117:168–172

    CAS  Google Scholar 

  • Grindle M (1979) Phenotypic differences between natural and induced variants of Botrytis cinerea. J Gen Microbiol 111:109–120

    Article  Google Scholar 

  • Groppe K, Sanders I, Wiemken A, Boller T (1995) A microsatellite marker for studying the ecology and diversity of fungal endophytes (Epichlöe spp.) in grasses. Appl Environ Microbiol 61:3943–3949

    CAS  Google Scholar 

  • Grünwald NJ, Goodwin SB, Milgroom MG, Fry WE (2003) Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 93:738–746

    Article  Google Scholar 

  • Hoffman GM (1974) Zum Vorkommen von Heterokaryose bei Monilinia laxa. Phytopathol Z 79:193–202

    Article  Google Scholar 

  • Holb IJ (2003) The brown rot fungi of fruit crops (Monilinia spp.). I. Important features of their biology. Int J Hort Sci 9(3–4):23–36

    Google Scholar 

  • Holb IJ (2004) The brown rot fungi of fruit crops (Monilinia spp.). III. Important features of their disease control. Int J Hort Sci 10(4):31–48

    Google Scholar 

  • Holb IJ (2008) Monitoring conidial density of Monilinia fructigena in the air in relation to brown rot development in integrated and organic apple orchards. Eur J Plant Pathol 120:397–408

    Article  Google Scholar 

  • Holb IJ, Scherm H (2007) Temporal dynamics of brown rot in different apple management systems and importance of dropped fruit for disease development. Phytopathology 97:1004–1011

    Article  Google Scholar 

  • Holb IJ, Schnabel G (2005) Comparison of fungicide treatments combined with sanitation practices on brown rot blossom blight incidence, phytotoxicity, and yield for organic sour cherry production. Plant Dis 89:1164–1170

    Article  CAS  Google Scholar 

  • Holb IJ, Schnabel G (2007) Differential effect of triazoles on mycelial growth and disease measurements of Monilinia fructicola isolates with reduced sensitivity to DMI fungicides. Crop Prot 26:753–759

    Article  CAS  Google Scholar 

  • Holb IJ, Schnabel G (2008) The benefits of combining elemental sulfur with a DMI fungicide to control Monilinia fructicola isolates resistant to propiconazole. Pest Manag Sci 64:156–164

    Article  CAS  Google Scholar 

  • Larena I, Torres R, De Cal A, Linan M, Melgarejo P, Domenichini P, Bellini A, Mandrin JF, Lichou J, Ochoa de Eribe X, Usall J (2005) Biological control of postharvest brown rot (Monilinia spp.) of peaches by field applications of Epicoccum nigrum. Biol Control 32:305–310

    Article  Google Scholar 

  • Lim S, Notley-McRobb L, Lim M, Carter DA (2004) A comparison of nature and abundance of microsatellite in 14 fungal genomes. Fungal Genet Biol 41:1025–1036

    Article  CAS  Google Scholar 

  • Ma ZH, Yoshimura MA, Michailides TJ (2003a) Identification and characterization of benzimidazole resistance in Monilinia fructicola from stone fruit orchards in California. Appl Environ Microbiol 69:7145–7152

    Article  CAS  Google Scholar 

  • Ma Z, Luo Y, Michailides TJ (2003b) Nested PCR assays for detection of Monilinia fructicola in stone fruit orchards and Botryosphaeria dothidea from pistachios in California. J Phytopathol 151:312–332

    Article  CAS  Google Scholar 

  • Ma ZH, Yoshimura MA, Holtz BA, Michailides TJ (2005) Characterization and PCR-based detection of benzimidazole-resistant isolates of Monilinia laxa in California. Pest Manag Sci 61:449–457

    Article  CAS  Google Scholar 

  • Majer D, Lewis PG, Mithen R (1998) Genetic variation among field isolates of Pyrenopeziza brassicae. Plant Pathol 47:22–28

    Article  Google Scholar 

  • Meyer W, Mitchell TG, Freedman EZ, Vilgalys R (1993) Hybridization probes for conventional DNA fingerprinting used as single primers in the polymerase chain reaction to distinguish strains of Cryptococcus neoformans. J Clinical Microbiol 31:2274–2280

    CAS  Google Scholar 

  • Moyano C, Alfonso C, Gallego J, Raposo R, Melgarejo P (2003) Comparison of RAPD and AFLP marker analysis as a means to study the genetic structure of Botrytis cinerea populations. Eur J Plant Pathol 109:515–522

    Article  CAS  Google Scholar 

  • Nei M (1975) Molecular population genetics and evolution. American Elsevier, New York, p 175

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, NY, p 187

    Google Scholar 

  • Ogawa JM, English H (1991) Diseases of temperate zone tree fruit and nut crops. University of California, Division of Agriculture and Natural Resources, Oakland, CA, USA, p 574

  • Ogawa JM, Manji BT, Sonoda RM (1985) Management of the brown rot disease on stone fruits and almonds in California. NY State Agric Exp Stn Geneva Specific Rep 55:8–15

    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 diseases. APS Press, St. Paul, MN, pp 7–10

    Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Rohlf FG (1992) NTSYS-pc numerical taxonomic and multivariate analysis system version 1.7. Owner manual, p 211

  • Sanoamuang N, Gaunt RE (1995) Persistence and fitness of carbendazim-resistant and dicarboximide-resistant isolates of Monilinia fructicola (Wint.) Honey in flowers, shoots and fruit of stone fruit. Plant Pathol 44:448–457

    Article  Google Scholar 

  • Scherm H, Emery KM (2003) Vegetative compatibility in populations of Monilinia fructicola from Georgia peach orchards. Acta Hort 592:725–728

    Google Scholar 

  • Sica M, Gamba G, Montieri S, Gaudio L, Aceto S (2005) ISSR markers show differentiation among Italian populations of Asparagus acutifolius L. BMC Genet 6:17

    Article  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy- the principles and practice of numerical classification. W. H. Freeman, San Francisco, CA, p 246

    Google Scholar 

  • Snyder CL, Jones AL (1999) Genetic variation between strains of Monilinia fructicola and Monilinia laxa isolated from cherries in Michigan. Can J Plant Pathol 21:70–77

    Article  CAS  Google Scholar 

  • Szabadi G (2010) Növényvédő szerek, termésnövelő anyagok I. [Plant protection products, plant growth promoting materials I.]. Agrinex Bt, Budapest, Hungary, p 540 (in Hungarian)

  • Tamm L (1994) Epidemiological aspects of sweet cherry blossom blight caused by Monilinia laxa. University of Basel, Schönenbuch, Switzerland, PhD Thesis

  • Tamm L, Minder CE, Flückinger W (1995) Phenological analyses of brown rot blossom blight of sweet cherry caused by Monilinia laxa. Phytopathology 85:401–418

    Google Scholar 

  • Tamm L, Häseli J, 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 Hort 638:333–339

    Google Scholar 

  • Topolovec-Pintaric S, Milicevic T, Cvjetkovic B (2004) Genetic diversity and dynamic of pyrimethanil-resistant phenotype in population of Botrytis cinerea Pers.: Fr. in one wine-growing area in Croatia. J Plant Dis Prot 111:451–460

    Google Scholar 

  • Vasseur V, Rey P, Bellanger E, Brygoo Y, Tirilly Y (2005) Molecular characterization of Pythium group F isolates by ribosomal- and intermicrosatellite-DNA regions analysis. Eur J Plant Pathol 112:301–310

    Article  CAS  Google Scholar 

  • Villarino M, Larena I, Martinez F, Melgarejo P, De Cal A (2012) Analysis of genetic diversity in Monilinia fructicola from the Ebro Valley in Spain using ISSR and RAPD markers. Eur J Plant Pathol 132:511–524

    Article  CAS  Google Scholar 

  • Wangsomboondee T, Groves CT, Shoemaker PB, Cubeta MA, Ristaino JB (2002) Phytophthora infestans populations from tomato and potato in North Carolina differ in genetic diversity and structure. Phytopathol 92:1189–1195

    Article  CAS  Google Scholar 

  • Wherrett AD, Sivasithamparam K, Kumar S (2001) Detection of possible systemic fungicide resistance in Western Australian Monilinia populations. Phytopathology 91:S95

    Google Scholar 

  • Wormald H (1954) The brown rot disease of fruit trees. Ministry of agriculture, fisheries and food, technical bulletin No. 3, Interscience Publishers, London

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Article  CAS  Google Scholar 

  • Xu XM, Robinson JD (2000) Epidemiology of brown rot (Monilinia fructigena) on apple: infection of fruits by conidia. Plant Pathol 49:201–206

    Article  Google Scholar 

  • Xu XM, Robinson JD, Berrie AM, Harris DC (2001) Spatio-temporal dynamics of brown rot (Monilinia fructigena) on apple and pear. Plant Pathol 50:569–578

    Article  Google Scholar 

  • Zehr EI, Toler JE, Luszcz LA (1991) Spread and persistence of benomyl-resistant Monilinia fructicola in South Carolina peach orchards. Plant Dis 75:590–593

    Article  CAS  Google Scholar 

  • Zehr EI, Luszcz LA, Olien WC, Newall WC, Toler JE (1999) Reduced sensitivity in Monilinia fructicola to propiconazole following prolonged exposure in peach orchards. Plant Dis 83:913–916

    Article  Google Scholar 

  • Zhou S, Smith DR, Stanosz GR (2001) Differentiation of Botryosphaeria species and related anamorphic fungi using Inter Simple or Short Sequence Repeat (ISSR) fingerprinting. Mycol Res 105:919–926

    Article  CAS  Google Scholar 

  • Zhu XQ, Chen XY, Guo LY (2011) Population structure of brown rot fungi on stone fruits in China. Plant Dis 95:1285–1291

    Article  Google Scholar 

  • Zietjiewicz E, Rafalski A, Labuda D (1994) Genome fingerprinting by simple sequence repeat (SSR)-anchored polymerase chain reaction amplification. Genomics 20:176–183

    Article  Google Scholar 

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Acknowledgments

Thanks are due to farm managers (F. Abonyi, F. Abonyi, Sr.) and J. Holb, Sr. for their excellent cooperation. This research was partly supported by grants of the Hungarian Scientific Research Fund (K78399 and K108333) and the NKTH-OM-00227/2008 as well as by a János Bolyai Research Fellowship awarded to Imre J. Holb. This research was also supported by the European Union and the State of Hungary, co-financed by the European Social Fund in the framework of TÁMOP-4.2.4.A/ 2-11/1-2012-0001 ‘National Excellence Program’ under the project number: A2-SZJ-TOK-13-0061.

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Fazekas, M., Madar, A., Sipiczki, M. et al. Genetic diversity in Monilinia laxa populations in stone fruit species in Hungary. World J Microbiol Biotechnol 30, 1879–1892 (2014). https://doi.org/10.1007/s11274-014-1613-4

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  • DOI: https://doi.org/10.1007/s11274-014-1613-4

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