Abstract
Monilinia fructicola, causal agent of brown rot of stone fruits, is an economically important problem worldwide. Six of the sequence tagged microsatellite sites developed for M. fructicola were used to genotype 68 M. fructicola isolates, which included isolates from three cities in Turkey (n = 42) that were compared to isolates from the USA (n = 15) and Italy (n = 11). AMOVA indicated a significant differentiation among samples from the three different countries. Samples from Turkey represented with nine haplotypes indicating a low diversity according to these markers. Samples from the USA with 12 haplotypes showed the highest genetic diversity values among the sample group from the three countries. However, all the samples from Italy were found as a single haplotype with those markers. Based on Nei’s genetic distance measurements, the single genotype from Italy was distinct from the others and samples from Turkey and the USA were genetically closer to each other, which also presented on the principal coordinate plot. While informative, these results suggest that ascertainment bias in marker development may limit the power of these markers when applied to populations of M. fructicola from other locations in the world. Knowledge on genetic diversities and comparative analysis provides valuable insight for recent changes and movements in pathogen populations which is important for the disease management.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs41348-021-00504-4/MediaObjects/41348_2021_504_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs41348-021-00504-4/MediaObjects/41348_2021_504_Fig2_HTML.png)
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Abate D, Pastore C, Gerin D, De Miccolis Angelini RM, Rotolo C, Pollastro S, Faretra F (2018a) Characterization of Monilinia spp. populations on stone fruit in South Italy. Plant Dis 102:1708–1717
Abate D, De Miccolis Angelini RM, Rotolo C, Pollastro S, Faretra F (2018b) Mating system in the brown rot pathogens Monilinia fructicola, M. laxa, and M. fructigena. Phytopathology 108(11):1315–1325
Attanayake RN, Xu L, Chen W (2019) Sclerotinia sclerotiorum populations: clonal or recombining? Tropical Plant Pathol 44(1):23–31
Blacket MJ, Robin C, Good RT, Lee SF, Miller AD (2012) Universal primers for fluorescent labelling of PCR fragments—an efficient and cost-effective approach to genoty** by fluorescence. Mol Ecol Resour 12(3):456–463
Bryde R, Willetts H (1977) The brown rot fungi of fruit: their biology and control. Pergamon Press, Oxford
Casals C, Teixidó N, Viñas I, Llauradó S, Usall J (2010) Control of Monilinia spp on stone fruit by curing treatments: Part I. The effect of temperature, exposure time and relative humidity on curing efficacy. Postharvest Biol Technol 56(1):19–25
Chen F, Liu X, Schnabel G (2013) First report of brown rot caused by Monilinia fructicola in sweet cherry in Maryland. Plant Dis 97(1):145–145
Everhart SE, Askew A, Seymour L, Glenn TC, Scherm H (2012) Spatial patterns of brown rot epidemics and development of microsatellite markers for analyzing fine-scale genetic structure of Monilinia fructicola populations within peach tree canopies. Plant Health Progress 13(1):28
Everhart SE, Scherm H (2015) Fine-scale genetic structure of Monilinia fructicola during brown rot epidemics within individual peach tree canopies. Phytopathology 105(4):542–549
Fan J-Y et al (2010) Genetic diversity of populations of Monilinia fructicola (Fungi, Ascomycota, Helotiales) from China. J Eukaryot Microbiol 57(2):206–212
Fazekas M et al (2014) Genetic diversity in Monilinia laxa populations in stone fruit species in Hungary. World J Microbiol Biotechnol 30(6):1879–1892
Glenn TC (2001) 5′ tags: A cheap way to fluorescently tag PCR products. Website http://dna.uga.edu/wp-content/uploads/sites/11/2013/12/5-Primer-Tags-PCR-products.pdf
Hartmann FE, Rodríguez de la Vega RC, Carpentier F, Gladieux P, Cornille A, Hood ME, Giraud T (2019) Understanding adaptation, coevolution, host specialization, and mating system in castrating anther-smut fungi by combining population and comparative genomics. Annu Rev Phytopathol 57:431–457
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(4):397
Hrustić J, Delibašić G, Stanković I, Grahovac M, Krstić B, Bulajić A, Tanović B (2015) Monilinia spp. causing brown rot of stone fruit in Serbia. Plant Dis 99(5):709–717
Jänsch M, Frey JE, Hilber-Bodmer M, Broggini GA, Weger J, Schnabel G, Patocchi A (2012) SSR marker analysis of Monilinia fructicola from Swiss apricots suggests introduction of the pathogen from neighbouring countries and the United States. Plant Pathol 61(2):247–254
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Kozhar O, Larsen MM, Grünwald NJ, Peever TL (2020) Fungal evolution in anthropogenic environments: Botrytis cinerea populations infecting small fruit hosts in the Pacific Northwest rapidly adapt to human-induced selection pressures. Appl Environ Microbiol 86(9):e02908–e02919
Lane C (2002) A synoptic key for differentiation of Monilinia fructicola, M. fructigena and M. laxa, based on examination of cultural characters. EPPO Bull 32(3):489–493
Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142(3):1061–1064
Möller M, Stukenbrock EH (2017) Evolution and genome architecture in fungal plant pathogens. Nat Rev Microbiol 15(12):756
Nei M (1972) Genetic distance between populations. Am Nat 106(949):283–292
Ozkilinc H, Frenkel O, Abbo S, Eshed R, Sherman A, Shtienberg D, Can C (2010) A comparative study of Turkish and Israeli populations of Didymella rabiei, the ascochyta blight pathogen of chickpea. Plant Pathol 59(3):492–503
Ozkilinc H, Akamatsu H, Abang M, Thomas K, Chilvers MI, Peever TL (2011) Development, characterization and linkage analysis of microsatellite loci for the Ascochyta blight pathogen of faba bean, Didymella fabae. J Microbiol Methods 87(1):128–130
Ozkilinc H, Thomas K, Abang M, Peever TL (2015) Population structure and reproductive mode of Didymella fabae in Syria. Plant Pathol 64(5):1110–1119
Ozkilinc H, Yildiz G, Silan E, Arslan K, Guven H, Altinok HH, Altindag R, Durak MR (2020) Species diversity, mating type assays and aggressiveness patterns of Monilinia pathogens causing brown rot of peach fruit in Turkey. Eur J Plant Pathol 157(4):799–814
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28(19):2537–2539
Schnabel G, Chen F, Everhart SE, Bridges WC, Liu X (2014) Studies on sensitivity reduction in solo and mixture treatments and fungicide-induced mutagenesis in Monilinia fructicola. In: Dehne HW, Deising HB et al (eds) Modern fungicides and antifungal compounds, vol 7. Deutsche Phytomedizinische Gesellschaft, Braunschweig, pp 263–2682014
Tran TT et al (2019) Genotypic structure of Monilinia populations in Western Australia two decades after incursion. Australas Plant Pathol 48(2):167–178
Villarino M et al (2012) Analysis of genetic diversity in Monilinia fructicola from the Ebro Valley in Spain using ISSR and RAPD markers. Eur J Plant Pathol 132(4):511–524
Acknowledgements
This study was supported by Scientific Research Projects Coordination Unit of Canakkale Onsekiz Mart University (Project Number: FYL-2018-2587). HO designed the research, contributed to analysis and interpretation of the data, wrote the manuscript; HG performed experimental part and some parts of data analysis; SEE advised in experimental protocols, organized sending samples from the USA and commented on manuscript, RMDMA arranged the Italian samples to send and commented on manuscript. Authors also thank to Dr. Harald Scherm (University of Georgia, Athens, GA/USA) and Prof. Francesco Faretra (University of Bari Aldo Moro, Italy) for providing and allowing the samples from their collections.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest in the publication.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Guven, H., Everhart, S.E., De Miccolis Angelini, R.M. et al. Genetic diversity assessments of brown rot pathogen Monilinia fructicola based on the six simple sequence repeat loci. J Plant Dis Prot 128, 1459–1465 (2021). https://doi.org/10.1007/s41348-021-00504-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41348-021-00504-4