The population of Sclerotinia sclerotiorum affecting common bean in Brazil is structured by mycelial compatibility groups

  • Miller da S. Lehner
  • Rhaphael A. Silva
  • Trazilbo J. Paula Júnior
  • José Eustáquio S. Carneiro
  • Eduardo S. G. Mizubuti


The genetic structure of a population of Sclerotinia sclerotiorum causing white mold on common bean in Brazil was studied using microsatellite (SSR) loci and mycelial compatibility groups (MCGs). A total of 300 isolates were analyzed and 154 SSR haplotypes and 32 MCGs were identified. Two MCGs were widely distributed and accounted for 70% of the isolates. Six SSR haplotypes were associated with more than one closely related MCG. There was no evidence of random association of alleles among loci when the population comprised by all MCGs was analyzed, suggesting that outcrossing is absent or rare. Nevertheless, there was evidence of random mating within the major MCGs. Seven genetic groups were identified, one of them comprising only highly pigmented isolates. Isolates of distinct MCGs did not differ in virulence. There was strong genetic differentiation among MCGs: more than 95% of the total genetic variation was attributed to differences among these groups. Therefore, MCGs contribute to the structure of the population of S. sclerotiorum in Brazil.


White mold Genetics Variability Resistance Phaseolus vulgaris 



The authors were supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq. This research was supported by FAPEMIG and CNPq. The authors thank Dr. Antônio Félix da Costa, Dr. Hélcio Costa and Airton Luiz Pazinato for sampling of S. sclerotiorum isolates in Pernambuco, Espírito Santo and São Paulo state, respectively. The authors thank Dr. Linda Kohn for sending DNA of S. sclerotiorum isolate LMK211.

Supplementary material

40858_2018_270_MOESM1_ESM.docx (59 kb)
Supplementary table 1 Geographic origin and allele size at each microsatellite locus of 182 isolates of Sclerotinia sclerotiorum from common bean fields in Brazil. The data related to the remaining 118 isolates can be found at: (DOCX 59 kb)
40858_2018_270_MOESM2_ESM.doc (36 kb)
Supplementary table 2 Number of alleles found in the Brazilian population of Sclerotinia sclerotiorum from common bean compared to those found in other studies, size range and gene diversity for each microsatellite locus. (DOC 36 kb)


  1. Abd-Elmagid A, Garrido PA, Robert H, Lyles JL, Mansfield MA, Gugino BK, Smith DL, Melouk HA, Garzon CD (2013) Discriminatory simplex and multiplex PCR for four species of the genus Sclerotinia. Journal of Microbiological Methods 92:293–300CrossRefGoogle Scholar
  2. Agapow PM, Burt A (2001) Indices of multilocus linkage disequilibrium. Molecular Ecology Notes 1:101–102CrossRefGoogle Scholar
  3. Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, Couloux A, Coutinho PM, de Vries RP, Dyer PS, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L, Lapalu N, Plummer KM, Pradier JM, Quévillon E, Sharon A, Simon A, ten Have A, Tudzynski B, Tudzynski P, Wincker P, Andrew M, Anthouard V, Beever RE, Beffa R, Benoit I, Bouzid O, Brault B, Chen Z, Choquer M, Collémare J, Cotton P, Danchin EG, da Silva C, Gautier A, Giraud C, Giraud T, Gonzalez C, Grossetete S, Güldener U, Henrissat B, Howlett BJ, Kodira C, Kretschmer M, Lappartient A, Leroch M, Levis C, Mauceli E, Neuvéglise C, Oeser B, Pearson M, Poulain J, Poussereau N, Quesneville H, Rascle C, Schumacher J, Ségurens B, Sexton A, Silva E, Sirven C, Soanes DM, Talbot NJ, Templeton M, Yandava C, Yarden O, Zeng Q, Rollins JA, Lebrun MH, Dickman M (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genetics 7:e1002230CrossRefGoogle Scholar
  4. Atallah ZK, Larget B, Chen X, Johnson DA (2004) High genetic diversity, phenotypic uniformity, and evidence of outcrossing in Sclerotinia sclerotiorum in the Columbia basin of Washington state. Phytopathology 94:737–742CrossRefGoogle Scholar
  5. Attanayake RN, Carter PA, Jiang D, Del Río-Mendoza L, Chen W (2013) Sclerotinia sclerotiorum populations infecting canola from China and the United States are genetically and phenotypically distinct. Phytopathology 103:750–761CrossRefGoogle Scholar
  6. Attanayake RN, Tennekoon V, Johnson DA, Porter LD, del Río-Mendoza L, Jiang D, Chen W (2014) Inferring outcrossing in the homothallic fungus Sclerotinia sclerotiorum using linkage disequilibrium decay. Heredity 113:353–363CrossRefGoogle Scholar
  7. Clarkson JP, Coventry E, Kitchen J, Carter HE, Whipps JM (2013) Population structure of Sclerotinia sclerotiorum in crop and wild hosts in the UK. Plant Pathology 62:309–324CrossRefGoogle Scholar
  8. CONAB (2018) Acompanhamento de Safra Brasileira de Grãos. CONAB survey, March 2018. Companhia Nacional de Abastecimento, BrasíliaGoogle Scholar
  9. Cubeta MA, Cody BR, Kohli Y, Kohn LM (1997) Clonality in Sclerotinia sclerotiorum on infected cabbage in eastern North Carolina. Phytopathology 87:1000–1004CrossRefGoogle Scholar
  10. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10:564–567CrossRefGoogle Scholar
  11. Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a bayesian perspective. Genetics 180:977–993CrossRefGoogle Scholar
  12. Gomes EV, Nascimento LB, Freitas MA, Nasser LCB, Petrofeza S (2011) Microsatellite markers reveal genetic variation within Sclerotinia sclerotiorum populations in irrigated dry bean crops in Brazil. Journal of Phytopathology 159:94–99CrossRefGoogle Scholar
  13. Grünwald NJ, Goodwin SB, Milgroom MG, Fry WE (2003). Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 93:738–746Google Scholar
  14. Hambleton S, Walker C, Kohn LM (2002) Clonal lineages of Sclerotinia sclerotiorum previously known from other crops predominate in 1999–2000 samples from Ontario and Quebec soybean. Canadian Journal of Plant Pathology 24:309–315CrossRefGoogle Scholar
  15. Hemmati R, Javan-Nikkhah M, Linde CC (2009) Population genetic structure of Sclerotinia sclerotiorum on canola in Iran. European Journal of Plant Pathology 125:617–628CrossRefGoogle Scholar
  16. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefGoogle Scholar
  17. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11:94CrossRefGoogle Scholar
  18. Kamvar ZN, Tabima JF, Grunwald NJ (2014) POPPR: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281CrossRefGoogle Scholar
  19. Kamvar ZN, Amaradasa BS, Jhala R, McCoy S, Steadman JR, Everhart SE (2017) Population structure and phenotypic variation of Sclerotinia sclerotiorum from dry bean (Phaseolus vulgaris) in the United States. PeerJ 5:e4152CrossRefGoogle Scholar
  20. Kohli Y, Morrall AA, Anderson JB, Kohn LM (1992) Local and trans-Canadian clonal distribution of Sclerotinia sclerotiorum on Canola. Phytopathology 82:875–880CrossRefGoogle Scholar
  21. Kohli Y, Kohn LM (1998) Random Association among Alleles in Clonal Populations of Sclerotinia sclerotiorum. Fungal Genet Biol 23:139–149Google Scholar
  22. Kull LS, Pederson WL, Palmquist D, Hartman GL (2004) Mycelial compatibility groupings and virulence of Sclerotinia sclerotiorum. Plant Disease 88:325–332CrossRefGoogle Scholar
  23. Lehner MS, Mizubuti ESG (2017) Are Sclerotinia sclerotiorum populations from the tropics more variable than those from subtropical and temperate zones? Tropical Plant Pathology 42:61–69CrossRefGoogle Scholar
  24. Lehner MS, Paula Júnior TJ, Hora Júnior BT, Teixeira H, Vieira RF, Carneiro JES, Mizubuti ESG (2015) Low genetic variability in Sclerotinia sclerotiorum populations from common bean fields in Minas Gerais state, Brazil, at regional, local and micro-scales. Plant Pathology 64:921–931CrossRefGoogle Scholar
  25. Lehner MS, Lima RC, Carneiro JES, Paula Júnior TJ, Vieira RF, Mizubuti ESG (2016a) Similar aggressiveness of phenotypically and genotypically distinct isolates of Sclerotinia sclerotiorum. Plant Disease 100:360–366CrossRefGoogle Scholar
  26. Lehner MS, Paula Júnior TJ, Mizubuti ESG (2016b) Does hyphal-tip ensure the same allelic composition as monosporic isolates of Sclerotinia sclerotiorum? Journal of Phytopathology 164:417–420CrossRefGoogle Scholar
  27. Lehner MS, Paula Júnior TJ, Del Ponte EM, Mizubuti ESG, Pethybridge SJ (2017) Independently founded populations of Sclerotinia sclerotiorum from a tropical and atemperate region have similar genetic structure. PLoS One 12:e0173915CrossRefGoogle Scholar
  28. Leslie JF (1993) Fungal vegetative compatibility. Annual Review of Phytopathology 31:127–150CrossRefGoogle Scholar
  29. Malvárez G, Carbone I, Grunwald NJ, Subbarao KV, Schafer M, Kohn LM (2007) New populations of Sclerotinia sclerotiorum from lettuce in California and peas and lentils in Washington. Phytopathology 97:470–483CrossRefGoogle Scholar
  30. Maynard-Smith J, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria? Proceedings of the National Academy of Sciences of the United States of America 90:4384–4388CrossRefGoogle Scholar
  31. McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology 40:349–379CrossRefGoogle Scholar
  32. Meirmans PG, van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes 4:792–794CrossRefGoogle Scholar
  33. Mert-Türk F, Ipek M, Mermer D, Nicholson P (2007) Microsatellite and morphological markers reveal genetic variation within a population of Sclerotinia sclerotiorum from oilseed rape in the Çanakkale Province of Turkey. Journal of Phytopathology 155:182–187CrossRefGoogle Scholar
  34. Milgroom MG (1996) Recombination and the multilocus structure of fungal populations. Annual Review of Phytopathology 34:457–477CrossRefGoogle Scholar
  35. Nei M (1973) Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America 70:3321–3323Google Scholar
  36. Nei M (1978) Estimation of average heterozygosity and genetic distance from a number of individuals. Genetics 89:538–590Google Scholar
  37. Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models: regression, analysis of variance, and experimental designs. Irwin, Burr Ridge, p 1181Google Scholar
  38. R Core Team (2018). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL
  39. Remesal E, Jordan-Ramírez R, Jimenez-Díaz RM, Navas-Cortes JA (2012) Mycelial compatibility groups and pathogenic diversity in Sclerotium rolfsii populations from sugar beet crops in Mediterranean-type climate regions. Plant Pathology 61:739–753CrossRefGoogle Scholar
  40. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8:103–106CrossRefGoogle Scholar
  41. Schafer MR, Kohn LM (2006) An optimized method for mycelial compatibility testing in Sclerotinia sclerotiorum. Mycologia 98:593–597CrossRefGoogle Scholar
  42. Sexton AC, Howlett BJ (2004) Microsatellite markers reveal genetic differentiation among populations of Sclerotinia sclerotiorum from Australian canola fields. Current Genetics 46:357–365CrossRefGoogle Scholar
  43. Sirjusingh C, Kohn LM (2001) Characterization of microsatellites in the fungal plant pathogen, Sclerotinia sclerotiorum. Molecular Ecology Notes 1:267–269CrossRefGoogle Scholar
  44. Taylor JM, Jacobson DJ, Fisher MC (1999) The evolution of asexual fungi: reproduction. speciation and classification. Annual Review of Phytopathology 37:197–246CrossRefGoogle Scholar
  45. Tibayrenc M, Ayala FJ (2012) Reproductive clonality of pathogens: a perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa. Proceedings of the National Academy of Sciences of the United States of America 109:3305–3313CrossRefGoogle Scholar
  46. Willetts HJ, Wong JA (1980) The biology of Sclerotinia sclerotiorum, S. trifoliorum, and S. minor with emphasis on specific nomenclature. Botanical Review 46:101–165CrossRefGoogle Scholar
  47. Zhou F, Zhang XL, Li JL, Zhu FX (2014) Dimethachlon resistance in Sclerotinia sclerotiorum in China. Plant Disease 98:1221–1226CrossRefGoogle Scholar

Copyright information

© Sociedade Brasileira de Fitopatologia 2018

Authors and Affiliations

  1. 1.Programa de Pós-graduação em Genética e MelhoramentoUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Departamento de FitopatologiaUniversidade Federal de ViçosaViçosaBrazil
  3. 3.Empresa de Pesquisa Agropecuária de Minas Gerais (EPAMIG)ViçosaBrazil
  4. 4.Departamento de FitotecniaUniversidade Federal de ViçosaViçosaBrazil

Personalised recommendations