Tropical Plant Pathology

, Volume 44, Issue 1, pp 32–40 | Cite as

Something in the agar does not compute: on the discriminatory power of mycelial compatibility in Sclerotinia sclerotiorum

  • Zhian N. Kamvar
  • Sydney E. EverhartEmail author


Mycelial compatibility, the ability for fungal isolates to grow together and form one single colony, was defined for Sclerotinia sclerotiorum nearly 30 years ago and has since been used as a marker to describe clonal variation in population genetic studies. While evidence suggests an associative relationship between mycelial compatibility and vegetative compatibility, contemporary research has treated these traits as analogous. As molecular markers have been developed to describe genetic variation, researchers combined these with the mycelial compatibility groups to assess and to define clonal lineages. However, several inconsistent relationships between mycelial compatibility groups, haplotypes, and even vegetative compatibility groups have been observed throughout the literature, suggesting that mycelial compatibility may not accurately reflect self-recognition. We argue that the Sclerotinia community needs to move beyond using MCG data in population genetic studies.


Vegetative compatibility Microsatellite genotyping 



We would like to thank Gerard Adams for stimulating discussions on the nature of vegetative compatibility in filamentous fungi. We additionally would like to thank two anonymous reviewers for their comments that improved the clarity of the final manuscript.

Funding Sources

Funding was provided for salaries and previous research on this topic that was also reviewed here. This includes partial support from the Nebraska Agricultural Experiment Station with funding from the Hatch Act (Accession Number 1007272) through the USDA National Institute of Food and Agriculture, grant #58-5442-2-209 from the USDA-ARS National Sclerotinia Initiative to SEE, and start-up funds from the University of Nebraska-Lincoln (UNL) to SEE. Funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.


  1. Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA (2007) Standardizing methods to address clonality in population studies. Molecular Ecology 16:5115–5139CrossRefGoogle Scholar
  2. 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
  3. Atehnkeng J, Donner M, Ojiambo PS, Ikotun B, Augusto J, Cotty PJ, Bandyopadhyay R (2016) Environmental distribution and genetic diversity of vegetative compatibility groups determine biocontrol strategies to mitigate aflatoxin contamination of maize by Aspergillus flavus. Microbial Biotechnology 9:75–88CrossRefGoogle Scholar
  4. Attanayake RN, Porter L, Johnson DA, Chen W (2012) Genetic and phenotypic diversity and random association of DNA markers of isolates of the fungal plant pathogen Sclerotinia sclerotiorum from soil on a fine geographic scale. Soil Biology and Biochemistry 55:28–36CrossRefGoogle Scholar
  5. 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
  6. Bailleul D, Stoeckel S, Arnaud-Haond S (2016) RClone: a package to identify MultiLocus clonal lineages and handle clonal data sets in R. Methods in Ecology and Evolution 7:966–970CrossRefGoogle Scholar
  7. Barari H, Alavi V, Badalyan SM (2012) Genetic and morphological differences among populations of Sclerotinia sclerotiorum by microsatellite markers, mycelial compatibility groups (MCGs) and aggressiveness in North Iran. Romanian Agricultural Research 29:323–331Google Scholar
  8. Carbone I, Kohn LM (2001) Multilocus nested haplotype networks extended with DNA fingerprints show common origin and fine-scale, ongoing genetic divergence in a wild microbial metapopulation. Molecular Ecology 10:2409–2422CrossRefGoogle Scholar
  9. Carling DE, Kuninaga S, Leiner RH (1988) Relatedness within and among intraspecific groups of Rhizoctonia solani: a comparison of grouping by anastomosis and by DNA hybridization. Phytoparasitica 16:209–210Google Scholar
  10. Chang SW, Jo Y-K, Chang T, Jung G (2014) Evidence for genetic similarity of vegetative compatibility groupings in Sclerotinia homoeocarpa. Plant Pathology 30:384–396CrossRefGoogle Scholar
  11. Correll JC (1987) Nitrate nonutilizing mutants of Fusarium oxysporum and their use in vegetative compatibility tests. Phytopathology 77:1640CrossRefGoogle Scholar
  12. 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
  13. Derbyshire M, Denton-Giles M, Hegedus D, Seifbarghy S, Rollins J, van KJ, Seidl MF, Faino L, Mbengue M, Navaud O, Raffaele S, Hammond-Kosack K, Heard S, Oliver R (2017) The complete genome sequence of the phytopathogenic fungus Sclerotinia sclerotiorum reveals insights into the genome architecture of broad host range pathogens. Genome Biology and Evolution 9:593–618CrossRefGoogle Scholar
  14. Ford EJ, Miller RV, Gray H, Sherwood JE (1995) Heterokaryon formation and vegetative compatibility in Sclerotinia sclerotiorum. Mycological Research 99:241–247CrossRefGoogle Scholar
  15. Glass NL, Kuldau GA (1992) Mating type and vegetative incompatibility in filamentous ascomycetes. Annual Review of Phytopathology 30:201–224CrossRefGoogle Scholar
  16. Glass NL, Jacobson DJ, Shiu PK (2000) The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annual Reviews of Genetics 34:165–186CrossRefGoogle Scholar
  17. Gordon TR, Okamoto D (1992) Variation in mitochondrial DNA among vegetatively compatible isolates of Fusarium oxysporum. Experimental Mycology 16:245–250CrossRefGoogle Scholar
  18. Goss EM (2015) Genome-enabled analysis of plant-pathogen migration. Annual Review of Phytopathology 53:121–135CrossRefGoogle Scholar
  19. Grubisha LC, Cotty PJ (2010) Genetic isolation among sympatric vegetative compatibility groups of the aflatoxin-producing fungus Aspergillus flavus. Molecular Ecology 19:269–280CrossRefGoogle Scholar
  20. Grünwald NJ, Everhart SE, Knaus BJ, Kamvar ZN (2017) Best practices for population genetic analyses. Phytopathology 107:1000–1010CrossRefGoogle Scholar
  21. 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
  22. Jo Y-K, Chang SW, Rees J, Jung G (2008) Reassessment of vegetative compatibility of Sclerotinia homoeocarpa using nitrate-nonutilizing mutants. Phytopathology 98:108–114CrossRefGoogle Scholar
  23. Kamvar ZN, Brooks JC, Grünwald NJ (2015) Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Frontiers in Genetics 6:208CrossRefGoogle Scholar
  24. Kamvar ZN, Sajeewa Amaradasa B, 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
  25. Kohli Y, Kohn LM (1998) Random association among alleles in clonal populations of Sclerotinia sclerotiorum. Fungal Genetics and Biology 23:139–149CrossRefGoogle Scholar
  26. Kohli Y, Morrall RAA, Anderson JB, Kohn LM (1992) Local and trans-Canadian clonal distribution of Sclerotinia sclerotiorum on canola. Phytopathology 82:480–485.875CrossRefGoogle Scholar
  27. Kohn LM, Carbone I, Anderson JB (1990) Mycelial interactions in Sclerotinia sclerotiorum. Experimental Mycology 14:255–267CrossRefGoogle Scholar
  28. Kohn LM, Stasovski E, Carbone I, Royer J, Anderson JB (1991) Mycelial incompatibility and molecular markers identify genetic variability in field populations of Sclerotinia sclerotiorum. Phytopathology 81:480CrossRefGoogle Scholar
  29. 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
  30. Lehner MS, de 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
  31. Lehner MS, de Paula Júnior TJ, Del Ponte EM, Mizubuti ESG, Pethybridge SJ (2017) Independently founded populations of Sclerotinia sclerotiorum from a tropical and a temperate region have similar genetic structure. PLoS One 12:e0173915CrossRefGoogle Scholar
  32. Leslie JF (1993) Fungal vegetative compatibility. Annual Review of Phytopathology 31:127–150CrossRefGoogle Scholar
  33. Leslie JF, Zeller KA (1996) Heterokaryon incompatibility in fungi—more than just another way to die. Journal of Genetics 75:415–424CrossRefGoogle Scholar
  34. Liu Y-C, Cortesi P, Double ML, MacDonald WL, Milgroom MG (1996) Diversity and multilocus genetic structure in populations of Cryphonectria parasitica. Phytopathology 86:1344–1351Google Scholar
  35. Malvárez G, Carbone I, Grünwald 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
  36. McDonald BA (1997) The population genetics of fungi: tools and techniques. Phytopathology 87:448–453CrossRefGoogle Scholar
  37. Micali CO, Smith ML (2003) On the independence of barrage formation and heterokaryon incompatibility in Neurospora crassa. Fungal Genetics Biology 38:209–219CrossRefGoogle Scholar
  38. Milgroom MG (1996) Recombination and the multilocus structure of fungal populations. Annual Review of Phytopathology 34:457–477CrossRefGoogle Scholar
  39. Milgroom MG, Peever TL (2003) Population biology of plant pathogens: the synthesis of plant disease epidemiology and population genetics. Plant Disease 87:608–617CrossRefGoogle Scholar
  40. Neigel JE, Avise JC (1983) Clonal diversity and population structure in a reef-building coral, Acropora cervicornis: self-recognition analysis and demographic interpretation. Evolution 37:437–453Google Scholar
  41. Papaioannou IA, Typas MA (2014) Barrage formation is independent from heterokaryon incompatibility in Verticillium dahliae. European Journal of Plant Pathology 141:71–82CrossRefGoogle Scholar
  42. Parks JC, Werth CR (1993) A study of spatial features of clones in a population of bracken fern, Pteridium aquilinum (Dennstaedtiaceae). American Journal of Botany 80:537–544CrossRefGoogle Scholar
  43. Perkins DD (1988) Main features of vegetative incompatibility in Neurospora. Fungal Genetic Reports 35:44CrossRefGoogle Scholar
  44. Phillips DV, Carbone I, Gold SE, Kohn LM (2002) Phylogeography and genotype-symptom associations in early and late season infections of canola by Sclerotinia sclerotiorum. Phytopathology 92:785–793CrossRefGoogle Scholar
  45. Prugnolle F, De Meeus T (2010) Apparent high recombination rates in clonal parasitic organisms due to inappropriate sampling design. Heredity 104:135–140CrossRefGoogle Scholar
  46. Puhalla JE (1985) Classification of strains of Fusarium oxysporum on the basis of vegetative compatibility. Canadian Journal of Botany 63:179–183CrossRefGoogle Scholar
  47. Schafer MR, Kohn LM (2006) An optimized method for mycelial compatibility testing in Sclerotinia sclerotiorum. Mycologia 98:593–597CrossRefGoogle Scholar
  48. Sirjusingh C, Kohn LM (2001) Characterization of microsatellites in the fungal plant pathogen, Sclerotinia sclerotiorum. Molecular Ecology Notes 1:267–269CrossRefGoogle Scholar
  49. Strom NB, Bushley KE (2016) Two genomes are better than one: history, genetics, and biotechnological applications of fungal heterokaryons. Fungal Biology and Biotechnology 3:4CrossRefGoogle Scholar
  50. Wu S, Cheng J, Fu Y, Chen T, Jiang D, Ghabrial SA, Xie J (2017) Virus-mediated suppression of host non-self recognition facilitates horizontal transmission of heterologous viruses. PLoS Pathogens 13:e1006234CrossRefGoogle Scholar

Copyright information

© Sociedade Brasileira de Fitopatologia 2018

Authors and Affiliations

  1. 1.Department of Plant PathologyUniversity of NebraskaLincolnUSA
  2. 2.MRC Centre for Global Infectious Disease Analysis, Department of Infectious Disease EpidemiologySchool of Public Health, Imperial CollegeLondonUK

Personalised recommendations