Skip to main content
Log in

Virulence differences among Sclerotinia sclerotiorum isolates determines host cotyledon resistance responses in Brassicaceae genotypes

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Differences in Sclerotinia rot (SR) disease severity, caused by two categorized pathotypes and one more recent isolate of S. sclerotiorum and measured in terms of cotyledon lesion diameter, were studied across diverse Brassicaceae hosts to characterize host response and pathogen virulence. There were significant differences (P ≤0.001) between genotypes, isolates and a significant genotype x isolate interaction. The mean diameter of cotyledon lesions ranged from 5 mm in the most resistant genotypes (e.g., Brassica juncea Ringot I and Seeta) to ≥ 13.6 mm in the most susceptible genotypes (e.g., B. tournefortii Wild turnip #1 and #2, Sisymbrium irio London rocket Wild #1 and #2, and B. nigra 4381). Responses, in at least one experiment for some B. juncea (e.g., Seeta, Ringot I) and Raphanus sativus (e.g., Colonel) genotypes, were generally highly resistant irrespective of the isolate used, making them ideal sources of resistance to exploit for developing new varieties with more effective resistance to SR across multiple pathotypes of this pathogen. In contrast, some other genotypes showed significant isolate dependency, with high levels of resistance against one isolate (e.g., B. napus Charlton against the WW4 isolate; B. napus Oscar against the ‘Cabbage’ isolate) but quite susceptible to other isolates (e.g., B. napus Charlton against the ‘Cabbage’ and MBRS1 isolates; B. napus Oscar against the WW4 isolate). These findings highlight the value from using pathotypes of different physiological specialization in screening programs to identify host resistance that is durable across multiple pathotypes. Distinct host resistance symptom types were reported for the first time on some genotypes against isolate WW4; including a distinct yellow halo observed around lesions on B. napus RQ001, indicative of leaf senescence involved in programmed cell death (PCD); a distinct dark brown margin observed around lesions on R. sativus, indicative of a hypersensitive response (HR); and the HR ‘flecking’ on Sinapis alba Concerta and B. juncea Seeta. That WW4 was the most pathogenic isolate for genotypes such as B. juncea Hetianyoucai and B. napus Oscar that showed high level resistance to the ‘Cabbage’ isolate and intermediate resistance to MBRS-1, dispels previously held views that WW4 was a largely avirulent pathotype of little consequence. Rather, isolate WW4 offers unique opportunities to investigate HR and PCD host resistance responses to S. sclerotiorum in Brassicaceae.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Barbetti, M. J., & Khangura. R., (2000). Fungal diseases of canola in Western Australia. Bulletin 4406, Agriculture Western Australia. 15pp.

  • Barbetti, M. J., Banga, S. K., Fu, T. D., Li, Y. C., Singh, D., Liu, S. Y., Ge, X. T., & Banga, S. S. (2014). Comparative genotype reactions to Sclerotinia sclerotiorum within breeding populations of Brassica napus and B. juncea from India and China. Euphytica, 197, 47–59.

    Article  Google Scholar 

  • Buchwaldt. L., Li, R., Hegedus, D.D., & Rimmer, S.R., (2005). Pathogenesis of Sclerotinia sclerotiorum in relation to screening for resistance. Proceedings of the 13th International Sclerotinia WS, Monterey, CA, USA. 22.

  • Clarkson, J. P., Clewes, E., & Whipps, J. M. (2008). Diversity of Sclerotinia sclerotiorum from agricultural crops and meadow buttercup in the UK. Journal of Plant Pathology, 90, S2.

    Google Scholar 

  • Clarkson, J. P., Coventry, E., Kitchen, J., & Whipps, J. M. (2013). Population structure of Sclerotinia sclerotiorum in crop and wild hosts in the UK. Plant Pathology, 62, 309–324.

    Article  Google Scholar 

  • Collmer, A., & Keen, N. T. (1986). The role of pectic enzymes in plant pathogenesis. Annual Review of Phytopathology, 24, 383–409.

    Article  CAS  Google Scholar 

  • Davis, K. R., Darvill, A. G., Albersheim, P., & Dell, A. (1986). Host pathogen interactions. XXIX. Oligogalacturonides released from sodium polypectate by endopolygalact-uronic acid lyase are elicitors of phytoalexin in soybean. Plant Physiology, 80, 568–577.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Delourme, R., Barbetti, M. J., Snowdon, R., Zhao, J., & Manzanares-Dauleux, M. (2011). Genetics and Genomics of Resistance. In D. Edwards, J. Batley, I. A. P. Parkin, & C. Kole (Eds.), Genetics, Genomics and Breeding of Oilseed Brassicas (pp. 276–318). USA: Science Publishers, CRC Press.

    Google Scholar 

  • Ekins, M. G., Aitken, E. A. B., & Goulter, K. C. (2007). Aggressiveness among isolates of Sclerotinia sclerotiorum from sunflower. Australasian Plant Pathology, 36, 580–586.

    Article  Google Scholar 

  • Garg, H., Sivasithamparam, K., Banga, S. S., & Barbetti, M. J. (2008). Cotyledon assay as a rapid and reliable method of screening for resistance against Sclerotinia sclerotiorum in Brassica napus genotypes. Australasian Plant Pathology, 37, 106–111.

    Article  Google Scholar 

  • Garg, H., Kohn, L. M., Andrew, M., Li, H., Sivasithamparam, K., & Barbetti, M. J. (2010a). Pathogenicity of morphologically different isolates of Sclerotinia sclerotiorum with Brassica napus and B. juncea genotypes. European Journal of Plant Pathology, 126, 305–315.

    Article  Google Scholar 

  • Garg, H., Atri, C., Sandhu, P. S., Kaur, B., Benton, M., Banga, S. K., Singh, H., Singh, C., Barbetti, M. J., & Banga, S. S. (2010b). High level of resistance of Sclerotinia sclerotiorum in introgression lines derived from hybridization between wild crucifers and the crop Brassica species B. napus and B. juncea. Field Crops Research, 117, 51–58.

    Article  Google Scholar 

  • Ge, X., Li, Y. P., Wan, Z. J., You, M. P., Finnegan, P. M., Banga, S. S., Sandhu, P. S., Garg, H., Salisbury, P. A., & Barbetti, M. J. (2012). Delineation of Sclerotinia sclerotiorum pathotypes using differential resistance responses on Brassica napus and B. juncea genotypes enables identification of resistance to prevailing pathotypes. Field Crop Research, 127, 248–258.

    Article  Google Scholar 

  • Goodwin, S. B., Allard, R. W., & Webster, R. (1990). A nomenclature for Rhynchosporium secalis pathotypes. Phytopathology, 80, 1330–1336.

    Article  Google Scholar 

  • Greenberg, J. T. (1997). Programmed Cell Death in plant-pathogen interactions. Annual Review of Plant Physiological and Plant Molecular Biology, 48, 525–545.

    Article  CAS  Google Scholar 

  • Harel, A., Bercovich, S., & Yarden, O. (2006). Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia Sclerotiorum in an oxalic acid-independent manner. Molecular Plant-Microbe Interactions, 19, 682–693.

    Article  CAS  PubMed  Google Scholar 

  • Jurick, W. M., & Rollins, J. A. (2007). Deletion of the adenylate cyclase (sac1) gene affects multiple developmental pathways and pathogenicity in Sclerotinia sclerotiorum. Fungal Genetics and Biology, 44, 521–530.

    Article  CAS  PubMed  Google Scholar 

  • Kim, W. G., & Gho, W. D. (2003). Occurrence of Sclerotinia rot in cruciferous crops caused by Sclerotinia spp. Plant Pathology Journal, 19, 69–74.

    Article  Google Scholar 

  • Kohn, L. M., Carbone, I., & Anderson, J. B. (1990). Mycelial interactions in Sclerotinia sclerotiorum. Experimental Mycology, 14, 255–267.

    Article  Google Scholar 

  • Kohn, L. M., Stasovski, E., Carbone, I., Royer, J., & Anderson, J. B. (1991). Mycelial incompatibility and molecular markers identify genetic variability in field populations of Sclerotinia sclerotiorum. Phytopathology, 81, 480–485.

    Article  Google Scholar 

  • Laemmlen, F., (2001) Damping-off diseases. Publ. No. 8041. University of California, Davis.

  • Li, C. X., Li, H., Sivasithamparam, K., Fu, T. D., Li, Y. C., Liu, S. Y., & Barbetti, M. J. (2006). Expression of field resistance under Western Australian conditions to Sclerotinia sclerotiorum in Chinese and Australian Brassica napus and Brassica juncea germplasm and its relation with stem diameter. Australian Journal of Agricultural Research, 57, 1131–1135.

    Article  Google Scholar 

  • Li, C. X., Li, H., Siddique, A. B., Sivasithamparam, K., Salisbury, P., Banga, S. S., Shashi Banga, Chattopadhyay, C., Kumar, A., Singh, R., Singh, D., Agnihotri, A., Liu, S. Y., Li, Y. C., Tu, J., Fu, T. D., Wang, Y. F., & Barbetti, M. J. (2007). The importance of the type and time of inoculation and assessment in the determination of resistance in Brassica napus and B. juncea to Sclerotinia sclerotiorum. Australian Journal of Agricultural Research, 58, 1198–1203.

    Article  Google Scholar 

  • Li, C. X., Liu, S. Y., Sivasithamparam, K., & Barbetti, M. J. (2009). New sources of resistance to Sclerotinia stem rot caused by Sclerotinia sclerotiorum in Chinese and Australian Brassica napus and Brassica juncea germplasm screened under Western Australian conditions. Australasian Plant Pathology, 38, 149–152.

    Article  Google Scholar 

  • McCartney, H. A., Cacey, M. E., Li, Q., & Heran, A., (2000). Airborne ascospores concentration and the infection of oilseed rape and sunflower by S. sclerotiorum. Proceedings of the 10th International Rapeseed Congress, Canberra, Australia.

  • Nelson, B. D., Helms, T. C., & Kural, I. (1991). Effect of temperature and pathogens isolates on laboratory screening of soybean for resistance to Sclerotinia sclerotiorum. Canadian Journal of Plant Science, 71, 347–352.

    Article  Google Scholar 

  • Otto-Hanson, L., Steadman, J. R., Higgins, R., & Eskridge, K. M. (2011). Variation in Sclerotinia sclerotiorum bean isolates from multisite resistance screening locations. Plant Disease, 95, 1370–1377.

    Article  Google Scholar 

  • Pedras, M. S. C., & Ahiahonu, P. W. K. (2004). Phytotoxin production and phytoalexin elicitation by the phytopathogenic fungus Sclerotinia sclerotiorum. Journal of Chemical Ecology, 30, 2163–2179.

    Article  CAS  PubMed  Google Scholar 

  • Prajapati, C. R., Shukla, H. P., & Pandey, R. (2005). Screening of Dolichos bean cultivars/germplasm against Sclerotinia sclerotiorum. Annals of Plant Protection Science, 13, 259–261.

    Google Scholar 

  • Purdy, L. H. (1979). Sclerotinia sclerotiorum: history, diseases and symptomatology, host range, geographic distribution and impact. Phytopathology, 69, 875–880.

    Article  Google Scholar 

  • Rahmanpour, S., Backhouse, D., & Nonhebel, H. M. (2010). Reaction of glucosinolate- myrosinase defence system in Brassica plants to pathogenicity factor of Sclerotinia sclerotiorum. European Journal of Plant Pathology, 128, 429–433.

    Article  CAS  Google Scholar 

  • Saharan, G. S., & Mehta, N., (2008). Sclerotinia Diseases of Crop plants: Biology, Ecology and Disease Management. Springer. ISBN 978-1-4020-8407-2.

  • Sexton, A. C., Whitten, A. R., & Howlett, B. J. (2006). Population structure of Sclerotinia sclerotiorum in an Australian canola field at flowering and stem-infection stages of the disease cycle. Genome, 49, 1408–1415.

    Article  PubMed  Google Scholar 

  • Singh, D., Singh, R., Salisbury, P., & Barbetti, M. J., (2011). Genetic diversity in Australian, Indian and Chinese oilseed Brassica germplasm against sclerotinia-rot resistance. Proceedings of the 13th International Rapeseed Congress, June 5 – 9, 2011, Prague, Czech Republic. p. 665–669.

  • Sutton, D. C., & Deverall, B. J. (1983). Studies on infection of bean (Phaseolus vulgaris) and soybean (Glycine max) by ascospores of Sclerotinia sclerotiorum. Plant Pathology, 32, 251–261.

    Article  Google Scholar 

  • Sylvester-Bradley, R., & Makepeace, R. J. (1984). A code for stages of development in oilseed rape (Brassica napus L.). Aspects of Applied Biology, 6, 399–419.

    Google Scholar 

  • Uloth, M., You, M. P., Finnegan, P. M., Banga, S. S., Banga, S. K., Yi, H., Salisbury, P., & Barbetti, M. J. (2013). New sources of resistance to Sclerotinia sclerotiorum for crucifer crops. Field Crops Research, 154, 40–52.

    Article  Google Scholar 

  • Uloth, M., You, M. P., Finnegan, P. M., Banga, S. S., Yi, H., & Barbetti, M. J. (2014). Seedling resistance to Sclerotinia sclerotiorum as expressed across diverse cruciferous species. Plant Disease, 98, 184–190.

    Article  Google Scholar 

  • Uloth, M., Clode, P. L., You, M. P., Cawthray, G., & Barbetti, M. J., (2015). Temperature adaptation in Sclerotinia sclerotiorum affects its ability to infect Brassica carinata. Plant Pathology (Online 8th January 2015 at doi: 10.1111/ppa.12338).

  • Uloth, M., Clode, P. L., You, M. P., & Barbetti, M. J. (2015b). Calcium oxalate crystals: an integral component of the Sclerotinia sclerotiorum/Brassica carinata pathosystem. PloS One, 10(3), e0122362. doi:10.1371/journal.pone.0122362.

    Article  PubMed Central  PubMed  Google Scholar 

  • van Doorn, W. G., & Woltering, E. J. (2004). Senescence and programmed cell death: substance or semantics? Journal of Experimental Botany, 55, 2147–2153.

    Article  PubMed  Google Scholar 

  • Yen, C. H., & Yang, C. H. (1998). Evidence for programmed cell death during leaf senescence in plants. Plant Cell Physiology, 39, 922–927.

    Article  CAS  Google Scholar 

  • Young, C. S., Clarkson, J. P., Smith, J. A., Watling, M., Phelps, K., & Whipps, J. M. (2004). Environmental conditions influencing Sclerotinia sclerotiorum infection and disease development in lettuce. Plant Pathology, 53, 387–397.

    Article  Google Scholar 

Download references

Acknowledgements

Xintian Ge is the recipient of an International Postgraduate Research Scholarship, The University of Western Australia, a scholarship from Kunming Floral World Bio-Tech Co. Ltd., Kunming, Peoples Republic of China, and ‘top-up’ funding by the Institute of Agriculture at the University of Western Australia. We appreciate the operational funding support for this research provided by the Australia Research Council and the Department of Agriculture and Food Western Australia (Project LP100200113, ‘Factors responsible for host resistance to the pathogen Sclerotinia sclerotiorum for developing effective disease management in vegetable Brassicas’); and the Australian Centre for International Agricultural Research and the Grains Research and Development Corporation, Canberra, along with the School of Plant Biology, The University of Western Australia, for additional operational funding this work. We gratefully acknowledge the provision of half the salary of Martin Barbetti during the early part of these studies by the Department of Agriculture and Food Western Australia. Exceptional technical support is acknowledged from Mr Robert Creasy and Mr Bill Piasini in the UWA Plant Growth Facilities.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin J. Barbetti.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ge, X.T., You, M.P. & Barbetti, M.J. Virulence differences among Sclerotinia sclerotiorum isolates determines host cotyledon resistance responses in Brassicaceae genotypes. Eur J Plant Pathol 143, 527–541 (2015). https://doi.org/10.1007/s10658-015-0696-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-015-0696-6

Keywords

Navigation