Skip to main content
Log in

Inheritance of leaf resistance to Sclerotinia sclerotiorum in Brassica napus and its genetic correlation with cotyledon resistance

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Research to control yield losses from Sclerotinia (Sclerotinia sclerotiorum) in oilseed rape (Brassica napus) has focused on stem resistance. However, resistance to leaf infection against this pathogen would also be beneficial, both in limiting additional plant leaf damage and in reducing inoculum build up within-crop and resultant spread onto stems. Three B. napus breeding populations, C2 (NC-8 × RQ-001-NCA-8 NC2-7), C5 (cv. Charlton × RQ-001-NCA-8 NC2-7) and C6 (cv. Charlton × NC4-5), were screened for leaf resistance (based on mean lesion diameter) under controlled environment conditions. Each population consisted of parents (P1 and P2), F1, F2, BC1P1 and BC2P2, except for C5 that lacked BC1P1. Moderate broad sense heritability for leaf resistance (0.45) to S. sclerotiorum was only found in population C6, where genetic variance was mostly non-additive. Analyses of generation means and variances indicated that both dominance and complex epistatic interactions were present in C6. Bivariate analysis revealed a positive genetic covariance between the non-additive effects for mean leaf lesion and cotyledon lesion diameters, and significant negative covariance of residuals, which supports a common genetic control of cotyledon and leaf resistance to S. sclerotiorum. These results will guide breeders in selection and development of genotypes with both cotyledon and leaf resistance against this important pathogen worldwide.

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

Similar content being viewed by others

Data availability

All critical data supporting the conclusions of this manuscript will be made available by the authors, without undue reservation, to any qualified researcher.

References

  • Amoozadeh A, Darvishzadeh R, Haddadi P, Abdollahi MB, Rezaee DY (2013) Genetic analysis of partial resistance to basal stem rot (Sclerotinia sclerotiorum) in Sunflower. Genetika 45:737–748

    Google Scholar 

  • Amoozadeh M, Darvishzadeh R, Davar R, Abdollahi MB, Haddadi P, Basirnia A (2015) Quantitative trait loci associated with isolate specific and isolate non-specific partial resistance to Sclerotinia sclerotiorum in sunflower. J Agric Sci Technol 17:213–226

    Google Scholar 

  • Atri C, Akhtar J, Gupta M, Gupta N, Goyal A, Rana K, Kaur R, Mittal M, Sharma A, Singh MP, Sandhu PS (2019) Molecular-genetic analysis of defensive responses of Brassica junceaB. fruticulosa introgression lines to Sclerotinia infestation. Sci Rep 9:17089 |. https://doi.org/10.1038/s41598-019-53444-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbetti MJ, Banga SK, Fu TD, Li YC, Singh D, Liu SY, Ge XT, Banga SS (2014) Comparative genotype reactions to Sclerotinia sclerotiorum within breeding populations of Brassica napus and B. juncea from India and China. Euphytica 197:47–59

    Google Scholar 

  • Barbetti MJ, Li CX, Banga SS, Banga SK, Singh D, Sandhu PS, Singh R, Liu SY, You MP (2015a) New host resistances in Brassica napus and Brassica juncea from Australia, China and India: Key to managing Sclerotinia stem rot (Sclerotinia sclerotiorum) without fungicides. Crop Prot 78:127–130

    Google Scholar 

  • Barbetti MJ, Uloth M, Banga SS, Liu SY, Salisbury PA, You MP (2015b) Managing Sclerotinia stem rot in oilseed Brassicas using pathotype-independent and pathotype-dependent host resistances. In: Proceedings of 13th international rapeseed congress, Saskatoon, July 2015

  • Barbetti MJ (2019) Breakthrough in Brassica disease (Sclerotinia). Austgrain, Moree, New South Wales, p 29

  • Baswana KS, Rastogi KB, Sharma PP (1991) Inheritance of stalk rot resistance in cauliflower (Brassica oleracea var. Botrytis L.). Euphytica 57:93–96

    Google Scholar 

  • Bolton MD, Thomma BP, Nelson BD (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7:1–16

  • Bradley CA, Henson RA, Porter PM, LeGare DG, Khot SD (2006) Response of canola cultivars to Sclerotinia sclerotiorum in controlled and field environments. Plant Dis 90:215–219

    CAS  PubMed  Google Scholar 

  • Butler DG, Cullis BR, Gilmour AR, Gogel BJ (2009) ASReml-R Reference Manual.V.3.0. Department of Primary Industries and Fisheries, Brisbane

    Google Scholar 

  • Clarkson JP, Staveley J, Phelps K, Young CS, Whipps JM (2003) Ascospore release and survival in Sclerotinia sclerotiorum. Mycol Res 107:213–222

    PubMed  Google Scholar 

  • Coombes NE (2009) DiGGer design search tool in R. http://nswdpibiom.org/austatgen/software/. Accessed April 2017

  • Delourme R, Barbetti MJ, Snowdon R, Zhao J, Manzanares-Dauleux M (2012) Genetics and Genomics of Resistance. In: Edwards D, Batley J, Parkin IAP, Kole C (eds) Genetics, genomics and breeding of oilseed Brassicas. Science Publishers, CRC Press, Boca Raton, pp 276–318

    Google Scholar 

  • Dickson MH, Petzoldt R (1993) Plant age and isolate source affect expression of downy mildew resistance in broccoli. Hortscience 28:730–731

    Google Scholar 

  • Disi JO, Mei J, Wei D, Ding Y, Qian W (2014) Inheritance of leaf and stem resistance to Sclerotinia sclerotiorum in a cross between Brassica incana and Brassica oleracea var. alboglabra. J Agric Sci 152:146–152

    Google Scholar 

  • Fuller PA, Coyne DP, Steadman JR (1984) Inheritance of resistance to white mold disease in a diallel cross of dry beans. Crop Sci 24:929–933

    Google Scholar 

  • Ganesalingam A, Smith AB, Beeck CP, Cowling WA, Cullis BR (2013) A bivariate mixed model approach for the analysis of plant survival data. Euphytica 190:371–383

    Google Scholar 

  • Garg H, Sivasithamparam K, Banga SS, Barbetti MJ (2008) Cotyledon assay as a rapid and reliable method of screening for resistance against Sclerotinia sclerotiorum in Brassica napus genotypes. Australas Plant Pathol 37:106–111

    Google Scholar 

  • Garg H, Atri C, Sandhu PS, Kaur B, Renton M, Banga SK, Singh H, Singh C, Barbetti MJ, Banga SS (2010a) High level of resistance to Sclerotinia sclerotiorum in introgression lines derived from hybridization between wild crucifers and the crop Brassica species B. napus and B. juncea. Field Crop Res 117:51–58

    Google Scholar 

  • Garg H, Kohn LM, Andrew M, Li H, Sivasithamparam K, Barbetti MJ (2010b) Pathogenicity of morphologically different isolates of Sclerotinia sclerotiorum with Brassica napus and B. juncea genotypes. Eur J Plant Pathol 126:305–315

    Google Scholar 

  • Garg H, Li H, Sivasithamparam K, Kuo J, Barbetti MJ (2010c) The infection processes of Sclerotinia sclerotiorum in cotyledon tissue of a resistant and a susceptible genotype of Brassica napus. Ann Bot 106:897–908

    PubMed  PubMed Central  Google Scholar 

  • Garg H, Sivasithamparam K, Barbetti MJ (2010d) Scarification and environmental factors that enhance carpogenic germination of sclerotia of Sclerotinia sclerotiorum. Plant Dis 94:1041–1047

    PubMed  Google Scholar 

  • Garg H, Li H, Sivasithamparam K, Barbetti MJ (2013) Differentially expressed proteins and associated histological and disease progression changes in cotyledon tissue of a resistant and susceptible genotype of Brassica napus infected with Sclerotinia sclerotiorum. PLoS ONE 8:e65205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ge XT, Li YP, Wan ZJ, You MP, Finnegan PM, Banga SS, Sandhu PS, Garg H, Salisbury PA, Barbetti MJ (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 Crops Res 127:248–258

    Google Scholar 

  • Ge XT, You MP, Barbetti MJ (2015) Virulence differences among Sclerotinia sclerotiorum isolates determines host cotyledon resistance responses in Brassicaceae genotypes. Eur J Plant Pathol 143:527–541

    CAS  Google Scholar 

  • Ge XT, Barbetti MJ (2019) Host response of Arabidopsis thaliana ecotypes is determined by Sclerotinia sclerotiorum isolate type. Eur J Plant Pathol 153:51–65

    CAS  Google Scholar 

  • Hims MJ (1979) Damping-off of Brassica napus (‘mustard and cress’) by Sclerotinia sclerotiorum. Plant Pathol 28:201–202

    Google Scholar 

  • Khan MA, Cowling W, Banga SS, You MP, Tyagi V, Bharti B, Barbetti MJ (2020) Patterns of inheritance for cotyledon resistance against Sclerotinia sclerotiorum in Brassica napus. Euphytica 216:79–89. https://doi.org/10.1007/s10681-020-02612-y

    Article  CAS  Google Scholar 

  • Khangura R, Burgel AV, Salam M, Aberra M, MacLeod WJ (2014) Why Sclerotinia was so bad in 2013? Understanding the disease and management options. Available from URL: http://www.giwa.org.au/pdfs/2014/Presented_Papers/Khangura%20et%20al%20presentation%20paper%20CU2014%20-DR.pdf (accessed June 2017)

  • Kim HS, Diers BW (2000) Inheritance of partial resistance to Sclerotinia stem rot in soybean. Crop Sci 40:55–61

    Google Scholar 

  • Kus JV, Zaton K, Sarkar R, Cameron RK (2002) Age-related resistance in Arabidopsis is a developmentally regulated defence response to Pseudomonas syringae. Plant Cell 14:479–490

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Lee N (2014) Prompt action on sclerotinia will reduce yield losses. https://grdc.com.au/news-and-media/news-and-media-releases/west/2014/07/prompt-action-on-sclerotinia-will-reduce-yield-losses. Accessed 10 July 2020

  • Leisner SM, Turgeon R, Howell SH (1993) The effects of host plant development and genetic determinants on the long-distance movement of cauliflower mosaic virus in infected turnip plants. Plant Cell 5:191–202

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li CX, Li H, Sivasithamparam K, Fu TD, Li YC, Liu SY, Barbetti MJ (2006a) 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. Aust J Agric Res 57:1131–1135

    Google Scholar 

  • Li H, Smyth F, Barbetti MJ, Sivasithamparam K (2006b) Relationship between Brassica napus seedling and adult plant responses to Leptosphaeria maculans is determined by plant growth stage at inoculation and temperature regime. Field Crops Res 96:428–437

    Google Scholar 

  • Li CX, Li H, Siddique AB, Sivasithamparam K, Salisbury P, Banga SS, Banga S, Chattopadhyay C, Kumar A, Singh R, Singh D, Agnihotri A, Liu SY, Li YC, Tu J, Fu TD, Wang YF, Barbetti MJ (2007) The importance of the type and time of inoculation and assessment in the determination of resistance in Brassia napus and B. juncea to Sclerotinia sclerotiorum. Aust J Agric Res 58:1198–1203

    Google Scholar 

  • Li CX, Liu SY, Sivasithamparam K, Barbetti MJ (2009) New sources of resistance to Sclerotinia stem rot caused by Sclerotinia sclerotiorum in Chinese and Australian Brassica napus and B. juncea germplasm screened under Western Australian conditions. Australas Plant Pathol 38:149–152

    Google Scholar 

  • Li J, Zhao Z, Hayward A, Cheng H, Fu D (2015) Integration analysis of quantitative trait loci for resistance to Sclerotinia sclerotiorum in Brassica napus. Euphytica 205:483–489

    CAS  Google Scholar 

  • Mather K, Jinks JL (1982) Biometrical Genetics, 3rd edn. Chapman and Hall, London, New York, ISBN-10: 0412228904

  • Mei J, Qian L, Disi JO, Yang X, Li Q, Li J (2011) Identification of resistant sources against Sclerotinia sclerotiorum in Brassica crops with emphasis on B. oleracea. Euphytica 177:393–399

    Google Scholar 

  • Mei J, Ding Y, Lu K, Wei D, Liu Y, Disi JO, Li J, Liu L, Liu S, McKay J, Qian W (2013) Identification of genomic regions involved in resistance against Sclerotinia sclerotiorum from wild Brassica oleracea. Theor Appl Genet 126:549–556

    CAS  PubMed  Google Scholar 

  • Murray GM, Brennan JP (2012) The current and potential costs from diseases of oilseed crops in Australia. (Grains Research and Development Corporation No. CER00002.)

  • Niemann J, Kaczmarek J, Ksiazczyk T, Wojciechowski A, Jedryczka M (2017) Chinese cabbage (Brassica rapa ssp pekinensis) - a valuable source of resistance to clubroot (Plasmodiophora brassicae). Eur J Plant Pathol 147:181–198

    CAS  Google Scholar 

  • Purnamasari MI, Cawthray GR, Barbetti MJ, Erskine W, Croser JS (2015) Camalexin production in Camelina sativa is independent of cotyledon resistance to Sclerotinia sclerotiorum. Plant Dis 99(11):1544–1549

    CAS  PubMed  Google Scholar 

  • Qasim MU, Zhao Q, Shahid M, Samad RA, Ahmar S, Wu J, Fan C, Zhou Y (2020) Identification of QTLs containing resistance genes for Sclerotinia stem rot in Brassica napus using comparative transcriptomic studies. Front Plant Sci 11:776. https://doi.org/10.3389/fpls.2020.00776

    Article  PubMed  PubMed Central  Google Scholar 

  • Rana K, Atri C, Gupta M, Akhatar J, Sandhu PS, Kumar N, Jaswal R, Barbetti MJ, Banga SS (2017) Mapping resistance responses to Sclerotinia infestation in introgression lines of Brassica juncea carrying genomic segments from wild Brassicaceae B. fruticulosa. Sci Rep 7:5904

    Google Scholar 

  • Rana K, Atri C, Akhatar J, Nagra R, Goyal A, Singh MP, Kumar N, Sharma A, Sandhu P, Kaur G, Barbetti MJ, Banga SS (2019) Detection of first marker trait associations for resistance against Sclerotinia sclerotiorum in Brassica junceaErucastrum cardaminoides introgression lines. Front Plant Sci 10:1015

    PubMed  PubMed Central  Google Scholar 

  • SAS Institute Inc (1999) SAS Online Doc®, Version 8, Cary, NC

  • Shashikumar KT, Pitchaimuthu M, Rawal RD (2010) Generation mean analysis of resistance to downy mildew in adult muskmelon plants. Euphytica 173:121–127

    Google Scholar 

  • Singh R, Singh D, Barbetti MJ, Wade SMS, Singh H, Banga SS, Kumar A, Caixia L, Sivasithamparam K, Salisbury P, Buraton W, FU T (2008a) Sclerotinia rot tolerance in oilseed Brassica. In: Proceedings of the 12th international rapeseed congress, March 2007, Wuhan, China, pp 94–97

  • Singh R, Singh D, Li H, Sivasithamparam K, Yadav NR, Salisbury, Barbetti MJ (2008b) Management of Sclerotinia rot of oilseed Brassicas- a focus on India. Brassica 10:1–27

    Google Scholar 

  • Singh R, Singh D, Salisbury P, Barbetti MJ (2010) Field evaluation of Indian and exotic oilseed Brassica napus and B. juncea germplasm against Sclerotinia stem rot. Indian J Agr Sci 80:1067–1071

    Google Scholar 

  • Taylor A, Coventry E, Jones JE, Clarkson JP (2015) Resistance to a highly aggressive isolate of Sclerotinia sclerotiorum in a Brassica napus diversity set. Plant Pathol 64:932–940. https://doi.org/10.1111/ppa.12327

    Article  Google Scholar 

  • Taylor A, Rana K, Handy C, Clarkson JP (2018) Resistance to Sclerotinia sclerotiorum in wild Brassica species and the importance of Sclerotinia subarctica as a Brassica pathogen. Plant Pathol 67:433–444. https://doi.org/10.1111/ppa.12745

    Article  CAS  Google Scholar 

  • Uloth MB, You MP, Finnegan PM, Banga SS, Banga SK, Sandhu PS, Yi H, Salisbury PA, Barbetti MJ (2013) New sources of resistance to Sclerotinia sclerotiorum for crucifer crops. Field Crop Res 154:40–52

    Google Scholar 

  • Uloth M, You MP, Finnegan PM, Banga SS, Yi H, Barbetti MJ (2014) Seedling resistance to Sclerotinia sclerotiorum as expressed across diverse cruciferous species. Plant Dis 98:184–190

    PubMed  Google Scholar 

  • Uloth MB, You MP, Barbetti MJ (2015a) Host resistance to Sclerotinia stem rot in historic and current Brassica napus and B. juncea varieties: critical management implications. Crop Pasture Sci 66:841–848

    Google Scholar 

  • Uloth MB, You MP, Cawthray G, Barbetti MJ (2015b) Temperature adaptation in isolates of Sclerotinia sclerotiorum affects their ability to infect Brassica carinata. Plant Pathol 64:1140–1148

    CAS  Google Scholar 

  • Uloth MB, Clode PL, You MP, Barbetti MJ (2016) Attack modes and defence reactions in pathosystems involving Sclerotinia sclerotiorum, Brassica carinata, B. juncea and B. napus. Ann Bot 117:79–95

  • Wei D, Mei J, Fu Y, Disi JO, Li J, Qian W (2014) Quantitative trait loci analyses for resistance to Sclerotinia sclerotiorum and flowering time in Brassica napus. Mol Breed 34:1797–1804

    CAS  Google Scholar 

  • Wei L, Jian H, Lu K, Filardo F, Yin N, Liu L, Qu C, Li W, Du H, Li J (2016) Genome-wide association analysis and differential expression analysis of resistance to Sclerotinia stem rot in Brassica napus. Plant Biotechnol J 14:1368–1380

    CAS  PubMed  Google Scholar 

  • Wu J, Cai G, Tu J, Li L, Liu S, Luo X, Zhou L, Fan C, Zhou Y (2013) Identification of QTLs for resistance to sclerotinia stem rot and BnaC.IGMT5.a as a candidate gene of the major resistant QTL SRC6 in Brassica napus. PLoS One 8(7):e67740

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Zhao Q, Liu S, Shahid M, Lan L, Cai G (2016) Genome-wide association study identifies new loci for resistance to Sclerotinia stem rot in Brassica napus. Front Plant Sci 7:1418. doi:https://doi.org/10.3389/fpls.2016.01418

    Article  PubMed  PubMed Central  Google Scholar 

  • You MP, Uloth MB, Li XX, Banga SS, Banga SK, Barbetti MJ (2016) Valuable new resistances ensure improved management of sclerotinia stem rot (Sclerotinia sclerotiorum) in horticultural and oilseed Brassica species. J Phytopath 164:291–299

    CAS  Google Scholar 

  • Zhang J, Qi C, Pu H, Chen S, Chen F (2011) Genetic map construction and Sclerotinia resistance QTLs identification in rapeseed (Brassica napus L.). In: Proceedings of the 13th international rapeseed congress, June 2011, Prague, Czech Republic, GCIRC, Paris, France, pp 713–715

  • Zhao JW, Meng JL (2003) Genetic analysis of loci associated with partial resistance to Sclerotinia sclerotiorum in rapeseed (Brassica napus L.). Theor Appl Genet 106:759–764

    PubMed  Google Scholar 

  • Zhao J, Peltier AJ, Meng J, Osborn TC, Grau CR (2004) Evaluation of Sclerotinia stem rot resistance in oilseed Brassica napus using a petiole inoculation technique under greenhouse conditions. Plant Dis 88:1033–1039

    CAS  PubMed  Google Scholar 

  • Zhao J, Udall JA, Quijada PA, Grau CR, Meng J, Osborn TC (2006) Quantitative trait loci for resistance to Sclerotinia sclerotiorum and its association with a homeologous non-reciprocal transposition in Brassica napus L. Theoret Appl Genet 112:509–516

    CAS  Google Scholar 

Download references

Acknowledgements

The first author gratefully acknowledges a UWA-UAF Scholarship jointly from the University of Agriculture, Faisalabad (38000) in Pakistan and the University of Western Australia. The authors gratefully acknowledge the exceptional technical support from Robert Creasy and Bill Piasini in the UWA Plant Growth Facilities.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin J. Barbetti.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, M.A., Cowling, W., Banga, S.S. et al. Inheritance of leaf resistance to Sclerotinia sclerotiorum in Brassica napus and its genetic correlation with cotyledon resistance. Euphytica 216, 188 (2020). https://doi.org/10.1007/s10681-020-02717-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-020-02717-4

Keywords

Navigation