Skip to main content
Log in

Studies on resistance phenotypes to Turnip mosaic virus in five species of Brassicaceae, and identification of a virus resistance gene in Brassica juncea

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

Abstract

Studies were done to: (i) establish the occurrence of different types of Turnip mosaic virus (TuMV) resistance phenotypes in 69 Brassica juncea, 11 Camelina sativa, 11 B. oleracea, five B. rapa and three Raphanus sativus lines, and (ii) characterise a TuMV resistance gene in B. juncea. An isolate of TuMV pathotype 8 (WA-Ap1) was employed to inoculate plants, except in one instance where isolates of pathotypes 1 (isolate NSW-2) and 7 (isolate NSW-1) were also used. The resistance phenotypes found were O (extreme resistance), RN (localised hypersensitivity), R (resistance to systemic movement without necrosis), +N (systemic infection with some necrosis), +N 1 (mild variant of +N), +ND (systemic hypersensitivity and plant death), + (susceptibility), +st (severe stunting variant of +), RN/+ (systemic infection with necrosis limited to inoculated leaves), and RN/st/+ (severe variant of RN/+). Seven different resistance or susceptibility phenotypes were found in B. juncea (codes: +N, RN/+, RN/st/+, +ND, +N 1, + and +st), 22 lines developing only one phenotype and the remaining 47 segregating for 2–3 different phenotypes. Ten B. oleracea cultivars developed phenotype O alone, and one segregated for phenotypes R and O. One B. rapa cultivar produced uniform phenotype +, but four segregated for phenotypes +, RN, O, RN/+, +N, or +st. Two R. sativus cultivars developed phenotype O alone, and one segregated for phenotypes O and RN. All 11 C. sativa lines developed uniform phenotype +ND. Increasing temperature from 16 to 28 °C decreased the time lag between inoculation and symptom development without altering overall phenotypic responses in B. juncea, B. oleracea, B. rapa and C. sativa plants. When one line each of these four species were inoculated with two other TuMV isolates, NSW-1 and NSW-2 belonging to pathotypes 7 and 1 respectively, phenotypic responses remained the same in the B. juncea, B. oleracea and B. rapa lines, but pathotype 8 caused a different phenotypic response in C. sativa. The genetics of resistance to TuMV was studied in a cross between two B. juncea parents with uniform phenotypes, JM 06006 (+) and Oasis Cl (+ND). The results of four tests on F2 progeny plants and three types of control plants (JM 06006, Oasis Cl and mock-inoculated F2 progeny plants) were analysed for their responses to inoculation with TuMV isolate WA-Ap1. Segregation of F2 progeny plants from B. juncea Oasis Cl X JM 06006 fitted a 3:1 ratio (systemic necrosis: susceptibility) at an early stage of TuMV infection, and a 1:2:1 ratio at a late stage of infection +ND: +N: +. These findings show that a single incompletely dominant resistance gene, designated here as TuRBJU 01 (TuMV resistance in B rassica ju ncea 01), was responsible for systemic necrosis phenotypes +ND (homozygous) and +N (heterozygous) in B. juncea. B. juncea resistance gene TuRBJU 01, along with lines of B. oleracea and R. sativus that developed phenotype O uniformly, and of C. sativa that developed phenotype +ND uniformly are potentially valuable in breeding TuMV-resistant cultivars of these three species.

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., Banga, S. S., & Salisbury, P. A. (2012). Challenges for crop production and management from pathogen biodiversity and diseases under current and future climate scenarios – case study with oilseed Brassicas. Field Crops Research, 127, 225–240.

    Article  Google Scholar 

  • Burton, W. A., Ripley, V. L., Potts, D. A., & Salisbury, P. A. (2004). Assesment of genetic diversity in selected breeding lines and cultivars of canola quality Brassica juncea and their implications for canola breeding. Euphytica, 136, 181–192.

  • Cai, Z., Cheung, C.-Y., Ma, W.-T., Au, W.-M., Zhang, X. Y., & Lee, A. (2004). Determination of two intact glucosinolates in vegetables and Chinese herbs. Analytical and Bioanalytical Chemistry, 378, 827–833.

    Article  CAS  PubMed  Google Scholar 

  • Cardone, M., Mazzoncini, M., Menini, S., Rocco, V., Senatore, A., Seggiani, M., et al. (2003). Brassica carinata as an alternative oil crop for the production of biodiesel in Italy: agronomic evaluation, fuel production by transesterification and characterization. Biomass and Bioenergy, 25, 623–636.

    Article  CAS  Google Scholar 

  • Chen, P., Buss, G. R., Roane, C. W., & Tolin, S. A. (1994). Inheritance in soybean of resistant and necrotic reactions to soybean mosaic virus strains. Crop Science, 34, 414–422.

    Article  Google Scholar 

  • Chen, X., Zhu, Z., Gerendás, J., & Zimmermann, N. (2008). Glucosinolates in Chinese Brassica campestris vegetables: Chinese cabbage, Purple Cai-tai, Choysum, Pakchoi, and Turnip. Hortscience, 43, 571–574.

    Google Scholar 

  • Clark, M. F., & Adams, A. N. (1977). Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology, 34, 475–483.

    Article  CAS  PubMed  Google Scholar 

  • Cockerham, G. (1970). Genetic studies on resistance to potato viruses X and Y. Heredity, 25, 309–348.

    Article  Google Scholar 

  • Coutts, B. A., Walsh, J. A., & Jones, R. A. C. (2007). Evaluation of resistance to Turnip mosaic virus in Australian Brassica napus genotypes. Australian Journal of Agricultural Research, 58, 67–74.

    Article  CAS  Google Scholar 

  • Coutts, B. A., Kehoe, M. A., & Jones, R. A. C. (2011). Minimising losses caused by Zucchini yellow mosaic virus in vegetable cucurbit crops in tropical, sub-tropical and Mediterranean environments through cultural methods and host resistance. Virus Research, 159, 141–160.

    Article  CAS  PubMed  Google Scholar 

  • Dixon, G. R. (2007). Vegetable Brassicas and related crucifers: CAB International.

  • Farzadfar, S., Tomitaka, Y., Ikematsu, M., Golnaraghi, A., Pourrahim, R., & Ohshima, K. (2009). Molecular characterisation of Turnip mosaic virus isolates from Brassicaceae weeds. European Journal of Plant Pathology, 124, 45–55.

    Article  CAS  Google Scholar 

  • Fjellstrom, R. G., & Williams, P. H. (1997). Fusarium yellows and turnip mosaic virus resistance in Brassica rapa and B. juncea. Hortscience, 32, 927–930.

    Google Scholar 

  • Ghamkhar, K., Croser, J., Aryamanesh, N., Campbell, M., Kon’kova, N., & Francis, C. (2010). Camelina (Camelina sativa (L.) Crantz) as an alternative oilseed: molecular and ecogeographic analyses. Genome, 53, 558–567.

    Article  CAS  PubMed  Google Scholar 

  • Gladysz, K., & Hanus-Fajerska, E. (2009). Evaluation of the infectivity of selected Turnip mosaic virus isolates towards white cabbage cultivars. Folia Horticulturae, 21, 129–138.

    Article  Google Scholar 

  • Gorecka, K., & Lehmann, P. (2001). Infectious diseases of horseradish (Cochlearia amoracia L.) in Poland. Plant Breeding and Seed Science, 45, 55–64.

  • Green, S. K., & Deng, T. C. (1985). Turnip mosaic virus strains in cruciferous hosts in Taiwan. Plant Disease, 69, 28–31.

    Article  Google Scholar 

  • Gunasekera, C. P., Martin, L. D., Siddique, K. H. M., & Walton, G. H. (2006). Genotype by environment interactions of Indian mustard (Brassica juncea L.) and canola (Brassica napus L.) in Mediterranean-type environments: II. Oil and protein concentrations in seed. European Journal of Agronomy, 25, 13–21.

    Article  Google Scholar 

  • Hardwick, N. V., Davies, J. M. L., & Wright, D. M. (1994). The incidence of three virus diseases of winter oilseed rape in England and Wales in the 1991/92 and 1992/93 growing seasons. Plant Pathology, 43, 1045–1049.

    Article  Google Scholar 

  • Hughes, S. L., Green, S. K., Lydiate, D. J., & Walsh, J. A. (2002). Resistance to Turnip mosaic virus in Brassica rapa and B. napus and the analysis of genetic inheritance in selected lines. Plant Pathology, 51, 567–573.

    Article  Google Scholar 

  • Hunter, P. J., Jones, J. E., & Walsh, J. A. (2002). Involvement of Beet western yellows virus, Cauliflower mosaic virus and Turnip mosaic virus in internal disorders of stored white cabbage. Phytopathology, 92, 816–826.

    Article  CAS  PubMed  Google Scholar 

  • Jenner, C. E., & Walsh, J. A. (1996). Pathotypic variation in turnip mosaic virus with special reference to European isolates. Plant Pathology, 45, 848–856.

    Article  Google Scholar 

  • Jenner, C. E., Tomimura, K., Ohshima, K., Hughes, S. L., & Walsh, J. A. (2002). Mutations in Turnip mosaic virus P3 and cylindrical inclusion proteins are separately required to overcome two Brassica napus resistance genes. Virology, 300, 50–59.

    Article  CAS  PubMed  Google Scholar 

  • Jenner, C. E., Wang, X., Tomimura, K., Ohshima, K., Ponz, F., & Walsh, J. A. (2003). The dual role of the potyvirus P3 protein of Turnip mosaic virus as a symptom and avirulence determinant in Brassicas. Molecular Plant-Microbe Interactions, 16, 777–784.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, Y., Tian, E., Li, R., Chen, L., & Meng, J. (2007). Genetic diversity of Brassica carinata with emphasis on the interspecific crossability with B. rapa. Plant Breeding, 126, 487–491.

    Article  CAS  Google Scholar 

  • Jones, R. A. C. (1985). Further studies on resistance-breaking strains of potato virus X. Plant Pathology, 34, 182–189.

    Article  Google Scholar 

  • Jones, R. A. C. (1990). Strain group specific and virus specific hypersensitive reactions to infection with potyviruses in potato cultivars. Annals of Applied Biology, 117, 93–105.

    Article  Google Scholar 

  • Jones, R. A. C. (2001). Developing integrated disease management strategies against non-persistently aphid-borne viruses: a model programme. Integrated Pest Management Reviews, 6, 15–46.

  • Jones, R. A. C. (2004). Using epidemiological information to develop effective integrated virus disease management strategies. Virus Research, 100, 5–30.

    Article  CAS  PubMed  Google Scholar 

  • Jones, R. A. C. (2005). Patterns of spread of two non-persistently aphid-borne viruses in lupin stands under four different infection scenarios. Annals of Applied Biology, 146, 337–350.

    Article  Google Scholar 

  • Jones, R. A. C. (2006). Control of plant virus diseases. Advances in Virus Research, 67, 205–244.

    Article  PubMed  Google Scholar 

  • Jones, R. A. C., & Barbetti, M. (2012). Influence of climate change on plant disease infections and epidemics caused by viruses and bacteria. CAB Reviews, 7(22), 1–32. (on-line publication) http://www.cabi.org/cabreviews.

    Article  Google Scholar 

  • Jones, R. A. C., & Smith, L. J. (2005). Inheritance of hypersensitive resistance to Bean yellow mosaic virus in narrow-leafed lupin (Lupinus angustifolius). Annals of Applied Biology, 146, 539–543.

    Article  Google Scholar 

  • Jones, R. A. C., Coutts, B. A., & Cheng, Y. (2003). Yield limiting potential of necrotic and non-necrotic strains of Bean yellow mosaic virus in narrow-leafed lupin (Lupinus angustifolius). Australian Journal of Agricultural Research, 54, 849–859.

    Article  Google Scholar 

  • Kehoe, M. A., Coutts, B. A., & Jones, R. A. C. (2010). Resistance phenotypes in diverse accessions, breeding lines, and cultivars of three mustard species inoculated with Turnip mosaic virus. Plant Disease, 94, 1290–1298.

    Article  Google Scholar 

  • Keogh, B., McGrath, T., & Grant, J. (2012). The effect of sowing date and nitrogen on the dry-matter yield and nitrogen content of forage rape (Brassica napus L.) and stubble turnips (Brassica rapa L.) in Ireland. Grass and Forage Science, 67, 2–12.

    Article  CAS  Google Scholar 

  • Király, L., Cole, A. B., Bourque, J. E., & Schoelz, J. E. (1999). Systemic cell death is elicited by the interaction of a single gene in Nicotiana clevelandii and gene VI of cauliflower mosaic virus. Molecular Plant-Microbe Interactions, 12, 919–925.

    Article  Google Scholar 

  • Korkmaz, S., Tomitaka, Y., Onder, S., & Ohshima, K. (2008). Occurrence and molecular characterization of Turkish isolates of Turnip mosaic virus. Plant Pathology, 57, 1155–1162.

    Article  Google Scholar 

  • Lewis, J., & Fenwick, G. R. (1988). Glucosinolate content of Brassica vegetables-Chinese cabbages Pe-tsai (Brassica pekinensis) and Pak-choi (Brassica chinensis). Journal of the Science of Food and Agriculture, 45, 379–386.

    Article  CAS  Google Scholar 

  • Liu, X. P., Lu, W. C., Liu, Y. K., & Li, J. L. (1990). A study of TuMV strain differentiation of cruciferous vegetables from ten provinces in China. Chinese Science Bulletin, 35, 1734–1739.

  • Liu, X. P., Lu, W. C., Liu, Y. K., Wei, S. Q., Xu, J. B., Liu, Z. R., et al. (1996). Occurrence and strain differentiation of turnip mosaic potyvirus and sources of resistance in chinese cabbage in China. Acta Horticulturae, 407, 431–440.

    Google Scholar 

  • Ma, G., Chen, P., Buss, G. R., & Tolin, S. A. (1995). Genetic characteristics of two genes for resistance to soybean mosaic virus in PI486355 soybean. Theoretical and Applied Genetics, 91, 907–914.

    CAS  PubMed  Google Scholar 

  • Malik, R. S. (1990). Prospects for Brassica carinata as an oilseed crop in India. Experimental Agriculture, 26, 125–129.

    Article  Google Scholar 

  • Martinez-Villaluenga, C., Peñas, E., Ciska, E., Piskula, M. K., Kozlowska, H., Vidal-Valverde, C., et al. (2010). Time dependence of bioactive compounds and antioxidant capacity during germination of different cultivars of broccoli and radish seeds. Food Chemistry, 120, 710–716.

    Article  CAS  Google Scholar 

  • Moser, B. R. (2012). Biodiesel from alternative oilseed feedstocks: camelina and field pennycress. Biofuels, 3, 193–209.

    Article  CAS  Google Scholar 

  • Nguyen, H. D., Tomitaka, Y., Ho, S. Y. W., Duchêne, S., Vetten, H.-J., Lesemann, D., et al. (2013). Turnip mosaic potyvirus probably first spread to Eurasian Brassica crops from wild orchids about 1000 years ago. PloS One, 8(2), e55336. doi:10.1371/journal.pone.0055336.

  • Niu, X. K., Leung, H., & Williams, P. H. (1983). Sources and nature of resistance to downy mildew and turnip mosaic virus in Chinese cabbage. Journal of American Society of Horticulture Science, 108, 775–777.

    Google Scholar 

  • Nyalugwe, E. P., Barbetti, M. J., & Jones, R. A. C. (2014). Preliminary studies on resistance phenotypes to Turnip mosaic virus in Brassica napus and B. carinata from different continents and effects of temperature on their expression. European Journal of Plant Pathology, 139, 687–706.

    Article  Google Scholar 

  • Odeh, I. A., Tan, D. Y., & Ancev, T. (2011). Potential suitability and viability of selected biodiesel crops in Australian marginal agricultural lands under current and future climates. BioEnergy Research, 4, 165–179.

    Article  Google Scholar 

  • Pallett, D. W., Thurston, M. I., Cortina-Borja, M., Edwards, M. L., Alexander, M., Mitchell, E., et al. (2002). The incidence of viruses in wild Brassica rapa ssp. sylvestris in southern England. Annals of Applied Biology, 141, 163–170.

    Article  Google Scholar 

  • Pathipanawat, W., Jones, R. A. C., & Sivasithamparam, K. (1996). Resistance to alfalfa mosaic virus in button medic (Medicago oribicularis). Australian Journal of Agricultural Research, 47, 1157–1167.

    Article  Google Scholar 

  • Pink, D. A. C., & Walkey, D. G. A. (1986). Resistance to turnip mosaic virus and cauliflower mosaic virus in horticultural brassicas. Aspects of Applied Biology, 12, 69–73.

    Google Scholar 

  • Potts, D. A., Rakow, G. W., & Males, D. R. (1999). Canola-quality Brassica juncea, a new oilseed crop for the Canadian prairies. Proceedings of the 10th International Rapeseed Congres Canberra, CD-ROM, Canberra, Australia.

  • Provvidenti, R. (1980). Evaluation of chinese cabbage cultivars from Japan and the People’s Republic of China for resistance to turnip mosaic virus and cauliflower mosaic virus. Journal of the American Society for Horticultural Science, 105, 571–573.

    Google Scholar 

  • Ravelo, G., Kagaya, U., Inukai, T., Masanao Sato, M., & Uyeda, I. (2007). Genetic analysis of lethal tip necrosis induced by Clover yellow vein virus infection in pea. Journal of General Plant Pathology, 73, 59–65.

    Article  CAS  Google Scholar 

  • Rowe, B. A., & Neilsen, J. E. (2011). Effects of irrigating forage turnips, Brassica rapa var. rapa cv. Barkant, during different periods of vegetative growth. 2. Nutritive characteristics of leaves and roots. Crop and Pasture Science, 62, 571–580.

    Article  Google Scholar 

  • Rusholme, R. L., Higgins, E. E., Walsh, J. A., & Lydiate, D. J. (2007). Genetic control of broad-spectrum resistance to Turnip mosaic virus in Brassica rapa (Chinese cabbage). Journal of General Virology, 88, 3177–3186.

  • Schwinghamer, M., Schilg, M., Walsh, J., Bambach, R., Cossu, R., Bambridge, J., Hind-Lanoiselet, T., McCorkell, B., & Cross, P. (2014). Turnip mosaic virus: potential for crop losses in the grain belt of New South Wales, Australia. Australasian Plant Pathology, 43, 663–678.

  • Shattuck, V. I., & Stobbs, L. W. (1987). Evaluation of rutabaga cultivars for turnip mosaic virus resistance and the inheritance of resistance. Hortscience, 22, 935–937.

    Google Scholar 

  • Si, P., & Walton, G. H. (2004). Determinants of oil concentration and seed yield in canola and Indian mustard in the lower rainfall areas of Western Australia. Australian Journal of Agricultural Research, 55, 367–377.

    Article  Google Scholar 

  • Spence, N. J., Phiri, N. A., Hughes, S. L., Mwaniki, A., Simons, S., Oduor, G., et al. (2007). Economic impact of Turnip mosaic virus, Cauliflower mosaic virus and Beet mosaic virus in three Kenyan vegetables. Plant Pathology, 56, 317–323.

    Article  Google Scholar 

  • Thomas, P. E., Evans, D. W., Fox, L., & Biever, K. D. (1990). Resistance to beet western yellows virus among forage Brassicas. Plant Disease, 74, 327–330.

    Article  Google Scholar 

  • Thresh, J. M. (1982). Cropping practices and virus spread. Annual Review of Phytopathology, 20, 193–218.

    Article  Google Scholar 

  • Thresh, J. M. (2006). Control of tropical plant virus diseases. Advances in Virus Research, 67, 245–295.

    Article  CAS  PubMed  Google Scholar 

  • Tomlinson, J. A. (1987). Epidemiology and control of virus diseases of vegetables. Annals of Applied Biology, 110, 661–681.

    Article  Google Scholar 

  • Vipond, J. E., Duncan, A. J., Turner, D., Goddyn, L., & Horgan, G. W. (1998). Effects of feeding ensiled kale (Brassica oleracea) on the performance of finishing lambs. Grass and Forage Science, 53, 346–352.

    Article  Google Scholar 

  • Walkey, D. G. A., & Neely, H. A. (1980). Resistance in white cabbage to necrosis caused by turnip and cauliflower mosaic viruses and pepper-spot. Journal of Agricultural Science, 95, 703–713.

  • Walkey, D. G. A., & Pink, D. A. C. (1988). Reactions of white cabbage (Brassica oleracea var. capitata) to four different strains of turnip mosaic virus. Annals of Applied Biology, 112, 273–284.

    Article  Google Scholar 

  • Walsh, J. A., & Jenner, C. E. (2002). Turnip mosaic virus and the quest for durable resistance. Molecular Plant Pathology, 3, 289–300.

    Article  CAS  PubMed  Google Scholar 

  • Walsh, J. A., & Jenner, C. E. (2006). Resistance to Turnip mosaic virus in the Brassicaceae. In G. Loebenstein & J. Carr (Eds.), Natural resistance mechanisms of plants to viruses (pp. 415–430). Netherlands: Springer.

  • Walsh, J. A., & Tomlinson, J. A. (1985). Viruses infecting winter oilseed rape (Brassica napus ssp. oleifera). Annals of Applied Biology, 107, 485–495.

    Article  Google Scholar 

  • Walsh, J. A., Sharpe, A. G., Jenner, C. E., & Lydiate, D. J. (1999). Characterisation of resistance to Turnip mosaic virus in oilseed rape (Brassica napus) and genetic mapping of TuRB01. Theoretical and Applied Genetics, 99, 1149–1154.

    Article  CAS  Google Scholar 

  • Walsh, J. A., Rusholme, R. L., Hughes, S. L., Jenner, C. E., Bambridge, J. M., Lydiate, D. J., et al. (2002). Different classes of resistance to Turnip mosaic virus in Brassica rapa. European Journal of Plant Pathology, 108, 15–20.

    Article  Google Scholar 

  • Yoon, J. Y., Green, S. K., & Opeña, R. T. (1993). Inheritance of resistance to turnip mosaic virus in chinese cabbage. Euphytica, 69, 103–108.

    Article  Google Scholar 

Download references

Acknowledgments

The first author acknowledges a Scholarship for International Research Fees (SIRF); operational funding support provided by the School of Plant Biology, The University of Western Australia and the Department of Agriculture and Food Western Australia; and help by Eva Gajda with ELISA testing of leaf samples. Seeds of the various Brassica lines used were provided by The University of Western Australia, a completed Australian Centre for International Agriculture collaborative Brassica project between Australia, India and China, and the Asian Vegetable Research and Development Centre (AVRDC, Tanzania).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roger A. C. Jones.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Figure 1

Histograms showing segregation ratios for phenotypic data from four individual tests, and pooled data from them, for F2 progeny plants of B. juncea from the cross of Oasis Cl (phenotype +ND) × JM 06006 (phenotype +) inoculated with isolate WA-Ap1 (pathotype 8) of Turnip mosaic virus (TuMV). The expected ratios were 3:1 (necrotic: non necrotic) for early infection (on left), and 1:2:1 (phenotype +ND :phenotype +N: phenotype +) for late infection (on right). For early infection, the observed data values showed minimal divergence from the values expected for the 3:1 ratio. For late infection, agreement between observed and expected data values for the 1:2:1 ratio were also convincing. (PPTX 361 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nyalugwe, E.P., Barbetti, M.J. & Jones, R.A.C. Studies on resistance phenotypes to Turnip mosaic virus in five species of Brassicaceae, and identification of a virus resistance gene in Brassica juncea . Eur J Plant Pathol 141, 647–666 (2015). https://doi.org/10.1007/s10658-014-0568-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-014-0568-5

Keywords

Navigation