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Host response of Arabidopsis thaliana ecotypes is determined by Sclerotinia sclerotiorum isolate type

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Abstract

Studies were undertaken to characterise the interactions of eight Sclerotinia sclerotiorum isolates/pathotypes on leaves of intact plants of 17 Arabidopsis thaliana ecotypes. For lesion diameter and lesion incidence, there were significant (P ≤ 0.001) effects of pathogen isolates, A. thaliana ecotypes, and a significant interaction between isolates and ecotypes in all three experiments. Resistance to S. sclerotiorum infection across the ecotypes ranged from highly susceptible through to resistant and the bioassay was sensitive enough to allow assessment of small differences in partial relative resistances across the ecotypes. While some A. thaliana ecotypes, such as Sha, Bay-0, Ws-1 and Ws-2, were found to be highly susceptible to all S. sclerotiorum isolates tested, others, such as Er-0, Jea and Cvi-0, showed a consistent level of resistance, and of these latter, Er-0 showed the highest and most consistent expression of resistance. In contrast, Col-0, Nd-0 and Oy-0 responses ranged from relative resistant to highly susceptible, depending upon the isolate being tested. Some isolates, such as MBRS1, elicited a wide range of resistance responses across the ecotypes, making these isolates most useful for screening the full range of A. thaliana ecotypes for their responses to S. sclerotiorum. In contrast, other isolates such as ‘Cabbage’ only generated lesions over a very narrow size range of host resistance response and hence could limit the ability of such isolates to differentiate resistances across diverse A. thaliana populations. Increasing the number of ecotypes tested increased the capacity to differentiate both the levels of relative resistance amongst test ecotypes and the varying levels of aggressiveness between different isolates. This is the first known study to demonstrate how Arabidopsis resistance responses can be expressed or compromised by variation in aggressiveness amongst different S. sclerotiorum isolates and/or pathotypes.

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References

  • Balague´, C., Lin, B., Alcon, C., Flottes, G., Malmstrom, S., Kohler, C., Neuhaus, G., Pelletier, G., Gaymard, F., & Roby, D. (2003). HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell, 15, 365–379.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Google Scholar 

  • Barbetti, M. J., Li, C. X., Banga, S. S., Banga, S. K., Singh, D., Singh, P. S., Singh, R., Liu, S. Y., & You, M. P. (2015). New host resistances in Brassica napus and B. juncea from Australia, China and India: Key to managing Sclerotinia stem rot (Sclerotinia sclerotiorum) without fungicides. Crop Protection, 78, 127–130.

    Article  Google Scholar 

  • Behla, R., Hirani, A. H., Zelmer, C. D., Yu, F., Fernando, W. G. D., McVetty, P., & Li, G. (2017). Identification of common QTL for resistance to Sclerotinia sclerotiorum in three doubled haploid populations of Brassica napus (L.). Euphytica, 213, 260.

    Article  Google Scholar 

  • Bert, P. F., Jouan, I., de Labrouhe, T. D., Serre, F., Nicolas, P., & Vear, F. (2002). Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L.) 1. QTL involved in resistance to Sclerotinia sclerotiorum and Diaporthe helianthi. Theoretical and Applied Genetics, 105, 985–993.

    Article  CAS  PubMed  Google Scholar 

  • Boccongelli, C., Buzi, A., Chilosi, G., Magro, P., & Bressan, R. A. (2003a). Evaluation of Arabidopsis thaliana ecotypes for resistance to damping-off caused by Pythium sylvaticum and stem rot caused by Sclerotinia sclerotiorum. Journal of Plant Pathology, 85, 286.

    Google Scholar 

  • Boccongelli, C., Chilosi, G., Magro, P., & Bressan, R. A. (2003b). Isolation of a new Arabidopsis mutant with enhanced disease tolerance to Sclerotinia sclerotiorum. Journal of Plant Pathology, 85, 277.

    Google Scholar 

  • Chen, X. T., Chen, F. F., Chen, L. Q., Zheng, L., Lu, G. D., & Wang, Z. H. (2008). Isolation and analysis of oxalic acid-insensitive mutant of Arabidopsis thaliana. Chinese Journal of Biotechnology, 24, 203–208.

    Article  CAS  PubMed  Google Scholar 

  • Clark, R. M., Schweikert, G., Toomajian, C., Ossowski, S., Zeller, G., Shinn, P., Warthmann, N., Hu, T. T., Fu, G., Hinds, D. A., Chen, H., Frazer, K. A., Huson, D. H., Scholkopf, B., Nordborg, M., Ratsch, G., Ecker, J. R., & Weigel, D. (2007). Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science, 317, 338–342.

    Article  CAS  PubMed  Google Scholar 

  • Clarkson, J. P., Coventry, E., Kitchen, J., Carter, H. E., & Whipps, J. M. (2017a). Population structure of Sclerotinia sclerotiorum in crop and wild hosts in the UK. Plant Pathology, 62, 309–324.

    Article  Google Scholar 

  • Clarkson, J. P., Warmington, R. J., Walley, P. G., Denton-Giles, M., Barbetti, M. J., Brodal, G., & Nordskog, B. (2017b). Population structure of Sclerotinia subarctica and Sclerotinia sclerotiorum in England, Scotland and Norway. Frontiers in Microbiology, 8(490). https://doi.org/10.3389/fmicb.2017.00490.

  • Dai, F. M., Xu, T., Wolf, G. A., & He, Z. H. (2006). Physiological and molecular features of the pathosystem Arabidopsis thaliana L.-Sclerotinia sclerotiorum Libert. Journal of Integrative Plant Biology, 48, 44–52.

    Article  CAS  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 

  • Dickman, M. B., & Mitra, A. (1992). Arabidopsis thaliana as a model for studying Sclerotinia sclerotiorum pathogenesis. Physiological and Molecular Plant Pathology, 41, 255–263.

    Article  Google Scholar 

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

  • Garg, H., Kohn, L. M., Andrew, M., Li, H., Sivasithamparam, K., & Barbetti, M. J. (2010). 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 

  • 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 

  • Ge, X. T., You, M. P., & Barbetti, M. J. (2015). Virulence differences among Sclerotinia sclerotiorum isolates determines host cotyledon resistance responses in Brassicaceae genotypes. European Journal of Plant Pathology, 143, 527–541.

    Article  CAS  Google Scholar 

  • Glazebrook, J., Rogers, E. E., & Ausubel, F. M. (1996). Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics, 143, 973–982.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Guo, X., & Stotz, H. U. (2007). Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmoic acid, salicylic acid, and ethylene signaling. Molecular Plant-Microbe Interactions, 20, 1384–1395.

    Article  CAS  PubMed  Google Scholar 

  • Kim, H. S., & Diers, B. W. (2000). Inheritance of partial resistance to Sclerotinia stem rot in soybean. Crop Science, 40, 55–61.

    Article  Google Scholar 

  • 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., Banga, S., 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 

  • Loudet, O., Chaillou, S., Camilleri, C., Bouchez, D., & Daniel-Vedele, F. (2002). Bay-0 x Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. Theoretical and Applied Genetics 104, 11730–1184.

  • Maxwell, J. J., Brick, M. A., Byrne, P. F., Schwartz, H. F., & Shan, X. (2007). Quantitative trait loci linked to white mold resistance in common bean. Crop Science, 47, 2285–2294.

    Article  Google Scholar 

  • Micic, Z., Hahn, V., Bauer, E., Schon, C. C., & Knapp, S. J. (2004). QTL mapping of Sclerotinia midstalk-rot resistance in sunflower. Theoretical and Applied Genetics, 109, 1474–1484.

    Article  CAS  PubMed  Google Scholar 

  • Mitchell-Olds, T., & Schmitt, J. (2006). Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441, 947–952.

  • Mullins, E., Quinlan, C., & Jones, P. (1999). Isolation of mutants exhibiting altered resistance to Sclerotinia sclerotiorum from small M2 populations of an oilseed rape (Brassica napus) variety. European Journal of Plant Pathology, 105, 465–475.

    Article  Google Scholar 

  • Nakazawa, M., Ichikawa, T., Ishikawa, A., Kobayashi, H., Tsuhara, Y., Kawashima, M., Suzuki, K., Muto, S., & Matsui, M. (2003). Activation tagging, a novel tool to dissect the functions of a gene family. Plant Journal, 34, 741–750.

    Article  CAS  PubMed  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 

  • Perchepied, L., Balagué, C., Riou, C., Claudel-Renard, C., Rivière, N., Grezes-Besset, B., & Roby, D. (2010). Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Molecular Plant-Microbe Interactions, 23, 846–860.

    Article  CAS  PubMed  Google Scholar 

  • Rana, K., Atri, C., Gupta, M., Akhatar, J., Sandhu, P. S., Kumar, N., Jaswal, R., Barbetti, M. J., & Banga, S. S. (2017). Mapping resistance responses to Sclerotinia infestation in introgression lines of Brassica juncea carrying genomic segments from wild Brassicaceae B. fruticulosa. Scientific Reports, 7, 5904. https://doi.org/10.1038/s41598-017-05992-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowe, H. C., & Kliebenstein, D. J. (2008). Complex genetics control natural variation in Arabidopsis thaliana resistance to Botrytis cinerea. Genetics, 180, 2237–2250.

    Article  PubMed  PubMed Central  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 International Rapeseed Congress, June 5–9, 2011, Prague, Czech Republic. pp. 665–669.

  • Taylor, A., Coventry, E., Jones, J. E., & Clarkson, J. P. (2015). Resistance to a highly aggressive isolate of Sclerotinia sclerotiorum in a Brassica napus diversity set. Plant Pathology, 64, 932–940.

    Article  Google Scholar 

  • Taylor, A., Rana, K., Handy, C., & Clarkson, J. P. (2018). Resistance to Sclerotinia sclerotiorum in wild Brassica species and the importance of Sclerotinia subarctica as a Brassica pathogen. Plant Pathology, 67, 433–444.

    Article  CAS  Google Scholar 

  • Thomma, B., Eggermont, K., Penninckx, I., Mauch-Mani, B., Vogelsang, R., Cammue, B., & Broekaert, W. (1998). Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proceedings of the National Academy of Science U.S.A., 95, 15107–15111.

    Article  CAS  Google Scholar 

  • Thomma, B. P., Eggermont, K., Tierens, K., & Broekaert, W. (1999). Requirement of functional ethylene-insensitive 2 gene for efficient resistanceof Arabidopsis to infection by Botrytis cinerea. Plant Physiology, 121, 1093–1102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomma, B. P., Penninckx, I. A., Cammue, B. P., & Broekaert, W. F. (2001). The complexity of disease signaling in Arabidopsis. Current Opinion in Immunology, 13, 63–68.

    Article  CAS  PubMed  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  PubMed  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, 64, 1140–1148.

    Article  CAS  Google Scholar 

  • Uloth, M., You, M. P., & Barbetti, M. J. (2016). Host resistance to Sclerotinia stem rot in historic and current Brassica napus and B. juncea varieties: Critical management implications. Crop and Pasture. Science, 66, 841–848.

    Google Scholar 

  • Volko, S. M., Boller, T., & Ausubel, F. M. (1998). Isolation of new Arabidopsis mutants with enhanced disease susceptibility to Pseudomonas syringae by direct screening. Genetics, 149, 5376–5548.

    Google Scholar 

  • Wang, A. R., Zhang, C. H., Zhang, L. L., Lin, W. W., Lin, D. S., Lu, G. D., Zhou, J., & Wang, Z. H. (2009). Identification of Arabidopsis mutants with enhanced resistance to Sclerotinia stem rot disease from an activation-tagged library. Journal of Phytopathology, 157, 63–69.

    Article  CAS  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, B., Srivastava, S., Deyholos, M. K., & Kav, N. N. V. (2007). Transcriptional profiling of canola (Brassica napus L.) responses to the fungal pathogen Sclerotinia sclerotiorum. Plant Science, 173, 156–171.

    Article  CAS  Google Scholar 

  • Yin, X., Yi, B., Chen, W., Zhang, W., Tu, J., Fernando, W. G. D., & Fu, T. (2010). Mapping of QTLs detected in a Brassica napus DH population for resistance to Sclerotinia sclerotiorum in multiple environments. Euphytica, 173, 25–35.

    Article  CAS  Google Scholar 

  • You, M. P., Uloth, M. B., Xi, X., Banga, S. S., Banga, S. K., & Barbetti, M. J. (2016). Valuable new resistances ensure improved management of Sclerotinia stem rot (Sclerotinia sclerotiorum) in horticultural and oilseed Brassica species. Journal of Phytopathology, 164, 291–299.

    Article  CAS  Google Scholar 

  • Zhao, J., & Meng, J. (2003). Genetic analysis of loci associated with partial resistance to Sclerotinia sclerotiorum in rapeseed (Brassica napus L.). Theoretical and Applied Genetics, 106, 759–764.

    Article  PubMed  Google Scholar 

  • Zhao, J., Udall, J., Quijada, P., Grau, C., Meng, J., & Osborn, T. (2006). Quantitative trait loci for resistance to Sclerotinia sclerotiorum and its association with a homeologous non-reciprocal transposition in Brassica napus L. Theoretical and Applied Genetics, 112, 509–516.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, L. C., Yu, Q., Liu, S. Y., & Zhou, B. W. (1994). Evaluation of Sclerotinia resistance in rapeseed. Chinese Oilseed Crops, 4((suppl.)), 69–72.

    Google Scholar 

  • Zhu, W., We, W., Fu, Y., Cheng, J., Xie, J., Li, G., Yi, X., & Jiang, D. H. (2013). A secretory protein of necrotrophic fungus Sclerotinia sclerotiorum that suppresses host resistance. PLoS One, 8(1), e53901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Xintian Ge was 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 University of Western Australia, for additional operational funding this work. We are greatly indebted to Dr. Oliver Berkowitz, Murdoch University, Western Australia for supplying seed of the Arabidopsis ecotypes. Exceptional technical support is acknowledged from Mr. Robert Creasy and Mr. Bill Piasini in the UWA Plant Growth Facilities.

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  1. Xin Tian Ge

    Present address: School of Molecular and Life Sciences, Faculty of Science and Engineering, Curtin University, Kent St, Bentley, WA, 6102, Australia

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  1. UWA School of Agriculture and Environment M084 and the UWA Institute of Agriculture, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Xin Tian Ge & Martin J. Barbetti

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Ge, X.T., Barbetti, M.J. Host response of Arabidopsis thaliana ecotypes is determined by Sclerotinia sclerotiorum isolate type. Eur J Plant Pathol 153, 583–597 (2019). https://doi.org/10.1007/s10658-018-1584-7

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