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Comparative proteomic analysis provides insight into the key proteins involved in novel stem-physical-strength-mediated resistance (SPSMR) mechanism against Sclerotinia sclerotiorum in Brassicaceae

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Abstract

Sclerotinia sclerotiorum stands out as the most destructive pathogen affecting oilseed Brassica crops. Our study unveils the proteomic basis of a novel resistance mechanism, termed "Stem-Physical-Strength-Mediated-Resistance (SPSMR)," against S. sclerotiorum in Brassicaceae through a comparative proteomic analysis. Field assessments highlight significant differences in stem-physical strength attributes between the resistant (R) and susceptible (S) genotypes, emphasizing the importance of SPSMR. Field evaluation revealed that the resistant genotype S. alba SA1 demonstrates significantly (P ≤ 0.01) superior stem traits at various time points post-inoculation as compared to susceptible genotypes. Pearson's correlation analysis establishes significant associations between lesion length and stem attributes, with stem breaking strength emerging as a key contributor to resistance. Proteomic profiling at different infection stages reveals temporal dynamics, showcasing the resistant genotype's robust and adaptive defense response. KEGG enrichment analysis underscores the significance of phenylalanine metabolism and phenylpropanoid biosynthesis pathways. Differentially Expressed Proteins (DEPs) in resistant and susceptible genotypes revealed intricate expression profiles, particularly in lignin biosynthesis. Proteins associated with cell wall fortification, especially in the lignin biosynthetic pathway, exhibit nuanced expression profiles. Specific proteins, including phenylalanine ammonia-lyase, shikimate dehydrogenase, cinnamyl alcohol dehydrogenase 5, and peroxidase, show significantly higher expression in the resistant genotype across infection stages. Additionally, proteins involved in plant-pathogen, intracellular pH regulation, and antioxidant defense exhibit differential expression, contributing to a comprehensive understanding of the complex regulatory network during S. sclerotiorum infection. This research not only enhances our understanding of the molecular mechanisms underlying resistance but also underscores the varied strategies utilized by Brassicaceae to combat pathogenic intrusion, emphasizing the potential for developing resistant cultivars against S. sclerotiorum.

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Data availability

The data of this study are available from the corresponding author upon reasonable request.

References

  • Agoda-Tandjawa, G., Durand, S., Gaillard, C., Garnier, C., & Doublier, J. L. (2012). Properties of cellulose/pectins composites: Implication for structural and mechanical properties of cell wall. Carbohydrate Polymers, 90(2), 1081–1091.

    Article  CAS  PubMed  Google Scholar 

  • Bai, H., Si, H., Zang, J., Pang, X., Yu, L., Cao, H., Xing, J., Zhang, K., & Dong, J. (2021). Comparative proteomic analysis of the defense response to Gibberella stalk rot in maize and reveals that ZmWRKY83 is involved in plant disease resistance. Frontiers in Plant Science, 12, 694973.

    Article  PubMed  PubMed Central  Google Scholar 

  • Balint-Kurti, P. (2019). The plant hypersensitive response: Concepts, control and consequences. Molecular Plant Pathology, 20(8), 1163–1178.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bissoli, G., Niñoles, R., Fresquet, S., Palombieri, S., Bueso, E., Rubio, L., García-Sánchez, M. J., Fernández, J. A., Mulet, J. M., & Serrano, R. (2012). Peptidyl-prolyl cis-trans isomerase ROF2 modulates intracellular pH homeostasis in Arabidopsis. The Plant Journal, 70(4), 704–716.

    Article  CAS  PubMed  Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Chand, S., Patidar, O. P., Chaudhary, R., Saroj, R., Chandra, K., Meena, V. K., Limbalkar, O. M., Patel, M. K., Pardeshi, P. P., & Vasisth, P. (2021). Rapeseed-mustard breeding in India: Scenario, achievements and research needs. In: Brassica breeding and biotechnology. IntechOpen. https://doi.org/10.5772/intechopen.96319

  • Derbyshire, M. C., & Denton-Giles, M. (2016). The control of sclerotinia stem rot on oilseed rape (Brassica napus): Current practices and future opportunities. Plant Pathology, 65(6), 859–877.

  • Ding, L. N., Li, T., Guo, X. J., Li, M., Liu, X. Y., Cao, J., & Tan, X. L. (2021). Sclerotinia stem rot resistance in rapeseed: Recent progress and future prospects. Journal of Agricultural and Food Chemistry, 69(10), 2965–2978.

    Article  CAS  PubMed  Google Scholar 

  • Eckardt, N. A., Ainsworth, E. A., Bahuguna, R. N., Broadley, M. R., Busch, W., Carpita, N. C., Castrillo, G., Chory, J., DeHaan, L. R., Duarte, C. M., & Henry, A. (2023). Climate change challenges, plant science solutions. The Plant Cell, 35(1), 24–66.

    Article  PubMed  Google Scholar 

  • Eklöf, J. M., & Brumer, H. (2010). The XTH gene family: An update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiology, 153(2), 456–466.

    Article  PubMed  PubMed Central  Google Scholar 

  • Eldakak, M., Milad, S. I., Nawar, A. I., & Rohila, J. S. (2013). Proteomics: A biotechnology tool for crop improvement. Frontiers in Plant Science, 4, 35.

    Article  PubMed  PubMed Central  Google Scholar 

  • Elmore, J. M., Griffin, B. D., & Walley, J. W. (2021). Advances in functional proteomics to study plant-pathogen interactions. Current Opinion in Plant Biology, 63, 102061.

    Article  CAS  PubMed  Google Scholar 

  • Fukushima, R. S., & Hatfield, R. D. (2001). Extraction and isolation of lignin for utilization as a standard to determine lignin concentration using the acetyl bromide spectrophotometric method. Journal of Agricultural and Food Chemistry, 49(7), 3133–3139.

    Article  CAS  PubMed  Google Scholar 

  • Hu, X., Puri, K. D., Gurung, S., Klosterman, S. J., Wallis, C. M., Britton, M., Durbin-Johnson, B., Phinney, B., Salemi, M., Short, D. P., & Subbarao, K. V. (2019). Proteome and metabolome analyses reveal differential responses in tomato-Verticillium dahliae-interactions. Journal of Proteomics, 207, 103449.

  • Karasov, T. L., Chae, E., Herman, J. J., & Bergelson, J. (2017). Mechanisms to mitigate the trade-off between growth and defense. The Plant Cell, 29(4), 666–680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur, S., Samota, M. K., Choudhary, M., Choudhary, M., Pandey, A. K., Sharma, A., & Thakur, J. (2022). How do plants defend themselves against pathogens-Biochemical mechanisms and genetic interventions. Physiology and Molecular Biology of Plants, 28(2), 485–504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, M. H., Jeon, H. S., Kim, S. H., Chung, J. H., Roppolo, D., Lee, H. J., Cho, H. J., Tobimatsu, Y., Ralph, J., & Park, O. K. (2019). Lignin-based barrier restricts pathogens to the infection site and confers resistance in plants. The EMBO Journal, 38(23), e101948.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Y., Feng, Y., Lü, Q., Yan, D., Liu, Z., & Zhang, X. (2019). Comparative proteomic analysis of plant–pathogen interactions in resistant and susceptible poplar ecotypes infected with Botryosphaeria dothidea. Phytopathology, 109(12), 2009–2021.

  • Li, Y., Yu, T., Wu, T., Wang, R., Wang, H., Du, H., Xu, X., Xie, D., & Xu, X. (2020). The dynamic transcriptome of pepper (Capsicum annuum) whole roots reveals an important role for the phenylpropanoid biosynthesis pathway in root resistance to Phytophthora capsici. Gene, 728, 144288.

  • Liu, Y., Lu, S., Liu, K., Wang, S., Huang, L., & Guo, L. (2019). Proteomics: A powerful tool to study plant responses to biotic stress. Plant Methods, 15, 1–20.

    Article  Google Scholar 

  • Macheroux, P., Schmid, J., Amrhein, N., & Schaller, A. (1999). A unique reaction in a common pathway: Mechanism and function of chorismate synthase in the shikimate pathway. Planta, 207, 325–334.

    Article  CAS  PubMed  Google Scholar 

  • Mamo, B. E., Eriksen, R. L., Adhikari, N. D., Hayes, R. J., Mou, B., & Simko, I. (2021). Epidemiological characterization of lettuce drop (Sclerotinia spp.) and biophysical features of the host identify soft stem as a susceptibility factor. PhytoFrontiers™, 1(3), 182–204.

  • Nascimento, L. B. D. S., & Tattini, M. (2022). Beyond photoprotection: The multifarious roles of flavonoids in plant terrestrialization. International Journal of Molecular Sciences, 23(9), 5284.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ninkuu, V., Yan, J., Fu, Z., Yang, T., Ziemah, J., Ullrich, M. S., Kuhnert, N., & Zeng, H. (2022). Lignin and its pathway-associated phytoalexins modulate plant defense against fungi. Journal of Fungi, 9(1), 52.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Sullivan, C. A., Belt, K., & Thatcher, L. F. (2021). Tackling control of a cosmopolitan phytopathogen: Sclerotinia. Frontiers in Plant Science, 12, 707509.

    Article  PubMed  PubMed Central  Google Scholar 

  • Orfila, C., Degan, F. D., Jørgensen, B., Scheller, H. V., Ray, P. M., & Ulvskov, P. (2012). Expression of mung bean pectin acetyl esterase in potato tubers: Effect on acetylation of cell wall polymers and tuber mechanical properties. Planta, 236, 185–196.

    Article  CAS  PubMed  Google Scholar 

  • Peng, Y., Li, S. J., Yan, J., Tang, Y., Cheng, J. P., Gao, A. J., Yao, X., Ruan, J. J., & Xu, B. L. (2021). Research progress on phytopathogenic fungi and their role as biocontrol agents. Frontiers in Microbiology, 12, 670135.

    Article  PubMed  PubMed Central  Google Scholar 

  • Peng, H., Feng, H., Zhang, T., & Wang, Q. (2023). Plant defense mechanisms in plant-pathogen interactions. Frontiers in Plant Science, 14, 1292294.

    Article  PubMed  PubMed Central  Google Scholar 

  • Perez-Harguindeguy, N., Diaz, S., Garnier, E., Lavorel, S., Poorter, H., Jaureguiberry, P., Bret-Harte, M. S., Cornwell, W. K., Craine, J. M., Gurvich, D. E., & Urcelay, C. (2016). Corrigendum to: New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany, 64(8), 715–716.

    Article  Google Scholar 

  • Porter, L. D., Hoheisel, G., & Coffman, V. A. (2009). Resistance of peas to Sclerotinia sclerotiorum in the Pisum core collection. Plant Pathology, 58(1), 52–60.

  • Quezada-Martinez, D., Addo Nyarko, C. P., Schiessl, S. V., & Mason, A. S. (2021). Using wild relatives and related species to build climate resilience in Brassica crops. Theoretical and Applied Genetics, 134(6), 1711–1728.

    Article  PubMed  Google Scholar 

  • Rai, P. K., Yadav, P., Kumar, A., Sharma, A., Kumar, V., & Rai, P. (2022). Brassica juncea: A crop for food and health. In: Kole, C., & Mohapatra, T. (Eds.), The Brassica juncea Genome. Compendium of Plant Genomes. Springer. https://doi.org/10.1007/978-3-030-91507-0_1

  • Raihan, M. R. H., Nahar, K., Nowroz, F., Siddika, A., & Hasanuzzaman, M. (2023). Oilseed brassica responses and tolerance to salt stress. In: Oilseed crops – biology. https://doi.org/10.5772/intechopen.109149

  • Ramaroson, M. L., Koutouan, C., Helesbeux, J. J., Le Clerc, V., Hamama, L., Geoffriau, E., & Briard, M. (2022). Role of phenylpropanoids and flavonoids in plant resistance to pests and diseases. Molecules, 27(23), 8371.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ranjan, A., Westrick, N. M., Jain, S., Piotrowski, J. S., Ranjan, M., Kessens, R., Stiegman, L., Grau, C. R., Conley, S. P., Smith, D. L., & Kabbage, M. (2019). Resistance against Sclerotinia sclerotiorum in soybean involves a reprogramming of the phenylpropanoid pathway and up-regulation of antifungal activity targeting ergosterol biosynthesis. Plant Biotechnology Journal, 17(8), 1567–1581.

  • Saharan, G. S., Mehta, N. K., & Meena, P. D. (2021). Biometabolomics of host resistance to hemi-biotrophs and necrotrophs. In Molecular Mechanism of Crucifer’s Host-Resistance. Springer. https://doi.org/10.1007/978-981-16-1974-8_5

  • Singh, B. K., Delgado-Baquerizo, M., Egidi, E., Guirado, E., Leach, J. E., Liu, H., & Trivedi, P. (2023a). Climate change impacts on plant pathogens, food security and paths forward. Nature Reviews Microbiology, 21, 640–656.

  • Singh, M., Avtar, R., Pal, A., Punia, R., Singh, V. K., Bishnoi, M., Singh, A., Choudhary, R. R., & Mandhania, S. (2020). Genotype-specific antioxidant responses and assessment of resistance against Sclerotinia sclerotiorum causing Sclerotinia rot in Indian mustard. Pathogens, 9(11), 892. https://doi.org/10.3390/pathogens9110892

  • Singh, M., Avtar, R., Lakra, N., Hooda, E., Singh, V. K., Bishnoi, M., Kumari, N., Punia, R., Kumar, N., & Choudhary, R. R. (2021). Genetic and proteomic basis of sclerotinia stem rot resistance in Indian mustard [Brassica juncea (L.) czern & coss.]. Genes, 12(11), 1784. https://doi.org/10.3390/genes12111784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, M., Avtar, R., Kumar, N., Punia, R., Pal, A., Lakra, N., Kumari, N., Kumar, D., Naruka, A., Bishnoi, M., & Khedwal, R. S. (2022a). Genetic analysis for resistance to sclerotinia stem rot, yield and its component traits in Indian mustard [Brassica juncea (L.) Czern & Coss.]. Plants, 11(5), 671. https://doi.org/10.3390/plants11050671

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh, M., Avtar, R., Lakra, N., Pal, A., Singh, V. K., Punia, R., Kumar, N., Bishnoi, M., Kumari, N., Khedwal, R. S., & Choudhary, R. R. (2022b). Early oxidative burst and anthocyanin-mediated antioxidant defense mechanism impart resistance against Sclerotinia sclerotiorum in Indian mustard. Physiological and Molecular Plant Pathology, 120, 101847. https://doi.org/10.1016/j.pmpp.2022.101847

    Article  CAS  Google Scholar 

  • Singh, M., Avtar, R., Bishnoi, M., & Kumari, N. (2023b). Unveiling the molecular basis of Stem-Physical-Strength-Mediated-Resistance (SPSMR) mechanism against Sclerotinia sclerotiorum in oilseed Brassica: A comparative transcriptome analysis between resistant Sinapis alba and susceptible Brassica juncea. Physiological and Molecular Plant Pathology, 128, 102179. https://doi.org/10.1016/j.pmpp.2023.102179

    Article  CAS  Google Scholar 

  • Singh, M., Avtar, R., Kumar, N., Punia, R., Lakra, N., Kumari, N., Bishnoi, M., Rohit, R., Choudhary, R. R., Khedwal, R. S., & Meena, R. K. (2023c). Assessment of sclerotinia stem and leaf rot resistance and its association with physical strength attributes in brassicaceae with special emphasis on Brassica Juncea. Journal of Plant Growth Regulation, 42(10), 6021–6037. https://doi.org/10.1007/s00344-022-10759-2

    Article  CAS  Google Scholar 

  • Singh, P., Song, Q. Q., Singh, R. K., Li, H. B., Solanki, M. K., Malviya, M. K., Verma, K. K., Yang, L. T., & Li, Y. R. (2019). Proteomic analysis of the resistance mechanisms in sugarcane during Sporisorium scitamineum infection. International Journal of Molecular Sciences, 20(3), 569.

  • Thakur, A. K., Parmar, N., Singh, K. H., & Nanjundan, J. (2020). Current achievements and future prospects of genetic engineering in Indian mustard (Brassica juncea L. Czern & Coss.). Planta, 252, 1–20.

  • USDA, Oilseeds: World Markets and Trade (2023). United States Department of Agriculture. https://www.fas.usda.gov/data/world-agricultural-production. Accessed 14 Jul 2023.

  • Yadav, V., Wang, Z., Wei, C., Amo, A., Ahmed, B., Yang, X., & Zhang, X. (2020). Phenylpropanoid pathway engineering: An emerging approach towards plant defense. Pathogens, 9(4), 312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav, V., Wang, Z., Guo, Y., & Zhang, X. (2022). Comparative transcriptome profiling reveals the role of phytohormones and phenylpropanoid pathway in early-stage resistance against powdery mildew in watermelon (Citrullus lanatus L.). Frontiers in Plant Science, 13, 1016822.

  • Zhang, R., Zheng, F., Wei, S., Zhang, S., Li, G., Cao, P., & Zhao, S. (2019). Evolution of disease defense genes and their regulators in plants. International Journal of Molecular Sciences, 20(2), 335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, Y., Shao, J., Zhou, Z., & Davis, R. E. (2019). Genotype-specific suppression of multiple defense pathways in apple root during infection by Pythium ultimum. Horticulture Research, 6, 10. https://doi.org/10.1038/s41438-018-0087-1

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Acknowledgements

Financial support received from Indian Council of Agricultural Research (ICAR); through an internal Grant [C (b) PB-170-ICAR (IRA-mustard)] is acknowledged.

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M.S., N.L. and R.A.: conceived and designed the experiment. M.S., N.L., R.R.C., R.P., A.D. and M.B.: experimented. R.A., N.L., N.K. and N.K.: supervised the work. M.S., N.N. and R.P.: analyzed the data and prepared the first draft. M.S., N.L. and RA: improved and finalized the manuscript.

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Correspondence to Manjeet Singh.

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Singh, M., Avtar, R., Lakra, N. et al. Comparative proteomic analysis provides insight into the key proteins involved in novel stem-physical-strength-mediated resistance (SPSMR) mechanism against Sclerotinia sclerotiorum in Brassicaceae. Eur J Plant Pathol (2024). https://doi.org/10.1007/s10658-024-02903-3

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