Skip to main content
Log in

Overlapping pathways involved in resistance against Sclerotinia stem rot in Brassica napus revealed through transcriptomic and metabolomic profiling

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Brassica napus is one of the most important oilseed crops in the world, yet there are many challenges to its potential production. Sclerotinia sclerotiorum, which causes Sclerotinia stem rot, is a major fungal disease that reduces seed yield and oil quality. Research has been conducted to understand the genetic basis of resistance to Sclerotinia stem rot, with the majority of studies based on the identification of single or few resistant genes for disease control. The aim of this study was to identify genes involved in horizontal resistance to achieve a stable resistance response by investigating the key pathways adopted by the resistant lines in response to Sclerotinia stem rot. Therefore, we conducted comparative transcriptomic and metabolomic profiling to identify overlapping pathways in gene expression and biosynthesis. The resistance response was activated with the induction of the biosynthesis of amino acids and the biosynthesis of secondary metabolites in the resistant line. Early induction of phenylpropanoid biosynthesis at 24 hours post inoculation and arginine biosynthesis at three time points, i.e., 24, 48, and 96 hours post inoculation, induced specificity in resistant line. Glucosinolate biosynthesis, flavonoid biosynthesis, and the alanine, aspartate, and glutamate metabolism pathways were induced in the resistant line in our transcriptomics and metabolomics study. The genes for ethylene, salicylic acid, and jasmonic acid were also highly induced in the resistant line compared to the susceptible line based on the annotation of biotic stress genes using MapMan analysis. Our results may allow for the achievement of horizontal resistance and provide insight to breeders developing resistant varieties.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aliferis KA, Faubert D, Jabaji S (2014) A metabolic profiling strategy for the dissection of plant defense against fungal pathogens. PLoS ONE 9:e111930

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Bar-Even A, Noor E, Lewis NE, Milo R (2010) Design and analysis of synthetic carbon fixation pathways. Proc Natl Acad Sci 107:8889

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  • Barrientos-Moreno L, Molina-Henares MA, Pastor-García M, Ramos-González MI, Espinosa-Urgel M (2019) Arginine biosynthesis modulates pyoverdine production and release in Pseudomonas putida as part of the mechanism of adaptation to oxidative stress. J Bacteriol 201:e00419-e0454

    Article  Google Scholar 

  • Castro-Moretti FR, Gentzel IN, Mackey D, Alonso AP (2020) Metabolomics as an emerging tool for the study of plant-pathogen interactions. Metabolites 10:52

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953

    Article  ADS  PubMed  CAS  Google Scholar 

  • De La Torre F, Cañas RA, Pascual MB, Avila C, Cánovas FM (2014) Plastidic aspartate aminotransferases and the biosynthesis of essential amino acids in plants. J Exp Bot 65:5527–5534

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ducat DC, Silver PA (2012) Improving carbon fixation pathways. Curr Opin Chem Biol 16:337–344

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Friedt W, Tu J, Fu T (2018) Academic and economic importance of Brassica napus rapeseed. In: Liu S, Snowdon R, Chalhoub B (eds) The Brassica napus genome. Springer, Cham, pp 1–20

    Google Scholar 

  • Girard IJ, Tong C, Becker MG, Mao X, Huang J, De Kievit T, Fernando WGD, Liu S, Belmonte MF (2017) RNA sequencing of Brassica napus reveals cellular redox control of Sclerotinia infection. J Exp Bot 68:5079–5091

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Halkier BA, Gershenzon J (2006) BIOLOGY AND BIOCHEMISTRY OF GLUCOSINOLATES. Annu Rev Plant Biol 57:303–333

    Article  PubMed  CAS  Google Scholar 

  • Hildebrandt TM, Nunesnesi A, Araújo WL, Braun HP (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579

    Article  PubMed  CAS  Google Scholar 

  • Hong J, Yang L, Zhang D, Shi J (2016) Plant metabolomics: an indispensable system biology tool for plant science. Int J Mol Sci 17:767

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanehisa M (2016) KEGG bioinformatics resource for plant genomics and metabolomics. Methods Mol Biol 1374:55–70

    Article  PubMed  CAS  Google Scholar 

  • Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2016) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45:D353–D361

    Article  PubMed  PubMed Central  Google Scholar 

  • Kostyn K, Czemplik M, Kulma A, Bortniczuk M, Skała J, Szopa J (2012) Genes of phenylpropanoid pathway are activated in early response to Fusarium attack in flax plants. Plant Sci 190:103–115

    Article  PubMed  CAS  Google Scholar 

  • Maramorosch K, Loebenstein G (2009) Plant disease resistance: natural, non-host innate or inducible. In: Schaechter M (ed) Encyclopedia of microbiology, 3rd edn. Academic Press, Oxford, pp 589–596

    Chapter  Google Scholar 

  • Martínez G, Regente M, Jacobi S, Del Rio M, Pinedo M, De La Canal L (2017) Chlorogenic acid is a fungicide active against phytopathogenic fungi. Pestic Biochem Physiol 140:30–35

    Article  PubMed  Google Scholar 

  • Moselhy SS, Asami T, Abualnaja KO, Al-Malki AL, Yamano H, Akiyama T, Wada R, Yamagishi T, Hikosaka M, Iwakawa J, Okada K, Mori M, Kumosani TA (2016) Spermidine, a polyamine, confers resistance to rice blast. J Pestic Sci 41:79–82

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Obermeier C, Hossain MA, Snowdon R, Knüfer J, Von Tiedemann A, Friedt W (2013) Genetic analysis of phenylpropanoid metabolites associated with resistance against Verticillium longisporum in Brassica napus. Mol Breeding 31:347–361

    Article  CAS  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiu X-M, Sun Y-Y, Ye X-Y, Li Z-G (2020) Signaling role of glutamate in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2019.01743

    Article  PubMed  PubMed Central  Google Scholar 

  • Ranjan A, Westrick NM, Jain S, Piotrowski JS, Ranjan M, Kessens R, Stiegman L, Grau CR, Conley SP, Smith DL, 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 Biotechnol J 17:1567–1581

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seifbarghi S, Borhan MH, Wei Y, Coutu C, Robinson SJ, Hegedus DD (2017) Changes in the Sclerotinia sclerotiorum transcriptome during infection of Brassica napus. BMC Genom 18:266

    Article  Google Scholar 

  • Suharti WS, Nose A, Zheng S-H (2016) Metabolite profiling of sheath blight disease resistance in rice: in the case of positive ion mode analysis by CE/TOF-MS. Plant Prod Sci 19:279–290

    Article  CAS  Google Scholar 

  • Sun H, Song N, Ma L, Li J, Ma L, Wu J, Wu J (2017) Ethylene signalling is essential for the resistance of Nicotiana attenuata against Alternaria alternata and phytoalexin scopoletin biosynthesis. Plant Pathol 66:277–284

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Wen B, Mei Z, Zeng C, Liu S (2017) metaX: a flexible and comprehensive software for processing metabolomics data. BMC Bioinform 18:183

    Article  Google Scholar 

  • Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00534

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu J, Zhao Q, Yang Q, Liu H, Li Q, Yi X, Cheng Y, Guo L, Fan C, Zhou Y (2016) Comparative transcriptomic analysis uncovers the complex genetic network for resistance to Sclerotinia sclerotiorum in Brassica napus. Sci Rep 6:19007

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang B, Srivastava S, Deyholos MK, Kav NNV (2007) Transcriptional profiling of canola (Brassica napus L.) responses to the fungal pathogen Sclerotinia sclerotiorum. Plant Sci 173:156–171

    Article  CAS  Google Scholar 

  • Zeier J (2013) New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant Cell Environ 36:2085–2103

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Stephanopoulos G (2016) Co-culture engineering for microbial biosynthesis of 3-amino-benzoic acid in Escherichia coli. Biotechnol J 11:981–987

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Shi H, Liang S, Ning G, Xu N, Lu J, Liu X, Lin F (2015) MoARG1, MoARG5,6 and MoARG7 involved in arginine biosynthesis are essential for growth, conidiogenesis, sexual reproduction, and pathogenicity in Magnaporthe oryzae. Microbiol Res 180:11–22

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Buchwaldt L, Rimmer SR, Sharpe A, Mcgregor L, Bekkaoui D, Hegedus D (2009) Patterns of differential gene expression in Brassica napus cultivars infected with Sclerotinia sclerotiorum. Mol Plant Pathol 10:635–649

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

This research was financially supported by the funding from the Ministry of Science and Technology of China (2017YFE0104800) and the Natural Science Foundation of China (31671725).

Author information

Authors and Affiliations

Authors

Contributions

MQ and YZ designed the study. MQ, MS and QZ performed the experiments. GC, HH, GL and CF helped in data analysis. MQ and YZ wrote the manuscript. YZ supervised the project. All the authors read and revised the manuscript.

Corresponding author

Correspondence to Yongming Zhou.

Additional information

Communicated by Daolong Dou.

Publisher's Note

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

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qasim, M.U., Zhao, Q., Shahid, M. et al. Overlapping pathways involved in resistance against Sclerotinia stem rot in Brassica napus revealed through transcriptomic and metabolomic profiling. Plant Growth Regul 102, 297–312 (2024). https://doi.org/10.1007/s10725-023-00998-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-023-00998-y

Keywords

Navigation