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A time-resolved dual transcriptome analysis reveals the molecular regulating network underlying the compatible/incompatible interactions between cabbage (Brassica oleracea) and Fusarium oxysporum f. sp. conglutinans

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Abstract

Aims

Cabbage Fusarium wilt (CFW) disease, caused by the soil-borne fungus Fusarium oxysporum f. sp. conglutinans (Foc), threatens cabbage production worldwide. We aimed to explore the molecular mechanism of CFW resistance and the avirulence/virulence factors of Foc.

Methods

The resistant ‘96–100’ and susceptible ‘01–20’ cabbage lines were examined histologically and in RNA-seq analyses. The key differentially expressed genes (DEGs) and pathways of both the host and fungus were determined via bioinformatics databases and tools.

Results

After inoculation, Foc began to colonize in the root of 01–20 at approximately 3 dpi and almost covered the root at 9 dpi, while the colonization was inhibited in 96–100. 96,142 and 3152 unigenes were generated for cabbage and Foc, respectively, by de novo assembly. For cabbage, there were 42,056 and 37,346 DEGs in 01–20 and 96–100 at all time points. Plant-pathogen interaction (map04626) was the major enrichment pathway among the DEGs. Many NBS-LRR genes and WRKY transcription factors were identified with different expression levels between 96 and 100 and 01–20. For Foc, 977 upregulated genes and 113 downregulated genes were identified, and the pathway of ribosome (map03010) was greatly enriched. There were 1 potential effectors, 2 elicitors and 6 virulence factors with increased or decreased transcript abundance among Foc DEGs, which deserved further functional validation. The RNA-seq data were further validated by qRT-PCR.

Conclusions

Our results provide a distinct dual transcriptomic landscape to reveal the molecular mechanisms of cabbage resistance to Foc, and expand our understanding of the interaction between plant hosts and their fungal pathogens.

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31701927), Central Public-interest Scientific Institution Basal Research Fund (Y2020PT01; Y2018YJ04), Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-IVFCAAS), and earmarked fund for the Modern Agro-Industry Technology Research System, China (CARS-23).

Data submissions

The raw reads of our RNA-seq data in this work were deposited in the Sequence Read Archive under accession numbers PRJNA548392 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA548392). This Transcriptome Shotgun Assembly project has been deposited at DDBJ/ENA/GenBank under the accession GIBT00000000. The version described in this paper is the first version, GIBT01000000.

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Correspondence to Honghao Lv.

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Responsible Editor: Hans Lambers.

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Fig. S1

197 Foc genes idetified in the present study and annotated in the pathogen host interactions (PHI) database. (JPG 633 kb)

Fig. S2

Heat maps of the enriched KEGG terms identified for the Foc DEGs; the blue colour represents zero DEGs, and a dark red colour represent a greater statistical enrichment. S-Foc: the Foc unigenes identified in the S-line; R-Foc: the Foc unigenes identified in the R-line. (JPG 148 kb)

Fig. S3

Heat maps of the genes involved in plant-pathogen interaction, plant hormone signal transduction, MAPK signalling and calcium signalling pathway related to the defence response of the R-line and S-line to CFW. (JPG 32951 kb)

Fig. S4

Heat maps of all NBS-LRR genes and transcription factors involved in plant-pathogen interaction, plant hormone signal transduction, MAPK signalling and calcium signalling pathway related to the defence response of the R-line and S-line to CFW. (JPG 21287 kb)

Fig. S5

Heat maps of the DEGs involved in the plant hormone signal transduction pathway in the R- and S-lines after inoculation. (JPG 6222 kb)

Fig. S6

Heat map of the 197 genes annotated in the PHI database at 3, 6 and 9 dpi. S-Foc: the Foc unigenes identified in the S-line; R-Foc: the Foc unigenes identified in the R-line. (JPG 2605 kb)

Fig. S7

Heat map of the 44 unigenes annotated in the carbohydrate-active enzymes (CAZy) database (A) and 12 unigenes annotated in the Fungal cytochrome P450 (FCPD) database (B) at 3, 6 and 9 dpi. S-Foc: the Foc unigenes identified in the S-line; R-Foc: the Foc unigenes identified in the R-line. (JPG 2367 kb)

Supplement Table 1

. Functional annotation results of all the unigenes in different database. (XLSX 13804 kb)

Supplement Table 2

. The enrichment results of the KEGG level2 for cabbage and Foc and the number of the DEGs in these terms (XLSX 26 kb)

Supplement Table 3

. The enrichment results of the KEGG pathway for cabbage and Foc and the number of the DEGs in these terms. (XLSX 17 kb)

Supplement Table 4

. The 64 NBS-LRR unigenes and 117 transcription factors identified in plant-pathogen interaction, plant hormone signal transduction, MAPK signaling and calcium signaling pathway in this study. (XLSX 21 kb)

Supplement Table 5

. Identification results of the cabbage DEGs involved in plant hormone signal transduction pathway in this study. (XLSX 45 kb)

Supplement Table 6

. The expression level of the Foc genes annotated in the PHI database in this study. (XLSX 88 kb)

Supplement Table 7

. The expression level of the Foc genes annotated in the CAZy database in this study. (XLSX 28 kb)

Supplement Table 8

. The expression level of the Foc genes annotated in the FCPD database in this study. (XLSX 16 kb)

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Liu, X., Zhao, C., Yang, L. et al. A time-resolved dual transcriptome analysis reveals the molecular regulating network underlying the compatible/incompatible interactions between cabbage (Brassica oleracea) and Fusarium oxysporum f. sp. conglutinans. Plant Soil 448, 455–478 (2020). https://doi.org/10.1007/s11104-020-04437-z

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