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. 2024 Apr 24;24(1):324.
doi: 10.1186/s12870-024-04994-w.

Study of cabbage antioxidant system response on early infection stage of Xanthomonas campestris pv. campestris

Zeci Liu  1 , Jie Wang  1 , Zhibin Yue  1 , Jue Wang  1 , Tingting Dou  1 , Tongyan Chen  1 , Jinbao Li  1 , Haojie Dai  1 , Jihua Yu  2
Affiliations

Study of cabbage antioxidant system response on early infection stage of Xanthomonas campestris pv. campestris

Zeci Liu et al. BMC Plant Biol. .

Abstract

Black rot, caused by Xanthomonas campestris pv. campestris (Xcc) significantly affects the production of cabbage and other cruciferous vegetables. Plant antioxidant system plays an important role in pathogen invasion and is one of the main mechanisms underlying resistance to biological stress. Therefore, it is important to study the resistance mechanisms of the cabbage antioxidant system during the early stages of Xcc. In this study, 108 CFU/mL (OD600 = 0.1) Xcc race1 was inoculated on "zhonggan 11" cabbage using the spraying method. The effects of Xcc infection on the antioxidant system before and after Xcc inoculation (0, 1, 3, and 5 d) were studied by physiological indexes determination, transcriptome and metabolome analyses. We concluded that early Xcc infection can destroy the balance of the active oxygen metabolism system, increase the generation of free radicals, and decrease the scavenging ability, leading to membrane lipid peroxidation, resulting in the destruction of the biofilm system and metabolic disorders. In response to Xcc infection, cabbage clears a series of reactive oxygen species (ROS) produced during Xcc infection via various antioxidant pathways. The activities of antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) increased after Xcc infection, and the ROS scavenging rate increased. The biosynthesis of non-obligate antioxidants, such as ascorbic acid (AsA) and glutathione (GSH), is also enhanced after Xcc infection. Moreover, the alkaloid and vitamin contents increased significantly after Xcc infection. We concluded that cabbage could resist Xcc invasion by maintaining the stability of the cell membrane system and improving the biosynthesis of antioxidant substances and enzymes after infection by Xcc. Our results provide theoretical basis and data support for subsequent research on the cruciferous vegetables resistance mechanism and breeding to Xcc.

Keywords: Brassica oleracea; Antioxidant system; Black rot; Omics; Resistance mechanism.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Effect of early Xcc infection on the osmotic regulation system. (A) soluble sugar; (B) soluble protein; (C) free proline; (D) malondialdehyde; (E) electrical conductivity. Mean ± standard error (SE), range, and coefficients of variation (CVs) for the antioxidant traits in the species analyzed. Species means with different letters are significantly different at p ≤ 0.05. Standard errors are indicated by bars. The same below
Fig. 2
Fig. 2
Effect of early Xcc infection on O2− and H2O2 contents. (A) DAB and NBT staining; (B) O2•− content; (C) H2O2 content
Fig. 3
Fig. 3
Effect of early Xcc infection on SOD, POD, and CAT enzymes. (A) SOD activity; (B) POD activity; (C) CAT activity; (D) SOD gene expression level; (E) POD gene expression level; (F) CAT gene expression level
Fig. 4
Fig. 4
Effect of early Xcc infection on non-enzymatic antioxidant contentin AsA-GSH cycle. (A) AsA content; (B) DHA content; (C) AsA/DHA ratio; (D) GSH content; (E) GSSG content; (F)GSH/GSSG ratio
Fig. 5
Fig. 5
Effect of early Xcc infection on antioxidant enzymes activities and related gene expression levels in AsA-GSH cycle.(A) APX activity; (B) DHAR activity; (C) GR activity; (D) MDHAR activity; (E)APX gene expression level; (F) DHAR gene expression level; (G) GR gene expression level; (F) MDHAR gene expression level
Fig. 6
Fig. 6
Differentially expressed antioxidant-related genes analysis. (A) Gene ontology (GO) classification of differentially expressed reactive oxygen species (ROS) genes. The horizontal coordinate is GO classification, the left side of the vertical coordinate is the percentage of the number of genes, and the right side is the number of genes. (B) Gene ontology of ROS genes. The horizontal coordinate is the proportion of the genes we’re interested and all the differentially expressed genes, while the vertical coordinate is each GO annotation entry. The size of the dots represents the number of differentially expressed genes annotated in the pathway, and the color of the dots represents the q-value of the hypergeometric test. (C) Kyoto Encyclopedia of Genes and Genomes (KEGG) classification of differentially expressed antioxidant-related genes. The horizontal coordinate is the number of genes annotated to this pathway and its proportion to the total number of genes annotated. (D) Cluster heat maps of antioxidant-related genes 0 d and 5 d after Xcc infection. Red and blue colour indicate up-regulated and down-regulated genes, respectively. The same below
Fig. 7
Fig. 7
Analysis of differentially expressed glutathione metabolism-related genes. (A, B, C) Gene ontology (GO) classification of differentially glutathione metabolism-related genes. (D, E) KEGG classification diagram and KEGG bubble diagram of glutathione metabolism. (F) Clustering heat map of glutathione metabolism-related differential gene expression
Fig. 8
Fig. 8
Analysis of differentially expressed ascorbate and aldarate metabolism-related genes. (A) GO classification of differentially expressed ascorbate and aldarate metabolism-related genes (biological processes). (B) KEGG classification diagram and KEGG bubble diagram of ascorbate and aldarate metabolism. (C) Clustering heat map of ascorbate and aldarate metabolism-related differential gene expression
Fig. 9
Fig. 9
Changes of enzyme activities and related gene expression levels involved in antioxidant defense under different Xcc infected days. (A) Expression levels of genes related to SOD, POD, and CAT enzymes biosynthesis. (B) Expression levels of genes related to APX, DHR, GR, MDHAR, and violanthine decycloxygenase (VDE) enzymes biosynthesis in AsA-GSH
Fig. 10
Fig. 10
Analysis of differential metabolites in cabbage leaves before and after Xcc infection. (A) Changes of alkaloid contents. (B) Changes of vitamin contents
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