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. 2024 Feb 14;13(2):233.
doi: 10.3390/antiox13020233.

Exogenous Calcium Alleviates Oxidative Stress Caused by Salt Stress in Peanut Seedling Roots by Regulating the Antioxidant Enzyme System and Flavonoid Biosynthesis

Yan Gao  1 , Xuan Dong  1 , Rongjin Wang  1 , Fei Hao  1 , Hui Zhang  1 , Yongyong Zhang  1 , Guolin Lin  1
Affiliations

Exogenous Calcium Alleviates Oxidative Stress Caused by Salt Stress in Peanut Seedling Roots by Regulating the Antioxidant Enzyme System and Flavonoid Biosynthesis

Yan Gao et al. Antioxidants (Basel). .

Abstract

Soil salinity is one of the adversity stresses plants face, and antioxidant defense mechanisms play an essential role in plant resistance. We investigated the effects of exogenous calcium on the antioxidant defense system in peanut seedling roots that are under salt stress by using indices including the transcriptome and absolute quantitative metabolome of flavonoids. Under salt stress conditions, the antioxidant defense capacity of enzymatic systems was weakened and the antioxidant capacity of the linked AsA-GSH cycle was effectively inhibited. In contrast, the ascorbate biosynthesis pathway and its upstream glycolysis metabolism pathway became active, which stimulated shikimate biosynthesis and the downstream phenylpropanoid metabolism pathway, resulting in an increased accumulation of flavonoids, which, as one of the antioxidants in the non-enzymatic system, provide hydroxyl radicals to scavenge the excess reactive oxygen species and maintain the plant's vital activities. However, the addition of exogenous calcium caused changes in the antioxidant defense system in the peanut root system. The activity of antioxidant enzymes and the antioxidant capacity of the AsA-GSH cycle were enhanced. Therefore, glycolysis and phenylpropanoid metabolism do not exert antioxidant function, and flavonoids were no longer synthesized. In addition, antioxidant enzymes and the AsA-GSH cycle showed a trade-off relationship with sugars and flavonoids.

Keywords: antioxidant; exogenous calcium; flavonoids; metabolomic; reactive oxygen species; salt stress; transcriptomic.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Changes in physiological indices of peanut roots under different treatments. (a) Phenotype of peanut roots under different treatments. (b) Root activity. (c) Superoxide dismutase, SOD. (d) Catalase, CAT. (e) Peroxidase, POD. (f) Malondialdehyde, MDA. (g) Superoxide anion, O2−. (h) Hydrogen peroxide, H2O2. (i) Soluble sugar. Different lowercase letters indicate differences between different treatments (p < 0.05).
Figure 2
Figure 2
Preliminary analysis of transcriptomics data. (a) Correction heat map of different treatment groups. (b) Volcano plots of DEGs between CK and Na. (c) Volcano plots of DEGs between Na and Na_Ca. (d) Volcano plots of DEGs between CK and Ca.
Figure 3
Figure 3
Venn diagram and enrichment analysis of DEGs. (a) Venn diagram of DEGs and circle plots of GO enrichment analysis. Three circles from inside out. First circle: enriched classifications; outside the circle is a sitting scale for the number of genes; different colors represent different classifications (yellow for molecular function, blue for cellular components, green for biological processes). Second circle: the number of background genes in that classification and the p-value. The more genes there are, the longer the bar, the smaller the value, and the darker the color. Third circle: the rich factor value of each classification (the number of foreground genes in that classification divided by the number of background genes), where each cell of the background auxiliary line represents 0.1. The results of the GO enrichment analysis were sorted according to the size of the P-value, and the top 30 results were selected and plotted in a circle graph. (b) KEGG enrichment analysis bar chart of DEGs (the length of the bar indicates the number of genes enriched into the pathway, and the darker the color, the smaller the p-value).
Figure 4
Figure 4
Heatmap of the pathway of glycolysis, antioxidant enzymes, and ascorbate–glutathione cycle. Pathways were constructed based on the KEGG pathway and references. The four treatments are CK, Na, Ca, and Na_Ca from left to right. The squares indicate the average expression of the genes corresponding to the key enzymes in the biosynthetic pathway under the four treatments, where orange indicates up-regulation and green indicates down-regulation.
Figure 5
Figure 5
Preliminary analysis of metabolomics data. (a) Three-dimensional PCA score plots of metabolite profiles from different treatment groups. (b) Venn diagram of DAMs. (c) Histograms of up-and down-regulated flavonoids in three two-by-two comparison groups. (d) Three-dimensional pie chart of classification and proportion of 68 flavonoids detected in the peanut root.
Figure 6
Figure 6
Heat map of the pathways of DEGs and DAMs in the flavonoid synthesis pathway under different treatments. Pathways were constructed based on the KEGG pathway and references. The four treatments are CK, Na, Ca, and Na_Ca from left to right. Data in boxes indicate the average expression of DAMs in the four treatments, indicated by circles, where red indicates up-regulation and blue indicates down-regulation. The square under the arrows indicates the average expression of genes corresponding to key enzymes in the biosynthetic pathway under the four treatments, where orange indicates up-regulation and green indicates down-regulation.
Figure 7
Figure 7
RT-qPCR was performed to verify the expression pattern of key enzyme genes involved in flavonoid synthesis in peanut roots under different treatments. Values presented are mean ± SD (n ≥ 3). (A–H) are the relative expression levels of 8 genes, and their abscissas are the corresponding genes. Bars represent the results of RT-qPCR, and lines represent the results of RNA-Seq. The scale on the left axis represents relative expression, and the right axis represents FPKM values.
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