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. 2023 Aug 7:14:1134585.
doi: 10.3389/fmicb.2023.1134585. eCollection 2023.

Non-targeted metabolomics analysis reveals the mechanism of arbuscular mycorrhizal symbiosis regulating the cold-resistance of Elymus nutans

Haijuan Zhang  1 , Hexing Qi  1 , Guangxin Lu  1 , Xueli Zhou  1   2 , Junbang Wang  3 , Jingjing Li  1 , Kaifu Zheng  1 , Yuejun Fan  4 , Huakun Zhou  5 , Jiuluan Wang  6 , Chu Wu  7
Affiliations

Non-targeted metabolomics analysis reveals the mechanism of arbuscular mycorrhizal symbiosis regulating the cold-resistance of Elymus nutans

Haijuan Zhang et al. Front Microbiol. .

Abstract

Elymus nutans is a perennial grass of the Gramineae family. Due to its cold-resistance and nutrition deficiency tolerance, it has been applied to the ecological restoration of degraded alpine grassland on the Qinghai-Tibet Plateau. As an important symbiotic microorganism, arbuscular mycorrhizal fungi (AMF) have been proven to have great potential in promoting the growth and stress resistance of Gramineae grasses. However, the response mechanism of the AMF needs to be clarified. Therefore, in this study, Rhizophagus irregularis was used to explore the mechanism regulating cold resistance of E. nutans. Based on pot experiments and metabolomics, the effects of R. irregularis were investigated on the activities of antioxidant enzyme and metabolites in the roots of E. nutans under cold stress (15/10°C, 16/8 h, day/night). The results showed that lipids and lipid molecules are the highest proportion of metabolites, accounting for 14.26% of the total metabolites. The inoculation with R. irregularis had no significant effects on the activities of antioxidant enzyme in the roots of E. nutans at room temperature. However, it can significantly change the levels of some lipids and other metabolites in the roots. Under cold stress, the antioxidant enzyme activities and the levels of some metabolites in the roots of E. nutans were significantly changed. Meanwhile, most of these metabolites were enriched in the pathways related to plant metabolism. According to the correlation analysis, the activities of antioxidant enzyme were closely related to the levels of some metabolites, such as flavonoids and lipids. In conclusion, AMF may regulate the cold-resistance of Gramineae grasses by affecting plant metabolism, antioxidant enzyme activities and antioxidant-related metabolites like flavonoids and lipids. These results can provide some basis for studying the molecular mechanism of AMF regulating stress resistance of Gramineae grasses.

Keywords: Gramineae grasses; arbuscular mycorrhizal fungi; metabolomics; resistance mechanism; stress resistance.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer JU declared a past co-authorship with the author HuZ to the handling editor.

Figures

Figure 1
Figure 1
Detection of mycorrhizal infection of root samples. NT, normal temperature; NT-AMF, normal temperature + Rhizophagus irregularis; LT, low temperature; LT-AMF, low-temperature + R. irregularis. In the figure, the length of scale bars was 20 μm, which was used to measure the size of vesicles and hyphae. The same below.
Figure 2
Figure 2
The activity of antioxidant enzymes. (A) APX activity, (B) POD activity, (C) SOD activity, (D) CAT activity. In the figure, different lowercase letters indicate significant one-way ANOVA results between groups at p = 0.05.
Figure 3
Figure 3
Classification ring diagram of metabolites of root samples at the super-class level. Different colors in the figure represent different classifications, and numbers in the figure represent the amounts of metabolites in each classification.
Figure 4
Figure 4
(A) PCA diagram in positive ion mode, (B) PCA diagram in negative ion mode, (C) PLS-DA analysis in positive ion mode, (D) PLS-DA analysis in negative ion mode, (E) permutation test in positive ion mode, and (F) permutation test in negative ion mode.
Figure 5
Figure 5
Volcano plots of different metabolites among sample groups. At room temperature, the differential metabolites between the inoculated and non-inoculated groups in the positive (A) and negative (B) ion modes. After low-temperature stress, the differential metabolites between inoculated and non-inoculated groups under positive (C) and negative (D) ion modes.
Figure 6
Figure 6
Venn diagrams of different metabolites between the inoculated and non-inoculated groups treated with normal or low temperature. (A) Common up-regulated metabolites in positive ion mode; (B) common down-regulated metabolites in positive ion mode; (C) common up-regulated metabolites in negative ion mode; (D) common down-regulated metabolites in negative ion mode.
Figure 7
Figure 7
Cluster heatmaps of common differential metabolites between the inoculated and non-inoculated groups treated with normal or low temperature. (A) The down-regulated metabolites in inoculated groups, (B) the up-regulated metabolites in inoculated groups.
Figure 8
Figure 8
KEGG enrichment analysis of differential metabolites. (A) Metabolic pathways of DAMs enrichment in positive ion mode (NT-AMF vs. NT), (B) metabolic pathways of DAMs enrichment in negative ion mode (NT-AMF vs. NT), (C) metabolic pathways of DAMs enrichment in positive ion mode (LT-AMF vs. LT), (D) metabolic pathways of DAMs enrichment in negative ion mode (LT-AMF vs. LT).
Figure 9
Figure 9
Correlation heatmaps between antioxidant enzyme activities and antioxidant related metabolites. (A) The correlation heatmap of antioxidant enzyme activities and flavonoid metabolites, (B) the correlation heatmap of antioxidant enzyme activities and lipids and lipid-like molecules.
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