Transcriptomic and metabolomic analyses reveal that bacteria promote plant defense during infection of soybean cyst nematode in soybean

Abstract

Background: Soybean cyst nematode (SCN) is the most devastating pathogen of soybean. Our previous study showed that the plant growth-promoting rhizobacterium Bacillus simplex strain Sneb545 promotes soybean resistance to SCN. Here, we conducted a combined metabolomic and transcriptomic analysis to gain information regarding the biological mechanism of defence enhancement against SCN in Sneb545-treated soybean. To this end, we compared the transcriptome and metabolome of Sneb545-treated and non-treated soybeans under SCN infection.

Results: Transcriptomic analysis showed that 6792 gene transcripts were common in Sneb545-treated and non-treated soybeans. However, Sneb545-treated soybeans showed a higher concentration of various nematicidal metabolites, including 4-vinylphenol, methionine, piperine, and palmitic acid, than non-treated soybeans under SCN infection.

Conclusions: Overall, our results validated and expanded the existing models regarding the co-regulation of gene expression and metabolites in plants, indicating the advantage of integrated system-oriented analysis.

Keywords: Bacillus simplex strain Sneb545; Metabolome; Nematicidal metabolites; Soybean; Soybean cyst nematode; Transcriptome.

Fig. 1

Graphical presentation of the laboratorial design. A float tray substrate was positioned in plastic pots reserved for two experiments (transcriptomic analysis and metabolomics analysis). The seeds were grown in a greenhouse with supplemental lighting (16 h light/8 h dark cycle, 26 ± 3 °C day/night). When the seeds were the two true leaves stage inoculated nematodes. There are three biological replicates in transcriptomic analysis and six biological replicates in metabolomics analysis. Per replicate of two plant roots is one sample. At 5 day post inoculation (dpi), roots samples were rapidly harvested, frozen in liquid N₂, and stored at − 80 °C for further experiments

Fig. 2

Number of different developmental stages soybean cyst nematode in roots of Sneb545 treatment and control treatment soybean roots at 5 day post inoculation (dpi). Each value represents the mean of five replicated±the standard error. Significant differences between Sneb545 treatment and control treatment soybean roots were identified with t test calculated with SPSS Base Ver.17.0, the significance threshold set at P < 0.05

Fig. 3

Venn diagrams showing commonality uniqueness of the constitutively-related genes between non-treated and Sneb545-treated soybeans infected with SCN. In total, 16,243 genes were constitutively regulated in the different treatment soybeans (p < 0.05). (Sneb545-treated soybeans infected with SCN (TI), non-treated soybeans infected with SCN (CI), Sneb545-treated soybeans not infected with SCN (TN), and non-treated soybeans not infected with SCN (CN)). a Transcripts represented different accumulation. b Transcripts represented up and down accumulation in different comparable group. c Transcripts represented that overlapped up and down accumulation

Fig. 4

OPLS-DA model analysis was performed using the most diverse sample. Sneb545-treated soybeans infected with SCN (TI), non-treated soybeans infected with SCN (CI), Sneb545-treated soybeans not infected with SCN (TN), non-treated soybeans not infected with SCN (CN). a OPLS-DA in CI vs CN group. b OPLS-DA in TI vs TN group

Fig. 5

Modulation of phenylpropanoid biosynthesis pathway under Sneb545-treated and non-treated soybean roots infected with SCN compared with not infected with SCN. Log2foldchange levels of different gene expression are presented at left triangle box (non-treated soybean roots infected with SCN compared with non-treated soybean roots not infected with SCN, CI vs CN), and at right square box (Sneb545-treated soybean roots infected with SCN compared with Sneb545-treated soybean roots not infected with SCN, TI vs TN). Green and red boxes indicate down- or up-regulation of the genes

Fig. 6

Modulation of cysteine and methionine metabolism pathway under Sneb545-treated and non-treated soybean roots infected with SCN compared with not infected with SCN. Log2foldchange levels of different gene expression are presented at left triangle box (non-treated soybean roots infected with SCN compared with non-treated soybean roots not infected with SCN, CI vs CN), and at right square box (Sneb545-treated soybean roots infected with SCN compared with Sneb545-treated soybean roots not infected with SCN, TI vs TN). Green and red boxes indicate down- or up-regulation of the genes

Fig. 7

Modulation of tropane, piperidine and pyridine alkaloid biosynthesis metabolism pathway under Sneb545-treated and non-treated soybean roots infected with SCN compared with not infected with SCN. Log2foldchange levels of different gene expression are presented at left triangle box (non-treated soybean roots infected with SCN compared with non-treated soybean roots not infected with SCN, CI vs CN), and at right square box (Sneb545-treated soybean roots infected with SCN compared with Sneb545-treated soybean roots not infected with SCN, TI vs TN). Green and red boxes indicate down- or up-regulation of the genes

Fig. 8

Modulation of biosynthesis of unsaturated fatty acids and Fatty acid metabolism pathway under Sneb545-treated and non-treated soybean roots infected with SCN compared with not infected with SCN. Log2foldchange levels of different gene expression are presented at left triangle box (non-treated soybean roots infected with SCN compared with non-treated soybean roots not infected with SCN, CI vs CN), and at right square box (Sneb545-treated soybean roots infected with SCN compared with Sneb545-treated soybean roots not infected with SCN, TI vs TN). Green and red boxes indicate down- or up-regulation of the genes