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. 2024 Feb 27:15:1334907.
doi: 10.3389/fpls.2024.1334907. eCollection 2024.

Molecular mechanism of endophytic bacteria DX120E regulating polyamine metabolism and promoting plant growth in sugarcane

Ying Qin  1 , Qaisar Khan  2 , Jia-Wei Yan  1 , Yu-Yi Wang  1 , Yang-Fei Pan  1 , Ying Huang  1 , Jiang-Lu Wei  3 , Dao-Jun Guo  4 , Yang-Rui Li  5 , Deng-Feng Dong  1 , Yong-Xiu Xing  1
Affiliations

Molecular mechanism of endophytic bacteria DX120E regulating polyamine metabolism and promoting plant growth in sugarcane

Ying Qin et al. Front Plant Sci. .

Abstract

Introduction: Sugarcane endophytic nitrogen-fixing bacterium Klebsiella variícola DX120E displayed broad impact on growth, but the exact biological mechanism, especially polyamines (PAs) role, is still meager.

Methods: To reveal this relationship, the content of polyamine oxidase (PAO), PAs, reactive oxygen species (ROS)-scavenging antioxidative enzymes, phytohormones, 1-aminocyclopropane-1-carboxylic synthase (ACS), chlorophyll content, and biomass were determined in sugarcane incubated with the DX120E strain. In addition, expression levels of the genes associated with polyamine metabolism were measured by transcriptomic analysis.

Results: Genomic analysis of Klebsiella variícola DX120E revealed that 39 genes were involved in polyamine metabolism, transport, and the strain secrete PAs in vitro. Following a 7-day inoculation period, DX120E stimulated an increase in the polyamine oxidase (PAO) enzyme in sugarcane leaves, however, the overall PAs content was reduced. At 15 days, the levels of PAs, ROS-scavenging antioxidative enzymes, and phytohormones showed an upward trend, especially spermidine (Spd), putrescine (Put), catalase (CAT), auxin (IAA), gibberellin (GA), and ACS showed a significant up-regulation. The GO and KEGG enrichment analysis found a total of 73 differentially expressed genes, involving in the cell wall (9), stimulus response (13), peroxidase activity (33), hormone (14) and polyamine metabolism (4).

Discussion: This study demonstrated that endophytic nitrogen-fixing bacteria stimulated polyamine metabolism and phytohormones production in sugarcane plant tissues, resulting in enhanced growth. Dual RNA-seq analyses provided insight into the early-stage interaction between sugarcane seedlings and endophytic bacteria at the transcriptional level. It showed how diverse metabolic processes selectively use distinct molecules to complete the cell functions under present circumstances.

Keywords: Klebsiella; antioxidative; interaction; phytohormone; transcriptomic.

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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.

Figures

Figure 1
Figure 1
Sugarcane tissue culture and endophytic bacterial inoculation process. (A, B), Differentiation; (B, C), Regeneration; (D), Emergence of seedlings; (E, F), Bacterial strain culture; (G), Uninoculated seedlings; (H), Inoculated seedlings.
Figure 2
Figure 2
Detection of polyamine production in Klebsiella variicola DX120E. (A) Uninoculated medium. (B) Inoculated medium. The strain was tested on Moeller’s decarboxylase agar medium amended with L-arginine-monohydrochloride, and the change from yellow to red color of the phenol-red in medium indicated the production of putrescine.
Figure 3
Figure 3
Effect of polyamine addition on growth of Klebsiella variicola DX120E. (A) Growth in response to different concentrations of exogenous spermine; (B) Growth in response to different concentrations of exogenous spermidine.
Figure 4
Figure 4
Effect of inoculation with Klebsiella variicola DX120E on polyamine content in sugarcane. (A) Polyamine oxidase; (B) Spermine; (C) Spermidine; (D) Putrescine; CK; Uninoculated; DX, Inoculated with Klebsiella variicola DX120E. The same lowercase letters above the bars indicate no significant difference between treatments in Duncan’s multiple range test, p > 0.05.
Figure 5
Figure 5
Effects of inoculation with Klebsiella variicola DX120E on the activeties of ROS-scavenging antioxidative enzymes in sugarcane leaves. (A) Superoxide dismutase (SOD) activity; (B) Catalase (CAT) activity. CK, Uninoculated; DX, Inoculated with Klebsiella variicola DX120E. The same lowercase letters above the bars indicate no significant difference between treatments in Duncan’s multiple range test, p > 0.05.
Figure 6
Figure 6
Effect of inoculation with Klebsiella variicola DX120E on the contents of phytohormones and 1-aminocyclopropane-1-carboxylic synthase (ACS) in sugarcane leaves. (A) Auxin (IAA) content; (B) Gibberellin (GA) content; (C) ACS content; (D) The growth of sugarcane plants. CK, Uninoculated; DX, Inoculated with Klebsiella variicola DX120E. The same lowercase letters above the bars indicate no significant difference between treatments in Duncan’s multiple range test, p > 0.05.
Figure 7
Figure 7
Volcano plot of differentially expressed genes (DEGs) statistics.
Figure 8
Figure 8
Functional enrichment analyses. (A) GO enrichment analysis of DEGs in L_DX vs L_CK. (B) KEGG pathway enrichment analysis of up-regulated DEGs in L_DX vs L_CK. The vertical axis indicates the pathways, the horizontal axis indicates the enrichment factor, the size of the dots indicates the number of genes in the pathway, and the color of the dots corresponds to the different P-adjustment ranges.
Figure 9
Figure 9
Correlation plot of qRT-PCR and RNA sequencing results.
Figure 10
Figure 10
DX120E inoculation effect on sugarcane polyamine metabolism and relevant pathways.
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