Rice Science ›› 2024, Vol. 31 ›› Issue (1): 87-102.DOI: 10.1016/j.rsci.2023.09.002
• Research Papers • Previous Articles Next Articles
Di Dongwei1, Ma Mingkun1,4, Zhang Xiaoyang1, Lu Yufang1, Herbert J. Kronzucker3, Shi Weiming1,2,4()
Received:
2023-06-01
Accepted:
2023-08-11
Online:
2024-01-28
Published:
2024-02-06
Contact:
Shi Weiming (Di Dongwei, Ma Mingkun, Zhang Xiaoyang, Lu Yufang, Herbert J. Kronzucker, Shi Weiming. Potential Secretory Transporters and Biosynthetic Precursors of Biological Nitrification Inhibitor 1,9-Decanediol in Rice as Revealed by Transcriptome and Metabolome Analyses[J]. Rice Science, 2024, 31(1): 87-102.
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Fig. 1. Influence of NH4+ and variety on 1,9-decanediol (1,9-D) release in rice. A, 1,9-D release from Wuyunjing 7 (WYJ7) roots with or without 1 mmol/L NH4Cl (NH4+) treatment. B, 1,9-D release in Wuyunjing 3 (WYJ3) and WYJ7 grown in control media. Six-week-old seedlings were transferred to new solutions with 1 mmol/L CaCl2 (control) or 1 mmol/L NH4Cl (NH4+ treatment) and grown for another 24 h prior to exudate collection. ND indicates not detected. Data are Mean ± SD with four replications. ***, P < 0.001 (t-test).
Fig. 2. Analysis of differentially synthesized metabolites (DSMs) based on gas chromatography-mass spectrometer (GC-MS). A and B, Orthogonal partial least squares-discriminant analysis (OPLS-DA) of NH4+-Wuyunjing 7 (N7)/CK-Wuyunjing 7 (C7) (A) and C7/CK- Wuyunjing 3 (C3) (B) groups. C and D, Volcano plots of DSMs in N7/C7 (C) and C7/C3 (D) groups. Each point in the volcano plot indicates an identified metabolite, and the red/blue/grey dots indicate up-/down-/unregulated metabolites. VIP, Variable importance of projection. E and F, Kyoto Encyclopedia of Genes and Genomes analysis of DSMs in N7/C7 (E) and C7/C3 (F) groups. The size and color of the dots indicate the number of DSMs and the significance (P < 0.05), respectively. ABC, ATP-binding cassette.
Fig. 3. Analysis of differentially synthesized metabolites (DSMs) based on liquid chromatography-mass spectrometer (LC-MS). A and B, Orthogonal partial least squares-discriminant analysis (OPLS-DA) of NH4+-Wuyunjing 7 (N7)/CK-Wuyunjing 7 (C7) (A) and C7/CK- Wuyunjing 3 (C3) (B) groups. C and D, Volcano plots of DSMs in N7/C7 (C) and C7/C3 (D) groups. Each point in the volcano plot indicates an identified metabolite, and the red/blue/grey dots indicate up-/down-/unregulated metabolites. VIP, Variable importance of projection. E and F, Kyoto Encyclopedia of Genes and Genomes analysis of DSMs in N7/C7 (E) and C7/C3 (F) groups. The size and color of the dots indicate the number of DSMs and the significance (P < 0.05), respectively. ABC, ATP-binding cassette.
Fig. 4. Analysis of differentially expressed unigenes (DEGs) based on RNA-seq analysis. A and B, Gene Ontology (GO) classification of DEGs in NH4+-Wuyunjing 7 (N7)/CK-Wuyunjing 7 (C7) (A) and C7/CK-Wuyunjing 3 (C3) (B) groups. C and D, Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis of DEGs in N7/C7 (C) and of C7/C3 (D) groups. E, Venn diagram showing co-regulated DEGs in N7/C7 and C7/C3 groups. F, Hierarchical clustering heatmap of co-upregulated DEGs in N7/C7 and C7/C3 groups.
Fig. 5. Identification of co-regulated differentially expressed unigenes (DEGs) and differentially synthesized metabolites (DSMs) via integrated analysis of metabolome and transcriptome. A and B, Correlation analysis of top 20 DEGs and DSMs in NH4+-Wuyunjing 7 (N7)/CK-Wuyunjing 7 (C7) (A) and C7/CK-Wuyunjing 3 (C3) (B) groups. Red/blue represents a positive/negative correlation. *, **, and *** represent 0.05, 0.01, and 0.001 levels, respectively. C, Venn analysis of co-regulated DEGs of top 100 correlation between DEGs and DSMs in N7/C7 and C7/C3 groups. D, Venn analysis of co-upregulated DSMs in N7/C7 and C7/C3 groups.
Fig. 6. Identification of possible genes involved in co-upregulated differentially expressed unigenes (DEGs) via qRT-PCR. A, Boxchart of three co-upregulated metabolites. B, qRT-PCR analysis of possible genes associated to DEGs. Six-week-old rice seedlings are transferred to fresh solutions with 1 mmol/L CaCl2 (control) or 1 mmol/L NH4Cl (NH4+ treatment) and grown for another 24 h prior to RNA extraction of roots. All data are normalized relative to OsUBI (LOC_Os03g13170). N7, C7, and C3 represent NH4+-Wuyunjing 7, CK-Wuyunjing 7, and CK-Wuyunjing 3, respectively. Values indicate Mean ± SD of three biological replicates. Error bars with different lowercase letters represent statistically significant differences (P < 0.05, Duncan’s test).
Fig. 7. Identification of possible 1,9-decanediol secretion-related genes. A and B, Hierarchical clustering heatmap of co-upregulated transporter-related differentially expressed unigenes (DEGs) in NH4+-Wuyunjing 7 (N7)/CK-Wuyunjing 7 (C7) (A) and C7/CK-Wuyunjing 3 (C3) (B) groups. C, Venn analysis of co-upregulated transporter-related genes in N7/C7 and C7/C3 groups. D, qRT-PCR analysis of co-upregulated genes. Six-week-old rice seedlings are transferred to fresh solutions with 1 mmol/L CaCl2 (control) or 1 mmol/L NH4Cl (NH4+ treatment) and grown for another 24 h prior to RNA extraction of roots. All data are normalized relative to OsUBI (LOC_Os03g13170). Values indicate Mean ± SD of three biological replicates. Error bars with different lowercase letters represent statistically significant differences (P < 0.05, Duncan’s test).
Fig. 8. Potential biosynthesis pathways and transporters responsible for 1,9-decanediol (1,9-D) synthesis and release in rice. A, Potential metabolic pathways involved in 1,9-D biosynthesis. B, Potential transporters responsible for 1,9-D release. ABC, ATP-binding cassette protein family; MATE, Multidrug and toxic compound extrusion family; MFS, Major facilitator superfamily. DSMs, Differentially synthesized metabolites; DEGs, Differentially expressed unigenes.
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