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. 2023 Sep 18:14:1267758.
doi: 10.3389/fpls.2023.1267758. eCollection 2023.

Metabolomics and transcriptomics analyses for characterizing the alkaloid metabolism of Chinese jujube and sour jujube fruits

Xiaofang Xue  1 , Ailing Zhao  1 , Yongkang Wang  1 , Haiyan Ren  1 , Wanlong Su  1 , Yi Li  1 , Meijuan Shi  1 , Li Liu  1 , Dengke Li  1
Affiliations

Metabolomics and transcriptomics analyses for characterizing the alkaloid metabolism of Chinese jujube and sour jujube fruits

Xiaofang Xue et al. Front Plant Sci. .

Abstract

Introduction: Jujube is an important economic forest tree whose fruit is rich in alkaloids. Chinese jujube (Ziziphus jujuba Mill.) and sour jujube (Ziziphus spinosa Hu.) are the two most important species of the jujube genus. However, the mechanisms underlying the synthesis and metabolism of alkaloids in jujube fruits remain poorly understood.

Methods: In this study, the fruits of Ziziphus jujuba 'Hupingzao' and Ziziphus spinosa 'Taigusuanzao' in different harvest stages were used as test materials, we first integrated widely targeted metabolomics and transcriptomics analyses to elucidate the metabolism of alkaloids of jujube fruits.

Results: In the metabolomics analysis, 44 alkaloid metabolites were identified in 4 samples, 3 of which were unique to sour jujube fruit. The differential alkaloid metabolites (DAMs) were more accumulated in sour jujube than in Chinese jujube; further, they were more accumulated in the white ripening stage than in the red stage. DAMs were annotated to 12 metabolic pathways. Additionally, transcriptomics data revealed 259 differentially expressed genes (DEGs) involved in alkaloid synthesis and metabolism. By mapping the regulatory networks of DAMs and DEGs, we screened out important metabolites and 11 candidate genes.

Discussion: This study preliminarily elucidated the molecular mechanism of jujube alkaloid synthesis. The candidate genes regulated the synthesis of key alkaloid metabolites, but the specific regulation mechanism is unclear. Taken together, our results provide insights into the metabolic networks of alkaloid synthesis in Chinese jujube and sour jujube fruits at different harvest stages, thereby providing a theoretical reference for further research on the regulatory mechanism of jujube alkaloids and their development and utilization.

Keywords: Chinese jujube; alkaloid metabolites; candidate genes; fruits; metabolome; regulatory network; sour jujube; transcriptome.

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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
Chinese jujube (Ziziphus jujuba ‘Hupingzao’) and sour jujube (Ziziphus spinosa ‘Taigusuanzao’) fruits at different harvest stages. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
Figure 2
Figure 2
Identification of alkaloid metabolites in Chinese jujube (Ziziphus jujuba ‘Hupingzao’) and sour jujube (Ziziphus spinosa ‘Taigusuanzao’). (A) Venn diagram of alkaloid metabolites in fruits of Chinese jujube and sour jujube at different harvest stages. (B) Quantitative analysis of alkaloid metabolites in different classes. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
Figure 3
Figure 3
Number of up- and downregulated alkaloid metabolites in various comparison groups. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
Figure 4
Figure 4
UpSet plot illustrating overlapping and specific alkaloid metabolites in various comparison groups. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
Figure 5
Figure 5
(A) Scatterplot based on the principal component analysis of DAMs. (B) Scatterplot based on the principal component analysis of the four samples. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
Figure 6
Figure 6
K-means cluster trend map of DAMs. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
Figure 7
Figure 7
KEGG enrichment of DAMs in each comparison group, where (A) indicates HR vs. SR, (B) indicates HW vs. HR, (C) indicates HW vs. SW, and (D) indicates SW vs. SR. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
Figure 8
Figure 8
UpSet plot revealing overlapping and specific genes related to alkaloid metabolism pathways in four samples.
Figure 9
Figure 9
(A) Venn diagram of DEGs in four samples. (B) UpSet plot illustrating the overlapping and specific DEGs in each comparison group. (C) Upregulated and downregulated DEGs in each comparison group. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
Figure 10
Figure 10
K-means cluster trend maps of DEGs. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
Figure 11
Figure 11
Regulatory network map of DAMs and DEGs.
Figure 12
Figure 12
Heatmap of differentially expressed genes. HW, HPZ white ripening stage; HR, HPZ red stage; SW, TGSZ white ripening stage; SR, TGSZ red stage.
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