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Genetics and metabolic responses of Artemisia annua L to the lake of phosphorus under the sparingly soluble phosphorus fertilizer: evidence from transcriptomics analysis

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Abstract

The medicinal herb Artemisia annua L. is prized for its capacity to generate artemisinin, which is used to cure malaria. Potentially influencing the biomass and secondary metabolite synthesis of A. annua is plant nutrition, particularly phosphorus (P). However, most soil P exist as insoluble inorganic and organic phosphates, which results to low P availability limiting plant growth and development. Although plants have developed several adaptation strategies to low P levels, genetics and metabolic responses to P status remain largely unknown. In a controlled greenhouse experiment, the sparingly soluble P form, hydroxyapatite (Ca5OH(PO4)3/CaP) was used to simulate calcareous soils with low P availability. In contrast, the soluble P form KH2PO4/KP was used as a control. A. annua’s morphological traits, growth, and artemisinin concentration were determined, and RNA sequencing was used to identify the differentially expressed genes (DEGs) under two different P forms. Total biomass, plant height, leaf number, and stem diameter, as well as leaf area, decreased by 64.83%, 27.49%, 30.47%, 38.70%, and 54.64% in CaP compared to KP; however, LC–MS tests showed an outstanding 37.97% rise in artemisinin content per unit biomass in CaP contrary to KP. Transcriptome analysis showed 2015 DEGs (1084 up-regulated and 931 down-regulated) between two P forms, including 39 transcription factor (TF) families. Further analysis showed that DEGs were mainly enriched in carbohydrate metabolism, secondary metabolites biosynthesis, enzyme catalytic activity, signal transduction, and so on, such as tricarboxylic acid (TCA) cycle, glycolysis, starch and sucrose metabolism, flavonoid biosynthesis, P metabolism, and plant hormone signal transduction. Meanwhile, several artemisinin biosynthesis genes were up-regulated, including DXS, GPPS, GGPS, MVD, and ALDH, potentially increasing artemisinin accumulation. Furthermore, 21 TF families, including WRKY, MYB, bHLH, and ERF, were up-regulated in reaction to CaP, confirming their importance in P absorption, internal P cycling, and artemisinin biosynthesis regulation. Our results will enable us to comprehend how low P availability impacts the parallel transcriptional control of plant development, growth, and artemisinin production in A. annua. This study could lay the groundwork for future research into the molecular mechanisms underlying A. annua’s low P adaptation.

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Data availability

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found at BIG Sub, accession number: PRJAC012205.

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Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 82360753), the Guangxi Major Science and Technology Project of China (Grant No. GuikeAA22096021), the Natural Science Foundation of Guangxi Province (Grant No. 2023GXNSFAA026330), the Innovative Team for Traditional Chinese Medicinal Materials Quality of Guangxi (Grant No. GZKJ2305), the Scientific Research Funding Project of Guangxi Botanical Garden of Medicinal Plants (Grant No. GYJ202013), the Research and Innovation Team Building Project of Guangxi Botanical Garden of Medicinal Plants (Grant No. GYCH2019008), National Natural Science Foundation of China (Grant No. 81560623), the Key Laboratory Construction Program of Guangxi Health commission (Grant No. ZJC2020003), and the Key Techniques Research and Promotion of Guangxi Medicinal Materials Varieties (Grant No. GZKJ2314).

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Author notes

  1. Lingyun Wan and Juan Huo contributed equally to this work.

Authors and Affiliations

  1. Guangxi Key Laboratory of High-Quality Formation and Utilization of Dao-di Herbs, Guangxi Botanical Garden of Medicinal Plants, Nanning, China

    Lingyun Wan, Juan Huo, Xiaowen Ji, Lisha Song, Zhanjiang Zhang, Limei Pan, Jine Fu & Shugen Wei

  2. Faculty of Agriculture, Forestry and Food Engineering, Yibin University, Yibin, China

    Qiulan Huang & Ahmed H. El- Sappah

  3. Genetics Department, Faculty of Agriculture, Zagazig University, Zagazig, Egypt

    Mohamed A. Abd Elhamid, Salma A. Soaud, Rania M. Y. Heakel & Ahmed H. El- Sappah

  4. School of Pharmacy, Chengdu University of Traditional Chinese Medicine, Chengdu, China

    Jihai Gao

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  1. Lingyun Wan
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Contributions

Conceptualization: LW, JH, WS, QH, SW, and AE-S. Designed the experiments: LW, IJ, and SW. Performed the experiments: LR, JH, WH, and LD. Analyzed the results: LW, JH, QH, and AE-S. Draw the figures: AE-S, LW, and QH. Contributed reagents/materials: LW, LS, JH, ZZ, LP, and JF. Contributed to writing the original manuscript draft: LW, QH, and AE-S. Review and editing of the manuscript: AE-S, HQ, RE, SS, RMYH, SAS, MAAE, and MA. Writing final copy: AE-S. All authors contributed to the article and approved the submitted version.

Corresponding authors

Correspondence to Shugen Wei or Ahmed H. El- Sappah.

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Wan, L., Huo, J., Huang, Q. et al. Genetics and metabolic responses of Artemisia annua L to the lake of phosphorus under the sparingly soluble phosphorus fertilizer: evidence from transcriptomics analysis. Funct Integr Genomics 24, 26 (2024). https://doi.org/10.1007/s10142-024-01301-6

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