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Comparative transcriptome analysis reveals the regulatory effects of exogenous auxin on lateral root development and tanshinone accumulation in Salvia miltiorrhiza

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Abstract

Main conclusion

The physiological and transcriptome analysis revealed that auxin was a positive regulator of lateral root development and tanshinone accumulation in Salvia miltiorrhiza .

Abstract

Roots of S. miltiorrhiza are widely used as medicinal materials in China, and the root morphology and content of bioactive compounds [such as phenolic acids and diterpenoid quinones (tanshinones)] are the main factors to determine the quality of this herb. Auxin regulates root development and secondary metabolism in many plant species, but little is known about its function in S. miltiorrhiza. In this study, S. miltiorrhiza seedlings were treated (exogenous application) with the auxin indole-3-acetic acid (IAA) and the polar auxin transport inhibitor N-1-naphthylphthalamic acid (NPA) to investigate the regulatory roles of auxin in S. miltiorrhiza. The results indicated that exogenous IAA promoted both lateral root development and tanshinones biosynthesis in S. miltiorrhiza. The NPA application suppressed the lateral root development but showed no obvious effects on tanshinones accumulation. Based on the RNA-seq analysis, expressions of genes related to auxin biosynthesis and signaling transduction were altered in both treated groups. Coincidental with the enhanced content of tanshinones, transcripts of several key enzyme genes in the tanshinones biosynthetic pathway were stimulated after the exogenous IAA application. The expression profiles of seven common transcription factor domain-containing gene families were analyzed, and the results implied that some AP2/ERF genes were probably responsible for the auxin-induced lateral root development in S. miltiorrhiza. These findings shed new light on the regulatory roles of auxin on root development and bioactive compounds biosynthesis in S. miltiorrhiza, and lay the groundwork for future research into the detailed molecular mechanism underlying these biological functions.

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Data availability

The raw data generated in this study have been deposited in the Sequence Read Archive (SRA) at NCBI (PRJNA913254) repository. The S. miltiorrhiza genome is publicly available in the National Genomics Data Center (https://bigd.big.ac.cn/), under accession number GWHAOSJ00000000 is publicly accessible at https://ngdc.cncb.ac.cn/gwh/.

Abbreviations

ARF:

Auxin response factor

DEG:

Differentially expressed gene

GO:

Gene Ontology

KEGG:

Kyoto Encyclopedia of Genes and Genomes

LRP:

Lateral root primordia

NPA:

N-1-naphthylphthalamic acid

TF:

Transcription factor

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Acknowledgements

This work was financially supported by Key project at the central government level: the ability establishment of sustainable use for valuable Chinese medicine resources (2060302), the National Natural Science Foundation of China (31700257), Zhejiang Provincial Natural Science Foundation of China (LR21H280002), the Major Science and Technology Projects of Breeding New Varieties of Agriculture in Zhejiang Province (2021C02074), and Key R&D Program of Shaanxi Province (2022SF-255).

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Correspondence to Shuncang Zhang or Dongfeng Yang.

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The authors declare that the research was conducted in the absence of any commercial or financial relationship that could be construed as a potential conflict of interest.

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Communicated by Dorothea Bartels.

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425_2023_4193_MOESM1_ESM.tif

Supplementary file1Fig. S1 The Principal Component Analysis (PCA) of the gene expressions in different sample sets. CK, the control group; IAA, the IAA treated group; NPA, the NPA treated group (TIF 796 KB)

425_2023_4193_MOESM2_ESM.tif

Supplementary file2Fig. S2 The heatmap of all DEGs in the exogenous IAA treated group (a) and NPA treated group (b). Changes in expression level are represented with different colors, the red indicates a higher expression level, and blue indicates a lower expression level. CK, the control group; IAA, the IAA treated group; NPA, the NPA treated group (TIF 5267 KB)

425_2023_4193_MOESM3_ESM.tif

Supplementary file3Fig. S3 Volcano plot of the DEGs with the cutoff (|log2(Fold change)| > 1 and FDR < 0.05) in the exogenous IAA treated group (a) and NPA treated group (b). The red color represents up-regulated DEGs, the green color represents down-regulated DEGs, the gray color represents the non-DEGs (TIF 3255 KB)

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Zhang, S., Qiu, L., Zheng, Y. et al. Comparative transcriptome analysis reveals the regulatory effects of exogenous auxin on lateral root development and tanshinone accumulation in Salvia miltiorrhiza. Planta 258, 33 (2023). https://doi.org/10.1007/s00425-023-04193-1

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