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NtERF4 promotes the biosynthesis of chlorogenic acid and flavonoids by targeting PAL genes in Nicotiana tabacum

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Abstract

Chlorogenic acid (CGA) and flavonoids are important secondary metabolites, which modulate plant growth and development, and contribute to plant resistance to various environmental stresses. ERF4 has been shown to be a repressor of anthocyanin accumulation in grape, but its full roles in regulating the biosynthesis of other phenylpropanoid compounds still needs to be further studied. In the present study, two NtERF4 genes were identified from N. tabacum genome. The expression level of NtERF4a was higher than that of NtERF4b in all the tobacco tissues examined. Over-expression of NtERF4a significantly promoted the accumulation of CGA and flavonoids in tobacco leaves, while silencing of NtERF4a significantly repressed the biosynthesis of CGA and flavonoids. RNA-seq analysis of NtERF4a-OE and WT plants revealed 8 phenylpropanoids-related differentially expressed genes (DEGs), including 4 NtPAL genes that encode key enzymes in the phenylpropanoid pathway. Activation of NtERF4a-GR fusion protein in tobacco significantly induced the transcription of NtPAL1 and NtPAL2 in the presence of protein synthesis inhibitor. Chromatin immunoprecipitation and Dual-Luc assays further indicated that NtERF4a could bind to the GCC box presented in the promoters of NtPAL1 and NtPAL2, thereby activating their transcription. Moreover, ectopic expression of NtERF4a induced the transcription of NtGSK1, NtMYC2, and NtJAZ3 genes, and enhanced the resistance of tobacco seedlings to salt and drought stresses, indicating multiple roles of NtERF4a in plants. Our findings revealed new roles of NtERF4a in modulating the accumulation of phenylpropanoid compounds in tobacco, and provided a putative target for improving phenylpropanoids synthesis and stress resistance in plants.

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All data generated or analyzed during this study are included in this published article and in its online supplemental material.

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Acknowledgements

This work was supported by Henan Natural Science Foundation (No. 222300420388), Tobacco Genome Projects of CNTC (Grant No. 110202201015 (JY-15) and 110202101044 (JY-21)), Foundation of Yunnan Tobacco Industry Co. Ltd (2022JY01), and Science and Technology Projects of HNTI (KY2022YC0003).

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  1. Shun He and Xin Xu have contributed equally to this work.

Authors and Affiliations

  1. China Tobacco Gene Research Center, Zhengzhou Tobacco Research Institute of CNTC, Zhengzhou, 450001, China

    Shun He, Xin Xu, Zhaopeng Luo, Pingping Liu, Mingzhu Wu, Jun Yang & Zhong Wang

  2. Yunnan Key Laboratory of Tobacco Chemistry, R&D Center of China Tobacco Yunnan Industrial Co. Ltd., Kunming, 650202, China

    Qian Gao & Haitao Huang

  3. Yunnan Academy of Tobacco Agricultural Sciences, Kunming, 650021, China

    Changjun Huang & Jianmin Zeng

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Contributions

ZW and JMZ conceived and supervised this study. SH, XX, QG, CJH, ZPL, PPL, MZW, and HTH conducted the experiments and data analysis. ZW and SH summarized the results and wrote the manuscript. JY advised and modified the manuscript. All authors reviewed the manuscript.

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He, S., Xu, X., Gao, Q. et al. NtERF4 promotes the biosynthesis of chlorogenic acid and flavonoids by targeting PAL genes in Nicotiana tabacum. Planta 259, 31 (2024). https://doi.org/10.1007/s00425-023-04301-1

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  • DOI: https://doi.org/10.1007/s00425-023-04301-1

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