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Transcriptomic analysis provides insights into the AUXIN RESPONSE FACTOR 6-mediated repression of nicotine biosynthesis in tobacco (Nicotiana tabacum L.)

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Abstract

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NtARF6 overexpression represses nicotine biosynthesis in tobacco. Transcriptome analysis suggests that NtARF6 acts as a regulatory hub that connect different phytohormone signaling pathways to antagonize the jasmonic acid-induced nicotine biosynthesis.

Abstract

Plant specialized metabolic pathways are regulated by a plethora of molecular regulators that form complex networks. In Nicotiana tabacum, nicotine biosynthesis is regulated by transcriptional activators, such as NtMYC2 and the NIC2-locus ERFs. However, the underlying molecular mechanism of the regulatory feedback is largely unknown. Previous research has shown that NbARF1, a nicotine synthesis repressor, reduces nicotine accumulation in N. benthamiana. In this study, we demonstrated that overexpression of NtARF6, an ortholog of NbARF1, was able to reduce pyridine alkaloid accumulation in tobacco. We found that NtARF6 could not directly repress the transcriptional activities of the key nicotine pathway structural gene promoters. Transcriptomic analysis suggested that this NtARF6-induced deactivation of alkaloid biosynthesis might be achieved by the antagonistic effect between jasmonic acid (JA) and other plant hormone signaling pathways, such as ethylene (ETH), salicylic acid (SA), abscisic acid (ABA). The repression of JA biosynthesis is accompanied by the induction of ETH, ABA, and SA signaling and pathogenic infection defensive responses, resulting in counteracting JA-induced metabolic reprogramming and decreasing the expression of nicotine biosynthetic genes in vivo. This study provides transcriptomic evidence for the regulatory mechanism of the NtARF6-mediated repression of alkaloid biosynthesis and indicates that this ARF transcription factor might act as a regulatory hub to connect different hormone signaling pathways in tobacco.

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Data availability

Sequencing data for root tissue RNA from the EV control line (SAMN18145490), three NtARF6-OE lines (SAMN18145491, SAMN18145492, and SAMN18145493 of N. tabacum cv. Coker176 were available from BioProject PRJNA706840 (https://www.ncbi.nlm.nih.gov/bioproject/). The genome and gene model of N. tabacum cv. K326 used for RNA-sequencing analysis were available at ftp://ftp.solgenomics . net/genomes/Nicotiana_tabacum/edwards_et_al_2017/assembly/Ntab-v4.5_genome_Scf_Edards2017.fasta.gz  and ftp://ftp.solgenomics.net/genomes/Nicotiana_tabacum/edwards_et_al_2017/annotation/Ntab-v4.5_gene_models_Scf_Edwards2017.gff , respectively. The differential expressed genes and enriched KEGG pathways are included in this published article and its supplementary information files.

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Acknowledgements

The authors thank Dr. Ge Bai (Yunnan Academy of Tobacco Agricultural Sciences, China) for critical comments on this manuscript. This research was supported by the Projects of YATAS (Contract No. 2019530000241005 and 2017YN05), and the National Natural Science Foundation of China (Grant No. 31860069) to XS.

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Authors and Affiliations

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

    Mengyang Hu, Bingwu Wang, Zhongbang Song, Yulong Gao, Cheng Yuan, Changjun Huang, Lu Zhao, Yihan Zhang, Congming Zou & Xueyi Sui

  2. Tobacco Research Institute of Chinese Academy of Agricultural Sciences, Qingdao, 266101, Shandong, China

    Hongbo Zhang

  3. College of Agronomy and Biotechnology, Southwest University, Chongqing, 400715, China

    Mengyang Hu & Longchang Wang

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  1. Mengyang Hu
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  2. Hongbo Zhang
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  3. Bingwu Wang
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  4. Zhongbang Song
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  6. Cheng Yuan
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  11. Congming Zou
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Contributions

XS designed the study; MH, YG, ZS, CY, CH, and LZ performed experiments; BW, CH, YZ, and CZ analyzed data; XS, ZH, HM, LW, and CZ wrote the paper. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Xueyi Sui.

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Hu, M., Zhang, H., Wang, B. et al. Transcriptomic analysis provides insights into the AUXIN RESPONSE FACTOR 6-mediated repression of nicotine biosynthesis in tobacco (Nicotiana tabacum L.). Plant Mol Biol 107, 21–36 (2021). https://doi.org/10.1007/s11103-021-01175-3

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