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

• Published in: Plant molecular biology Vol. 107; no. 1-2; pp. 21 - 36
• Main Authors: Hu, Mengyang, Zhang, Hongbo, Wang, Bingwu, Song, Zhongbang, Gao, Yulong, Yuan, Cheng, Huang, Changjun, Zhao, Lu, Zhang, Yihan, Wang, Longchang, Zou, Congming, Sui, Xueyi
• Format: Journal Article
• Language: English
• Published: Dordrecht Springer Netherlands 01-09-2021; Springer Nature B.V
• Subjects: Abscisic acid; Alkaloids; Alkaloids - metabolism; Amino Acid Sequence; Biochemistry; Biomedical and Life Sciences; Biosynthesis; Biosynthetic Pathways - genetics; Cluster Analysis; Deactivation; Gene Expression Profiling; Gene Expression Regulation, Plant; Gene Ontology; Genes, Regulator; Genome, Plant; Jasmonic acid; Life Sciences; Metabolic pathways; Metabolism; Nicotiana - genetics; Nicotiana tabacum; Nicotine; Nicotine - biosynthesis; Organ Specificity - genetics; Phylogeny; Plant Cells - metabolism; Plant Pathology; Plant Proteins - chemistry; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Sciences; Plants, Genetically Modified; Promoter Regions, Genetic - genetics; Protein Binding; Saccharomyces cerevisiae - metabolism; Salicylic acid; Signal transduction; Subcellular Fractions - metabolism; Tobacco; Transcription factors; Transcriptome - genetics; Transcriptomes; Signal crosstalk; Nicotine biosynthesis; Auxin response factor; Transcription factor; Transcriptomic analysis; Nicotiana tabacum
• ISSN: 0167-4412; 1573-5028
• DOI: 10.1007/s11103-021-01175-3

Key message
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.
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.