Natural and induced variations in transcriptional regulator genes result in low‐nicotine phenotypes in tobacco

• Published in: The Plant journal : for cell and molecular biology 2022-09, Vol.111 (6), p.1768-1779
• Main Authors: Shoji, Tsubasa, Moriyama, Koki, Sierro, Nicolas, Ouadi, Sonia, Ivanov, Nikolai V., Hashimoto, Takashi, Saito, Kazuki
• Format: Article
• Language: English
• Subjects: Alkaloids; Alleles; Biosynthesis; Cyclopentanes - metabolism; ethylene response factor; Ethylenes - metabolism; Gene expression; Gene Expression Regulation, Plant - genetics; Genes; Genes, Regulator; Genetic resources; Germplasm; Homology; low‐nicotine phenotype; Nicotiana - genetics; Nicotiana - metabolism; Nicotine; Nicotine - genetics; Nicotine - metabolism; Oxylipins - metabolism; Phenotype; Phenotypes; Plant Breeding; Plant Proteins - genetics; Plant Proteins - metabolism; Tobacco; transcription factor; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.15923

SUMMARY In tobacco, the homologous ETHYLENE RESPONSE FACTOR (ERF) transcription factors ERF199 and ERF189 coordinate the transcription of multiple metabolic genes involved in nicotine biosynthesis. Natural alleles at the NIC1 and NIC2 loci greatly affect alkaloid accumulation and overlap with ERF199 and ERF189 in the tobacco genome, respectively. In this study, we identified several low‐nicotine tobacco varieties lacking ERF199 or ERF189 from a tobacco germplasm collection. We characterized the sequence of these new nic1 and nic2 alleles, as well as the previously defined alleles nic1‐1 and nic2‐1. Moreover, we examined the influence of different nic alleles on alkaloid contents and expression levels of genes related to nicotine biosynthesis. We also demonstrated that the deletion of a distal genomic region attenuates ERF199 expression, resulting in a moderately negative effect on the alkaloid phenotype. Our study provides new insights into the regulation of nicotine biosynthesis and novel genetic resources to breed low‐nicotine tobacco. Significance Statement Reducing the accumulation of addictive substance nicotine is a major focus of tobacco breeding to mitigate health concerns. We studied the genomic structures and phenotypic effects of an allelic series for the NIC1 and NIC2 genes, which encode ETHYLENE RESPONSE FACTOR transcription factors that regulate nicotine biosynthesis, revealing the genomic basis of low‐nicotine phenotypes in tobacco.