Wild tobacco genomes reveal the evolution of nicotine biosynthesis

Shuqing Xu, Thomas Brockmöller, Aura Navarro-Quezada, Heiner Kuhl, Klaus Gase, Zhihao Ling, Wenwu Zhou, Christoph Kreitzer, Mario Stanke, Haibao Tang, Eric Lyons, Priyanka Pandey, Shree P. Pandey, Bernd Timmermann, Emmanuel Gaquerel, Ian T. Baldwin

Research output: Contribution to journalArticle

49 Scopus citations

Abstract

Nicotine, the signature alkaloid of Nicotiana species responsible for the addictive properties of human tobacco smoking, functions as a defensive neurotoxin against attacking herbivores. However, the evolution of the genetic features that contributed to the assembly of the nicotine biosynthetic pathway remains unknown. We sequenced and assembled genomes of two wild tobaccos, Nicotiana attenuata (2.5 Gb) and Nicotiana obtusifolia (1.5 Gb), two ecological models for investigating adaptive traits in nature. We show that after the Solanaceae whole-genome triplication event, a repertoire of rapidly expanding transposable elements (TEs) bloated these Nicotiana genomes, promoted expression divergences among duplicated genes, and contributed to the evolution of herbivoryinduced signaling and defenses, including nicotine biosynthesis. The biosynthetic machinery that allows for nicotine synthesis in the roots evolved from the stepwise duplications of two ancient primary metabolic pathways: the polyamine and nicotinamide adenine dinucleotide (NAD) pathways. In contrast to the duplication of the polyamine pathway that is shared among several solanaceous genera producing polyamine-derived tropane alkaloids, we found that lineage-specific duplications within the NAD pathway and the evolution of rootspecific expression of the duplicated Solanaceae-specific ethylene response factor that activates the expression of all nicotine biosynthetic genes resulted in the innovative and efficient production of nicotine in the genus Nicotiana. Transcription factor binding motifs derived from TEs may have contributed to the coexpression of nicotine biosynthetic pathway genes and coordinated the metabolic flux. Together, these results provide evidence that TEs and gene duplications facilitated the emergence of a key metabolic innovation relevant to plant fitness.

Original languageEnglish (US)
Pages (from-to)6133-6138
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number23
DOIs
StatePublished - Jun 6 2017

Keywords

  • Expression divergence
  • Genome-wide multiplications
  • Nicotiana genomes
  • Nicotine biosynthesis
  • Transposable elements

ASJC Scopus subject areas

  • General

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    Xu, S., Brockmöller, T., Navarro-Quezada, A., Kuhl, H., Gase, K., Ling, Z., Zhou, W., Kreitzer, C., Stanke, M., Tang, H., Lyons, E., Pandey, P., Pandey, S. P., Timmermann, B., Gaquerel, E., & Baldwin, I. T. (2017). Wild tobacco genomes reveal the evolution of nicotine biosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 114(23), 6133-6138. https://doi.org/10.1073/pnas.1700073114