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  Wild tobacco genomes reveal the evolution of nicotine biosynthesis

Xu, S., Brockmoeller, T., Navarro-Quezada, A., Kuhl, H., Gase, K., Ling, Z., et al. (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. doi:10.1101/107565.

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 Creators:
Xu, Shuqing1, Author              
Brockmoeller, Thomas1, 2, Author              
Navarro-Quezada, Aura, Author
Kuhl, Heiner, Author
Gase, Klaus1, Author              
Ling, Zhihao1, 2, Author              
Zhou, Wenwu1, Author              
Kreitzer, Christoph1, Author              
Stanke, Mario, Author
Tang, Haibao, Author
Lyons, Eric, Author
Pandey, Priyanka, Author
Pandey, Shree Prakash1, Author              
Timmermann, Bernd, Author
Gaquerel, Emmanuel, Author
Baldwin, Ian Thomas1, Author              
Affiliations:
1Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society, ou_24029              
2IMPRS on Ecological Interactions, MPI for Chemical Ecology, Max Planck Society, Jena, DE, ou_421900              

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 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 N. 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 herbivory-induced 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 nicotinic acid dinucleotide (NAD) pathways. While the duplication of the former is shared among several Solanaceous genera which produce polyamine-derived tropane alkaloids, the innovation and efficient production of nicotine in the genus Nicotiana required lineage-specific duplications within the NAD pathway and the evolution of root-specific expression of the duplicated Solanaceae-specific ethylene response factor (ERF) that activates the expression of all nicotine biosynthetic genes. Furthermore, TE insertions that incorporated transcription factor binding motifs also likely contributed to the coordinated metabolic flux of the nicotine biosynthetic pathway. Together, these results provide evidence that TEs and gene duplications facilitated the emergence of a key metabolic innovation relevant to plant fitness.

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 Dates: 2017-04-272017-05-232017-06-06
 Publication Status: Published in print
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 Identifiers: Other: ITB540
DOI: 10.1101/107565
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Title: Proceedings of the National Academy of Sciences of the United States of America
  Other : Proc. Acad. Sci. USA
  Other : Proc. Acad. Sci. U.S.A.
  Abbreviation : PNAS
Source Genre: Journal
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Publ. Info: Washington, D.C. : National Academy of Sciences
Pages: - Volume / Issue: 114 (23) Sequence Number: - Start / End Page: 6133 - 6138 Identifier: ISSN: 0027-8424
CoNE: https://pure.mpg.de/cone/journals/resource/954925427230