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Proc Natl Acad Sci U S A. 2017 Jun 6;114(23):6133-6138. doi: 10.1073/pnas.1700073114. Epub 2017 May 23.

Wild tobacco genomes reveal the evolution of nicotine biosynthesis.

Author information

1
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; sxu@ice.mpg.de emmanuel.gaquerel@cos.uni-heidelberg.de baldwin@ice.mpg.de.
2
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
3
Centre for Organismal Studies, University of Heidelberg, 69120 Heidelberg, Germany.
4
Sequencing Core Facility, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany.
5
Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary Medicine, 1210 Vienna, Austria.
6
Institute for Mathematics and Computer Science, Universität Greifswald, 17489 Greifswald, Germany.
7
Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, 350002 Fuzhou, Fujian, China.
8
School of Plant Sciences, BIO5 Institute, CyVerse, University of Arizona, Tucson, AZ 85721.
9
National Institute of Biomedical Genomics, Kalyani, 741251 West Bengal, India.
10
Department of Biological Sciences, Indian Institute of Science Education and Research-Kolkata, Mohanpur, 700064 West Bengal, India.
11
Centre for Organismal Studies, University of Heidelberg, 69120 Heidelberg, Germany; sxu@ice.mpg.de emmanuel.gaquerel@cos.uni-heidelberg.de baldwin@ice.mpg.de.

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 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 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 root-specific 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.

KEYWORDS:

Nicotiana genomes; expression divergence; genome-wide multiplications; nicotine biosynthesis; transposable elements

PMID:
28536194
PMCID:
PMC5468653
DOI:
10.1073/pnas.1700073114
[Indexed for MEDLINE]
Free PMC Article

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