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Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture

BACKGROUND: Datura stramonium (Jimsonweed) is a medicinally and pharmaceutically important plant in the nightshade family (Solanaceae) known for its production of various toxic, hallucinogenic, and therapeutic tropane alkaloids. Recently, we published a tissue-culture based transformation protocol f...

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Autores principales: Rajewski, Alex, Carter-House, Derreck, Stajich, Jason, Litt, Amy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7986286/
https://www.ncbi.nlm.nih.gov/pubmed/33752605
http://dx.doi.org/10.1186/s12864-021-07489-2
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author Rajewski, Alex
Carter-House, Derreck
Stajich, Jason
Litt, Amy
author_facet Rajewski, Alex
Carter-House, Derreck
Stajich, Jason
Litt, Amy
author_sort Rajewski, Alex
collection PubMed
description BACKGROUND: Datura stramonium (Jimsonweed) is a medicinally and pharmaceutically important plant in the nightshade family (Solanaceae) known for its production of various toxic, hallucinogenic, and therapeutic tropane alkaloids. Recently, we published a tissue-culture based transformation protocol for D. stramonium that enables more thorough functional genomics studies of this plant. However, the tissue culture process can lead to undesirable phenotypic and genomic consequences independent of the transgene used. Here, we have assembled and annotated a draft genome of D. stramonium with a focus on tropane alkaloid biosynthetic genes. We then use mRNA sequencing and genome resequencing of transformants to characterize changes following tissue culture. RESULTS: Our draft assembly conforms to the expected 2 gigabasepair haploid genome size of this plant and achieved a BUSCO score of 94.7% complete, single-copy genes. The repetitive content of the genome is 61%, with Gypsy-type retrotransposons accounting for half of this. Our gene annotation estimates the number of protein-coding genes at 52,149 and shows evidence of duplications in two key alkaloid biosynthetic genes, tropinone reductase I and hyoscyamine 6 β-hydroxylase. Following tissue culture, we detected only 186 differentially expressed genes, but were unable to correlate these changes in expression with either polymorphisms from resequencing or positional effects of transposons. CONCLUSIONS: We have assembled, annotated, and characterized the first draft genome for this important model plant species. Using this resource, we show duplications of genes leading to the synthesis of the medicinally important alkaloid, scopolamine. Our results also demonstrate that following tissue culture, mutation rates of transformed plants are quite high (1.16 × 10(− 3) mutations per site), but do not have a drastic impact on gene expression. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07489-2.
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spelling pubmed-79862862021-03-24 Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture Rajewski, Alex Carter-House, Derreck Stajich, Jason Litt, Amy BMC Genomics Research Article BACKGROUND: Datura stramonium (Jimsonweed) is a medicinally and pharmaceutically important plant in the nightshade family (Solanaceae) known for its production of various toxic, hallucinogenic, and therapeutic tropane alkaloids. Recently, we published a tissue-culture based transformation protocol for D. stramonium that enables more thorough functional genomics studies of this plant. However, the tissue culture process can lead to undesirable phenotypic and genomic consequences independent of the transgene used. Here, we have assembled and annotated a draft genome of D. stramonium with a focus on tropane alkaloid biosynthetic genes. We then use mRNA sequencing and genome resequencing of transformants to characterize changes following tissue culture. RESULTS: Our draft assembly conforms to the expected 2 gigabasepair haploid genome size of this plant and achieved a BUSCO score of 94.7% complete, single-copy genes. The repetitive content of the genome is 61%, with Gypsy-type retrotransposons accounting for half of this. Our gene annotation estimates the number of protein-coding genes at 52,149 and shows evidence of duplications in two key alkaloid biosynthetic genes, tropinone reductase I and hyoscyamine 6 β-hydroxylase. Following tissue culture, we detected only 186 differentially expressed genes, but were unable to correlate these changes in expression with either polymorphisms from resequencing or positional effects of transposons. CONCLUSIONS: We have assembled, annotated, and characterized the first draft genome for this important model plant species. Using this resource, we show duplications of genes leading to the synthesis of the medicinally important alkaloid, scopolamine. Our results also demonstrate that following tissue culture, mutation rates of transformed plants are quite high (1.16 × 10(− 3) mutations per site), but do not have a drastic impact on gene expression. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07489-2. BioMed Central 2021-03-22 /pmc/articles/PMC7986286/ /pubmed/33752605 http://dx.doi.org/10.1186/s12864-021-07489-2 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Rajewski, Alex
Carter-House, Derreck
Stajich, Jason
Litt, Amy
Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
title Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
title_full Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
title_fullStr Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
title_full_unstemmed Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
title_short Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
title_sort datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7986286/
https://www.ncbi.nlm.nih.gov/pubmed/33752605
http://dx.doi.org/10.1186/s12864-021-07489-2
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