An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L.
Flower colour is an important trait for plants to attract pollinators and ensure their reproductive success. Among yellow flower pigments, the nudicaulins in Papaver nudicaule L. (Iceland poppy) are unique due to their rarity and unparalleled flavoalkaloid structure. Nudicaulins are derived from pel...
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ftdoajarticles:oai:doaj.org/article:9433c37727e843e5973630a9b73eeffa 2023-05-15T16:51:25+02:00 An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L. Bettina Dudek Anne-Christin Warskulat Heiko Vogel Natalie Wielsch Riya Christina Menezes Yvonne Hupfer Christian Paetz Steffi Gebauer-Jung Aleš Svatoš Bernd Schneider 2021-04-01T00:00:00Z https://doi.org/10.3390/ijms22084129 https://doaj.org/article/9433c37727e843e5973630a9b73eeffa EN eng MDPI AG https://www.mdpi.com/1422-0067/22/8/4129 https://doaj.org/toc/1661-6596 https://doaj.org/toc/1422-0067 doi:10.3390/ijms22084129 1422-0067 1661-6596 https://doaj.org/article/9433c37727e843e5973630a9b73eeffa International Journal of Molecular Sciences, Vol 22, Iss 4129, p 4129 (2021) Papaver nudicaule nudicaulin biosynthesis flower pigments indole alkaloids indole-3-glycerol-phosphate lyase transcriptomics Biology (General) QH301-705.5 Chemistry QD1-999 article 2021 ftdoajarticles https://doi.org/10.3390/ijms22084129 2022-12-31T05:50:56Z Flower colour is an important trait for plants to attract pollinators and ensure their reproductive success. Among yellow flower pigments, the nudicaulins in Papaver nudicaule L. (Iceland poppy) are unique due to their rarity and unparalleled flavoalkaloid structure. Nudicaulins are derived from pelargonidin glycoside and indole, products of the flavonoid and indole/tryptophan biosynthetic pathway, respectively. To gain insight into the molecular and chemical basis of nudicaulin biosynthesis, we combined transcriptome, differential gel electrophoresis (DIGE)-based proteome, and ultra-performance liquid chromatography–high resolution mass spectrometry (UPLC-HRMS)-based metabolome data of P. nudicaule petals with chemical investigations. We identified candidate genes and proteins for all biosynthetic steps as well as some key metabolites across five stages of petal development. Candidate genes of amino acid biosynthesis showed a relatively stable expression throughout petal development, whereas most candidate genes of flavonoid biosynthesis showed increasing expression during development followed by downregulation in the final stage. Notably, gene candidates of indole-3-glycerol-phosphate lyase (IGL), sharing characteristic sequence motifs with known plant IGL genes, were co-expressed with flavonoid biosynthesis genes, and are probably providing free indole. The fusion of indole with pelargonidin glycosides was retraced synthetically and promoted by high precursor concentrations, an excess of indole, and a specific glycosylation pattern of pelargonidin. Thus, nudicaulin biosynthesis combines the enzymatic steps of two different pathways with a spontaneous fusion of indole and pelargonidin glycoside under precisely tuned reaction conditions. Article in Journal/Newspaper Iceland Directory of Open Access Journals: DOAJ Articles International Journal of Molecular Sciences 22 8 4129 |
institution |
Open Polar |
collection |
Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
Papaver nudicaule nudicaulin biosynthesis flower pigments indole alkaloids indole-3-glycerol-phosphate lyase transcriptomics Biology (General) QH301-705.5 Chemistry QD1-999 |
spellingShingle |
Papaver nudicaule nudicaulin biosynthesis flower pigments indole alkaloids indole-3-glycerol-phosphate lyase transcriptomics Biology (General) QH301-705.5 Chemistry QD1-999 Bettina Dudek Anne-Christin Warskulat Heiko Vogel Natalie Wielsch Riya Christina Menezes Yvonne Hupfer Christian Paetz Steffi Gebauer-Jung Aleš Svatoš Bernd Schneider An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L. |
topic_facet |
Papaver nudicaule nudicaulin biosynthesis flower pigments indole alkaloids indole-3-glycerol-phosphate lyase transcriptomics Biology (General) QH301-705.5 Chemistry QD1-999 |
description |
Flower colour is an important trait for plants to attract pollinators and ensure their reproductive success. Among yellow flower pigments, the nudicaulins in Papaver nudicaule L. (Iceland poppy) are unique due to their rarity and unparalleled flavoalkaloid structure. Nudicaulins are derived from pelargonidin glycoside and indole, products of the flavonoid and indole/tryptophan biosynthetic pathway, respectively. To gain insight into the molecular and chemical basis of nudicaulin biosynthesis, we combined transcriptome, differential gel electrophoresis (DIGE)-based proteome, and ultra-performance liquid chromatography–high resolution mass spectrometry (UPLC-HRMS)-based metabolome data of P. nudicaule petals with chemical investigations. We identified candidate genes and proteins for all biosynthetic steps as well as some key metabolites across five stages of petal development. Candidate genes of amino acid biosynthesis showed a relatively stable expression throughout petal development, whereas most candidate genes of flavonoid biosynthesis showed increasing expression during development followed by downregulation in the final stage. Notably, gene candidates of indole-3-glycerol-phosphate lyase (IGL), sharing characteristic sequence motifs with known plant IGL genes, were co-expressed with flavonoid biosynthesis genes, and are probably providing free indole. The fusion of indole with pelargonidin glycosides was retraced synthetically and promoted by high precursor concentrations, an excess of indole, and a specific glycosylation pattern of pelargonidin. Thus, nudicaulin biosynthesis combines the enzymatic steps of two different pathways with a spontaneous fusion of indole and pelargonidin glycoside under precisely tuned reaction conditions. |
format |
Article in Journal/Newspaper |
author |
Bettina Dudek Anne-Christin Warskulat Heiko Vogel Natalie Wielsch Riya Christina Menezes Yvonne Hupfer Christian Paetz Steffi Gebauer-Jung Aleš Svatoš Bernd Schneider |
author_facet |
Bettina Dudek Anne-Christin Warskulat Heiko Vogel Natalie Wielsch Riya Christina Menezes Yvonne Hupfer Christian Paetz Steffi Gebauer-Jung Aleš Svatoš Bernd Schneider |
author_sort |
Bettina Dudek |
title |
An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L. |
title_short |
An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L. |
title_full |
An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L. |
title_fullStr |
An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L. |
title_full_unstemmed |
An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L. |
title_sort |
integrated—omics/chemistry approach unravels enzymatic and spontaneous steps to form flavoalkaloidal nudicaulin pigments in flowers of papaver nudicaule l. |
publisher |
MDPI AG |
publishDate |
2021 |
url |
https://doi.org/10.3390/ijms22084129 https://doaj.org/article/9433c37727e843e5973630a9b73eeffa |
genre |
Iceland |
genre_facet |
Iceland |
op_source |
International Journal of Molecular Sciences, Vol 22, Iss 4129, p 4129 (2021) |
op_relation |
https://www.mdpi.com/1422-0067/22/8/4129 https://doaj.org/toc/1661-6596 https://doaj.org/toc/1422-0067 doi:10.3390/ijms22084129 1422-0067 1661-6596 https://doaj.org/article/9433c37727e843e5973630a9b73eeffa |
op_doi |
https://doi.org/10.3390/ijms22084129 |
container_title |
International Journal of Molecular Sciences |
container_volume |
22 |
container_issue |
8 |
container_start_page |
4129 |
_version_ |
1766041529216925696 |