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ODORANT1 targets multiple metabolic networks in petunia flowers

Scent bouquets produced by the flowers of Petunia spp. (petunia) are composed of a complex mixture of floral volatile benzenoid and phenylpropanoid compounds (FVBPs), which are specialized metabolites derived from phenylalanine (Phe) through an interconnected network of enzymes. The biosynthesis and...

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Autores principales: Boersma, Maaike R., Patrick, Ryan M., Jillings, Sonia L., Shaipulah, Nur Fariza M., Sun, Pulu, Haring, Michel A., Dudareva, Natalia, Li, Ying, Schuurink, Robert C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9306810/
https://www.ncbi.nlm.nih.gov/pubmed/34863006
http://dx.doi.org/10.1111/tpj.15618
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author Boersma, Maaike R.
Patrick, Ryan M.
Jillings, Sonia L.
Shaipulah, Nur Fariza M.
Sun, Pulu
Haring, Michel A.
Dudareva, Natalia
Li, Ying
Schuurink, Robert C.
author_facet Boersma, Maaike R.
Patrick, Ryan M.
Jillings, Sonia L.
Shaipulah, Nur Fariza M.
Sun, Pulu
Haring, Michel A.
Dudareva, Natalia
Li, Ying
Schuurink, Robert C.
author_sort Boersma, Maaike R.
collection PubMed
description Scent bouquets produced by the flowers of Petunia spp. (petunia) are composed of a complex mixture of floral volatile benzenoid and phenylpropanoid compounds (FVBPs), which are specialized metabolites derived from phenylalanine (Phe) through an interconnected network of enzymes. The biosynthesis and emission of high levels of these volatiles requires coordinated transcriptional activation of both primary and specialized metabolic networks. The petunia R2R3‐MYB transcription factor ODORANT 1 (ODO1) was identified as a master regulator of FVBP production and emission; however, our knowledge of the direct regulatory targets of ODO1 has remained limited. Using chromatin immunoprecipitation followed by sequencing (ChIP‐seq) in petunia flowers, we identify genome‐wide ODO1‐bound genes that are enriched not only in genes involved in the biosynthesis of the Phe precursor, as previously reported, but also genes associated with the specialized metabolic pathways involved in generating phenylpropanoid intermediates for FVBPs. ODO1‐bound genes are also involved in methionine and S‐adenosylmethionine metabolism, which could modulate methyl group supplies for certain FVBPs. Quantitative reverse transcription polymerase chain reaction (qRT‐PCR) and RNA‐seq analysis in an ODO1 RNAi knockdown line revealed that ODO1‐bound targets are expressed at lower levels when ODO1 is suppressed. A cis‐regulatory motif, CACCAACCCC, was identified as a potential binding site for ODO1 in the promoters of genes that are both bound and activated by ODO1, which was validated by in planta promoter reporter assays with wild‐type and mutated promoters. Overall, our work presents a mechanistic model for ODO1 controlling an extensive gene regulatory network that contributes to FVBP production to give rise to floral scent.
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spelling pubmed-93068102022-07-28 ODORANT1 targets multiple metabolic networks in petunia flowers Boersma, Maaike R. Patrick, Ryan M. Jillings, Sonia L. Shaipulah, Nur Fariza M. Sun, Pulu Haring, Michel A. Dudareva, Natalia Li, Ying Schuurink, Robert C. Plant J Original Articles Scent bouquets produced by the flowers of Petunia spp. (petunia) are composed of a complex mixture of floral volatile benzenoid and phenylpropanoid compounds (FVBPs), which are specialized metabolites derived from phenylalanine (Phe) through an interconnected network of enzymes. The biosynthesis and emission of high levels of these volatiles requires coordinated transcriptional activation of both primary and specialized metabolic networks. The petunia R2R3‐MYB transcription factor ODORANT 1 (ODO1) was identified as a master regulator of FVBP production and emission; however, our knowledge of the direct regulatory targets of ODO1 has remained limited. Using chromatin immunoprecipitation followed by sequencing (ChIP‐seq) in petunia flowers, we identify genome‐wide ODO1‐bound genes that are enriched not only in genes involved in the biosynthesis of the Phe precursor, as previously reported, but also genes associated with the specialized metabolic pathways involved in generating phenylpropanoid intermediates for FVBPs. ODO1‐bound genes are also involved in methionine and S‐adenosylmethionine metabolism, which could modulate methyl group supplies for certain FVBPs. Quantitative reverse transcription polymerase chain reaction (qRT‐PCR) and RNA‐seq analysis in an ODO1 RNAi knockdown line revealed that ODO1‐bound targets are expressed at lower levels when ODO1 is suppressed. A cis‐regulatory motif, CACCAACCCC, was identified as a potential binding site for ODO1 in the promoters of genes that are both bound and activated by ODO1, which was validated by in planta promoter reporter assays with wild‐type and mutated promoters. Overall, our work presents a mechanistic model for ODO1 controlling an extensive gene regulatory network that contributes to FVBP production to give rise to floral scent. John Wiley and Sons Inc. 2021-12-27 2022-03 /pmc/articles/PMC9306810/ /pubmed/34863006 http://dx.doi.org/10.1111/tpj.15618 Text en © 2021 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Original Articles
Boersma, Maaike R.
Patrick, Ryan M.
Jillings, Sonia L.
Shaipulah, Nur Fariza M.
Sun, Pulu
Haring, Michel A.
Dudareva, Natalia
Li, Ying
Schuurink, Robert C.
ODORANT1 targets multiple metabolic networks in petunia flowers
title ODORANT1 targets multiple metabolic networks in petunia flowers
title_full ODORANT1 targets multiple metabolic networks in petunia flowers
title_fullStr ODORANT1 targets multiple metabolic networks in petunia flowers
title_full_unstemmed ODORANT1 targets multiple metabolic networks in petunia flowers
title_short ODORANT1 targets multiple metabolic networks in petunia flowers
title_sort odorant1 targets multiple metabolic networks in petunia flowers
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9306810/
https://www.ncbi.nlm.nih.gov/pubmed/34863006
http://dx.doi.org/10.1111/tpj.15618
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