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Cell type matters: competence for alkaloid metabolism differs in two seed-derived cell strains of Catharanthus roseus

Since the discovery of the anticancer drugs vinblastine and vincristine, Catharanthus roseus has been intensively studied for biosynthesis of several terpene indole alkaloids (TIAs). Due to their low abundance in plant tissues at a simultaneously high demand, modes of production alternative to conve...

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Autores principales: Raorane, Manish L., Manz, Christina, Hildebrandt, Sarah, Mielke, Marion, Thieme, Marc, Keller, Judith, Bunzel, Mirko, Nick, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Vienna 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9931846/
https://www.ncbi.nlm.nih.gov/pubmed/35697946
http://dx.doi.org/10.1007/s00709-022-01781-y
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author Raorane, Manish L.
Manz, Christina
Hildebrandt, Sarah
Mielke, Marion
Thieme, Marc
Keller, Judith
Bunzel, Mirko
Nick, Peter
author_facet Raorane, Manish L.
Manz, Christina
Hildebrandt, Sarah
Mielke, Marion
Thieme, Marc
Keller, Judith
Bunzel, Mirko
Nick, Peter
author_sort Raorane, Manish L.
collection PubMed
description Since the discovery of the anticancer drugs vinblastine and vincristine, Catharanthus roseus has been intensively studied for biosynthesis of several terpene indole alkaloids (TIAs). Due to their low abundance in plant tissues at a simultaneously high demand, modes of production alternative to conventional extraction are mandatory. Plant cell fermentation might become one of these alternatives, yet decades of research have shown limited success to certain product classes, leading to the question: how to preserve the intrinsic ability to produce TIAs (metabolic competence) in cell culture? We used the strategy to use the developmental potency of mature embryos to generate such strains. Two cell strains (C1and C4) from seed embryos of Catharanthus roseus were found to differ not only morphologically, but also in their metabolic competence. This differential competence became manifest not only under phytohormone elicitation, but also upon feeding with alkaloid pathway precursors. The more active strain C4 formed larger cell aggregates and was endowed with longer mitochondria. These cellular features were accompanied by higher alkaloid accumulation in response to methyl jasmonate (MeJA) elicitation. The levels of catharanthine could be increased significantly, while the concurrent vindoline branch of the pathway was blocked, such that no bisindole alkaloids were detectable. By feeding vindoline to MeJA-elicited C4 cells, vincristine became detectable; however, only to marginal amounts. In conclusion, these results show that cultured cells are not “de-differentiated”, but can differ in metabolic competence. In addition to elicitation and precursor feeding, the cellular properties of the “biomatter” are highly relevant for the success of plant cell fermentation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00709-022-01781-y.
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spelling pubmed-99318462023-02-17 Cell type matters: competence for alkaloid metabolism differs in two seed-derived cell strains of Catharanthus roseus Raorane, Manish L. Manz, Christina Hildebrandt, Sarah Mielke, Marion Thieme, Marc Keller, Judith Bunzel, Mirko Nick, Peter Protoplasma Original Article Since the discovery of the anticancer drugs vinblastine and vincristine, Catharanthus roseus has been intensively studied for biosynthesis of several terpene indole alkaloids (TIAs). Due to their low abundance in plant tissues at a simultaneously high demand, modes of production alternative to conventional extraction are mandatory. Plant cell fermentation might become one of these alternatives, yet decades of research have shown limited success to certain product classes, leading to the question: how to preserve the intrinsic ability to produce TIAs (metabolic competence) in cell culture? We used the strategy to use the developmental potency of mature embryos to generate such strains. Two cell strains (C1and C4) from seed embryos of Catharanthus roseus were found to differ not only morphologically, but also in their metabolic competence. This differential competence became manifest not only under phytohormone elicitation, but also upon feeding with alkaloid pathway precursors. The more active strain C4 formed larger cell aggregates and was endowed with longer mitochondria. These cellular features were accompanied by higher alkaloid accumulation in response to methyl jasmonate (MeJA) elicitation. The levels of catharanthine could be increased significantly, while the concurrent vindoline branch of the pathway was blocked, such that no bisindole alkaloids were detectable. By feeding vindoline to MeJA-elicited C4 cells, vincristine became detectable; however, only to marginal amounts. In conclusion, these results show that cultured cells are not “de-differentiated”, but can differ in metabolic competence. In addition to elicitation and precursor feeding, the cellular properties of the “biomatter” are highly relevant for the success of plant cell fermentation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00709-022-01781-y. Springer Vienna 2022-06-13 2023 /pmc/articles/PMC9931846/ /pubmed/35697946 http://dx.doi.org/10.1007/s00709-022-01781-y Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Article
Raorane, Manish L.
Manz, Christina
Hildebrandt, Sarah
Mielke, Marion
Thieme, Marc
Keller, Judith
Bunzel, Mirko
Nick, Peter
Cell type matters: competence for alkaloid metabolism differs in two seed-derived cell strains of Catharanthus roseus
title Cell type matters: competence for alkaloid metabolism differs in two seed-derived cell strains of Catharanthus roseus
title_full Cell type matters: competence for alkaloid metabolism differs in two seed-derived cell strains of Catharanthus roseus
title_fullStr Cell type matters: competence for alkaloid metabolism differs in two seed-derived cell strains of Catharanthus roseus
title_full_unstemmed Cell type matters: competence for alkaloid metabolism differs in two seed-derived cell strains of Catharanthus roseus
title_short Cell type matters: competence for alkaloid metabolism differs in two seed-derived cell strains of Catharanthus roseus
title_sort cell type matters: competence for alkaloid metabolism differs in two seed-derived cell strains of catharanthus roseus
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9931846/
https://www.ncbi.nlm.nih.gov/pubmed/35697946
http://dx.doi.org/10.1007/s00709-022-01781-y
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