Cargando…

MALDI-HRMS Imaging Maps the Localization of Skyrin, the Precursor of Hypericin, and Pathway Intermediates in Leaves of Hypericum Species

Hypericum perforatum and related species (Hypericaceae) are a reservoir of pharmacologically important secondary metabolites, including the well-known naphthodianthrone hypericin. However, the exact biosynthetic steps in the hypericin biosynthetic pathway, vis-à-vis the essential precursors and thei...

Descripción completa

Detalles Bibliográficos
Autores principales: Revuru, Bharadwaj, Bálintová, Miroslava, Henzelyová, Jana, Čellárová, Eva, Kusari, Souvik
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7504759/
https://www.ncbi.nlm.nih.gov/pubmed/32878122
http://dx.doi.org/10.3390/molecules25173964
_version_ 1783584697788399616
author Revuru, Bharadwaj
Bálintová, Miroslava
Henzelyová, Jana
Čellárová, Eva
Kusari, Souvik
author_facet Revuru, Bharadwaj
Bálintová, Miroslava
Henzelyová, Jana
Čellárová, Eva
Kusari, Souvik
author_sort Revuru, Bharadwaj
collection PubMed
description Hypericum perforatum and related species (Hypericaceae) are a reservoir of pharmacologically important secondary metabolites, including the well-known naphthodianthrone hypericin. However, the exact biosynthetic steps in the hypericin biosynthetic pathway, vis-à-vis the essential precursors and their localization in plants, remain unestablished. Recently, we proposed a novel biosynthetic pathway of hypericin, not through emodin and emodin anthrone, but skyrin. However, the localization of skyrin and its precursors in Hypericum plants, as well as the correlation between their spatial distribution with the hypericin pathway intermediates and the produced naphthodianthrones, are not known. Herein, we report the spatial distribution of skyrin and its precursors in leaves of five in vitro cultivated Hypericum plant species concomitant to hypericin, its analogs, as well as its previously proposed precursors emodin and emodin anthrone, using MALDI-HRMS imaging. Firstly, we employed HPLC-HRMS to confirm the presence of skyrin in all analyzed species, namely H. humifusum, H. bupleuroides, H. annulatum, H. tetrapterum, and H. rumeliacum. Thereafter, MALDI-HRMS imaging of the skyrin-containing leaves revealed a species-specific distribution and localization pattern of skyrin. Skyrin is localized in the dark glands in H. humifusum and H. tetrapterum leaves together with hypericin but remains scattered throughout the leaves in H. annulatum, H. bupleuroides, and H. rumeliacum. The distribution and localization of related compounds were also mapped and are discussed concomitant to the incidence of skyrin. Taken together, our study establishes and correlates for the first time, the high spatial distribution of skyrin and its precursors, as well as of hypericin, its analogs, and previously proposed precursors emodin and emodin anthrone in the leaves of Hypericum plants.
format Online
Article
Text
id pubmed-7504759
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-75047592020-09-26 MALDI-HRMS Imaging Maps the Localization of Skyrin, the Precursor of Hypericin, and Pathway Intermediates in Leaves of Hypericum Species Revuru, Bharadwaj Bálintová, Miroslava Henzelyová, Jana Čellárová, Eva Kusari, Souvik Molecules Article Hypericum perforatum and related species (Hypericaceae) are a reservoir of pharmacologically important secondary metabolites, including the well-known naphthodianthrone hypericin. However, the exact biosynthetic steps in the hypericin biosynthetic pathway, vis-à-vis the essential precursors and their localization in plants, remain unestablished. Recently, we proposed a novel biosynthetic pathway of hypericin, not through emodin and emodin anthrone, but skyrin. However, the localization of skyrin and its precursors in Hypericum plants, as well as the correlation between their spatial distribution with the hypericin pathway intermediates and the produced naphthodianthrones, are not known. Herein, we report the spatial distribution of skyrin and its precursors in leaves of five in vitro cultivated Hypericum plant species concomitant to hypericin, its analogs, as well as its previously proposed precursors emodin and emodin anthrone, using MALDI-HRMS imaging. Firstly, we employed HPLC-HRMS to confirm the presence of skyrin in all analyzed species, namely H. humifusum, H. bupleuroides, H. annulatum, H. tetrapterum, and H. rumeliacum. Thereafter, MALDI-HRMS imaging of the skyrin-containing leaves revealed a species-specific distribution and localization pattern of skyrin. Skyrin is localized in the dark glands in H. humifusum and H. tetrapterum leaves together with hypericin but remains scattered throughout the leaves in H. annulatum, H. bupleuroides, and H. rumeliacum. The distribution and localization of related compounds were also mapped and are discussed concomitant to the incidence of skyrin. Taken together, our study establishes and correlates for the first time, the high spatial distribution of skyrin and its precursors, as well as of hypericin, its analogs, and previously proposed precursors emodin and emodin anthrone in the leaves of Hypericum plants. MDPI 2020-08-31 /pmc/articles/PMC7504759/ /pubmed/32878122 http://dx.doi.org/10.3390/molecules25173964 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Revuru, Bharadwaj
Bálintová, Miroslava
Henzelyová, Jana
Čellárová, Eva
Kusari, Souvik
MALDI-HRMS Imaging Maps the Localization of Skyrin, the Precursor of Hypericin, and Pathway Intermediates in Leaves of Hypericum Species
title MALDI-HRMS Imaging Maps the Localization of Skyrin, the Precursor of Hypericin, and Pathway Intermediates in Leaves of Hypericum Species
title_full MALDI-HRMS Imaging Maps the Localization of Skyrin, the Precursor of Hypericin, and Pathway Intermediates in Leaves of Hypericum Species
title_fullStr MALDI-HRMS Imaging Maps the Localization of Skyrin, the Precursor of Hypericin, and Pathway Intermediates in Leaves of Hypericum Species
title_full_unstemmed MALDI-HRMS Imaging Maps the Localization of Skyrin, the Precursor of Hypericin, and Pathway Intermediates in Leaves of Hypericum Species
title_short MALDI-HRMS Imaging Maps the Localization of Skyrin, the Precursor of Hypericin, and Pathway Intermediates in Leaves of Hypericum Species
title_sort maldi-hrms imaging maps the localization of skyrin, the precursor of hypericin, and pathway intermediates in leaves of hypericum species
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7504759/
https://www.ncbi.nlm.nih.gov/pubmed/32878122
http://dx.doi.org/10.3390/molecules25173964
work_keys_str_mv AT revurubharadwaj maldihrmsimagingmapsthelocalizationofskyrintheprecursorofhypericinandpathwayintermediatesinleavesofhypericumspecies
AT balintovamiroslava maldihrmsimagingmapsthelocalizationofskyrintheprecursorofhypericinandpathwayintermediatesinleavesofhypericumspecies
AT henzelyovajana maldihrmsimagingmapsthelocalizationofskyrintheprecursorofhypericinandpathwayintermediatesinleavesofhypericumspecies
AT cellarovaeva maldihrmsimagingmapsthelocalizationofskyrintheprecursorofhypericinandpathwayintermediatesinleavesofhypericumspecies
AT kusarisouvik maldihrmsimagingmapsthelocalizationofskyrintheprecursorofhypericinandpathwayintermediatesinleavesofhypericumspecies