Accumulation of azafrin in the root apoplast of the medicinal plant Escobedia grandiflora might play a role in parasitism

Societal Impact Statement Escobedia grandiflora is a medicinal hemiparasite that occurs naturally in non‐forested communities in Central and South America. Parasitic plants accumulate high levels of a water‐soluble orange pigment in roots that was once among the most important food dyes in the Andea...

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Main Authors: Edison Cardona‐Medina, Marisa Santos, Rubens Nodari, Dámaso Hornero‐Méndez, Arnau Peris, Darren C. J. Wong, José Tomás Matus, Manuel Rodríguez‐Concepción
Format: Article
Language:English
Published: Wiley 2023-05-01
Series:Plants, People, Planet
Subjects:
Online Access:https://doi.org/10.1002/ppp3.10353
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author Edison Cardona‐Medina
Marisa Santos
Rubens Nodari
Dámaso Hornero‐Méndez
Arnau Peris
Darren C. J. Wong
José Tomás Matus
Manuel Rodríguez‐Concepción
author_facet Edison Cardona‐Medina
Marisa Santos
Rubens Nodari
Dámaso Hornero‐Méndez
Arnau Peris
Darren C. J. Wong
José Tomás Matus
Manuel Rodríguez‐Concepción
author_sort Edison Cardona‐Medina
collection DOAJ
description Societal Impact Statement Escobedia grandiflora is a medicinal hemiparasite that occurs naturally in non‐forested communities in Central and South America. Parasitic plants accumulate high levels of a water‐soluble orange pigment in roots that was once among the most important food dyes in the Andean region. We conclusively address the chemical identification of this pigment and provide molecular and cellular insights on its biosynthesis and possible function. Summary The herbaceous hemiparasite Escobedia grandiflora (Orobanchaceae) is used in traditional medicine in the Andean region. Escobedia roots accumulate high levels of an orange pigment with a significant relevance as a cooking dye that exhibits antioxidant and cardioprotective properties. Here, we aimed to confirm the chemical identity of the pigment and investigate its biosynthesis and function in Escobedia roots. We combined metabolic and cytological analyses with de novo transcriptome assembly, gene expression studies, and phylogenetic analyses. The pigment was conclusively shown to be azafrin, an apocarotenoid likely derived from the cleavage of β‐carotene. RNA‐seq supported by multispecies comparative transcriptome analysis and qRT‐PCR allowed to propose candidate genes for the production of azafrin in Escobedia roots. We also showed that azafrin is delivered to the root apoplast and that it accumulates in the area where the Escobedia haustorium contacts the host's root. Our data suggest that azafrin production might rely on a carotenoid cleavage dioxygenase (CCD) different from CCD7 and that this apocarotenoid might function in the parasitism process. Together, our work represents an unprecedented step forward in our understanding of the Escobedia parasitization system.
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spelling doaj.art-177948312f1d4c5cb9c57b8f808359082023-04-26T08:17:25ZengWileyPlants, People, Planet2572-26112023-05-015335436710.1002/ppp3.10353Accumulation of azafrin in the root apoplast of the medicinal plant Escobedia grandiflora might play a role in parasitismEdison Cardona‐Medina0Marisa Santos1Rubens Nodari2Dámaso Hornero‐Méndez3Arnau Peris4Darren C. J. Wong5José Tomás Matus6Manuel Rodríguez‐Concepción7Departamento de Fitotecnia Universidade Federal de Santa Catarina Florianópolis BrazilDepartment of Botany Universidade Federal de Santa Catarina Florianópolis BrazilDepartamento de Fitotecnia Universidade Federal de Santa Catarina Florianópolis BrazilDepartment of Food Phytochemistry Instituto de la Grasa (IG‐CSIC) Seville SpainInstitute for Integrative Systems Biology (I2SysBio) Universitat de València‐CSIC Paterna Valencia SpainEcology and Evolution, Research School of Biology The Australian National University Acton AustraliaInstitute for Integrative Systems Biology (I2SysBio) Universitat de València‐CSIC Paterna Valencia SpainInstitute for Plant Molecular and Cell Biology (IBMCP) CSIC‐Universitat Politècnica de València Valencia SpainSocietal Impact Statement Escobedia grandiflora is a medicinal hemiparasite that occurs naturally in non‐forested communities in Central and South America. Parasitic plants accumulate high levels of a water‐soluble orange pigment in roots that was once among the most important food dyes in the Andean region. We conclusively address the chemical identification of this pigment and provide molecular and cellular insights on its biosynthesis and possible function. Summary The herbaceous hemiparasite Escobedia grandiflora (Orobanchaceae) is used in traditional medicine in the Andean region. Escobedia roots accumulate high levels of an orange pigment with a significant relevance as a cooking dye that exhibits antioxidant and cardioprotective properties. Here, we aimed to confirm the chemical identity of the pigment and investigate its biosynthesis and function in Escobedia roots. We combined metabolic and cytological analyses with de novo transcriptome assembly, gene expression studies, and phylogenetic analyses. The pigment was conclusively shown to be azafrin, an apocarotenoid likely derived from the cleavage of β‐carotene. RNA‐seq supported by multispecies comparative transcriptome analysis and qRT‐PCR allowed to propose candidate genes for the production of azafrin in Escobedia roots. We also showed that azafrin is delivered to the root apoplast and that it accumulates in the area where the Escobedia haustorium contacts the host's root. Our data suggest that azafrin production might rely on a carotenoid cleavage dioxygenase (CCD) different from CCD7 and that this apocarotenoid might function in the parasitism process. Together, our work represents an unprecedented step forward in our understanding of the Escobedia parasitization system.https://doi.org/10.1002/ppp3.10353apocarotenoidazafrinde novo transcriptome assemblyEscobediahaustoriumhemiparasite
spellingShingle Edison Cardona‐Medina
Marisa Santos
Rubens Nodari
Dámaso Hornero‐Méndez
Arnau Peris
Darren C. J. Wong
José Tomás Matus
Manuel Rodríguez‐Concepción
Accumulation of azafrin in the root apoplast of the medicinal plant Escobedia grandiflora might play a role in parasitism
Plants, People, Planet
apocarotenoid
azafrin
de novo transcriptome assembly
Escobedia
haustorium
hemiparasite
title Accumulation of azafrin in the root apoplast of the medicinal plant Escobedia grandiflora might play a role in parasitism
title_full Accumulation of azafrin in the root apoplast of the medicinal plant Escobedia grandiflora might play a role in parasitism
title_fullStr Accumulation of azafrin in the root apoplast of the medicinal plant Escobedia grandiflora might play a role in parasitism
title_full_unstemmed Accumulation of azafrin in the root apoplast of the medicinal plant Escobedia grandiflora might play a role in parasitism
title_short Accumulation of azafrin in the root apoplast of the medicinal plant Escobedia grandiflora might play a role in parasitism
title_sort accumulation of azafrin in the root apoplast of the medicinal plant escobedia grandiflora might play a role in parasitism
topic apocarotenoid
azafrin
de novo transcriptome assembly
Escobedia
haustorium
hemiparasite
url https://doi.org/10.1002/ppp3.10353
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