Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems

IntroductionAlkanna tinctoria Tausch. is a medicinal plant well-known to produce important therapeutic compounds, such as alkannin/shikonin and their derivatives (A/Sd). It associates with arbuscular mycorrhizal fungi (AMF), which are known, amongst others beneficial effects, to modulate the plant s...

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Main Authors: Yanyan Zhao, Annalisa Cartabia, Mónica Garcés-Ruiz, Marie-France Herent, Joëlle Quetin-Leclercq, Sergio Ortiz, Stéphane Declerck, Ismahen Lalaymia
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1216029/full
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author Yanyan Zhao
Annalisa Cartabia
Mónica Garcés-Ruiz
Marie-France Herent
Joëlle Quetin-Leclercq
Sergio Ortiz
Sergio Ortiz
Stéphane Declerck
Ismahen Lalaymia
author_facet Yanyan Zhao
Annalisa Cartabia
Mónica Garcés-Ruiz
Marie-France Herent
Joëlle Quetin-Leclercq
Sergio Ortiz
Sergio Ortiz
Stéphane Declerck
Ismahen Lalaymia
author_sort Yanyan Zhao
collection DOAJ
description IntroductionAlkanna tinctoria Tausch. is a medicinal plant well-known to produce important therapeutic compounds, such as alkannin/shikonin and their derivatives (A/Sd). It associates with arbuscular mycorrhizal fungi (AMF), which are known, amongst others beneficial effects, to modulate the plant secondary metabolites (SMs) biosynthesis. However, to the best of our knowledge, no study on the effects of AMF strains on the growth and production of A/Sd in A. tinctoria has been reported in the literature.MethodsHere, three experiments were conducted. In Experiment 1, plants were associated with the GINCO strain Rhizophagus irregularis MUCL 41833 and, in Experiment 2, with two strains of GINCO (R. irregularis MUCL 41833 and Rhizophagus aggregatus MUCL 49408) and two native strains isolated from wild growing A. tinctoria (R. irregularis and Septoglomus viscosum) and were grown in a semi-hydroponic (S-H) cultivation system. Plants were harvested after 9 and 37 days in Experiment 1 and 9 days in Experiment 2. In Experiment 3, plants were associated with the two native AMF strains and with R. irregularis MUCL 41833 and were grown for 85 days in pots under greenhouse conditions. Quantification and identification of A/Sd were performed by HPLC-PDA and by HPLC-HRMS/MS, respectively. LePGT1, LePGT2, and GHQH genes involved in the A/Sd biosynthesis were analyzed through RT-qPCR.ResultsIn Experiment 1, no significant differences were noticed in the production of A/Sd. Conversely, in Experiments 2 and 3, plants associated with the native AMF R. irregularis had the highest content of total A/Sd expressed as shikonin equivalent. In Experiment 1, a significantly higher relative expression of both LePGT1 and LePGT2 was observed in plants inoculated with R. irregularis MUCL 41833 compared with control plants after 37 days in the S-H cultivation system. Similarly, a significantly higher relative expression of LePGT2 in plants inoculated with R. irregularis MUCL 41833 was noticed after 9 versus 37 days in the S-H cultivation system. In Experiment 2, a significant lower relative expression of LePGT2 was observed in native AMF R. irregularis inoculated plants compared to the control.DiscussionOverall, our study showed that the native R. irregularis strain increased A/Sd production in A. tinctoria regardless of the growing system used, further suggesting that the inoculation of native/best performing AMF is a promising method to improve the production of important SMs.
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spelling doaj.art-7efe588787ff4c41ae72b08555b5efa22023-08-10T08:58:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-08-011410.3389/fmicb.2023.12160291216029Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systemsYanyan Zhao0Annalisa Cartabia1Mónica Garcés-Ruiz2Marie-France Herent3Joëlle Quetin-Leclercq4Sergio Ortiz5Sergio Ortiz6Stéphane Declerck7Ismahen Lalaymia8Mycology, Earth and Life Institute, Université catholique de Louvain – UCLouvain, Louvain-la-Neuve, BelgiumMycology, Earth and Life Institute, Université catholique de Louvain – UCLouvain, Louvain-la-Neuve, BelgiumMycology, Earth and Life Institute, Université catholique de Louvain – UCLouvain, Louvain-la-Neuve, BelgiumPharmacognosy Research Group, Louvain Drug Research Institute (LDRI), Université catholique de Louvain – UCLouvain, Brussels, BelgiumPharmacognosy Research Group, Louvain Drug Research Institute (LDRI), Université catholique de Louvain – UCLouvain, Brussels, BelgiumPharmacognosy Research Group, Louvain Drug Research Institute (LDRI), Université catholique de Louvain – UCLouvain, Brussels, BelgiumUMR 7200, Laboratoire d’Innovation Thérapeutique, Université de Strasbourg, CNRS, Strasbourg Drug Discovery and Development Institute (IMS), Illkirch-Graffenstaden, FranceMycology, Earth and Life Institute, Université catholique de Louvain – UCLouvain, Louvain-la-Neuve, BelgiumMycology, Earth and Life Institute, Université catholique de Louvain – UCLouvain, Louvain-la-Neuve, BelgiumIntroductionAlkanna tinctoria Tausch. is a medicinal plant well-known to produce important therapeutic compounds, such as alkannin/shikonin and their derivatives (A/Sd). It associates with arbuscular mycorrhizal fungi (AMF), which are known, amongst others beneficial effects, to modulate the plant secondary metabolites (SMs) biosynthesis. However, to the best of our knowledge, no study on the effects of AMF strains on the growth and production of A/Sd in A. tinctoria has been reported in the literature.MethodsHere, three experiments were conducted. In Experiment 1, plants were associated with the GINCO strain Rhizophagus irregularis MUCL 41833 and, in Experiment 2, with two strains of GINCO (R. irregularis MUCL 41833 and Rhizophagus aggregatus MUCL 49408) and two native strains isolated from wild growing A. tinctoria (R. irregularis and Septoglomus viscosum) and were grown in a semi-hydroponic (S-H) cultivation system. Plants were harvested after 9 and 37 days in Experiment 1 and 9 days in Experiment 2. In Experiment 3, plants were associated with the two native AMF strains and with R. irregularis MUCL 41833 and were grown for 85 days in pots under greenhouse conditions. Quantification and identification of A/Sd were performed by HPLC-PDA and by HPLC-HRMS/MS, respectively. LePGT1, LePGT2, and GHQH genes involved in the A/Sd biosynthesis were analyzed through RT-qPCR.ResultsIn Experiment 1, no significant differences were noticed in the production of A/Sd. Conversely, in Experiments 2 and 3, plants associated with the native AMF R. irregularis had the highest content of total A/Sd expressed as shikonin equivalent. In Experiment 1, a significantly higher relative expression of both LePGT1 and LePGT2 was observed in plants inoculated with R. irregularis MUCL 41833 compared with control plants after 37 days in the S-H cultivation system. Similarly, a significantly higher relative expression of LePGT2 in plants inoculated with R. irregularis MUCL 41833 was noticed after 9 versus 37 days in the S-H cultivation system. In Experiment 2, a significant lower relative expression of LePGT2 was observed in native AMF R. irregularis inoculated plants compared to the control.DiscussionOverall, our study showed that the native R. irregularis strain increased A/Sd production in A. tinctoria regardless of the growing system used, further suggesting that the inoculation of native/best performing AMF is a promising method to improve the production of important SMs.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1216029/fullarbuscular mycorrhizal fungiAlkanna tinctoriasemi-hydroponic cultivation systemalkannin/shikonin derivativesnative strains
spellingShingle Yanyan Zhao
Annalisa Cartabia
Mónica Garcés-Ruiz
Marie-France Herent
Joëlle Quetin-Leclercq
Sergio Ortiz
Sergio Ortiz
Stéphane Declerck
Ismahen Lalaymia
Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems
Frontiers in Microbiology
arbuscular mycorrhizal fungi
Alkanna tinctoria
semi-hydroponic cultivation system
alkannin/shikonin derivatives
native strains
title Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems
title_full Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems
title_fullStr Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems
title_full_unstemmed Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems
title_short Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems
title_sort arbuscular mycorrhizal fungi impact the production of alkannin shikonin and their derivatives in alkanna tinctoria tausch grown in semi hydroponic and pot cultivation systems
topic arbuscular mycorrhizal fungi
Alkanna tinctoria
semi-hydroponic cultivation system
alkannin/shikonin derivatives
native strains
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1216029/full
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