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Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata

Root-microbe interaction and its specialized root nodule structures and functions are well studied. In contrast, leaf nodules harboring microbial endophytes in special glandular leaf structures have only recently gained increased interest as plant-microbe phyllosphere interactions. Here, we applied...

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Autores principales: Schindler, Florian, Fragner, Lena, Herpell, Johannes B., Berger, Andreas, Brenner, Martin, Tischler, Sonja, Bellaire, Anke, Schönenberger, Jürg, Li, Weimin, Sun, Xiaoliang, Schinnerl, Johann, Brecker, Lothar, Weckwerth, Wolfram
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8362603/
https://www.ncbi.nlm.nih.gov/pubmed/34395523
http://dx.doi.org/10.3389/fmolb.2021.683671
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author Schindler, Florian
Fragner, Lena
Herpell, Johannes B.
Berger, Andreas
Brenner, Martin
Tischler, Sonja
Bellaire, Anke
Schönenberger, Jürg
Li, Weimin
Sun, Xiaoliang
Schinnerl, Johann
Brecker, Lothar
Weckwerth, Wolfram
author_facet Schindler, Florian
Fragner, Lena
Herpell, Johannes B.
Berger, Andreas
Brenner, Martin
Tischler, Sonja
Bellaire, Anke
Schönenberger, Jürg
Li, Weimin
Sun, Xiaoliang
Schinnerl, Johann
Brecker, Lothar
Weckwerth, Wolfram
author_sort Schindler, Florian
collection PubMed
description Root-microbe interaction and its specialized root nodule structures and functions are well studied. In contrast, leaf nodules harboring microbial endophytes in special glandular leaf structures have only recently gained increased interest as plant-microbe phyllosphere interactions. Here, we applied a comprehensive metabolomics platform in combination with natural product isolation and characterization to dissect leaf and leaf nodule metabolism and functions in Ardisia crenata (Primulaceae) and Psychotria punctata (Rubiaceae). The results indicate that abiotic stress resilience plays an important part within the leaf nodule symbiosis of both species. Both species showed metabolic signatures of enhanced nitrogen assimilation/dissimilation pattern and increased polyamine levels in nodules compared to leaf lamina tissue potentially involved in senescence processes and photosynthesis. Multiple links to cytokinin and REDOX-active pathways were found. Our results further demonstrate that secondary metabolite production by endophytes is a key feature of this symbiotic system. Multiple anhydromuropeptides (AhMP) and their derivatives were identified as highly characteristic biomarkers for nodulation within both species. A novel epicatechin derivative was structurally elucidated with NMR and shown to be enriched within the leaf nodules of A. crenata. This enrichment within nodulated tissues was also observed for catechin and other flavonoids indicating that flavonoid metabolism may play an important role for leaf nodule symbiosis of A. crenata. In contrast, pavettamine was only detected in P. punctata and showed no nodule specific enrichment but a developmental effect. Further natural products were detected, including three putative unknown depsipeptide structures in A. crenata leaf nodules. The analysis presents a first metabolomics reference data set for the intimate interaction of microbes and plants in leaf nodules, reveals novel metabolic processes of plant-microbe interaction as well as the potential of natural product discovery in these systems.
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spelling pubmed-83626032021-08-14 Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata Schindler, Florian Fragner, Lena Herpell, Johannes B. Berger, Andreas Brenner, Martin Tischler, Sonja Bellaire, Anke Schönenberger, Jürg Li, Weimin Sun, Xiaoliang Schinnerl, Johann Brecker, Lothar Weckwerth, Wolfram Front Mol Biosci Molecular Biosciences Root-microbe interaction and its specialized root nodule structures and functions are well studied. In contrast, leaf nodules harboring microbial endophytes in special glandular leaf structures have only recently gained increased interest as plant-microbe phyllosphere interactions. Here, we applied a comprehensive metabolomics platform in combination with natural product isolation and characterization to dissect leaf and leaf nodule metabolism and functions in Ardisia crenata (Primulaceae) and Psychotria punctata (Rubiaceae). The results indicate that abiotic stress resilience plays an important part within the leaf nodule symbiosis of both species. Both species showed metabolic signatures of enhanced nitrogen assimilation/dissimilation pattern and increased polyamine levels in nodules compared to leaf lamina tissue potentially involved in senescence processes and photosynthesis. Multiple links to cytokinin and REDOX-active pathways were found. Our results further demonstrate that secondary metabolite production by endophytes is a key feature of this symbiotic system. Multiple anhydromuropeptides (AhMP) and their derivatives were identified as highly characteristic biomarkers for nodulation within both species. A novel epicatechin derivative was structurally elucidated with NMR and shown to be enriched within the leaf nodules of A. crenata. This enrichment within nodulated tissues was also observed for catechin and other flavonoids indicating that flavonoid metabolism may play an important role for leaf nodule symbiosis of A. crenata. In contrast, pavettamine was only detected in P. punctata and showed no nodule specific enrichment but a developmental effect. Further natural products were detected, including three putative unknown depsipeptide structures in A. crenata leaf nodules. The analysis presents a first metabolomics reference data set for the intimate interaction of microbes and plants in leaf nodules, reveals novel metabolic processes of plant-microbe interaction as well as the potential of natural product discovery in these systems. Frontiers Media S.A. 2021-07-30 /pmc/articles/PMC8362603/ /pubmed/34395523 http://dx.doi.org/10.3389/fmolb.2021.683671 Text en Copyright © 2021 Schindler, Fragner, Herpell, Berger, Brenner, Tischler, Bellaire, Schönenberger, Li, Sun, Schinnerl, Brecker and Weckwerth. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Molecular Biosciences
Schindler, Florian
Fragner, Lena
Herpell, Johannes B.
Berger, Andreas
Brenner, Martin
Tischler, Sonja
Bellaire, Anke
Schönenberger, Jürg
Li, Weimin
Sun, Xiaoliang
Schinnerl, Johann
Brecker, Lothar
Weckwerth, Wolfram
Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata
title Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata
title_full Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata
title_fullStr Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata
title_full_unstemmed Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata
title_short Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata
title_sort dissecting metabolism of leaf nodules in ardisia crenata and psychotria punctata
topic Molecular Biosciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8362603/
https://www.ncbi.nlm.nih.gov/pubmed/34395523
http://dx.doi.org/10.3389/fmolb.2021.683671
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