Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata

Author(s)
Florian Schindler, Lena Fragner, Johannes B. Herpell, Andreas Berger, Martin Brenner, Sonja Tischler, Anke Bellaire, Jurg Schoenenberger, Weimin Li, Xiaoliang Sun, Johann Schinnerl, Lothar Brecker, Wolfram Weckwerth
Abstract

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 REDOXactive 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.

Organisation(s)
Functional and Evolutionary Ecology, Department of Pharmaceutical Sciences, Department of Botany and Biodiversity Research, Department of Organic Chemistry, Large-Instrument Facility for Mass Spectrometry in Life Sciences
Journal
Frontiers in Molecular Biosciences
Volume
8
No. of pages
23
ISSN
2296-889X
DOI
https://doi.org/10.3389/fmolb.2021.683671
Publication date
07-2021
Peer reviewed
Yes
Austrian Fields of Science 2012
106034 Phytochemistry, 106002 Biochemistry, 104002 Analytical chemistry, 104026 Spectroscopy
Keywords
Portal url
https://ucris.univie.ac.at/portal/en/publications/dissecting-metabolism-of-leaf-nodules-in-ardisia-crenata-and-psychotria-punctata(d4a14757-da6e-48f3-8c14-dd9037c01294).html