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Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata.

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 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.

SUBMITTER: Schindler F

PROVIDER: S-EPMC8362603 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project 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.

Project description:The genus Ardisia (Myrsinoideae, Primulaceae) has 16 subgenera and over 700 accepted names, mainly distributed in tropical Asia and America. The circumscription of Ardisia is not well-defined and sometimes confounded with the separation of some small genera. A taxonomic revision focusing on Ardisia and allies is necessary. In the Ardisia subgenus Crispardisia, symbiotic association with leaf-nodule bacteria is a unique character within the genus. The endosymbionts are vertically transmitted, highly specific and highly dependent on the hosts, suggesting strict cospeciation may have occurred in the evolutionary history. In the present study, we aimed to establish a phylogenetic framework for further taxonomic revision. We also aimed to test the cospeciation hypothesis of the leaf-nodulate Ardisia and their endosymbiotic bacteria. Nuclear ITS and two chloroplast intergenic spaces were used to reconstruct the phylogeny of Asian Ardisia and relatives in Myrsinoideae, Primulaceae. The 16S-23S rRNA were used to reconstruct the bacterial symbionts' phylogeny. To understand the evolutionary association of the Ardisia and symbionts, topology tests and cophylogenetic analyses were conducted. The molecular phylogeny suggested Ardisia is not monophyletic, unless Sardiria, Hymenandra, Badula and Oncostemum are included. The results suggest the generic limit within Myrsinoideae (Primulaceae) needs to be further revised. The subgenera Crispardisia, Pimelandra, and Stylardisia were supported as monophyly, while the subgenus Bladhia was separated into two distant clades. We proposed to divide the subgenus Bladhia into subgenus Bladhia s.str. and subgenus Odontophylla. Both of the cophylogenetic analyses and topology tests rejected strict cospeciation hypothesis between Ardisia hosts and symbiotic Burkholderia. Cophylogenetic analyses showed general phylogenetic concordance of Ardisia and Burkholderia, and cospeciation events, host-switching events and loss events were all inferred.

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Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata.

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