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Investigations on the obligate leave nodule symbiosis

English title Investigations on the obligate leave nodule symbiosis
Applicant Eberl Leo
Number 154430
Funding scheme Sinergia
Research institution Institut für Pflanzen- und Mikrobiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Molecular Biology
Start/End 01.01.2015 - 30.06.2018
Approved amount 1'037'274.00
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All Disciplines (3)

Discipline
Molecular Biology
Organic Chemistry
Botany

Keywords (10)

Symbiosis; Burkholderia; Plant-microbe interaction; Plant genomics; Organic synthesis; Chemical ecology; Comparative genomics; Chemical biology; Psychotria; Aminocyclitol

Lay Summary (German)

Lead
Symbiosen zwischen Bakterien und höheren Organismen kommen in der Natur häufig vor und wurden unter anderem für Insekten, Nematoden, Schwämme, Mollusken und Moostierchen beschrieben. Während einige dieser Symbiosen fakultativ sind, sind andere hochspezifisch und obligat. In diesem Projekt soll die ungewöhnliche Symbiose zwischen der Pflanze Psychotria kirkii und ihrem obligaten bakteriellen Symbiont untersucht werden.
Lay summary
Durch den Einsatz molekularer Techniken, besonders von Sequenzierungsverfahren der nächsten Generation, wurden in den letzten Jahren viele Symbiosen entdeckt, die zumindest für dem Wirt obligat sind. In diesen Fällen ist der Symbiont zumeist für die Entwicklung und Reproduktion des Wirtsorganismus unerlässlich. Im Gegensatz zu Tieren ist bei Pflanzen nur eine einzige obligate Symbiose mit Bakterien bekannt, nämlich die Blattknöllchen-Symbiose einiger tropischer Pflanzen, bei der weder die symbiotischen Bakterien ausserhalb der Pflanze kultiviert werden können,  noch kann die Pflanze ohne Symbiont überleben. Obschon diese Symbiose vor mehr als 100 Jahren erstmals beschrieben wurde, sind die Gründe für die strikten Abhängigkeiten von Pflanze und Bakterium nicht bekannt. In einem interdisziplinären Ansatz, bei der drei Gruppen mit Expertisen in  Mikrobiology (Eberl/Carlier, UZH), Chemie (Gademann, UniBas) und Pflanzenbiologie (Wicker, UZH) soll im Rahmen des Sinergia Projektes die molekulare Basis der Symbiose aufgeklärt werden. Diese Untersuchungen sollen nicht nur grundlegende Einsichten in die enzig bekannte obligate Pflanzen-Bakterien Symbiose gewähren, sondern könnte auch neue Möglichenkeiten für die Pflanzenbiotechnologie aufzeigen.
Direct link to Lay Summary Last update: 26.11.2014

Responsible applicant and co-applicants

Employees

Publications

Publication
Synthesis and Biological Evaluation of the Novel Growth Inhibitor Streptol Glucoside, Isolated from an Obligate Plant Symbiont
Hsiao Chien-Chi, Sieber Simon, Georgiou Antri, Bailly Aurélien, Emmanouilidou Despina, Carlier Aurélien, Eberl Leo, Gademann Karl (2019), Synthesis and Biological Evaluation of the Novel Growth Inhibitor Streptol Glucoside, Isolated from an Obligate Plant Symbiont, in Chemistry - A European Journal, 25(7), 1722-1726.
Leaf nodule symbiosis: function and transmission of obligate bacterial endophytes
Gademann Karl, Eberl Leo, Carlier Aurelien, Pinto-Carbó Marta (2018), Leaf nodule symbiosis: function and transmission of obligate bacterial endophytes, in Current Opinion in Plant Biology, 44, 23-31.
The endophyte Candidatus Burkholderia crenata of the TCM plant Ardisia crenata produces the selective Gq-inhibitor FR900359
Reher R, Schamari I, Kehraus S, Annala S, Kuschak M, Schäberle T, Crüsemann M, Carlier A, Eberl L, Müller CE, Kostenis E, König GM (2016), The endophyte Candidatus Burkholderia crenata of the TCM plant Ardisia crenata produces the selective Gq-inhibitor FR900359, in Planta Medica, 81(S 01), S1-S381.
The genome analysis of Candidatus Burkholderia crenata reveals that secondary metabolism may be a key function of the Ardisia crenata leaf nodule symbiosis Ca . B. crenata genome
Carlier Aurelien, Fehr Linda, Pinto-Carbó Marta, Schäberle Till, Reher Raphael, Dessein Steven, König Gabriele, Eberl Leo (2016), The genome analysis of Candidatus Burkholderia crenata reveals that secondary metabolism may be a key function of the Ardisia crenata leaf nodule symbiosis Ca . B. crenata genome, in Environmental Microbiology, 18(8), 2507-2522.
Evidence of horizontal gene transfer between obligate leaf nodule symbionts
Pinto-Carbó Marta, Sieber Simon, Dessein Steven, Wicker Thomas, Verstraete Brecht, Gademann Karl, Eberl Leo, Carlier Aurelien (2016), Evidence of horizontal gene transfer between obligate leaf nodule symbionts, in The ISME Journal, 10(9), 2092-2105.
The endophyte Candidatus Burkholderia crenata of the TCM plant Ardisia crenata produces the selective Gq-inhibitor FR900359.
Reher R, Schamari I, Kehraus S, Annala S, Kuschak M, Schäberle T, Crüsemann M, Carlier A, Eberl L, Müller C E, Kostenis E, König G M (2016), The endophyte Candidatus Burkholderia crenata of the TCM plant Ardisia crenata produces the selective Gq-inhibitor FR900359., in The endophyte Candidatus Burkholderia crenata of the TCM plant Ardisia crenata produces the selectiv, Planta Medica, Georg Thieme Verlag KG Stuttgart · New York.
Isolation and Total Synthesis of Kirkamide, an Aminocyclitol from an Obligate Leaf Nodule Symbiont
Carlier Aurelien, Gademann Karl, Sieber Simon, Neuburger Markus, Grabenweger Giselher, Eberl Leo (2015), Isolation and Total Synthesis of Kirkamide, an Aminocyclitol from an Obligate Leaf Nodule Symbiont, in ANGEWANDTE CHEMIE-INTERNATIONAL EDITION, (27), 7968-7970.
The genome analysis of Candidatus Burkholderia crenata reveals that secondary metabolism may be a key function of the Ardisia crenata leaf nodule symbiosis
Carlier Aurelien (2015), The genome analysis of Candidatus Burkholderia crenata reveals that secondary metabolism may be a key function of the Ardisia crenata leaf nodule symbiosis, in Environ Microbiol., 13184.

Collaboration

Group / person Country
Types of collaboration
Institute of Bioinformatics and Systems Biology, Munich Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Novartis Institutes for Biomedical Research (NIBR) Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
- Industry/business/other use-inspired collaboration
Syngenta, Stein Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Industry/business/other use-inspired collaboration
University of Leiden Netherlands (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Max Planck Institute for Plant Breeding Research Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Imperial College, London Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Chemical Proteomics, TU München Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel

Scientific events



Self-organised

Title Date Place
The Biology and Chemistry of Bacteria-Plant Interactions 11.05.2017 Zürich, Switzerland

Associated projects

Number Title Start Funding scheme
169307 Communication in bacterial biofilms 01.01.2017 Project funding
183310 Ion Mobility Mass Spectrometry to Unscramble Complex Biological Samples 01.09.2019 R'EQUIP

Abstract

Symbioses between prokaryotes and eukaryotes are very common and are known from many animal phyla, including insects, nematodes, sponges, annelids, mollusks and bryozoans. While some associations are facultative others are highly specific and perpetual. The application of molecular and more recently of next generation sequencing technologies led to the identification of many symbioses that are obligate, at least from the host perspective. In these cases the bacterial symbionts are essential for host development and reproduction; they are usually transmitted maternally, are often unable to proliferate outside of the host, frequently provide the host with nutrients, and are sometimes restricted to a specialized organ within the host. In stark contrast to animals, only two symbioses have been described for plants in which the bacteria are vertically transmitted. One is the association of cyanobacteria and the water fern Azolla sp., where the colonizing cyanobionts fix atmospheric nitrogen and release nitrogen-rich metabolites into the leaf cavity. Although the bacteria are transmitted between the plant generations, Azolla can survive without its symbiont. The other plant-bacterium association is the bacterial plant leaf symbiosis, which is obligate for both partners and was described by Zimmermann already in 1902. Evidence that has accumulated since then has demonstrated that leaf nodules represent the arguably most complex, and certainly most intimate associations between bacteria and higher plants, as neither the host nor the bacterial symbiont can exist outside the symbiosis. In spite of more than a century of research, the reasons for the strict interdependence of this plant-bacterium association are unknown. In an interdisciplinary approach, involving three groups with complementary expertise in microbiology (Eberl/Carlier, UZH), chemistry (Gademann, UniBas) and plant biology (Wicker, UZH) the proposed Sinergia project aims at unraveling the molecular basis of this unique symbiosis. Our preliminary data indicate that the bacterial symbiont is involved in the biosynthesis of a novel C7N aminocyclitol (Eberl/Carlier), the structure of which was determined by the Gademann group. Given that compounds of the C7N aminocyclitol family display various biological activities, often inhibiting glycosidases, we hypothesize that kirkamide is central to the symbiosis. In this project, we intend to demonstrate that leaf nodule bacteria are directly responsible for kirkamide biosynthesis (Eberl/Carlier). We want to chemically synthesize kirkamide (Gademann) and investigate its biological effects, notably on plant growth and development using RNA-Seq (Wicker). In a collaborative effort of the three groups we want to unravel the biosynthetic pathway of kirkamide and reconstitute it in a heterologous host (Eberl/Carlier) that will be used in attempts to replace the bacterial symbiont. We will look for evidence of co-evolution of the symbiotic partners by sequencing respective genomes to investigate whether the symbionts are strictly vertically transmitted or host switching occurs (Eberl/Carlier & Wicker). The plant genome data will also form the basis for a bioinformatic-guided identification of putative kirkamide targets in the plant (Wicker & Gademann), which will be validated by appropriate bioassays. The results of this project are expected to not only reveal fundamental insights into the only known obligate bacterium-plant symbiosis but may also lead to novel biotechnological applications.
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