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PHYLLOSYM

PLANT-BACTERIA ASSOCIATIONS IN THE PHYLLOSPHERE

We are interested in the interactions between bacteria and their hosts. The microbiota play a critical role for the health and growth of plants, but how beneficial microbes are recognized remains poorly understood. This is especially true in the phyllosphere, the compartment composed of the aboveground organs of the plant which includes stem, leaves, flowers and fruits. Recent evidence suggests that several plant species have evolved or co-opted an ancient pathway enabling symbiont capture and consistent vertical transmission. Gaining insight into the mechanisms used to recognize beneficial symbionts at the leaf surface is essential in order to leverage the richness and diversity of the plant microbiome in agriculture.
 

More specifically, our research focuses on obligate or vertically-transmitted mutualistic symbioses. These are notoriously difficult to study by traditional methods because molecular processes between the host and symbionts have often been intertwined by millions of years of co-evolution. They are however the most promising in terms of application and understanding of co-evolution between host and bacteria. Obligate symbioses can be viewed as some of the most successful biological partnerships and a tremendous source of biological innovation.

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Nom equipe

RESEARCH THEMES

Evolution of leaf symbioses

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 


 

Various plant species of the Rubiaceae and Primulaceae form permanent associations with bacteria, often visible in the form of galls on the leaves (Figure, reproduced from Pinto-Carbó et al., 2018, doi: 10.1016 / j.pbi .2018.01.001).

Uncommonly in plants, symbiotic bacteria seem to be transmitted vertically via seeds, and to be necessary for the normal development of their host. We have demonstrated that symbiotic bacteria produce copious amounts of secondary metabolites with insecticidal or allelopathic properties, possibly playing a role in the protection of the host plant. The group continues to study these binary associations, which provide a valuable model to study the evolution of beneficial associations between endophytic bacteria and their hosts.
 

Publications on the topic:

  • Pinto-Carbó, M., Gademann, K., Eberl, L., and Carlier, A. 2018. “Leaf Nodule Symbiosis: Function and Transmission of Obligate Bacterial Endophytes.” Ed. Sebastian Schormack and Caroline Gutjahr. Current Opinion in Plant Biology 44: 23–31.

  • Pinto-Carbó, M., Sieber, S., Dessein, S., Wicker, T., Verstraete, B., Gademann, K., Eberl, L., and Carlier, A *. Evidence of horizontal gene transfer between obligate leaf nodule symbionts. 2016. ISME J. 10 (9): 2092– 2105.

  • Crüsemann, M .; Reher, R .; Schamari, I .; Brachmann, A .; Ohbayashi, T .; Kuschak, M .; Malfacini, D .; Seidinger, A .; Pinto-Carbó, M .; Reuter, T .; Kehraus, S .; Hallab, A .; Mergaert, P .; Kikuchi, Y .; Schäberle, T, Fleischmann, B., Kostenis, E., Wenzel, D., Müller, C., Piel, J, Carlier, A., Eberl, L., König, G. Heterologous expression, biosynthetic studies and ecological function of the selective Gq-signaling inhibitor FR900359. 2018. Angewandte Chemie Intl. Ed. (3): 836–840.

  • Carlier, A., Fehr, L., Pinto-Carbó, M., Schäberle, T., Reher, R., Dessein, S., König, G., and Eberl, L. 2016. “The Genome Analysis of Candidatus Burkholderia Crenata Reveals That Secondary Metabolism May Be a Key Function of the Ardisia Crenata Leaf Nodule Symbiosis. ” Environmental Microbiology 18 (8): 2507–2522.


The model symbiosis Dioscorea sansibarensis / Orrella dioscoreae


Unlike the leaf symbiosis of Primulaceae and Rubiaceae which are difficult to manipulate in the laboratory, the symbiosis between the species of wild yam Dioscorea sansibarensis and the bacterium Orrella dioscoreae offers an ideal experimental system to understand the recruitment of symbiotic functions in the phyllosphere. The team establishes innovative methods for the manipulation of the symbiotic cycle in order to better understand the bases of the specificity between plants and extracellular bacteria in the phyllosphere.

 

Recent publications on the topic:

  • Bram Danneels, Juan Viruel, Krista Mcgrath, Steven B. Janssens, Nathan Wales, Paul Wilkin, Aurelien Carlier *. Patterns of transmission and horizontal gene transfer in the Dioscorea sansibarensis leaf symbiosis revealed by whole-genome sequencing. Current Biology. (2021). https://doi.org/10.1016/j.cub.2021.03.049.

  • De Meyer, F., Danneels, B., Acar, T. et al. Adaptations and evolution of a heritable leaf nodule symbiosis between Dioscorea sansibarensis and Orrella dioscoreae. ISME J 13, 1831–1844 (2019). https://doi.org/10.1038/s41396-019-0398-8

Job opportunities

*** Postdoc opportunity beginning 2023 ***

We seek a candidate for a 3-year ANR-funded project aiming at understanding the function and ecological role of plant leaf symbioses. The project is at the interface between the fields of microbiology/plant biology and natural product chemistry and focuses on understanding the mechanisms driving the ecological success of plant-bacteria symbioses, especially leaf symbioses. The ideal candidate should have demonstrated experience in multi-omics (genomics, transcriptomics or metabolomics), a good understanding of host-bacteria associations, and a strong interest for chemical ecology. 

To apply, please send your cv and cover letter (including names and contact of 2 references) to aurelien.carlier (at) inrae.fr

Collaborations

 

Our main collaborations are with the groups of Petya Krasteva (with Thibault Sana, IECB CNRS, France), Leo Eberl, University of Zurich (CH); Paul Wilkin, Kew Botanical Garden (UK); Steven Janssens (Meise Botanical Garden, BE); Max Crüsemann and Gabriele König (Bonn University, DE). We also maintain close collaborations with the Laboratory of Microbiology of the University of Ghent (BE, chair Prof. Peter Vandamme).

Ongoing funding

 

Our research is possible thanks to the support of:

  • ANR project "RESIDE" 2023-2026

  • INRAE ​​SPE Camessym project (2019-2022)

  • ANR PHYLLOSYM project (2019-2022)

  • LabEx TULIP "Junior" Chair (2019-2024)

 

Former members

At LIPME:

  • Tessa Acar (PhD student 2017-2021)

  • Bram Danneels (PhD student and postdoc, 2017-2022)

  • Thibault Sana (postdoc 2020-2021)

  • Marine Beaumel (intern, summers 2021 and 2022)

  • Sarah Ranty-Roby (2019-2021)

  • Dr. Olivier Coen (postdoc 2020-2021)

  • Adrien Javois (Master student 2021)

  • Tim Stralla (Master 1 student 2020)

At LM-UGent:

  • Dr. Shanshan Qi (PhD student 2017-2021)

  • Mathijs Deprez (Master student 2020)

  • Youness Assoued (Master student 2018)

  • Diete Van Steenbergen (Master student 2017)

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Thèmes de recherche

PUBLICATIONS

Complete list on HAL (lien externe)​

Selected publications:
 

Hereditary Leaf Symbiosis in Tropical Plants: Evolution and Function of Vertically Transmitted Bacterial Symbionts

Léa Ninzatti, Marie-Françoise Jardinaud, and Aurélien Carlier

Phytobiomes Journal 2025 10.1094/PBIOMES-11-24-0111-RVW


Thibault Sana, Areti Notopoulou, Lucie Puygrenier, Marion Decossas, Sandra Moreau, et al.. Structures and roles of BcsD and partner scaffold proteins in proteobacterial cellulose secretion. Current Biology, 2024, 34 (1), 6 p. 10.1016/j.cub.2023.11.057hal-04474396

Tessa Acar, Sandra Moreau, Marie-Françoise Jardinaud, Gabriella Houdinet, Felicia Maviane-Macia, et al.. The association between Dioscorea sansibarensis and Orrella dioscoreae as a model for hereditary leaf symbiosis. PLoS ONE, 2024, 19 (4), pp.e0302377. ⟨10.1371/journal.pone.0302377⟩⟨hal-04670561⟩

 

Tessa Acar, Sandra Moreau, Olivier Coen, Frédéric de Meyer, Olivier Leroux, et al.. Motility-Independent Vertical Transmission of Bacteria in Leaf Symbiosis. mBio, 2022, 15 p. ⟨10.1128/mbio.01033-22⟩. ⟨hal-03778794

Bram Danneels, Juan Viruel, Krista Mcgrath, Steven Janssens, Nathan Wales, et al.. Patterns of transmission and horizontal gene transfer in the Dioscorea sansibarensis leaf symbiosis revealed by whole-genome sequencing. Current Biology, 2021, 31 (12), pp.2666-2673.e4. ⟨10.1016/j.cub.2021.03.049⟩. ⟨hal-03272495

Charles Dumolin, Maarten Aerts, Bart Verheyde, Simon Schellaert, Tim Vandamme, et al.. Introducing SPeDE: High-Throughput Dereplication and Accurate Determination of Microbial Diversity from Matrix-Assisted Laser Desorption–Ionization Time of Flight Mass Spectrometry Data. mSystems, 2019, 4 (5), pp.e00437-19. ⟨10.1128/mSystems.00437-19⟩. ⟨hal-02961994

 

Frédéric de Meyer, Bram Danneels, Tessa Acar, Rado Rasolomampianina, Mamy Tiana Rajaonah, et al.. Adaptations and evolution of a heritable leaf nodule symbiosis between Dioscorea sansibarensis and Orrella dioscoreae. The International Society of Microbiologial Ecology Journal, 2019, 13 (7), pp.1831-1844. ⟨10.1038/s41396-019-0398-8⟩. ⟨hal-02961999

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