A unique ability of all living organisms is to perceive and respond to the presence of other organisms. These responses, and the quality of the resulting interaction, vary along a continuum from immune response to the recruitment of cellular and molecular mechanisms that allow the formation of close symbiotic associations that benefit both partner organisms. Interactions between plants and microorganisms are particularly well suited to the study of these mechanisms, studies facilitated by the use of genome editing methods in model species that can be analyzed at high throughput. As a young researcher, and then within my research team since 2020, I seek to dissect the symbiotic molecular mechanisms deployed by plants to accommodate their symbionts. This work is based on the use of comparative biology tools at the genomic, transcriptomic, metabolomic and phenotypic scales, coupled with reverse genetics and more recently with synthetic biology. Two main directions emerge from my work that I wish to explore in the future.
My team and our international collaborators have discovered the existence of a 450 million year old signaling pathway (Rich et al. 2021), composed of membrane receptors, kinases and transcript factors, common to all plant species capable of redifferentiating their cells to accommodate a symbiotic microorganism, bacterium or fungus, within their cells (Radhakrishnan et al. 2020). How is this signaling pathway regulated by symbiotic organisms? What mechanisms prevent its recruitment by pathogenic organisms? How has it been maintained over evolutionary time? I am now exploring these questions through my ERC project CoG ORIGINS, and trying to recapitulate our findings to generate new symbioses beneficial for global agriculture in the framework of the Engineering Nitrogen-fixing Symbiosis for Africa project supported by the Bill & Melinda Gates Foundation.
Caption: A signaling pathway comprising kinases and a transcription factor (CYCLOPS) is associated with all intracellular symbioses in plants. Shrubby, ericoides, orchidoides, nitrogen-fixing and jungermanniales mycorrhizal symbioses are represented.
The second direction I wish to explore is built on the discovery of the existence of a symbiotic genome in plants, a portion of the genome dedicated to setting up symbiotic interactions with the microbiota (Griesman et al. 2018; Radhakrishnan et al. 2020). This symbiotic genome could be identified using phylogenomic comparison tools to associate symbiotic capacity with the presence or rate of evolution of genes and, more recently, cis-regulatory elements. This type of evolutionary gene-for-trait association has also been observed by others in animals for developmental traits such as hairiness in mammals. By exploring the genomes, microbiota and symbiotic capacities already described in mammals, insects or fungi, would we be able to identify symbiotic genomes in all living things? Eventually, could we define general rules to position interactions between two organisms on the continuum between immunity and symbiosis?
Beyond these two lines of work, a new direction initiated in my team consists in studying the evolution of parasite-host interactions. Contrary to mutualistic interactions, the evolution of parasitic relationships is constrained on the one hand by the host’s immune mechanisms and on the other hand by the hijacking of these mechanisms by the parasites. These relationships are therefore based on a rapid evolution, well described in flowering plants. The immune mechanisms of other plants, such as bryophytes and green algae, remain unknown. We aim to discover these mechanisms by studying their evolution at intra- and inter-specific scales. In the long term, we hope to isolate new sources of resistance to pathogens, potentially usable in agriculture.
