Periodic Reporting for period 2 - ORIGINS (Origin and evolution of intracellular symbioses in plants)
Período documentado: 2022-11-01 hasta 2024-04-30
Mutualism between plants and microorganisms has been essential for the evolution of terrestrial ecosystems for millions of years. It has been proposed that even the colonization of lands by plants was facilitated by a mutualistic symbiosis formed with arbuscular mycorrhizal fungi. This symbiosis, by far the most widespread in land plants, results in the accommodation of the symbiotic fungus inside the plant cells. Following this initial symbiosis, multiple other intracellular symbioses have evolved in plants as diverse as orchids, Ericaceae such as cranberry, legumes or the Jungermanniales, a group of bryophytes. These symbioses provide numerous benefits, improving plant nutrient acquisition and fitness.
Despite their absolute importance in terrestrial ecosystems, the molecular mechanisms underlying the origin and subsequent evolution of intracellular symbioses in plants remain poorly understood, limiting our understanding of this hidden part of the biodiversity surrounding us. In the ORIGINS project, we will address the question of the origin and functionning of this symbiosis.
In a first objective (Objective 1), we will use CRISPR/Cas9 in the bryophyte Marchantia paleacea to test the conservation across land plants of symbiotic mechanisms known in angiosperms. Then, we will decipher how these mechanisms evolved by comparing land plants with their closest algal relatives.
In a second objective (Objective 2), we will conduct transcriptomics coupled with genetic manipulations of most known intracellular symbioses in plants. This will allow determining how the ability to host intracellularly microbial symbionts recruited in the environment evolved repeatedly in land plants and how functional specificity evolved in these different symbioses.
Lastly (Objective 3), we will investigate why the evolution of intracellular symbioses is constrained to a unique genetic pathway.
Through this project, combining phylogenomics, biochemistry, transcriptomics and genetic validations in six plant lineages covering more than 500 million years of evolution, we will provide a comprehensive understanding of the molecular mechanisms underlying the evolution of intracellular mutualistic symbioses in plants. We hope to generate sufficient understanding of these processes, that they can be deployed to improve the use of symbiosis in agricultural contexts. In the long term, this may provide tools for a more sustainable agriculture.
Despite their absolute importance in terrestrial ecosystems, the molecular mechanisms underlying the origin and subsequent evolution of intracellular symbioses in plants remain poorly understood, limiting our understanding of this hidden part of the biodiversity surrounding us. In the ORIGINS project, we will address the question of the origin and functionning of this symbiosis.
In a first objective (Objective 1), we will use CRISPR/Cas9 in the bryophyte Marchantia paleacea to test the conservation across land plants of symbiotic mechanisms known in angiosperms. Then, we will decipher how these mechanisms evolved by comparing land plants with their closest algal relatives.
In a second objective (Objective 2), we will conduct transcriptomics coupled with genetic manipulations of most known intracellular symbioses in plants. This will allow determining how the ability to host intracellularly microbial symbionts recruited in the environment evolved repeatedly in land plants and how functional specificity evolved in these different symbioses.
Lastly (Objective 3), we will investigate why the evolution of intracellular symbioses is constrained to a unique genetic pathway.
Through this project, combining phylogenomics, biochemistry, transcriptomics and genetic validations in six plant lineages covering more than 500 million years of evolution, we will provide a comprehensive understanding of the molecular mechanisms underlying the evolution of intracellular mutualistic symbioses in plants. We hope to generate sufficient understanding of these processes, that they can be deployed to improve the use of symbiosis in agricultural contexts. In the long term, this may provide tools for a more sustainable agriculture.
During the first phase of the project, the work has been initiated for most of the Objectives.
Marchantia paleacea mutants have been generated for pathways important for symbiotic signaling, as well as for sensing microorganisms. Symbioses between diverse microorganisms and a diversity of plants species have been established in controlled laboratory conditions. A clear growth-promotion has been measured for a number of them in this controlled environment, indicating that we can succesfuly replicate what is known from samples collected in naturae.
We have positioned on gene in the symbiosis signalling pathway (Ferrer-Orgza et al. 2023 10.1111/nph.19423)
In parallel, we have developed a conceptual framework for the evolution of plant symbioses evolution, beyond the usually studied symbioses, including lichens (Puginier et al. 2022 10.1093/plphys/kiac258)
We have also developed technical tools to be used to study the evolution of symbiosis and applied them to symbiosis in flowering plants (Libourel et al. 2023 10.1038/s41477-023-01441-w).
By using a genome of green algae closely related to land plants and unable to form known symbioses, we have found that the symbiotic genes are not expressed in response to the same stimuli. This indicate that they may play roles in different biological processes in this alga. This tell us, for the first time, that what has been called the "symbiotic signalling pathway" may have originated in land plants by compiling genes acting in separate pathways.
Marchantia paleacea mutants have been generated for pathways important for symbiotic signaling, as well as for sensing microorganisms. Symbioses between diverse microorganisms and a diversity of plants species have been established in controlled laboratory conditions. A clear growth-promotion has been measured for a number of them in this controlled environment, indicating that we can succesfuly replicate what is known from samples collected in naturae.
We have positioned on gene in the symbiosis signalling pathway (Ferrer-Orgza et al. 2023 10.1111/nph.19423)
In parallel, we have developed a conceptual framework for the evolution of plant symbioses evolution, beyond the usually studied symbioses, including lichens (Puginier et al. 2022 10.1093/plphys/kiac258)
We have also developed technical tools to be used to study the evolution of symbiosis and applied them to symbiosis in flowering plants (Libourel et al. 2023 10.1038/s41477-023-01441-w).
By using a genome of green algae closely related to land plants and unable to form known symbioses, we have found that the symbiotic genes are not expressed in response to the same stimuli. This indicate that they may play roles in different biological processes in this alga. This tell us, for the first time, that what has been called the "symbiotic signalling pathway" may have originated in land plants by compiling genes acting in separate pathways.
The project should deliver on the three main objectives.
The connection betweent signalling pathway and the infection program for the arbuscular mycorrhizal symbiosis will be deciphered, and how it expands to other intracellular symbiosis determined.
A first glimpse on the role of the symbiotic signalling genes in green algae will be revealed, and how this pathway was connected during evolution to other genetic modules will be discovered.
The function of receptors in guarding the symbiosis pathway will be explored.
The specific transfer machinery required for symbionts to provide benefit to their host plants will be discovered and will provide options to improve plant symbiosis in field settings.
The connection betweent signalling pathway and the infection program for the arbuscular mycorrhizal symbiosis will be deciphered, and how it expands to other intracellular symbiosis determined.
A first glimpse on the role of the symbiotic signalling genes in green algae will be revealed, and how this pathway was connected during evolution to other genetic modules will be discovered.
The function of receptors in guarding the symbiosis pathway will be explored.
The specific transfer machinery required for symbionts to provide benefit to their host plants will be discovered and will provide options to improve plant symbiosis in field settings.