Evolution of receptor signalling specificity for symbiosis and development

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A key event in the evolution of complex life on earth is the transition of plants from water to land. To conquer the terrestrial environment plants had to develop strategies for the acquisition of soil nutrients with initially primitive root precursors. Ever since, plants have lived in symbioses with nutrient-delivering beneficial fungi. Today, the arbuscular mycorrhizal (AM) symbiosis is the most commonly occurring beneficial plant-fungal interaction on Earth, contributing to plant fitness, plant biodiversity and global nutrient cycles. Yet, we are only beginning to unveil the molecular processes leading to the establishment of this intimate association and to control it for modern crop breeding. The Paszkowski group has found that an alpha/beta hydrolase receptor, called DWARF 14 LIKE (D14L), is essential for fungal perception of rice in the rhizosphere. The activation of this receptor is necessary for the unblocking of genetic programmes that enable symbiosis development and induce production of the phytohormone strigolactone (Gutjahr et al., Science 2015; Choi et al., Nat Commun 2020). The receptor is present across the plant kingdom and serves multifunctional roles, including the detection of the smoke constituent karrikin and the modulation of seedling development amongst others. However, D14L receptors from different plant species are functionally not necessarily equivalent. The Paszkowski lab recently found that the D14L homologue from Arabidopsis thaliana was only able to complement the developmental phenotype of rice d14l mutants, but failed to restore AM symbiosis.As D14L receptors are present across terrestrial plants, including early divergent plants and even Charophyte algae, they may have distinctly and successively diversified to acquire the signalling roles we observe today. We now wish to reproduce the evolutionary trajectory in order to define the protein features that condition signalling specificity, and to better understand their emergence. Exploiting the exponentially growing genome sequence resource, we propose here a high-resolution metagenomics approach, employing and developing computational tools that are significantly superior relative to conventional practices. This includes the development of new algorithmic steps enabling 10,000-fold computational acceleration compared to previous approaches. Results obtained from these in silico efforts are then functionally validated in rice to confirm their relevance in vivo.Insights generated here are vital for understanding how receptor functioning integrates and specifies different signalling cues. In doing so, this will open up new areas of research in computational and plant biology and provide a paradigm for which other examples of signalling processes can be assessed.