Origin of the Molecular "Toolkit" for Plant – Microbe Symbioses

Plants interact constantly with microbes in their environment. Many of these interactions are strongly beneficial for the plants and play a very important role in the sustainability of our agricultural systems. The most ancient and widespread symbiosis is the association between land plants and arbuscular mycorrhizal (AM) fungi. Studies in model angiosperms led to the characterization of a symbiotic “toolkit” encompassing small molecules and gene networks required for this AM symbiosis. Several components of this toolkit are also required for other symbiotic associations such as the rhizobia-legume association. However, the origin and evolution of this toolkit remain poorly understood.

We first determined the evolutionary pattern of all the known components of this toolkit by in silico screening of genomic and transcriptomic datasets from green algae and land plants. Based on this approach, we found that some of these components are present in green algae, therefore pre-dating the appearance of the AM symbiosis.

We then characterized more in detail the strigolactones as well as their biosynthetic and signaling pathways. Strigolactones produced by plant roots activate AM fungi and prepare them for the colonization process. In addition, strigolactones have been characterized as a bona fide plant hormones controlling both root and shoot development in angiosperms. We found that strigolactones are produced by liverworts, the most basal land plants, as well as charophyte green algae but not by chlorophyte green algae. The appearance of strigolactones in the green lineage is also concomitant with the appearance of the corresponding signaling pathway. In addition, we found that strigolactones treatments on mosses, liverworts and Charophyte green algae stimulate rhizoid elongation. Based on these results, we propose that strigolactones appeared with Charophytes where they act as phytohormone and were later recruited as signals for the AM symbiosis.