A plant-fungus partnership is at the origin of terrestrial vegetation

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Phylogenetic tree of plants. Vascular and non-vascular plants form a symbiosis w

Phylogenetic tree of plants. Vascular and non-vascular plants form a symbiosis with fungi. Circles on the left: the fungus is stained blue in a truncated alfalfa root (top) or a thallus of M. paleacea (bottom). Right-hand circles: stubby alfalfa (top), M. paleacea (bottom). Aurélie Le Ru/Mélanie Rich/Pierre-Marc Delaux

Plants that exist on land today have genes that allow them to exchange valuable lipids with beneficial fungi. This plant-fungus partnership is at the origin of the transition of plants from aquatic life to terrestrial life.

A long-standing theory assumes that terrestrial plants could only have developed by entering into a symbiosis with fungi, whereby the two organisms exchange resources in a mutually beneficial way. A new study by an international group of scientists has now confirmed this theory. By studying a liverwort species (a bryophyte related to mosses), the scientists succeeded in demonstrating that a lipid transfer takes place between the plant and the fungus similar to that already known to exist in plants with stems and roots - so called vascular plants. The study was led by French researchers from the Centre national de la recherche scientifique (CNRS) and the Université de Toulouse III - Paul Sabatier, in collaboration with the Institut national de la recherche agronomique (INRA) and has been published in Science on 21 May.Marcel Bucher from the Institute for Plant Sciences and the CEPLAS Cluster of Excellence on Plant Science in Cologne participated in the study and contributed essential genetic information at the beginning and experimental results on the molecular mechanism underlying the symbiotic exchange of lipids throughout the collaboration. The CIBSS - Centre for Integrative Biological Signalling Studies at the University of Freiburg was also involved.

About 450 million years ago, the first plants left the freshwater to live on land. To do this, they had to adapt to the aridity and nutrient scarcity of the land. In the 1980s, the study of fossils led to the hypothesis that a plant-fungus alliance has been at the origin of plant vegetation. Previous studies have shown the existence of genes that are essential for the proper functioning of this symbiosis, particularly in vascular plants. In the present study, the scientists focused on a bryophyte resembling a succulent plant, for which such genes had not yet been studied: Marchantia paleacea. Validating this forty-year-old hypothesis allows the scientists to understand a stage that was crucial to the development of life on Earth.

By adapting the use of CRISPR, a molecular tool that allows DNA to be cleaved precisely, the team modified a gene predicted as ’symbiotic’. As in vascular plants, the interruption of lipid exchange between the plant and the fungus leads to symbiosis failure in the liverwort. ’The beauty of the work lies in the use of different complementary molecular genetic approaches which have shown that this "symbiotic gene" encodes a key regulator, a so-called transcription factor, which directly regulates the expression of other symbiosis genes, among them genes required for "feeding" the fungus,’ Marcel Bucher remarked. These are involved in lipid metabolism and transport in cells in M. paleacea, leading to the transfer of valuable carbon derived from the photosynthetic plant host in the form of fatty acids as a building material and energy source to the fungal symbiotic partner.

The results of the study show that the common ancestor of liverworts and vascular plants, which colonised dry land, must therefore have exchanged lipids with the fungus, as do the plants of today. Thus, 450 million years later, one of the secrets of life’s first steps on land has finally been elucidated.

Publication:
science.sciencemag.o­rg/content/372/6544/864

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