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Conservation of symbiotic signalling across 450 million years of plant evolution
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Summary Highlight The common symbiotic pathway is activated during arbuscular mycorrhizal symbiosis in Marchantia paleacea The three core members of the common symbiotic pathway are essential for symbiosis in Marchantia paleacea The molecular function of the CCaMK/CYCLOPS module is conserved across land plants Symbiotic signalling has been conserved in plants for 450 million years The colonization of land by plants 450 million years ago revolutionized life on Earth 1 . The fossil record 2 and genetic evidence in extant species 3 suggest that this transition was facilitated by interactions with symbiotic arbuscular mycorrhizal (AM) fungi 4 . This ancestral symbiosis relied on the biosynthesis of chemicals by the host plant, both as signals 5 and as nutrients 3 . In angiosperms, a signalling pathway involving the receptor-like kinase SYMRK/DMI2 6,7 , the Calcium and Calmodulin-dependent protein kinase CCaMK/DMI3 8 and the transcription factor CYCLOPS/IPD3 9,10 has been described as the common symbiosis pathway (CSP), essential for the establishment of the AM symbiosis and the root-nodule symbiosis 11 . Phylogenetic and comparative phylogenomic analyses indicated an ancient origin of the CSP, present in all extant land plants forming intracellular symbioses 12–15 . Trans-complementation assays of the angiosperm mutants with orthologs from diverse species further indicated the conservation of the molecular function of the CSP across the embryophytes 9,12,14–16 . However, this correlative evidence did not allow testing the ancestral biological function of the CSP. In this study we demonstrate that SYMRK, CCaMK and CYCLOPS are essential for the colonization by AM fungi in bryophytes, indicating that plants have maintained a dedicated signalling pathway to support symbiotic interactions for 450 million years.
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