Conservation of symbiotic signalling across 450 million years of plant evolution

Abstract

SummaryHighlightThe common symbiotic pathway is activated during arbuscular mycorrhizal symbiosis inMarchantia paleaceaThe three core members of the common symbiotic pathway are essential for symbiosis inMarchantia paleaceaThe molecular function of the CCaMK/CYCLOPS module is conserved across land plantsSymbiotic signalling has been conserved in plants for 450 million yearsThe colonization of land by plants 450 million years ago revolutionized life on Earth1. The fossil record2and genetic evidence in extant species3suggest that this transition was facilitated by interactions with symbiotic arbuscular mycorrhizal (AM) fungi4. This ancestral symbiosis relied on the biosynthesis of chemicals by the host plant, both as signals5and as nutrients3. In angiosperms, a signalling pathway involving the receptor-like kinase SYMRK/DMI26,7, the Calcium and Calmodulin-dependent protein kinase CCaMK/DMI38and the transcription factor CYCLOPS/IPD39,10has been described as the common symbiosis pathway (CSP), essential for the establishment of the AM symbiosis and the root-nodule symbiosis11. Phylogenetic and comparative phylogenomic analyses indicated an ancient origin of the CSP, present in all extant land plants forming intracellular symbioses12–15. 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 embryophytes9,12,14–16. 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.