Evolution of endosymbiosis-mediated nuclear calcium signaling in land plants

The ability of fungi to establish mycorrhizal associations with plants and enhance the acquisition of mineral nutrients stands out as a key feature of terrestrial life. Evidence indicates that arbuscular mycorrhizal (AM) association is a trait present in the common ancestor of land plants,1,2,3,4 suggesting that AM symbiosis was an important adaptation for plants in terrestrial environments.5 The activation of nuclear calcium signaling in roots is essential for AM within flowering plants.6 Given that the earliest land plants lacked roots, whether nuclear calcium signals are required for AM in non-flowering plants is unknown. To address this question, we explored the functional conservation of symbiont-induced nuclear calcium signals between the liverwort Marchantia paleacea and the legume Medicago truncatula. In M. paleacea, AM fungi penetrate the rhizoids and form arbuscules in the thalli.7 Here, we demonstrate that AM germinating spore exudate (GSE) activates nuclear calcium signals in the rhizoids of M. paleacea and that this activation is dependent on the nuclear-localized ion channel DOES NOT MAKE INFECTIONS 1 (MpaDMI1). However, unlike flowering plants, MpaDMI1-mediated calcium signaling is only required for the thalli colonization but not for the AM penetration within rhizoids. We further demonstrate that the mechanism of regulation of DMI1 has diverged between M. paleacea and M. truncatula, including a key amino acid residue essential to sustain DMI1 in an inactive state. Our study reveals functional evolution of nuclear calcium signaling between liverworts and flowering plants and opens new avenues of research into the mechanism of endosymbiosis signaling. [Display omitted] •The symbiosis-induced nuclear calcium signal is ancestral in land plants•DMI1 is required for arbuscular mycorrhiza colonization of M. paleacea thalli•AM colonization of M. paleacea rhizoid is independent of nuclear calcium signaling•The activation mechanism of DMI1 has diverged between M. paleacea and flowering plants Lam et al. show that arbuscular-mycorrhiza-induced nuclear calcium signaling is ancestral in land plants. It is necessary for the colonization of liverwort thalli by arbuscular mycorrhiza, but not for the rhizoid infection. It is dependent on DMI1, whose gating mechanism has diverged between liverwort and flowering plants.