Evolution of endosymbiosis-mediated nuclear calcium signaling in land plants
Year: 2024
Type: article
Abstract: 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 1. Remy, W. ∙ Taylor, T.N. ∙ Hass, H. ... Four hundred-million-year-old vesicular arbuscular mycorrhizae Proc. Natl. Acad. Sci. USA. 1994; 91 :11841-11843 Crossref Scopus (841) PubMed Google Scholar , 2 2. Redecker, D. ∙ Kodner, R. ∙ Graham, L.E. Glomalean fungi from the Ordovician Science. 2000; 289 :1920-1921 Crossref Scopus (822) PubMed Google Scholar , 3 3. Rich, M.K. ∙ Vigneron, N. ∙ Libourel, C. ... Lipid exchanges drove the evolution of mutualism during plant terrestrialization Science. 2021; 372 :864-868 Crossref Scopus (79) PubMed Google Scholar , 4 4. Radhakrishnan, G.V. ∙ Keller, J. ∙ Rich, M.K. ... An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages Nat. Plants. 2020; 6 :280-289 Crossref Scopus (115) PubMed Google Scholar suggesting that AM symbiosis was an important adaptation for plants in terrestrial environments. 5 5. Pirozynski, K.A. ∙ Malloch, D.W. The origin of land plants: a matter of mycotrophism Biosystems. 1975; 6 :153-164 Crossref Scopus (450) PubMed Google Scholar The activation of nuclear calcium signaling in roots is essential for AM within flowering plants. 6 6. Charpentier, M. ∙ Sun, J. ∙ Vaz Martins, T. ... Nuclear-localized cyclic nucleotide-gated channels mediate symbiotic calcium oscillations Science. 2016; 352 :1102-1105 Crossref Scopus (207) PubMed Google Scholar 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 7. Kobae, Y. ∙ Ohtomo, R. ∙ Morimoto, S. ... Isolation of native arbuscular mycorrhizal fungi within young Thalli of the liverwort Marchantia paleacea Plants (Basel). 2019; 8 , 142 Crossref Scopus (5) PubMed Google Scholar 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 ( Mpa DMI1). However, unlike flowering plants, Mpa DMI1-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.
Source: Current Biology
Authors: Anson H.C. Lam, Aisling Cooke, Hannah Wright, David M. Lawson, Myriam Charpentier
Institutions: John Innes Centre, Norwich Research Park
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: hybrid
Estimated APC paid: $7,030
OpenAlex ID: W4394965017