Title: Formin-mediated bridging of cell wall, plasma membrane, and cytoskeleton in symbiotic infections of Medicago truncatula
Abstract: Legumes have maintained the ability to associate with rhizobia to sustain the nitrogen-fixing root nodule symbiosis (RNS). In Medicago truncatula, the Nod factor (NF)-dependent intracellular root colonization by Sinorhizobium meliloti initiates from young, growing root hairs. They form rhizobial traps by physically curling around the symbiont.1Brewin N.J. Plant cell wall remodelling in the rhizobium-legume symbiosis.Crit. Rev. Plant Sci. 2004; 23: 293-316Crossref Scopus (207) Google Scholar,2Gage D.J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes.Microbiol. Mol. Biol. Rev. 2004; 68: 280-300Crossref PubMed Scopus (526) Google Scholar Although alterations in root hair morphology like branching and swelling have been observed in other plants in response to drug treatments3Bibikova T.N. Blancaflor E.B. Gilroy S. 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The entrapment of the symbiont completes with its full enclosure in a structure called the “infection chamber” (IC),1Brewin N.J. Plant cell wall remodelling in the rhizobium-legume symbiosis.Crit. Rev. Plant Sci. 2004; 23: 293-316Crossref Scopus (207) Google Scholar,2Gage D.J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes.Microbiol. Mol. Biol. Rev. 2004; 68: 280-300Crossref PubMed Scopus (526) Google Scholar,7Esseling J.J. Lhuissier F.G.P. Emons A.M.C. Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application.Plant Physiol. 2003; 132: 1982-1988Crossref PubMed Scopus (92) Google Scholar,8Fournier J. Teillet A. Chabaud M. Ivanov S. Genre A. Limpens E. de Carvalho-Niebel F. Barker D.G. Remodeling of the infection chamber before infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair.Plant Physiol. 2015; 167: 1233-1242Crossref PubMed Scopus (79) Google Scholar from which a tube-like membrane channel, the “infection thread” (IT), initiates.1Brewin N.J. Plant cell wall remodelling in the rhizobium-legume symbiosis.Crit. Rev. Plant Sci. 2004; 23: 293-316Crossref Scopus (207) Google Scholar,2Gage D.J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes.Microbiol. Mol. Biol. Rev. 2004; 68: 280-300Crossref PubMed Scopus (526) Google Scholar,9Gage D.J. Margolin W. Hanging by a thread: invasion of legume plants by rhizobia.Curr. Opin. Microbiol. 2000; 3: 613-617Crossref PubMed Scopus (82) Google Scholar All steps of rhizobium-induced root hair alterations are aided by a tip-localized cytosolic calcium gradient,10Ruijter N.C.A.D. Rook M.B. Bisseling T. Emons A.M.C. 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Parniske M. Wang T.L. Downie J.A. Xie F. SCARN a novel class of SCAR protein that is required for root-hair infection during legume nodulation.PLoS Genet. 2015; 11: e1005623Crossref PubMed Scopus (41) Google Scholar, 18Gavrin A. Rey T. Torode T.A. Toulotte J. Chatterjee A. Kaplan J.L. Evangelisti E. Takagi H. Charoensawan V. Rengel D. et al.Developmental modulation of root cell wall architecture confers resistance to an oomycete pathogen.Curr. Biol. 2020; 30: 4165-4176.e5Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar Here, we identified a polarly localized SYMBIOTIC FORMIN 1 (SYFO1) to be required for NF-dependent alterations in membrane organization and symbiotic root hair responses. We demonstrate that SYFO1 mediates a continuum between the plasma membrane and the cell wall that is required for the onset of rhizobial infections.