title: A role for the mevalonate pathway in early plant symbiotic signaling.
abstract: Rhizobia and arbuscular mycorrhizal fungi produce signals that are perceived by host legume receptors at the plasma membrane and trigger sustained oscillations of the nuclear and perinuclear Ca(2+) concentration (Ca(2+) spiking), which in turn leads to gene expression and downstream symbiotic responses. The activation of Ca(2+) spiking requires the plasma membrane-localized receptor-like kinase Does not Make Infections 2 (DMI2) as well as the nuclear cation channel DMI1. A key enzyme regulating the mevalonate (MVA) pathway, 3-Hydroxy-3-Methylglutaryl CoA Reductase 1 (HMGR1), interacts with DMI2 and is required for the legume-rhizobium symbiosis. Here, we show that HMGR1 is required to initiate Ca(2+) spiking and symbiotic gene expression in Medicago truncatula roots in response to rhizobial and arbuscular mycorrhizal fungal signals. Furthermore, MVA, the direct product of HMGR1 activity, is sufficient to induce nuclear-associated Ca(2+) spiking and symbiotic gene expression in both wild-type plants and dmi2 mutants, but interestingly not in dmi1 mutants. Finally, MVA induced Ca(2+) spiking in Human Embryonic Kidney 293 cells expressing DMI1. This demonstrates that the nuclear cation channel DMI1 is sufficient to support MVA-induced Ca(2+) spiking in this heterologous system.
authors.affiliation: Department of Agronomy, University of Wisconsin-Madison, Madison, WI 53706; venkateshwam@uwplatt.edu.
authors.forename: Muthusubramanian
authors.initials: M
authors.lastname: Venkateshwaran
authors.affiliation: Department of Agronomy, University of Wisconsin-Madison, Madison, WI 53706;
authors.forename: Dhileepkumar
authors.initials: D
authors.lastname: Jayaraman
authors.affiliation: Laboratory of Plant-Microbe Interactions, Institut National de Recherche Agronomique (UMR 441), Centre Nationale de Recherche Scientifique (UMR 2594), F-31320 Castanet-Tolosan, France;
authors.forename: Mireille
authors.initials: M
authors.lastname: Chabaud
authors.affiliation: Department of Life Sciences and Systems Biology, University of Torino, 10125 Torino, Italy;
authors.forename: Andrea
authors.initials: A
authors.lastname: Genre
authors.affiliation: Department of Chemistry, University of Wisconsin-Madison, Madison, WI 53706;
authors.forename: Allison J
authors.initials: AJ
authors.lastname: Balloon
authors.affiliation: Department of Agronomy, University of Wisconsin-Madison, Madison, WI 53706;
authors.forename: Junko
authors.initials: J
authors.lastname: Maeda
authors.affiliation: Department of Agronomy, University of Wisconsin-Madison, Madison, WI 53706;
authors.forename: Kari
authors.initials: K
authors.lastname: Forshey
authors.affiliation: Department of Agronomy, University of Wisconsin-Madison, Madison, WI 53706;
authors.forename: Désirée
authors.initials: D
authors.lastname: den Os
authors.affiliation: Department of Chemistry, University of Wisconsin-Madison, Madison, WI 53706;
authors.forename: Nicholas W
authors.initials: NW
authors.lastname: Kwiecien
authors.affiliation: Department of Chemistry, University of Wisconsin-Madison, Madison, WI 53706; Department of Biomolecular Chemistry, University of Wisconsin-Madison, Madison, WI 53706;
authors.forename: Joshua J
authors.initials: JJ
authors.lastname: Coon
authors.affiliation: Laboratory of Plant-Microbe Interactions, Institut National de Recherche Agronomique (UMR 441), Centre Nationale de Recherche Scientifique (UMR 2594), F-31320 Castanet-Tolosan, France;
authors.forename: David G
authors.initials: DG
authors.lastname: Barker
authors.affiliation: Department of Agronomy, University of Wisconsin-Madison, Madison, WI 53706; Department of Bacteriology, University of Wisconsin-Madison, Madison, WI 53706.
authors.forename: Jean-Michel
authors.initials: JM
authors.lastname: Ané
mesh_terms: D017360:Arabidopsis / Q000235:genetics; D020013:Calcium Signaling / Q000187:drug effects / Q000235:genetics; D002467:Cell Nucleus / Q000187:drug effects / Q000378:metabolism; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D020868:Gene Silencing / Q000187:drug effects; D057809:HEK293 Cells; D006801:Humans; D006903:Hydroxymethylglutaryl CoA Reductases / Q000378:metabolism; D046913:Medicago truncatula / Q000187:drug effects / Q000235:genetics / Q000382:microbiology; D053858:Metabolic Networks and Pathways / Q000187:drug effects; D008798:Mevalonic Acid / Q000378:metabolism* / Q000494:pharmacology; D009154:Mutation / Q000235:genetics; D038821:Mycorrhizae / Q000187:drug effects / Q000502:physiology; D019441:Plant Epidermis / Q000166:cytology / Q000187:drug effects; D010940:Plant Proteins / Q000378:metabolism; D030821:Plants, Genetically Modified; D015398:Signal Transduction / Q000187:drug effects; D013559:Symbiosis / Q000187:drug effects / Q000235:genetics
chemical_list: D010940:Plant Proteins; D006903:Hydroxymethylglutaryl CoA Reductases; D008798:Mevalonic Acid
keywords: HMG-CoA reductase; arbuscular mycorrhization; calcium signaling; legume nodulation; mevalonate