title: Nuclear membranes control symbiotic calcium signaling of legumes.
abstract: Nuclear-associated oscillations in calcium act as a secondary messenger in the symbiotic signaling pathway of legumes. These are decoded by a nuclear-localized calcium and calmodulin-dependent protein kinase, the activation of which is sufficient to drive downstream responses. This implies that the calcium oscillations within the nucleus are the predominant signals for legume symbiosis. However, the mechanisms that allow targeted release of calcium in the nuclear region have not been defined. Here we show that symbiosis-induced calcium changes occur in both the nucleoplasm and the perinuclear cytoplasm and seem to originate from the nuclear membranes. Reaction diffusion simulations suggest that spike generation within the nucleoplasm is not possible through transmission of a calcium wave from the cytoplasm alone and that calcium is likely to be released across the inner nuclear membrane to allow nuclear calcium changes. In agreement with this, we found that the cation channel DMI1, which is essential for symbiotic calcium oscillations, is preferentially located on the inner nuclear membrane, implying an essential function for the inner nuclear membrane in symbiotic calcium signaling. Furthermore, a sarco/endoplasmic reticulum calcium ATPase (SERCA) essential for symbiotic calcium oscillations is targeted to the inner nuclear membrane, as well as the outer nuclear membrane and endoplasmic reticulum (ER). We propose that release of calcium across the inner nuclear membrane allows targeted release of the ER calcium store, and efficient reloading of this calcium store necessitates the capture of calcium from the nucleoplasm and nuclear-associated cytoplasm.
authors.affiliation: John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom.
authors.forename: Ward
authors.initials: W
authors.lastname: Capoen
authors.forename: Jongho
authors.initials: J
authors.lastname: Sun
authors.forename: Derin
authors.initials: D
authors.lastname: Wysham
authors.forename: Marisa S
authors.initials: MS
authors.lastname: Otegui
authors.forename: Muthusubramanian
authors.initials: M
authors.lastname: Venkateshwaran
authors.forename: Sibylle
authors.initials: S
authors.lastname: Hirsch
authors.forename: Hiroki
authors.initials: H
authors.lastname: Miwa
authors.forename: J Allan
authors.initials: JA
authors.lastname: Downie
authors.forename: Richard J
authors.initials: RJ
authors.lastname: Morris
authors.forename: Jean-Michel
authors.initials: JM
authors.lastname: Ané
authors.forename: Giles E D
authors.initials: GE
authors.lastname: Oldroyd
mesh_terms: D020013:Calcium Signaling / Q000187:drug effects; D003600:Cytosol / Q000187:drug effects / Q000378:metabolism; D004058:Diffusion / Q000187:drug effects; D004721:Endoplasmic Reticulum / Q000187:drug effects / Q000378:metabolism; D020868:Gene Silencing / Q000187:drug effects; D007473:Ion Channels / Q000378:metabolism; D008070:Lipopolysaccharides / Q000494:pharmacology; D046913:Medicago truncatula / Q000166:cytology* / Q000201:enzymology / Q000378:metabolism* / Q000648:ultrastructure; D008954:Models, Biological; D008969:Molecular Sequence Data; D009685:Nuclear Envelope / Q000187:drug effects / Q000378:metabolism* / Q000648:ultrastructure; D019441:Plant Epidermis / Q000166:cytology / Q000187:drug effects / Q000378:metabolism; D010940:Plant Proteins / Q000378:metabolism; D018517:Plant Roots / Q000166:cytology / Q000187:drug effects / Q000648:ultrastructure; D021381:Protein Transport / Q000187:drug effects; D053498:Sarcoplasmic Reticulum Calcium-Transporting ATPases / Q000378:metabolism; D013559:Symbiosis / Q000187:drug effects / Q000502:physiology*
chemical_list: D007473:Ion Channels; D008070:Lipopolysaccharides; D010940:Plant Proteins; D053498:Sarcoplasmic Reticulum Calcium-Transporting ATPases