Buffering Capacity Explains Signal Variation in Symbiotic Calcium Oscillations      

Abstract

Legumes form symbioses with rhizobial bacteria and arbuscular mycorrhizal fungi that aid plant nutrition. A critical component in the establishment of these symbioses is nuclear-localized calcium (Ca 2+ ) oscillations. Different components on the nuclear envelope have been identified as being required for the generation of the Ca 2+ oscillations. Among these an ion channel, Doesn't Make Infections1, is preferentially localized on the inner nuclear envelope and a Ca 2+ ATPase is localized on both the inner and outer nuclear envelopes. Doesn't Make Infections1 is conserved across plants and has a weak but broad similarity to bacterial potassium channels. A possible role for this cation channel could be hyperpolarization of the nuclear envelope to counterbalance the charge caused by the influx of Ca 2+ into the nucleus. Ca 2+ channels and Ca 2+ pumps are needed for the release and reuptake of Ca 2+ from the internal store, which is hypothesized to be the nuclear envelope lumen and endoplasmic reticulum, but the release mechanism of Ca 2+ remains to be identified and characterized. Here, we develop a mathematical model based on these components to describe the observed symbiotic Ca 2+ oscillations. This model can recapitulate Ca 2+ oscillations, and with the inclusion of Ca 2+ -binding proteins it offers a simple explanation for several previously unexplained phenomena. These include long periods of frequency variation, changes in spike shape, and the initiation and termination of oscillations. The model also predicts that an increase in buffering capacity in the nucleoplasm would cause a period of rapid oscillations. This phenomenon was observed experimentally by adding more of the inducing signal.

Nuclear Calcium Signaling in Plants

“…Indeed, pharmacological and yeast expression analyses highlight that DMI1 might be a tight regulator of the yet unidentified symbiotic Ca 2+ channel (Peiter et al, 2007). In agreement with this observation, mathematical modeling reveals that the association of three components (DMI1, a putative voltage/ligand-activated Ca 2+ channel, and a Ca 2+ pump) is sufficient to produce the symbiotic Ca 2+ oscillations (Granqvist et al, 2012). This mathematical modeling suggests that DMI1 functions to regulate the Ca 2+ channel as a counter ion channel and a modulator of membrane potential in two steps (Charpentier et al, 2013).…”

“…1). Although mathematical modeling suggests that the short burst of oscillations can be generated by a different buffering capacity of the cell (Granqvist et al, 2012), the biological relevance of this initial rapid burst of Ca 2+ spikes remains to be determined. Initial studies of Ca 2+ oscillations induced at early stages of AM-fungal interactions before contact with the epidermal cell indicated differences to the Ca 2+ oscillations activated by Nod factor, providing the basis for hypothesizing that the specificity of symbiosis signaling may be encoded within the structure of the Ca 2+ response (Kosuta et al, 2008;Chabaud et al, 2011).…”

A role for the mevalonate pathway in early plant symbiotic signaling

“…Elegant mathematical models have been developed to explain the mechanism of nuclear Ca 2+ spiking and the primary role of DMI1 (a nuclear envelope-localized cation channel) in its initiation and maintenance (13,18,(20)(21)(22). Downstream decoding of Ca 2+ spiking involves the nuclear Ca…”

The role of DMI1 in establishing Ca2+oscillations in legume symbioses

“…As explained in our recent study, we envisage the membrane potential of the nuclear envelope to be negatively charged on the nucleoplasmic side relative to the perinuclear space 3 . In this context our mathematical model reveals that Ca 2+ spiking is only initiated upon the simultaneous activation of both DMI1 and the Ca 2+ channel; we hypothesize that this may be triggered by unidentified symbiotic secondary messengers.…”

“…In a recent study 3 we presented a mathematical model based on three key components involved in the production of the Ca 2+ oscillations in the SYM pathway: a cation channel, 4 , 5 a Ca 2+ pump 2 and an as yet unidentified Ca 2+ channel 1 . The components involved in the model are located on the inner nuclear membrane 2 and therefore the model hypothesizes that the lumen of the nuclear envelope contiguous with the ER is the Ca 2+ store.…”