Buffering Capacity Explains Signal Variation in Symbiotic Calcium Oscillations

Emma Granqvist,Wojciech Kozlowski,Krasimira Tsaneva-Atanasova,Myriam Charpentier,Derin Wysham,Pauline Haleux,J Allan Downie,Teresa Vaz Martins,Jongho Sun,Richard J Morris,Giles E.D Oldroyd,Saul Hazledine

doi:10.1104/pp.112.205682

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.

Highlights

Legumes form symbioses with rhizobial bacteria and arbuscular mycorrhizal fungi that aid plant nutrition
We propose a mathematical model based on three key proteins; a Ca2+ ATPase, a voltagegated Ca2+ channel, and the cation channel Doesn’t Make Infections1 (DMI1)
The K+ channel represents the protein DMI1 (Venkateshwaran et al, 2012), which is modeled as a driver of changes in membrane voltage (Table I; Supplemental Fig. S5)

Summary

Introduction

Legumes form symbioses with rhizobial bacteria and arbuscular mycorrhizal fungi that aid plant nutrition. In addition to the symbiotic relationship with arbuscular mycorrhizal fungi that many plants establish in order to secure their uptake of water, phosphorus, and other nutrients (Harrison, 2005; Parniske, 2008), legumes have developed interactions with bacteria called rhizobia, Root symbioses initiate with signal exchanges in the soil. Upon receiving diffusible signals from the microsymbionts, the plant roots initiate developmental programs that lead to infection by rhizobia or arbuscular mycorrhizal fungi Both programs employ the same signaling pathway with several components being common to both mycorrhizal and rhizobial interactions (Kistner and Parniske, 2002; Lima et al, 2009). CASTOR and POLLUX, as well as calcium calmodulin-dependent protein kinase, are highly conserved both in legumes and nonlegumes (Banba et al, 2008; Chen et al, 2009) This highlights the essential role of the Ca2+ oscillations in mycorrhizal signaling

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