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A role for the mevalonate pathway in early plant symbiotic signaling
Thursday, 2015/08/06 | 13:28:09
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Muthusubramanian Venkateshwaran, Dhileepkumar Jayaraman, Mireille Chabaud, Andrea Genre, Allison J. Balloon, Junko Maeda, Kari Forshey, Désirée den Os, Nicholas W. Kwiecien, Joshua J. Coon, David G. Barker, and Jean-Michel Ané SignificanceMetabolites of the mevalonate (MVA) pathway play essential roles in the regulation of growth and development in many organisms. In this study, we demonstrate that a key regulatory enzyme of the MVA pathway is directly involved in the signaling pathway that transduces endosymbiotic microbial signals in Medicago truncatula. Furthermore, we show that exogenous MVA application is sufficient to activate this transduction pathway. The use of mutants in the signaling pathway and a heterologous expression system provides evidence that the MVA pathway is a missing link between the initial perception of microbial signals at the host plasma membrane and the regulation of symbiotic gene expression in the nucleus. AbstractRhizobia 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 Ca2+ concentration (Ca2+ spiking), which in turn leads to gene expression and downstream symbiotic responses. The activation of Ca2+ 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 Ca2+ 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 Ca2+ spiking and symbiotic gene expression in both wild-type plants and dmi2 mutants, but interestingly not in dmi1 mutants. Finally, MVA induced Ca2+ spiking in Human Embryonic Kidney 293 cells expressing DMI1. This demonstrates that the nuclear cation channel DMI1 is sufficient to support MVA-induced Ca2+ spiking in this heterologous system. See http://www.pnas.org/content/112/31/9781.abstract.html?etoc PNAS August 4, 2015 vol. 112 no. 31 9781-9786
Fig. 5. Model illustrating the proposed role of MVA within the common symbiosis pathway. Nod and Myc factors are perceived at the plasma membrane by a complex including the receptor-like kinase DMI2, interacting with either the Nod factor receptor component NFP or the so far unidentified Myc factor receptor. Based on our observations, we propose that HMGR1—which is known to interact with DMI2—generates MVA as a second messenger, transducing the signal from the plasma membrane to the nuclear compartment where DMI1, the nuclear envelope-localized cation channel, is required for the initiation of nuclear Ca2+ spiking. This Ca2+ response is then decoded by the Ca2+ and calmodulin-dependent kinase DMI3, which in turn leads to downstream endosymbiosis-related gene activation. In our experiments, the exogenous application of MVA is sufficient to activate the common symbiosis pathway and trigger nuclear Ca2+ spiking in the absence of receptor activation. |
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