The role of DMI1 in establishing Ca<sup>2+</sup>oscillations in legume symbioses

Charpentier, Myriam; Martins, Teresa Vaz; Granqvist, Emma; Oldroyd, Giles; Morris, Richard J.

doi:10.4161/psb.22894

Cited by 22 publications

(20 citation statements)

References 10 publications

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“…This demonstrates that the apoplast is an important Ca 2+ source for flg22‐induced oscillations and that Ca 2+ influx over the plasma membrane is required to sustain the response. By contrast, inhibitor and modelling studies demonstrated that Ca 2+ oscillations induced during symbiosis signalling do not depend on extracellular Ca 2+ (Engstrom et al ., ; Charpentier et al ., ), further demonstrating a difference in their way of generation.…”

Section: Discussionmentioning

confidence: 95%

Cytosolic calcium signals elicited by the pathogen‐associated molecular pattern flg22 in stomatal guard cells are of an oscillatory nature

Thor

Peiter

2014

New Phytologist

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SummaryChanges in cytosolic free calcium ([Ca 2+ ] cyt ) are an early and essential element of signalling networks activated by the perception of pathogen-associated molecular patterns (PAMPs), such as flg22. The flg22-induced calcium signal has been described on whole-plant, but not on singlecell scale so far. Also, the Ca 2+ sources and channels contributing to its generation are still obscure. Ratiometric fluorescence imaging employing the calcium reporter Yellow Cameleon 3.6 was performed to analyse the flg22-induced calcium signature in single guard cells of Arabidopsis thaliana. Calcium stores and channel types involved in its generation were determined by a pharmacological approach.In contrast to the calcium signal determined on whole-plant level, the signature on single-cell level is not characterized by one sustained response, but by oscillations in [Ca 2+ ] cyt . These oscillations were abolished by EGTA and lanthanum, as well as by U73122, neomycin and TMB-8, but only partially or not at all affected by inhibitors of glutamate receptor-like channels and cyclic nucleotide-gated channels.Our analyses suggest that the response observed on whole-plant level is the summary of oscillations occurring in single cells. Parallel to external calcium, influx via channels located at internal stores contributes to the signal.

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Section: Discussionmentioning

confidence: 95%

Cytosolic calcium signals elicited by the pathogen‐associated molecular pattern flg22 in stomatal guard cells are of an oscillatory nature

Thor

Peiter

2014

New Phytologist

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“…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…”

mentioning

confidence: 99%

A role for the mevalonate pathway in early plant symbiotic signaling

Venkateshwaran

Jayaraman

Chabaud

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

115

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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 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.

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“…Already several components of the Ca 2+ nuclear signalling machinery have been identified, which according to mathematical models [10] can be enough to sustain periodic oscillations, once Ca 2+ spiking is initiated. These mechanistic models are valid if several unknown parameters are tuned adequately.…”

Section: Ca 2+ Signals and Other Signals At The Tipmentioning

confidence: 99%

“…This has profoundly impacted the field, as it indicated where to look for the components of the Ca 2+ signalling machinery. This inspired mathematical models [10,11], which attempted to explain the generation of Ca 2+ signals.…”

Section: Introductionmentioning

confidence: 99%

What Drives Symbiotic Calcium Signalling In Legumes? Insights And Challenges Of Imaging

Martins

Livina

2019

Preprint

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We review the contribution of bioimaging in building a coherent understanding of Ca 2+ signalling during legume-bacteria symbiosis. Currently, two different calcium signals are believed to control key steps of the symbiosis: a Ca 2+ gradient at the tip of the legume root hair is involved in the development of an infection thread, while nuclear Ca 2+ oscillations, the hallmark signal of this symbiosis, controls the formation of the root nodule, where bacteria fix nitrogen. Additionally, different Ca 2+ spiking signatures have been associated with specific infection stages. Bioimaging is intrinsically a cross-disciplinary area that requires integration of image recording, processing and analysis. We use experimental examples to critically evaluate previously established conclusions and draw attention to challenges caused by the varying nature of the signal-to-noise ratio in live imaging. We hypothesise that nuclear Ca 2+ spiking is a wide-range signal involving the entire root hair, and that Ca 2+ signature may be related to cytoplasmic streaming.

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

Cited by 22 publications

References 10 publications

Cytosolic calcium signals elicited by the pathogen‐associated molecular pattern flg22 in stomatal guard cells are of an oscillatory nature

Cytosolic calcium signals elicited by the pathogen‐associated molecular pattern flg22 in stomatal guard cells are of an oscillatory nature

A role for the mevalonate pathway in early plant symbiotic signaling

What Drives Symbiotic Calcium Signalling In Legumes? Insights And Challenges Of Imaging

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

Cited by 22 publications

References 10 publications

Cytosolic calcium signals elicited by the pathogen‐associated molecular pattern flg22 in stomatal guard cells are of an oscillatory nature

Cytosolic calcium signals elicited by the pathogen‐associated molecular pattern flg22 in stomatal guard cells are of an oscillatory nature

A role for the mevalonate pathway in early plant symbiotic signaling

What Drives Symbiotic Calcium Signalling In Legumes? Insights And Challenges Of Imaging

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