Engineered CaM2 modulates nuclear calcium oscillation and enhances legume root nodule symbiosis

SignificanceOscillations in intracellular calcium concentration play an essential role in the regulation of multiple cellular processes. In plants capable of root endosymbiosis with nitrogen-fixing bacteria and/or arbuscular mycorrhizal fungi, nuclear localized calcium oscillations are essential to...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 119; no. 13; p. e2200099119
Main Authors Del Cerro, Pablo, Cook, Nicola M, Huisman, Rik, Dangeville, Pierre, Grubb, Lauren E, Marchal, Clemence, Ho Ching Lam, Anson, Charpentier, Myriam
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 29.03.2022
Subjects
Arbuscular mycorrhizas
Bacteria
Biological Sciences
Calcium
Calcium Signaling - physiology
Calcium signalling
Calcium-binding protein
Calmodulin
Fabaceae
Ion channels
Legumes
Mycorrhizae - physiology
Negative feedback
Nitrogen fixation
Nitrogen-fixing bacteria
Nitrogenation
Nucleotides
Signaling
Symbiosis
calmodulin
calcium signaling
root legume symbiosis
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Summary:SignificanceOscillations in intracellular calcium concentration play an essential role in the regulation of multiple cellular processes. In plants capable of root endosymbiosis with nitrogen-fixing bacteria and/or arbuscular mycorrhizal fungi, nuclear localized calcium oscillations are essential to transduce the microbial signal. Although the ion channels required to generate the nuclear localized calcium oscillations have been identified, their mechanisms of regulation are unknown. Here, we combined proteomics and engineering approaches to demonstrate that the calcium-bound form of the calmodulin 2 (CaM2) associates with CYCLIC NUCLEOTIDE GATED CHANNEL 15 (CNGC15s), closing the channels and providing the negative feedback to sustain the oscillatory mechanism. We further unraveled that the engineered CaM2 accelerates early endosymbioses and enhanced root nodule symbiosis but not arbuscular mycorrhization.
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Edited by Sharon Long, Stanford University, Stanford, CA; received January 6, 2022; accepted February 22, 2022
Author contributions: M.C. designed research; P.d.C, N.M.C., R.H., P.D., L.E.G., C.M., and A.H.C.L. performed research; P.d.C., N.M.C., P.D., and M.C. analyzed data; and M.C. wrote the paper.
3Present address: The Sainsbury Laboratory, Norwich NR4 7UH, United Kingdom.
2Present address: Laboratory of Molecular Biology, 6708 PB, Wageningen, The Netherlands.
1P.d.C. and N.M.C contributed equally to this work.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2200099119