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

The key physiological event essential to the establishment of nitrogen-fixing bacteria and phosphate-delivering arbuscular mycorrhizal symbioses is the induction of nuclear calcium oscillations that are required for endosymbioses. These regular fluctuations in nucleoplasmic calcium concentrations ar...

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Autores principales: del Cerro, Pablo, Cook, Nicola M., Huisman, Rik, Dangeville, Pierre, Grubb, Lauren E., Marchal, Clemence, Ho Ching Lam, Anson, Charpentier, Myriam
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9060481/
https://www.ncbi.nlm.nih.gov/pubmed/35324326
http://dx.doi.org/10.1073/pnas.2200099119
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author del Cerro, Pablo
Cook, Nicola M.
Huisman, Rik
Dangeville, Pierre
Grubb, Lauren E.
Marchal, Clemence
Ho Ching Lam, Anson
Charpentier, Myriam
author_facet del Cerro, Pablo
Cook, Nicola M.
Huisman, Rik
Dangeville, Pierre
Grubb, Lauren E.
Marchal, Clemence
Ho Ching Lam, Anson
Charpentier, Myriam
author_sort del Cerro, Pablo
collection PubMed
description The key physiological event essential to the establishment of nitrogen-fixing bacteria and phosphate-delivering arbuscular mycorrhizal symbioses is the induction of nuclear calcium oscillations that are required for endosymbioses. These regular fluctuations in nucleoplasmic calcium concentrations are generated by ion channels and a pump located at the nuclear envelope, including the CYCLIC NUCLEOTIDE GATED CHANNEL 15 (CNGC15). However, how the CNGC15s are regulated in planta to sustain a calcium oscillatory mechanism remains unknown. Here, we demonstrate that the CNGC15s are regulated by the calcium-bound form of the calmodulin 2 (holo-CaM2), which, upon release of calcium, provides negative feedback to close the CNGC15s. Combining structural and evolutionary analyses of CaM residues with bioinformatic analysis, we engineered a holo-CaM2 with an increased affinity for CNGC15s. In planta, the expression of the engineered holo-CaM2 accelerates the calcium oscillation frequency, early endosymbioses signaling and is sufficient to sustain over time an enhanced root nodule symbiosis but not an increased arbuscular mycorrhization. Together, these results reveal that holo-CaM2 is a component of endosymbiosis signaling required to modulate CNGC15s activity and the downstream root nodule symbiosis pathway.
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spelling pubmed-90604812022-05-03 Engineered CaM2 modulates nuclear calcium oscillation and enhances legume root nodule symbiosis del Cerro, Pablo Cook, Nicola M. Huisman, Rik Dangeville, Pierre Grubb, Lauren E. Marchal, Clemence Ho Ching Lam, Anson Charpentier, Myriam Proc Natl Acad Sci U S A Biological Sciences The key physiological event essential to the establishment of nitrogen-fixing bacteria and phosphate-delivering arbuscular mycorrhizal symbioses is the induction of nuclear calcium oscillations that are required for endosymbioses. These regular fluctuations in nucleoplasmic calcium concentrations are generated by ion channels and a pump located at the nuclear envelope, including the CYCLIC NUCLEOTIDE GATED CHANNEL 15 (CNGC15). However, how the CNGC15s are regulated in planta to sustain a calcium oscillatory mechanism remains unknown. Here, we demonstrate that the CNGC15s are regulated by the calcium-bound form of the calmodulin 2 (holo-CaM2), which, upon release of calcium, provides negative feedback to close the CNGC15s. Combining structural and evolutionary analyses of CaM residues with bioinformatic analysis, we engineered a holo-CaM2 with an increased affinity for CNGC15s. In planta, the expression of the engineered holo-CaM2 accelerates the calcium oscillation frequency, early endosymbioses signaling and is sufficient to sustain over time an enhanced root nodule symbiosis but not an increased arbuscular mycorrhization. Together, these results reveal that holo-CaM2 is a component of endosymbiosis signaling required to modulate CNGC15s activity and the downstream root nodule symbiosis pathway. National Academy of Sciences 2022-03-24 2022-03-29 /pmc/articles/PMC9060481/ /pubmed/35324326 http://dx.doi.org/10.1073/pnas.2200099119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
del Cerro, Pablo
Cook, Nicola M.
Huisman, Rik
Dangeville, Pierre
Grubb, Lauren E.
Marchal, Clemence
Ho Ching Lam, Anson
Charpentier, Myriam
Engineered CaM2 modulates nuclear calcium oscillation and enhances legume root nodule symbiosis
title Engineered CaM2 modulates nuclear calcium oscillation and enhances legume root nodule symbiosis
title_full Engineered CaM2 modulates nuclear calcium oscillation and enhances legume root nodule symbiosis
title_fullStr Engineered CaM2 modulates nuclear calcium oscillation and enhances legume root nodule symbiosis
title_full_unstemmed Engineered CaM2 modulates nuclear calcium oscillation and enhances legume root nodule symbiosis
title_short Engineered CaM2 modulates nuclear calcium oscillation and enhances legume root nodule symbiosis
title_sort engineered cam2 modulates nuclear calcium oscillation and enhances legume root nodule symbiosis
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9060481/
https://www.ncbi.nlm.nih.gov/pubmed/35324326
http://dx.doi.org/10.1073/pnas.2200099119
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