Stochastic Spatial Heterogeneity in Activities of H<sup>+</sup>-ATP-Ases in Electrically Connected Plant Cells Decreases Threshold for Cooling-Induced Electrical Responses

H<sup>+</sup>-ATP-ases, which support proton efflux through the plasma membrane, are key molecular transporters for electrogenesis in cells of higher plants. Initial activities of the transporters can influence the thresholds of generation of electrical responses induced by stressors and...

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Main Authors: Ekaterina Sukhova, Daria Ratnitsyna, Vladimir Sukhov
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/22/15/8254
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author Ekaterina Sukhova
Daria Ratnitsyna
Vladimir Sukhov
author_facet Ekaterina Sukhova
Daria Ratnitsyna
Vladimir Sukhov
author_sort Ekaterina Sukhova
collection DOAJ
description H<sup>+</sup>-ATP-ases, which support proton efflux through the plasma membrane, are key molecular transporters for electrogenesis in cells of higher plants. Initial activities of the transporters can influence the thresholds of generation of electrical responses induced by stressors and modify other parameters of these responses. Previously, it was theoretically shown that the stochastic heterogeneity of individual cell thresholds for electrical responses in a system of electrically connected neuronal cells can decrease the total threshold of the system (“diversity-induced resonance”, DIR). In the current work, we tested a hypothesis about decreasing the thresholds of generation of cooling-induced electrical responses in a system of electrically connected plant cells with increasing stochastic spatial heterogeny in the initial activities of H<sup>+</sup>-ATP-ases in these cells. A two-dimensional model of the system of electrically connected excitable cells (simple imitation of plant leaf), which was based on a model previously developed in our works, was used for the present investigation. Simulation showed that increasing dispersion in the distribution of initial activities of H<sup>+</sup>-ATP-ases between cells decreased the thresholds of generation of cooling-induced electrical responses. In addition, the increasing weakly influenced the amplitudes of electrical responses. Additional analysis showed two different mechanisms of the revealed effect. The increasing spatial heterogeneity in activities of H<sup>+</sup>-ATP-ases induced a weak positive shift of the membrane potential at rest. The shift decreased the threshold of electrical response generation. However, the decreased threshold induced by increasing the H<sup>+</sup>-ATP-ase activity heterogeneity was also observed after the elimination of the positive shift. The result showed that the “DIR-like” mechanism also participated in the revealed effect. Finally, we showed that the standard deviation of the membrane potentials before the induction of action potentials could be used for the estimation of thresholds of cooling-induced plant electrical responses. Thus, spatial heterogeneity in the initial activities of H<sup>+</sup>-ATP-ases can be a new regulatory mechanism influencing the generation of electrical responses in plants under actions of stressors.
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spelling doaj.art-bd24d295332149aeb9901a6b75b51f292023-11-22T05:45:37ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-07-012215825410.3390/ijms22158254Stochastic Spatial Heterogeneity in Activities of H<sup>+</sup>-ATP-Ases in Electrically Connected Plant Cells Decreases Threshold for Cooling-Induced Electrical ResponsesEkaterina Sukhova0Daria Ratnitsyna1Vladimir Sukhov2Department of Biophysics, N.I. Lobachevsky State University of Nizhny Novgorod, 603950 Nizhny Novgorod, RussiaDepartment of Biophysics, N.I. Lobachevsky State University of Nizhny Novgorod, 603950 Nizhny Novgorod, RussiaDepartment of Biophysics, N.I. Lobachevsky State University of Nizhny Novgorod, 603950 Nizhny Novgorod, RussiaH<sup>+</sup>-ATP-ases, which support proton efflux through the plasma membrane, are key molecular transporters for electrogenesis in cells of higher plants. Initial activities of the transporters can influence the thresholds of generation of electrical responses induced by stressors and modify other parameters of these responses. Previously, it was theoretically shown that the stochastic heterogeneity of individual cell thresholds for electrical responses in a system of electrically connected neuronal cells can decrease the total threshold of the system (“diversity-induced resonance”, DIR). In the current work, we tested a hypothesis about decreasing the thresholds of generation of cooling-induced electrical responses in a system of electrically connected plant cells with increasing stochastic spatial heterogeny in the initial activities of H<sup>+</sup>-ATP-ases in these cells. A two-dimensional model of the system of electrically connected excitable cells (simple imitation of plant leaf), which was based on a model previously developed in our works, was used for the present investigation. Simulation showed that increasing dispersion in the distribution of initial activities of H<sup>+</sup>-ATP-ases between cells decreased the thresholds of generation of cooling-induced electrical responses. In addition, the increasing weakly influenced the amplitudes of electrical responses. Additional analysis showed two different mechanisms of the revealed effect. The increasing spatial heterogeneity in activities of H<sup>+</sup>-ATP-ases induced a weak positive shift of the membrane potential at rest. The shift decreased the threshold of electrical response generation. However, the decreased threshold induced by increasing the H<sup>+</sup>-ATP-ase activity heterogeneity was also observed after the elimination of the positive shift. The result showed that the “DIR-like” mechanism also participated in the revealed effect. Finally, we showed that the standard deviation of the membrane potentials before the induction of action potentials could be used for the estimation of thresholds of cooling-induced plant electrical responses. Thus, spatial heterogeneity in the initial activities of H<sup>+</sup>-ATP-ases can be a new regulatory mechanism influencing the generation of electrical responses in plants under actions of stressors.https://www.mdpi.com/1422-0067/22/15/8254H<sup>+</sup>-ATP-aseplant electrical responsesstochastic spatial heterogeneitydiversity-induced resonancecoolingsimulation
spellingShingle Ekaterina Sukhova
Daria Ratnitsyna
Vladimir Sukhov
Stochastic Spatial Heterogeneity in Activities of H<sup>+</sup>-ATP-Ases in Electrically Connected Plant Cells Decreases Threshold for Cooling-Induced Electrical Responses
International Journal of Molecular Sciences
H<sup>+</sup>-ATP-ase
plant electrical responses
stochastic spatial heterogeneity
diversity-induced resonance
cooling
simulation
title Stochastic Spatial Heterogeneity in Activities of H<sup>+</sup>-ATP-Ases in Electrically Connected Plant Cells Decreases Threshold for Cooling-Induced Electrical Responses
title_full Stochastic Spatial Heterogeneity in Activities of H<sup>+</sup>-ATP-Ases in Electrically Connected Plant Cells Decreases Threshold for Cooling-Induced Electrical Responses
title_fullStr Stochastic Spatial Heterogeneity in Activities of H<sup>+</sup>-ATP-Ases in Electrically Connected Plant Cells Decreases Threshold for Cooling-Induced Electrical Responses
title_full_unstemmed Stochastic Spatial Heterogeneity in Activities of H<sup>+</sup>-ATP-Ases in Electrically Connected Plant Cells Decreases Threshold for Cooling-Induced Electrical Responses
title_short Stochastic Spatial Heterogeneity in Activities of H<sup>+</sup>-ATP-Ases in Electrically Connected Plant Cells Decreases Threshold for Cooling-Induced Electrical Responses
title_sort stochastic spatial heterogeneity in activities of h sup sup atp ases in electrically connected plant cells decreases threshold for cooling induced electrical responses
topic H<sup>+</sup>-ATP-ase
plant electrical responses
stochastic spatial heterogeneity
diversity-induced resonance
cooling
simulation
url https://www.mdpi.com/1422-0067/22/15/8254
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AT dariaratnitsyna stochasticspatialheterogeneityinactivitiesofhsupsupatpasesinelectricallyconnectedplantcellsdecreasesthresholdforcoolinginducedelectricalresponses
AT vladimirsukhov stochasticspatialheterogeneityinactivitiesofhsupsupatpasesinelectricallyconnectedplantcellsdecreasesthresholdforcoolinginducedelectricalresponses