Acidic Stress Induces Cytosolic Free Calcium Oscillation, and an Appropriate Low pH Helps Maintain the Circadian Clock in Arabidopsis

Acidic stress is a formidable environmental factor that exerts adverse effects on plant growth and development, ultimately leading to a potential reduction in agricultural productivity. A low pH triggers Ca<sup>2+</sup> influx across the plasma membrane (PM), eliciting distinct responses...

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Main Authors: Wei Chen, Jing Xu, Jia Chen, Jun-Feng Wang, Shu Zhang, Zhen-Ming Pei
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/13/21/3107
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author Wei Chen
Jing Xu
Jia Chen
Jun-Feng Wang
Shu Zhang
Zhen-Ming Pei
author_facet Wei Chen
Jing Xu
Jia Chen
Jun-Feng Wang
Shu Zhang
Zhen-Ming Pei
author_sort Wei Chen
collection DOAJ
description Acidic stress is a formidable environmental factor that exerts adverse effects on plant growth and development, ultimately leading to a potential reduction in agricultural productivity. A low pH triggers Ca<sup>2+</sup> influx across the plasma membrane (PM), eliciting distinct responses under various acidic pH levels. However, the underlying mechanisms by which Arabidopsis plant cells generate stimulus-specific Ca<sup>2+</sup> signals in response to acidic stress remain largely unexplored. The experimentally induced stimulus may elicit spikes in cytosolic free Ca<sup>2+</sup> concentration ([Ca<sup>2+</sup>]<sub>i</sub>) spikes or complex [Ca<sup>2+</sup>]<sub>i</sub> oscillations that persist for 20 min over a long-term of 24 h or even several days within the plant cytosol and chloroplast. This study investigated the increase in [Ca<sup>2+</sup>]<sub>i</sub> under a gradient of low pH stress ranging from pH 3.0 to 6.0. Notably, the peak of [Ca<sup>2+</sup>]<sub>i</sub> elevation was lower at pH 4.0 than at pH 3.0 during the initial 8 h, while other pH levels did not significantly increase [Ca<sup>2+</sup>]<sub>i</sub> compared to low acidic stress conditions. Lanthanum chloride (LaCl<sub>3</sub>) can effectively suppress the influx of [Ca<sup>2+</sup>]<sub>i</sub> from the apoplastic to the cytoplasm in plants under acid stress, with no discernible difference in intracellular calcium levels observed in Arabidopsis. Following 8 h of acid treatment in the darkness, the intracellular baseline Ca<sup>2+</sup> levels in Arabidopsis were significantly elevated when exposed to low pH stress. A moderately low pH, specifically 4.0, may function as a spatial-temporal input into the circadian clock system. These findings suggest that acid stimulation can exert a continuous influence on intracellular calcium levels, as well as plant growth and development.
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spelling doaj-art-b458098cd8b745dca3d3f9cbc53ea4a52024-11-08T14:39:39ZengMDPI AGPlants2223-77472024-11-011321310710.3390/plants13213107Acidic Stress Induces Cytosolic Free Calcium Oscillation, and an Appropriate Low pH Helps Maintain the Circadian Clock in ArabidopsisWei Chen0Jing Xu1Jia Chen2Jun-Feng Wang3Shu Zhang4Zhen-Ming Pei5College of Life Sciences, Zhejiang University, Hangzhou 310027, ChinaCenter on Plant Environmental Sensing, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310036, ChinaCenter on Plant Environmental Sensing, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310036, ChinaInstitute of Vegetables, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaInstitute of Vegetables, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaDepartment of Biology, Duke University, Durham, NC 27708, USAAcidic stress is a formidable environmental factor that exerts adverse effects on plant growth and development, ultimately leading to a potential reduction in agricultural productivity. A low pH triggers Ca<sup>2+</sup> influx across the plasma membrane (PM), eliciting distinct responses under various acidic pH levels. However, the underlying mechanisms by which Arabidopsis plant cells generate stimulus-specific Ca<sup>2+</sup> signals in response to acidic stress remain largely unexplored. The experimentally induced stimulus may elicit spikes in cytosolic free Ca<sup>2+</sup> concentration ([Ca<sup>2+</sup>]<sub>i</sub>) spikes or complex [Ca<sup>2+</sup>]<sub>i</sub> oscillations that persist for 20 min over a long-term of 24 h or even several days within the plant cytosol and chloroplast. This study investigated the increase in [Ca<sup>2+</sup>]<sub>i</sub> under a gradient of low pH stress ranging from pH 3.0 to 6.0. Notably, the peak of [Ca<sup>2+</sup>]<sub>i</sub> elevation was lower at pH 4.0 than at pH 3.0 during the initial 8 h, while other pH levels did not significantly increase [Ca<sup>2+</sup>]<sub>i</sub> compared to low acidic stress conditions. Lanthanum chloride (LaCl<sub>3</sub>) can effectively suppress the influx of [Ca<sup>2+</sup>]<sub>i</sub> from the apoplastic to the cytoplasm in plants under acid stress, with no discernible difference in intracellular calcium levels observed in Arabidopsis. Following 8 h of acid treatment in the darkness, the intracellular baseline Ca<sup>2+</sup> levels in Arabidopsis were significantly elevated when exposed to low pH stress. A moderately low pH, specifically 4.0, may function as a spatial-temporal input into the circadian clock system. These findings suggest that acid stimulation can exert a continuous influence on intracellular calcium levels, as well as plant growth and development.https://www.mdpi.com/2223-7747/13/21/3107<i>Arabidopsis thaliana</i>calcium imagingaequorincalcium signalingbasal cytosolic Ca<sup>2+</sup> levelacid stress
spellingShingle Wei Chen
Jing Xu
Jia Chen
Jun-Feng Wang
Shu Zhang
Zhen-Ming Pei
Acidic Stress Induces Cytosolic Free Calcium Oscillation, and an Appropriate Low pH Helps Maintain the Circadian Clock in Arabidopsis
Plants
<i>Arabidopsis thaliana</i>
calcium imaging
aequorin
calcium signaling
basal cytosolic Ca<sup>2+</sup> level
acid stress
title Acidic Stress Induces Cytosolic Free Calcium Oscillation, and an Appropriate Low pH Helps Maintain the Circadian Clock in Arabidopsis
title_full Acidic Stress Induces Cytosolic Free Calcium Oscillation, and an Appropriate Low pH Helps Maintain the Circadian Clock in Arabidopsis
title_fullStr Acidic Stress Induces Cytosolic Free Calcium Oscillation, and an Appropriate Low pH Helps Maintain the Circadian Clock in Arabidopsis
title_full_unstemmed Acidic Stress Induces Cytosolic Free Calcium Oscillation, and an Appropriate Low pH Helps Maintain the Circadian Clock in Arabidopsis
title_short Acidic Stress Induces Cytosolic Free Calcium Oscillation, and an Appropriate Low pH Helps Maintain the Circadian Clock in Arabidopsis
title_sort acidic stress induces cytosolic free calcium oscillation and an appropriate low ph helps maintain the circadian clock in arabidopsis
topic <i>Arabidopsis thaliana</i>
calcium imaging
aequorin
calcium signaling
basal cytosolic Ca<sup>2+</sup> level
acid stress
url https://www.mdpi.com/2223-7747/13/21/3107
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