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      Disruption of actin filaments induces mitochondrial Ca 2+ release to the cytoplasm and [Ca 2+] c changes in Arabidopsis root hairs

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          Abstract

          Background

          Mitochondria are dynamic organelles that move along actin filaments, and serve as calcium stores in plant cells. The positioning and dynamics of mitochondria depend on membrane-cytoskeleton interactions, but it is not clear whether microfilament cytoskeleton has a direct effect on mitochondrial function and Ca 2+ storage. Therefore, we designed a series of experiments to clarify the effects of actin filaments on mitochondrial Ca 2+ storage, cytoplasmic Ca 2+ concentration ([Ca 2+] c), and the interaction between mitochondrial Ca 2+ and cytoplasmic Ca 2+ in Arabidopsis root hairs.

          Results

          In this study, we found that treatments with latrunculin B (Lat-B) and jasplakinolide (Jas), which depolymerize and polymerize actin filaments respectively, decreased membrane potential and Ca 2+ stores in the mitochondria of Arabidopsis root hairs. Simultaneously, these treatments induced an instantaneous increase of cytoplasmic Ca 2+, followed by a continuous decrease. All of these effects were inhibited by pretreatment with cyclosporin A (Cs A), a representative blocker of the mitochondrial permeability transition pore (mPTP). Moreover, we found there was a Ca 2+ concentration gradient in mitochondria from the tip to the base of the root hair, and this gradient could be disrupted by actin-acting drugs.

          Conclusions

          Based on these results, we concluded that the disruption of actin filaments caused by Lat-B or Jas promoted irreversible opening of the mPTP, resulting in mitochondrial Ca 2+ release into the cytoplasm, and consequent changes in [Ca 2+] c. We suggest that normal polymerization and depolymerization of actin filaments are essential for mitochondrial Ca 2+ storage in root hairs.

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          Most cited references67

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          Cellular motility driven by assembly and disassembly of actin filaments.

          Motile cells extend a leading edge by assembling a branched network of actin filaments that produces physical force as the polymers grow beneath the plasma membrane. A core set of proteins including actin, Arp2/3 complex, profilin, capping protein, and ADF/cofilin can reconstitute the process in vitro, and mathematical models of the constituent reactions predict the rate of motion. Signaling pathways converging on WASp/Scar proteins regulate the activity of Arp2/3 complex, which mediates the initiation of new filaments as branches on preexisting filaments. After a brief spurt of growth, capping protein terminates the elongation of the filaments. After filaments have aged by hydrolysis of their bound ATP and dissociation of the gamma phosphate, ADF/cofilin proteins promote debranching and depolymerization. Profilin catalyzes the exchange of ADP for ATP, refilling the pool of ATP-actin monomers bound to profilin, ready for elongation.
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            Calcium: a central regulator of plant growth and development.

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              Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development.

              Nonselective cation channels (NSCCs) catalyse passive fluxes of cations through plant membranes. NSCCs do not, or only to a small extent, select between monovalent cations, and several are also permeable to divalent cations. Although a number of NSCC genes has been identified in plant genomes, a direct correlation between gene products and in vivo observed currents is still largely absent for most NSCCs. In this review, physiological functions and molecular properties of NSCCs are critically discussed. Recent studies have demonstrated that NSCCs are directly involved in a multitude of stress responses, growth and development, uptake of nutrients and calcium signalling. NSCCs can also function in the perception of external stimuli and as signal transducers for reactive oxygen species, pathogen elicitors, cyclic nucleotides, membrane stretch, amino acids and purines.
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                Author and article information

                Journal
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central
                1471-2229
                2010
                24 March 2010
                : 10
                : 53
                Affiliations
                [1 ]Key Laboratory of Photosynthesis and Molecular Environmental Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
                [2 ]Graduate School of Chinese Academy of Sciences, Beijing 100049, China
                [3 ]College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China
                [4 ]Institute of Cellular and Molecular Botany, University of Bonn, Department of Plant Cell Biology, Kirschallee 1, D-53115 Bonn, Germany
                [5 ]Centre of the Region Hana for Biotechnological and Agricultural Research, Faculty of Science, Palacky University, 78301 Olomouc, Czech Republic
                Article
                1471-2229-10-53
                10.1186/1471-2229-10-53
                2923527
                20334630
                2e1501ff-7a9b-46f3-bed5-8f16eb8eba43
                Copyright ©2010 Wang et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 20 July 2009
                : 24 March 2010
                Categories
                Research Article

                Plant science & Botany
                Plant science & Botany

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