Disruption of actin filaments induces mitochondrial Ca2+ release to the cytoplasm and [Ca2+]c changes in Arabidopsis root hairs

BMC Plant Biol. 2010 Mar 24:10:53. doi: 10.1186/1471-2229-10-53.

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 Ca2+ storage. Therefore, we designed a series of experiments to clarify the effects of actin filaments on mitochondrial Ca2+ storage, cytoplasmic Ca2+ concentration ([Ca2+]c), and the interaction between mitochondrial Ca2+ and cytoplasmic Ca2+ 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 Ca2+ stores in the mitochondria of Arabidopsis root hairs. Simultaneously, these treatments induced an instantaneous increase of cytoplasmic Ca2+, 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 Ca2+ 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 Ca2+ release into the cytoplasm, and consequent changes in [Ca2+]c. We suggest that normal polymerization and depolymerization of actin filaments are essential for mitochondrial Ca2+ storage in root hairs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / drug effects
  • Actin Cytoskeleton / metabolism*
  • Arabidopsis / cytology
  • Arabidopsis / drug effects
  • Arabidopsis / metabolism*
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Calcium / metabolism*
  • Depsipeptides / pharmacology
  • Electrodes
  • Endoplasmic Reticulum / drug effects
  • Endoplasmic Reticulum / metabolism
  • Fluoresceins / metabolism
  • Fluorescence
  • Intracellular Space / drug effects
  • Intracellular Space / metabolism
  • Membrane Potential, Mitochondrial / drug effects
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Mitochondrial Membrane Transport Proteins / metabolism
  • Mitochondrial Permeability Transition Pore
  • Models, Biological
  • Plant Roots / cytology
  • Plant Roots / drug effects
  • Plant Roots / metabolism*
  • Thiazolidines / pharmacology

Substances

  • Bridged Bicyclo Compounds, Heterocyclic
  • Depsipeptides
  • Fluoresceins
  • Mitochondrial Membrane Transport Proteins
  • Mitochondrial Permeability Transition Pore
  • Thiazolidines
  • jasplakinolide
  • latrunculin B
  • Calcium
  • fluorexon