Multi-Scale Characean Experimental System: From Electrophysiology of Membrane Transporters to Cell-to-Cell Connectivity, Cytoplasmic Streaming and Auxin Metabolism

The morphology of characean algae could be mistaken for a higher plant: stem-like axes with leaf-like branchlets anchored in the soil by root-like rhizoids. However, all of these structures are made up of giant multinucleate cells separated by multicellular nodal complexes. The excised internodal cells survive long enough for the nodes to give rise to new thallus. The size of the internodes and their thick cytoplasmic layer minimize impalement injury and allow specific micro-electrode placement. The cell structure can be manipulated by centrifugation, perfusion of cell contents or creation of cytoplasmic droplets, allowing access to both vacuolar and cytoplasmic compartments and both sides of the cell membranes. Thousands of electrical measurements on intact or altered cells and cytoplasmic droplets laid down basis to modern plant electrophysiology. Furthermore, the giant internodal cells and whole thalli facilitate research into many other plant properties. As nutrients have to be transported from rhizoids to growing parts of the thallus and hormonal signals need to pass from cell to cell, Characeae possess very fast cytoplasmic streaming. The mechanism was resolved in the characean model. Plasmodesmata between the internodal cells and nodal complexes facilitate transport of ions, nutrients and photosynthates across the nodes. The internal structure was found to be similar to those of higher plants. Recent experiments suggest a strong circadian influence on metabolic pathways producing indole-3-acetic acid (IAA) and serotonin/melatonin. The review will discuss the impact of the characean models arising from fragments of cells, single cells, cell-to-cell transport or whole thalli on understanding of plant evolution and physiology.

• Publication year

  2016

• Venue

  Frontiers in Plant Science

• Publication date

  2016-07-25

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.3389/fpls.2016.01052PMID 27504112PMCID 4958633
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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• Streptophyte Terrestrialization in Light of Plastid Evolution.

  2016cited by this paper
• A physical perspective on cytoplasmic streaming

  2015cited by this paper
• Plant auxin biosynthesis did not originate in charophytes.

  2015cited by this paper
• Rethinking the Origin of Auxin Biosynthesis in Plants

  2015cited by this paper
• Circadian changes in endogenous concentrations of indole-3-acetic acid, melatonin, serotonin, abscisic acid and jasmonic acid in Characeae (Chara australis Brown)

  2015cited by this paper
• Salt tolerance at single cell level in giant-celled Characeae

  2015cited by this paper
• Origin of plant auxin biosynthesis in charophyte algae.

  2014cited by this paper
• Plasma Membrane-Targeted PIN Proteins Drive Shoot Development in a Moss

  2014cited by this paper
• Phylotranscriptomic analysis of the origin and early diversification of land plants

  2014cited by this paper
• Exploring emergent properties in cellular homeostasis using OnGuard to model K+ and other ion transport in guard cells☆☆☆

  2014cited by this paper
• Evolutionary aspects of non-cell-autonomous regulation in vascular plants: structural background and models to study

  2014cited by this paper
• From algae to angiosperms–inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes

  2014cited by this paper
• Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation

  2014cited by this paper
• Cation-permeable vacuolar ion channels in the moss Physcomitrella patens: a patch-clamp study

  2013cited by this paper
• Auxin metabolism and homeostasis during plant development

  2013cited by this paper
• Polar auxin transport in relation to long-distance transport of nutrients in the Charales.

  2013cited by this paper
• Intercellular Transport

  2013cited by this paper
• The Physiology of Characean Cells

  2013cited by this paper
• High Affinity Ammonium Transporters: Molecular Mechanism of Action

  2012cited by this paper
• Multiple horizontal gene transfers of ammonium transporters/ammonia permeases from prokaryotes to eukaryotes: toward a new functional and evolutionary classification.

  2012cited by this paper
• Broad Phylogenomic Sampling and the Sister Lineage of Land Plants

  2012cited by this paper
• pH Banding in Charophyte Algae

  2012cited by this paper
• Ion channels in plants.

  2012cited by this paper
• The pathway of auxin biosynthesis in plants.

  2012cited by this paper
• Plasmodesmata paradigm shift: regulation from without versus within.

  2012cited by this paper
• Polar auxin transport: an early invention

  2012cited by this paper
• Origin of land plants: Do conjugating green algae hold the key?

  2011cited by this paper
• High resolution scanning electron microscopy of plasmodesmata

  2011cited by this paper
• Phosphate Import in Plants: Focus on the PHT1 Transporters

  2011cited by this paper
• Mechanisms of Cl(-) transport contributing to salt tolerance.

  2010cited by this paper
• Unraveling the Evolution of Auxin Signaling1[C][W]

  2010cited by this paper
• Homologues of the Arabidopsis thaliana SHI/STY/LRP1 genes control auxin biosynthesis and affect growth and development in the moss Physcomitrella patens

  2010cited by this paper
• PHYSIOLOGICAL and BIOCHEMICAL ASPECTS

  2009cited by this paper
• Auxin transport routes in plant development

  2009cited by this paper
• Unique charge distribution in surface loops confers high velocity on the fast motor protein Chara myosin

  2009cited by this paper
• TRANSPORT OF POTASSIUM

  2009cited by this paper
• Molecular mechanisms of ammonium transport and accumulation in plants

  2007cited by this paper
• The sliding theory of cytoplasmic streaming: fifty years of progress

  2007cited by this paper
• The V-type H+ ATPase: molecular structure and function, physiological roles and regulation

  2006cited by this paper
• Vacuolar transporters and their essential role in plant metabolism.

  2006cited by this paper
• Argonaute—a database for gene regulation by mammalian microRNAs

  2005cited by this paper
• Mechanism of plasmodesmata formation in characean algae in relation to evolution of intercellular communication in higher plants

  2004cited by this paper
• Plasmodesmal changes are related to different developmental stages of antheridia of Chara species

  2003cited by this paper
• Induction of the Na+/Pi cotransport system in the plasma membrane of Chara corallina requires external Na+ and low levels of Pi

  2002cited by this paper
• The Closest Living Relatives of Land Plants

  2001cited by this paper
• Tonoplast Anion Channel Activity Modulation by pH in Chara corallina

  2001influential reference
• Physiological control of phosphate uptake and phosphate homeostasis in plant cells

  2001cited by this paper
• Phosphate uptake in Chara : membrane transport via Na/Pi cotransport

  2000cited by this paper
• The Moss, Physcomitrella patens

  2000cited by this paper
• Anion channels in higher plants: functional characterization, molecular structure and physiological role.

  2000cited by this paper
• Evolution of Plasmodesmata

  1999cited by this paper
• Regulation of Phosphate Transport and Homeostasis in Plant Cells

  1999cited by this paper
• Molecular cloning and sequencing of the cDNA for vacuolar H+-pyrophosphatase from Chara corallina1.

  1999cited by this paper
• Dual turgor regulation response to hypotonic stress in Lamprothamnium papulosum

  1999cited by this paper
• Anion Channels in Chara corallina Tonoplast Membrane: Calcium Dependence and Rectification

  1999cited by this paper
• Control of phosphate transport across the plasma membrane of Chara corallina

  1998cited by this paper
• Phosphate Uptake in the Cyanobacterium Synechococcus R-2 PCC 7942

  1997cited by this paper
• Comparative ultrastructure of plasmodesmata of Chara and selected bryophytes: toward an elucidation of the evolutionary origin of plant plasmodesmata.

  1997cited by this paper
• The Actions of Calmodulin Antagonists W-7 and TFP and of Calcium on the Gating Kinetics of the Calcium-activated Large Conductance Potassium Channel of the Chara Protoplasmic Drop: A Substate-sensitive Analysis

  1997cited by this paper
• The Physiological Relevance of Na+-Coupled K+-Transport

  1996cited by this paper
• Physiological and Biochemical Aspects of Cytoplasmic Streaming

  1994cited by this paper
• The H+/Cl- Symporter in Root-Hair Cells of Sinapis alba (An Electrophysiological Study Using Ion-Selective Microelectrodes)

  1994cited by this paper
• Sodium-coupled symports in the plasma membranes of plant cells.

  1994cited by this paper
• The regulation of ammonia uptake in Chara australis

  1994cited by this paper
• Depolarization-Activated K+ Channel in Chara Droplets

  1994cited by this paper
• Analysis of temperature dependence of cytoplasmic streaming using tonoplast-free cells of Characeae

  1993cited by this paper
• A nonlinear filter algorithm for the detection of jumps in patch-clamp data

  1993cited by this paper
• Cooperative behavior of K+ channels in the tonoplast of Chara corallina.

  1993cited by this paper
• The uptake and metabolism of urea by Chara australis: IV. Symport with sodium—A slip model for the high and low affinity systems

  1993cited by this paper
• Malate Accumulates in the Vacuole of Chara australis During Uptake of Ammonium From Chloride-free Solution

  1993cited by this paper
• Direct evidence for pressure-generated closure of plasmodesmata

  1992cited by this paper
• Quantitative Analysis of Intercellularly-Transported Photoassimilates in Chara corallina

  1992cited by this paper
• Seasonal patterns of cell-to-cell communication in Chara corallina Klein ex Willd. I: Cell-to-cell communication in vegetative lateral branches during winter and spring

  1992cited by this paper
• Multiple conductances in the large K+ channel from Chara corallina shown by a transient analysis method.

  1992cited by this paper
• Auxin dependent growth of rhizoids of Chara globularis

  1992cited by this paper
• Divalent cation block and competition between divalent and monovalent cations in the large-conductance K+ channel from Chara australis

  1992cited by this paper
• Light dependence of protoplasmic streaming in Nitella flexilis L. as measured by means of laser-velocimetry

  1992cited by this paper
• Seasonal patterns of cell‐to‐cell communication in Chara corallina Klein ex Willd. II. Cell‐to‐cell communication during the development of antheridia

  1992cited by this paper
• Intercellular communication in Chara: factors affecting transnodal electrical resistance and solute fluxes

  1992influential reference
• Quantitative Analysis of Single K+ Channels in the Tonoplast of Chara corallina: Selectivity and TEA Blockade

  1991cited by this paper
• Activation by Ca2+ and block by divalent ions of the K+ channel in the membrane of cytoplasmic drops fromChara australis

  1991influential reference
• Transport of potassium inChara australis: II. Kinetics of a symport with sodium

  1990cited by this paper
• [27] Electrophysiology of giant algal cells

  1989cited by this paper
• Current-voltage relationships of a sodium-sensitive potassium channel in the tonoplast ofChara corallina

  1989cited by this paper
• Transport of potassium inChara australis: I. A symport with sodium

  1989cited by this paper
• Ion permeation in a K+ channel inChara australis: Direct evidence for diffusion limitation of ion flow in a maxi-K channel

  1989cited by this paper
• Influence of Cytoplasmic Streaming and Turgor Pressure Gradient on the Transnodal Transport of Rubidium and Electrical Conductance in Chara corallina

  1989cited by this paper
• Patch-Clamp Study on a Ca2+-Regulated K+ Channel in the Tonoplast of the Brackish Characeae Lamprothamnium succinctum

  1989cited by this paper
• The Physiology of ION Channels and Electrogenic Pumps in Higher Plants

  1989cited by this paper
• Current-Voltage Curves of Single CI− Channels which Coexist with Two Types of K+ Channel in the Tonoplast of Chara corallina

  1989cited by this paper
• Transnodal Transport of 14C in Nitella flexilisIII. FURTHER STUDIES ON DISSOLVED INORGANIC CARBON MOVEMENTS IN TANDEM CELLS

  1988cited by this paper
• The mechanism of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actin filaments

  1988cited by this paper
• Cytoplasmic Streaming Regulated by Adenine Nucleotides and Inorganic Phosphates in Characeae

  1988influential reference
• The Permeability of Ammonia, Methylamine and Ethylamine in the Charophyte Chara corallina (C. australis)

  1987influential reference
• Tonoplast energization: Two H+ pumps, one membrane

  1987cited by this paper
• Steady-state voltage-dependent gating and conduction kinetics of single K+ channels in the membrane of cytoplasmic drops ofChara australis

  1987cited by this paper
• Electrical Characteristics of the Tonoplast of Cham corallincr. A Study Using Permeabilised Cells

  1987cited by this paper
• Increase in electrical resistance of plasmodesmata of Chara induced by an applied pressure gradient across nodes

  1987cited by this paper
• Depletion of cytosolic free calcium induced by photosynthesis

  1987cited by this paper

• Selective permeability of Chara nodal complex for cell-to-cell passage of photometabolites exerting opposite action on chlorophyll fluorescence.

  2025cites this paper
• Recovery of the cortical chloroplast layer in the green alga Chara after local irradiation

  2025cites this paper
• Dependence of cell's membrane potential on extracellular voltage observed in Chara globularis.

  2024cites this paper
• Role of Membrane H+ Transport and Plasmalemma Excitability in Pattern Formation, Long-Distance Transport and Photosynthesis of Characean Algae

  2024cites this paper
• Intercellular Highways in Transport Processes.

  2024cites this paper
• What we really know about the dormancy, reproduction, germination and cultivation of charophytes (Characeae)

  2024cites this paper
• Spatiotemporal Cytosolic Ca2+ Signals in Plants and Algae: Divergent Means to an End

  2023cites this paper
• Insight into the nodal cells transcriptome of the streptophyte green alga Chara braunii S276.

  2023cites this paper
• Insight into the central and nodal cells transcriptome of the streptophyte green alga Chara braunii S276

  2023cites this paper
• Effects of cell excitation on photosynthetic electron flow and intercellular transport in Chara

  2022cites this paper
• Detection of Cell-to-Cell Transport with Chlorophyll Microfluorometry: Selectivity of Metabolite Passage and Sensitivity to Sodium and Potassium Ions

  2022cites this paper
• Intercellular permeation and cyclosis-mediated transport of a fluorescent probe in Characeae.

  2022cites this paper
• The cell biology of charophytes: Exploring the past and models for the future

  2022cites this paper
• Evolution of long-distance signaling upon plant terrestrialization: comparison of action potentials in Characean algae and in liverworts.

  2022cites this paper
• Detection of Cell-to-Cell Transport with Chlorophyll Microfluorometry: Selectivity of Metabolite Passage and Sensitivity to Sodium and Potassium Ions

  2022cites this paper
• The Whimsical History of Proposed Motors for Diatom Motility

  2021cites this paper
• Melatonin and the Transmission of Light and Auxin Signals in Plants

  2020cites this paper
• Using Plant Cells of Nitellopsis obtusa for Biophysical Education

  2020cites this paper
• Cytoplasmic Streaming as an Intracellular Conveyer: Effect on Photosynthesis and H+ Fluxes in Chara Cells

  2020cites this paper
• Brefeldin A inhibits clathrin‐dependent endocytosis and ion transport in Chara internodal cells

  2020cites this paper
• Coenocytic Growth Phases in Land Plant Development: A Paleo-Evo-Devo Perspective

  2019cites this paper
• Actin Cytoskeleton and Action Potentials: Forgotten Connections

  2019cites this paper
• Cyclosis-mediated intercellular transmission of photosynthetic metabolites in Chara revealed with chlorophyll microfluorometry

  2019cites this paper
• Inhibition of endosomal trafficking by brefeldin A interferes with long‐distance interaction between chloroplasts and plasma membrane transporters

  2019cites this paper
• Dissecting the subcellular membrane proteome reveals enrichment of H+ (co-)transporters and vesicle trafficking proteins in acidic zones of Chara internodal cells

  2018cites this paper
• Brg1 subunit of chromatin remodelling complex is present during Chara vulgaris (Charophyceae) spermatogenesis

  2018cites this paper
• Electrical signalling in Nitellopsis obtusa: potential biomarkers of biologically active compounds.

  2018cites this paper
• Dynamical Patterning Modules, Biogeneric Materials, and the Evolution of Multicellular Plants

  2018cites this paper
• Biology of SLAC1-type anion channels - from nutrient uptake to stomatal closure.

  2017cites this paper
• Modeling the light-induced electric potential difference ΔΨ across the thylakoid membrane based on the transition state rate theory.

  2017cites this paper
• Charophytes: Evolutionary Giants and Emerging Model Organisms

  2016cites this paper